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Risk factors associated with clinical outcomes of endoscopic mucosal resection for colorectal laterally spreading tumors: A Honam Association for the Study of Intestinal Diseases (HASID) multicenter study.

INTRODUCTION

Colorectal laterally spreading tumors (LSTs) are superficial and flat neoplasms with a diameter [greater than or equal to]10 mm. They extend laterally and circumferentially along the colorectal luminal wall. They are classified as either granular (LST-G) or non-granular (LST-NG) type according to their endoscopic macroscopic morphology. Kudo et al. proposed a subclassification of the LST-G and LST-NG types; LST-Gs are subclassified as homogeneous (HG) and nodular mixed (NM) subtypes, and LST-NGs are subclassified into flat elevated (FE) and pseudo-depressed (PD) subtypes (1-4). Invasive carcinomas are more frequent in the LST-NG type than in the LST-G type. The PD and NM subtypes have higher malignant potentials (5-9). However, most LSTs are of the LST-G type and are adenomatous lesions. Therefore, LSTs are usually removed using endoscopic resection techniques (10-18).

Endoscopic mucosal resection (EMR) is a safe and effective technique for the treatment of precursor colorectal lesions. This technique involves the injection of a mixture of normal saline, contrast dye, and diluted epinephrine into the submucosal layer of the lesion to lift the lesion off the muscle layer and create a dye-stained "submucosal cushion" between the mucosal layer and the proper muscle layer of the lesion. The lifted lesion is then excised through constriction with an electrical current using a snare wire. Colorectal neoplasms up to 20 mm can be removed en bloc using an EMR and >20 mm can be removed using a piecemeal EMR. However, it is difficult to obtain an accurate histopathological diagnosis in a piecemeal EMR, and the approach tends to lead to incomplete resection and local recurrence (19-22).

Endoscopic submucosal dissection (ESD) is a recently introduced advanced technique for treating large colorectal neoplasms that allows complete en bloc resection for an accurate histopathological evaluation, regardless of lesion size, shape, and location. However, it is a more complex, expensive, and time-consuming technique with higher rates of perforation and a longer learning curve (19-24). Therefore, it has not been extensively used for the treatment of large colorectal lesions, such as LSTs. EMR of lesions [less than or equal to]20 mm and piecemeal EMR of colorectal lesions >20 mm are the standard techniques worldwide (19-22).

The aim of the present study was to investigate the factors associated with the clinical outcomes of EMR for colorectal LSTs.

MATERIALS AND METHODS

Patients

A total of 275 patients with LSTs that were resected using an EMR from January 2012 to December 2013 at five university hospitals in Honam Province, South Korea were enrolled in the study. Patient's medical records were collected and analyzed retrospectively. EMR was performed after explaining the procedure and its related complications, including bleeding and perforation. Informed consent was obtained from the patients after explaining the possibility of potential complications and additional surgery according to complications or pathological diagnosis of resected specimens. The institutional review board of each participating hospital approved the study protocol.

Definition and classification of colorectal LSTs

Laterally spreading tumor is defined as a lesion [greater than or equal to]10 mm in size that extends laterally along the interior luminal wall with a short vertical axis. Endoscopic macroscopic morphology was classified in accordance with a prior endoscopic classification using chromoendoscopy with a 0.5% indigo carmine with or without magnified examination (4). LSTs were then classified into the LST-G or LST-NG type based on endoscopic macroscopic morphology. The LST-G type was further subclassified into the HG and NM subtypes, and the LST-NG type was further subclassified into the FE and PD subtypes (4). The pit pattern of lesions was evaluated retrospectively by analyzing the results of conventional colonoscopy and chromoendoscopy with or without examination at higher magnification. The pit pattern was divided into six types as I, II, [III.sub.s], [III.sub.L], IV, and V (25). The location of the LST was either the distal colon (rectosigmoid colon and descending colon) or the proximal colon (transverse colon, ascending colon, and cecum). Two endoscopists blinded to the study reviewed all cases and subclassified them as described above. In cases of classification discrepancies, they discussed the results to reach a consensus and a single diagnosis.

