Wang J, Liang JC, Lin FT, Ma J. Energy spectrum computed tomography multi-parameter imaging in preoperative assessment of vascular and neuroinvasive status in gastric cancer. World J Gastrointest Surg 2024; 16(8): 2511-2520 [PMID: 39220074 DOI: 10.4240/wjgs.v16.i8.2511]
Corresponding Author of This Article
Jun Ma, Doctor, Department of Radiology, Pingluo County People's Hospital, No. 2 Tuanjie West Road, Shizuishan 753400, Ningxia Hui Autonomous Region, China. majun63211@163.com
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Jing Wang, Jian-Cheng Liang, Jun Ma, Department of Radiology, Pingluo County People's Hospital, Shizuishan 753400, Ningxia Hui Autonomous Region, China
Fa-Te Lin, Department of Gastrointestinal Surgery, Jiangsu Provincial People's Hospital, Nanjing 210029, Jiangsu Province, China
Author contributions: Wang J wrote the manuscript; Liang JC and Lin FT collected the data; and Ma J guided the study. All authors reviewed, edited, and approved the final manuscript and revised it critically for important intellectual content, gave final approval of the version to be published, and agreed to be accountable for all aspects of the work. Wang J and Liang JC contributed equally to this work as co-first authors.
Institutional review board statement: This study was reviewed and approved by the Ethics Committee of Jiangsu Provincial People's Hospital.
Informed consent statement: All study participants or their legal guardian provided informed written consent about personal and medical data collection prior to study enrolment.
Conflict-of-interest statement: The authors declare no conflicts of interest.
Data sharing statement: Subject to patient privacy and data security, research data may be made available to qualified researchers upon reasonable request for scientific research and academic exchange. E-mail: majun63211@163.com.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Jun Ma, Doctor, Department of Radiology, Pingluo County People's Hospital, No. 2 Tuanjie West Road, Shizuishan 753400, Ningxia Hui Autonomous Region, China. majun63211@163.com
Received: February 22, 2024 Revised: June 25, 2024 Accepted: July 2, 2024 Published online: August 27, 2024 Processing time: 176 Days and 7.6 Hours
Abstract
BACKGROUND
Vascular and nerve infiltration are important indicators for the progression and prognosis of gastric cancer (GC), but traditional imaging methods have some limitations in preoperative evaluation. In recent years, energy spectrum computed tomography (CT) multiparameter imaging technology has been gradually applied in clinical practice because of its advantages in tissue contrast and lesion detail display.
AIM
To explore and analyze the value of multiparameter energy spectrum CT imaging in the preoperative assessment of vascular invasion (LVI) and nerve invasion (PNI) in GC patients.
METHODS
Data from 62 patients with GC confirmed by pathology and accompanied by energy spectrum CT scanning at our hospital between September 2022 and September 2023, including 46 males and 16 females aged 36-71 (57.5 ± 9.1) years, were retrospectively collected. The patients were divided into a positive group (42 patients) and a negative group (20 patients) according to the presence of LVI/PNI. The CT values (CT40 keV, CT70 keV), iodine concentration (IC), and normalized IC (NIC) of lesions in the upper energy spectrum CT images of the arterial phase, venous phase, and delayed phase 40 and 70 keV were measured, and the slopes of the energy spectrum curves [K (40-70)] from 40 to 70 keV were calculated. Arterial phase combined parameter, venous phase combined parameters (VP-ALLs), and delayed phase association parameters were calculated for patients with late-stage disease. The differences in the energy spectrum parameters between the positive and negative groups were compared, receiver operating characteristic (ROC) curves were plotted, and the area under the curve (AUC), sensitivity, specificity, and optimal threshold were calculated to measure the diagnostic efficiency of each parameter.
RESULTS
In the delayed phase, the CT40 keV, CT70 keV, K (40-70), IC, NIC, and CT70 keV and the NIC in the upper arterial and venous phases of energy spectrum CT were greater in the LVI/PNI-positive group than in the LVI-negative group. The representative parameters for the arterial phase NIC were 0.14 ± 0.04 in the positive group and 0.12 ± 0.04 in the negative group. The venous phase NIC was 0.5 (0.5, 0.6) in the positive group and 0.4 (0.4, 0.5) in the negative group. Last, for the delayed phase NIC, it was 0.6 ± 0.1 in the positive group and 0.5 ± 0.1 in the negative group (all P values are less than 0.05). ROC curve analysis demonstrated that the diagnostic efficacy of each parameter during the venous stage was superior to that during the arterial and delayed stages. Furthermore, the diagnostic efficacy of the combined parameter throughout all three stages was superior to that of any single parameter. The AUC, sensitivity, and specificity of the optimal parameter, VP-ALL, were 0.931 (95% confidence interval: 0.872-0.990), 80.95%, and 95.00%, respectively.
CONCLUSION
When assessing the condition of LVI and PNI (perineural invasion) in patients with GC prior to surgery, the ability to diagnose these conditions using venous stage parameters was superior to that using arterial stage and delayed stage parameters. Furthermore, the diagnostic accuracy of using a combination