EMR procedure

Endoscopic mucosal resection was performed using a CF-Q260AI endoscope model (Olympus, Tokyo, Japan) at all participating institutions. Chromoendoscopy with a 0.4% indigo carmine dye or narrow band imaging was performed to delineate the margins of the lesions and to evaluate their pit patterns. A mixture of normal saline and indigo carmine with diluted epinephrine (1:5000-1:10,000) was injected into the submucosal layer below the lesion using an NM-4U-1 23-gauge needle (Olympus) until the mucosa lifted. The lifted lesion was excised through constriction with electrical current using an SD12L/U-1 snare wire model (Olympus) and an electrocautery device (ERBE Elektromedizin, Tubingen, Germany). The resected specimens were fixed in 10% buffered formalin, embedded in paraffin, sliced in 2 mm sections, stained with hematoxylin and eosin, and, finally, assessed microscopically. The histopathological diagnosis was based on the World Health Organization classifications of gastrointestinal epithelial neoplasia (26).

Definition of en bloc, piecemeal, RO resection, and procedure time

En bloc and piecemeal resections were defined as resection with a single piece and resection with multiple pieces, respectively. R0 resection was defined as the removal of the specimen with tumor-free lateral and basal margins. Procedure time was counted from the start of local injection to the end of lesion removal.

Definition of adverse events

Procedure-related bleeding after EMR was defined as bleeding that required transfusion or surgical intervention or bleeding that decreased the hemoglobin level to >2 g/dL. Perforation was defined as the endoscopic finding of a full-thickness defect formed all the way through the colon wall or the presence of free air on abdominal plain radiography or computed tomography images.

Statistical analysis

Data were analyzed using the Statistical Package for the Social Sciences, version 22.0 software (IBM Corp.; Armonk, NY, USA). Continuous variables with normal distribution are expressed as mean [+ or -] standard deviation, and categorical variables are expressed as frequency and percentage (%). Differences were analyzed using the chi-square test, Student's t-test, or analysis of variance, as appropriate. Risk factors associated with piecemeal resection after EMR were determined using a logistic regression model. All risk factors were analyzed using univariate logistic regression analysis, and factors with a p-value of <0.05 were included in the multivariate logistic regression model. A P-value of <0.05 was considered statistically significant.

RESULTS

Clinicopathological characteristics of the study population

Table 1 shows the clinicopathological characteristics of the study populationhttps://link.springer.com/article/10.1007%2Fs00384-012-1543-2 - Tab1. The mean age of the patients was 65.9[+ or -]9.7 (42.0-90.0) years. There were 171 (62.2%) male and 104 (37.8%) female patients in the study group. The mean tumor size was 18.0[+ or -]7.9 (10.0-85.0) mm. Of the tumors, there were 147 (53.5%) localized in the proximal colon and 128 (46.5%) localized in the distal colon. Among the 275 LSTs treated with EMR, there were 184 (66.9%) LST-Gs and 91 (33.1%) LST-NGs. According to the classification by Kudo et al., 69 (38.5%) lesions had a non-neoplastic pit pattern (type I/II), 103 (57.6%) had an adenomatous pit pattern (type [III.sub.s]/[III.sub.L]/IV), and 7 (3.9%) had a cancerous pit pattern (type V/[V.sub.N] in terms of pit pattern (4). Histological grading revealed 207 (75.3%) low-grade dysplasias, 39 (14.2%) high-grade dysplasias, and 29 (10.5%) adenocarcinomas. In 239 out of 275 LSTs, the en bloc resection rate was 86.9%. In 221 out of 275, the R0 resection rate was 80.4%. The bleeding and perforation rates after EMR were 7.6% (21 out of 275) and 0.4% (1 out of 275), respectively.

Clinical outcome and safety of EMR for colorectal LSTs according to endoscopic macroscopic morphology and size of the lesion

Tables 2 and 3 summarize the clinical outcomes and safety of EMR for colorectal LSTs according to the endoscopic macroscopic morphology and size of the lesions. LST-NGs were more commonly found in the distal colon, and LST-Gs were more commonly found in the proximal colon (p=0.013). The mean size of LST-Gs tended to be larger than that of LST-NGs (p=0.052). The bleeding rate tended to be higher in LST-NGs than in LST-Gs (p=0.079). There were no statistically significant differences in pit pattern, histological grade, resection method, mean procedure time, RO resection, and perforation between the LST-G and LST-NG types. The frequency of LST-G type and cancerous pit pattern tended to be higher in LSTs >20 mm than in those [less than or equal to]20 mm (p=0.052 and p=0.067, respectively). The frequency of high-grade dysplasia and adenocarcinoma histology was significantly higher in LSTs >20 mm than in those [less than or equal to]20 mm (p=0.001). The en bloc resection rate tended to be higher in LSTs [less than or equal to]20 mm than in those >20 mm (p=0.073). The mean procedure time was significantly longer in LSTs >20 mm than in those [less than or equal to]20 mm (p=0.004). The RO resection rate was significantly higher in LSTs [less than or equal to]20 mm than in those >20 mm (p=0.013). There were no statistically significant differences in location, bleeding, and perforation rates between LSTs [less than or equal to]20 and >20 mm.

Univariate analysis of risk factors associated with piecemeal resection after EMR for colorectal LSTs

Table 4 shows the clinicopathological factors associated with en bloc or piecemeal resection after EMR for colorectal LSTs. There was no significant difference between en bloc and piecemeal resection in terms of age, sex, comorbidity, smoking, alcohol drinking, body mass index, use of aspirin and nonsteroidal anti-inflammatory drugs, tumor location, and endoscopic macroscopic morphology. The rate of piecemeal resection tended to be higher in LSTs >20 mm than in those [less than or equal to]20 mm (odds ratio (OR) 1.990, 95% confidence interval (CI) 0.929-4.262, p=0.077). The frequency of piecemeal resection was significantly higher in LSTs with an adenomatous and cancerous pit pattern than in those with a non-neoplastic pit pattern (OR 10.177, 95% CI 2.320-44.653, p=0.002 and OR 13.400, 95% CI 1.545-116.233, p=0.019, respectively). The frequency of piecemeal resection was significantly higher in LSTs with adenocarcinoma histology than in those with low-grade dysplasia histology (OR 2.676, 95% CI 1.026-6.978, p=0.044). There was no significant difference between en bloc and piecemeal resection in terms of procedure time.

Multivariate analysis of risk factors associated with piecemeal resection after EMR for colorectal LSTs

Table 5 summarizes the results of multivariate analysis of risk factors associated with piecemeal resection after EMR for colorectal LSTs. For regression analysis, LSTs with an adenomatous pit pattern, high-grade dysplasia histology, or adenocarcinoma histology were significant independent risk factors for piecemeal resection after EMR (OR 14.036, 95% CI 2.882-68.360, p=0.001; OR 3.418, 95% CI 1.129-10.346, p=0.030; and OR 12.979, 95% CI 2.377-70.855, p=0.003, respectively).

DISCUSSION

Colorectal LSTs are increasingly being reported in the literature owing to increased awareness of these lesions and the introduction of chromoscopic and magnifying colonoscopy (1-4). These lesions are usually adenomatous and are removed by endoscopic resection (5-9). However, the rate of colorectal LSTs with advanced histology varies according to endoscopic morphology and lesion size (5-9). Therefore, the appropriate therapeutic strategy for each colorectal LST must be selected with caution (10-18).

Endoscopic mucosal resection is an easy-to-learn, safe, and effective therapeutic technique for superficial colorectal neoplasms. However, if the lesion size is >20 mm, this technique is not feasible and safe for an en bloc resection owing to the size limitation of the snare (19-22). ESD is a recently developed technique with therapeutic advantages over EMR in terms of allowing a complete en bloc resection of a lesion irrespective of its size. However, it is a difficult technique with a high risk of perforation and a long learning curve (19-24). Therefore, it is not currently widely used as the standard method for treating large superficial colorectal neoplasms, such as LSTs, and EMR remains to be used for treating large superficial colorectal neoplasms, such as LSTs, in the clinical research setting.

Currently, we evaluated the efficacy and safety of EMR for colorectal LSTs. The en bloc and R0 resection rates were 86.9% and 80.4%, respectively. Generally, the en bloc and R0 resection rates were 88.5% and 94.1%, respectively, in LSTs [less than or equal to]20 mm. However, the en bloc and R0 resection rates were 81.0% and 82.5%, respectively, in LSTs >20 mm. Furthermore, the mean procedure time in the larger LSTs was significantly longer than that in LSTs <20 mm. Our results are comparable to previous studies (19-22) and indicate that EMR remains an acceptable method for treating <20 mm colorectal LSTs with regard to mean procedure time, en bloc resection rate, and complete resection rate.

The main complications of colorectal EMR are bleeding and perforation (19-22). Currently, the bleeding and perforation rates after EMR were 7.6% and 0.4%, respectively. Previous studies reported that the factors affecting the risk of bleeding after colorectal EMR include the type and size of the lesion, the lesion location, and the patient's coagulation status (19-22). The bleeding rate after colorectal EMR was 1.0%-18.0% (19-22). In the present study, the bleeding rate tended to be higher in LST-NGs than in LST-Gs. There were no statistically significant differences in bleeding rate according to lesion size. Reported risk factors of perforation after colorectal EMR include the size and location of the lesion and the presence of fibrosis (19-22). The perforation rate after colorectal EMR was 0.31%-1.7% of the cases (19-22). Only one case of perforation was observed in the present study. This case was managed using a clip application. These results indicate that EMR for colorectal LSTs is a safe procedure with a low incidence of main complications, such as bleeding and perforation.

En bloc resection is a prerequisite for obtaining a precise histological diagnosis and for deciding complete curative resection after endoscopic resection of colorectal neoplasms (19-24). Then, we evaluated the clinicopathological factors associated with en bloc or piecemeal resection after EMR for colorectal LSTs. Most LSTs can be resected en bloc and completely with EMR (11-13). However, the present frequency of piecemeal resection was significantly higher in LSTs with an adenomatous and cancerous pit pattern or with adenocarcinoma histology. The frequency of piecemeal resection tended to be higher in LSTs >20 mm than in those [less than or equal to]20 mm, but no statistical significance was found. However, EMR is difficult to perform en bloc resection of a colorectal neoplasm >20 mm owing to snare size limitation (19-22). Therefore, a larger size can still be a risk factor for piecemeal resection. There could be a significant difference if many colorectal neoplasms with a size >20 mm are enrolled in the study. For multivariate analysis, LSTs with an adenomatous pit pattern, high-grade dysplasia histology, or adenocarcinoma histology were significant independent risk factors for piecemeal resection after EMR. In previous studies, the frequency of piecemeal resection was reported to be increased in superficial colorectal neoplasms, including LSTs with a larger size, LST-NG type, and advanced histology (11-13, 19-24), similar to our results. Generally, since these lesions have a higher malignant potential, careful consideration is needed in selecting the endoscopic treatment modality for the en bloc and curative resection of these tumors. ESD may be considered as an alternative to EMR for en bloc and curative resection.

The present study has some limitations. The study was retrospectively and nonrandomly designed. Cases with colorectal LSTs treated only by EMR were enrolled in the study. LSTs with risk factors, such as large size and type V pit pattern, were usually resected by ESD (10-18). Therefore, LSTs with risk factors were excluded. For this reason, there could be selection biases in size and pit patterns of colorectal LSTs.

In conclusion, EMR is useful for treating [less than or equal to]20 mm colorectal LSTs with regard to curative resection and procedure time, and LSTs with an adenomatous pit pattern, high-grade dysplasia histology, or adenocarcinoma histology are significant independent risk factors for piecemeal resection after EMR for colorectal LSTs. If EMR is considered as the endoscopic treatment for these lesions, the lesions should be removed en bloc with great caution to ensure an accurate histopathological diagnosis.

Ethics Committee Approval: The institutional review board of each participating hospital approved the study protocol.

Informed Consent: Written informed consent was obtained from the patients who participated in this study.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - Y.E.J.; Design - D.J.S.; Supervision - Y.E.J.; Data Collection and/or Processing - J.L, S.W.K., G.S.S.; Analysis and/or Interpretation - S.S.K.; Writing Manuscript - Y.E.S., D.J.S.; Critical Review - H.S.K.

Conflict of Interest: The authors have no conflict of interest to declare.

Financial Disclosure: The authors declared that this study has received no financial support.

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Dong-Jun Son (1) [iD], Sun-Seog Kweon (2) [iD], Jun Lee (3) [iD], Sang-Wook Kim (4) [iD], Geom-Seog Seo (5) [iD], Hyun-Soo Kim (1) [iD], Young-Eun Joo (1) [iD]

(1) Department of Internal Medicine, Chonnam National University Medical School, Gwangju, Korea

(2) Department of Preventive Medicine, Chonnam National University Medical School, Gwangju, Korea

(3) Department of Internal Medicine, Chosun University College of Medicine, Gwangju, Korea

(4) Department of Internal Medicine, Chonbuk National University Medical School, Jeonju, Korea

(5) Department of Internal Medicine, Wonkwang University College of Medicine, Iksan, Korea

Corresponding Author: Young-Eun Joo; yejoo@chonnam.ac.kr

Received: May 31, 2018 Accepted: September 26, 2018 Available online date: March 29, 2019

DOI: 10.5152/tjg.2019.18393
Table 1. Clinicopathological characteristics of colorectal laterally
spreading tumors treated by endoscopic mucosal resection

Factors

Age (years)        Mean[+ or -]SD (range)
Sex                Male/female
Comorbidity        No/yes
Smoking status     Non-/current smoker
                   or ex-smoker
Alcohol drinking   No/yes
BMI (kg/m2)        Mean[+ or -]SD (range)
Aspirin or NSAIDs  No/yes
Location           Proximal colon
                   Distal colon
Size (mm)          Mean[+ or -]SD (range)
                   [less than or equal to]20 mm
                   >20 mm
Macroscopic type   Granular
                   Homogeneous
                   Nodular mixed
                   Non-granular
                   Flat elevated
                   Pseudo-depressed
Pit pattern        Non-neoplastic
(n=179)            (type I/II)
                   Adenomatous
                   (type IIIS/IIIL/IV)
                   Cancerous (type VI/VN)
Histology          Low-grade dysplasia
                   High-grade dysplasia
                   Adenocarcinoma
Resection type     En bloc resection
                   Piecemeal resection
Procedure          Mean[+ or -]SD (range)
time (min)
Complete r
esection (RO)      Margin (-)
                   Margin (+)
                   Undetermined
Bleeding           No/yes
Perforation        No/yes

Factors            n=275 (%)

Age (years)         65.9[+ or -]9.7 (42.0-90.0)
Sex                171/104 (62.2/37.8)
Comorbidity        131/144 (47.6/52.4)
Smoking status     210/65 (76.4/23.6)
Alcohol drinking   195/80 (70.9/29.1)
BMI (kg/m2)         24.1[+ or -]3.5 (16.0-39.0)
Aspirin or NSAIDs  245/30 (89.1/10.9)
Location           147 (53.5)
                   128 (46.5)
Size (mm)           18.0[+ or -]7.9 (10.0-85.0)
                   215 (78.2)
                    60 (21.8)
Macroscopic type   184 (66.9)
                    91 (33.1)
                    93 (33.8)
                    91 (33.1)
                    83 (30.2)
                     8 (2.9)
Pit pattern         69 (38.5)
(n=179)
                   103 (57.6)
                     7 (3.9)
Histology          207 (75.3)
                    39 (14.2)
                    29 (10.5)
Resection type     239 (86.9)
                    36 (13.1)
Procedure           12.2[+ or -]16.7 (1.0-110.0)
time (min)
Complete r
esection (RO)      221 (80.4)
                    21 (7.6)
                    33 (12.0)
Bleeding           254/21 (92.4/76)
Perforation        274/1 (99.6/0.4)

SD, standard deviation; BMI, body mass index; NSAIDs, nonsteroidal
antiinflammatory drugs.

Table 2. Clinical outcome and safety of colorectal laterally spreading
tumors treated by endoscopic mucosal resection according to endoscopic
macroscopic morphology

Factors                                Macroscopic type
                                       Granular
                                       type
                                       n=184
                                       (%)

Location
--Proximal colon                       108 (58.7)
--Distal colon                          76 (41.3)
Size (mm) (mean[+ or -]SD)              18.8[+ or -]8.6
--[less than or equal to]20 mm         139 (75.5)
-->20 mm                                45 (24.5)
Pit pattern (n=175)
--Non-neoplastic (type I/II)            52 (40.6)
--Adenomatous (type IIIS/IIIL/IV)       72 (56.3)
--Cancerous (type VI/VN)                 4 (3.1)
Histological grade
--Low-grade dysplasia                  138 (75.0)
--High-grade dysplasia                  30 (16.3)
--Adenocarcinoma                        16 (8.7)
Resection type
--En bloc resection                    158 (85.9)
--Piecemeal resection                   26 (14.1)
Procedure time (min) (mean[+ or -]SD)   12.3[+ or -]16.6
RO resection (n=242)                   154 (89.5)
Bleeding                                11 (6.0)
Perforation                              1 (0.5)

Factors                                Macroscopic type
                                       Non-granular
                                       type
                                       n=91
                                       (%)               P

Location                                                 0.013
--Proximal colon                       39 (42.9)
--Distal colon                         52 (57.1)
Size (mm) (mean[+ or -]SD)             16.5[+ or -]6.0
--[less than or equal to]20 mm         78 (85.7)         0.052
-->20 mm                               13 (14.3)
Pit pattern (n=175)                                      0.511
--Non-neoplastic (type I/II)           17 (33.3)
--Adenomatous (type IIIS/IIIL/IV)      31 (60.8)
--Cancerous (type VI/VN)                3 (5.9)
Histological grade                                       0.167
--Low-grade dysplasia                  69 (75.8)
--High-grade dysplasia                  9 (9.9)
--Adenocarcinoma                       13 (14.3)
Resection type                                           0.467
--En bloc resection                    81 (89.0)
--Piecemeal resection                  10 (11.0)
Procedure time (min) (mean[+ or -]SD)  11.8[+ or -]17.1  0.801
RO resection (n=242)                   67 (95.7)         0.122
Bleeding                               11 (12.1)         0.079
Perforation                             0 (0.0)

SD, standard deviation.

Table 3. Clinical outcome and safety of endoscopic mucosal resection
according to the size of the lesion

Factors                                Size
                                       [less than or equal to]20 mm
                                       n=217 (%)

Location
--Proximal colon                       114 (52.5)
--Distal colon                         103 (475)
Macroscopic type
--Granular                             139 (64.1)
--Non-granular                          78 (35.9)
Pit pattern (n=179)
--Non-neoplastic (type I/II)            59 (42.8)
--Adenomatous (type IIIS/IIIL/IV)       75 (54.3)
--Cancerous (type VI/VN)                 4 (2.9)
Histology
--Low-grade dysplasia                  174 (80.2)
--High-grade dysplasia                  23 (10.6)
--Adenocarcinoma                        20 (9.2)
Resection type
--En bloc resection                    192 (88.5)
--Piecemeal resection                   25 (11.5)
Procedure time (min) (mean[+ or -]SD)   10.2[+ or -]14.3
R0 resection (n=242)                   174 (94.1)
Bleeding                                20 (9.2)
Perforation                              1 (0.5)

Factors                                Size
                                        >20 mm
                                        n=58 (%)          P

Location                                                  0.554
--Proximal colon                        33 (56.9)
--Distal colon                          25 (43.1)
Macroscopic type                                          0.052
--Granular                              45 (77.6)
--Non-granular                          13 (22.4)
Pit pattern (n=179)                                       0.067
--Non-neoplastic (type I/II)            10 (24.4)
--Adenomatous (type IIIS/IIIL/IV)       28 (68.3)
--Cancerous (type VI/VN)                 3 (7.3)
Histology                                                 0.001
--Low-grade dysplasia                   33 (56.9)
--High-grade dysplasia                  16 (27.6)
--Adenocarcinoma                         9 (15.5)
Resection type                                            0.073
--En bloc resection                     47 (81.0)
--Piecemeal resection                   11 (19.0)
Procedure time (min) (mean[+ or -]SD)   19.1[+ or -]22.2  0.004
R0 resection (n=242)                    47 (82.5)         0.013
Bleeding                                 2 (3.4)          0.182
Perforation                              0 (0.0)

SD, standard deviation.

Table 4. Univariate analysis of risk factors associated with piecemeal
resection after endoscopic mucosal resection for colorectal laterally
spreading tumors

En                                   bloc resection n=239 (%)

Age (years) (mean[+ or -]SD)         66.0[+ or -]9.5
Male sex                             146 (85.4)
Comorbidity (+)                      126 (87.5)
Current or ex-smoker                  52 (80.0)
Alcohol drinking                      68 (85.0)
BMI (kg/[m.sup.2]) (mean[+ or -]SD)   24.3[+ or -]3.5
Use of aspirin or NSAIDs              20 (83.3)
Size (mean[+ or -]SD)                 17.8[+ or -]8.1
--Size[less than or equal to]20 mm   191 (88.5)
--Size>20 mm                          48 (81.0)
Location
--Proximal colon                     127 (86.4)
--Distal colon                       112 (87.5)
Macroscopic type
--Granular                           158 (85.9)
--Non-granular                        81 (89.0)
Pit pattern (n=179)
--Non-neoplastic (type I/II)          67 (97.1)
--Adenomatous (type IIIS/IIIL/IV)     79 (76.7)
--Cancerous (type VI/VN)               5 (71.4)
P-value for trend
Histological grade
--Low-grade dysplasia                185 (89.4)
--High-grade dysplasia                32 (82.1)
--Adenocarcinoma                      22 (75.9)
P-value for trend

En                                   Piecemeal resection n=36 (%)

Age (years) (mean[+ or -]SD)         65.5[+ or -]10.7
Male sex                             25 (14.6)
Comorbidity (+)                      18 (12.5)
Current or ex-smoker                 13 (20.0)
Alcohol drinking                     12 (15.0)
BMI (kg/[m.sup.2]) (mean[+ or -]SD)  11.5[+ or -]3.3
Use of aspirin or NSAIDs              5 (16.7)
Size (mean[+ or -]SD)                19.9[+ or -]6.2
--Size[less than or equal to]20 mm   24 (11.5)
--Size>20 mm                         12 (19.0)
Location
--Proximal colon                     20 (13.6)
--Distal colon                       16 (12.5)
Macroscopic type
--Granular                           26 (14.1)
--Non-granular                       10 (11.0)
Pit pattern (n=179)
--Non-neoplastic (type I/II)          2 (2.9)
--Adenomatous (type IIIS/IIIL/IV)    24 (23.3)
--Cancerous (type VI/VN)              2 (28.6)
P-value for trend
Histological grade
--Low-grade dysplasia                22 (10.6)
--High-grade dysplasia                7 (17.9)
--Adenocarcinoma                      7 (24.1)
P-value for trend

                                     Univariate analysi:
En                                   OR (95% CI)            P

Age (years) (mean[+ or -]SD)          0.995 (0.960-1.032)   0.782
Male sex                              1.448 (0.680-3.081)   0.337
Comorbidity (+)                       0.897 (0.445-1.808)   0.761
Current or ex-smoker                  2.033 (0.964-4.287)   0.062
Alcohol drinking                      1.257 (0.595-2.656)   0.548
BMI (kg/[m.sup.2]) (mean[+ or -]SD)   0.915 (0.810-1.032)   0.148
Use of aspirin or NSAIDs              1.381 (0.492-3.873)   0.540
Size (mean[+ or -]SD)
--Size[less than or equal to]20 mm    1.000 (ref)
--Size>20 mm                          1.990 (0.929-4.262)   0.077
Location
--Proximal colon                      1.000 (ref)
--Distal colon                        0.907 (0.448-1.836)   0.786
Macroscopic type
--Granular                            1.000 (ref)
--Non-granular                        0.750 (0.345-1.632)   0.468
Pit pattern (n=179)
--Non-neoplastic (type I/II)          1.000 (ref)
--Adenomatous (type IIIS/IIIL/IV)    10.177 (2.320-44.653)  0.002
--Cancerous (type VI/VN)             13.400 (1.545-116.233) 0.019
P-value for trend                                           0.001
Histological grade
--Low-grade dysplasia                 1.000 (ref)
--High-grade dysplasia                1.839 (0.726-4.660)   0.199
--Adenocarcinoma                      2.676 (1.026-6.978)   0.044
P-value for trend                                           0.029

OR, odds ratio; SD, standard deviation; CI, confidence interval; BMI,
body mass index; NSAIDs, nonsteroidal anti-inflammatory drugs.

Table 5. Multivariate analysis of risk factors associated with
piecemeal resection after endoscopic mucosal resection for colorectal
laterally spreading tumors

                                  Multivariate analysis
Factors                           aOR(95%CI)             P

Pit pattern
--Non-neoplastic (type I/II)       1.000 (ref)
-Adenomatous (type IIIS/IIIL/IV)  14.036 (2.882-68.360)  0.001
--Cancerous (type VI/VN)           4.293 (0.418-44.121)  0.220
Histological grade
--Low-grade dysplasia              1.000 (ref)
--High-grade dysplasia             3.418 (1.129-10.346)  0.030
--Adenocarcinoma                  12.979 (2.377-70.855)  0.003

aOR, adjusted odds ratio; CI, confidence interval.
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Title Annotation:ORIGINAL ARTICLE
Author:Son, Dong-Jun; Kweon, Sun-Seog; Lee, Jun; Kim, Sang-Wook; Seo, Geom-Seog; Kim, Hyun-Soo; Joo, Young-
Publication:The Turkish Journal of Gastroenterology
Article Type:Report
Date:Apr 1, 2019
Words:5227
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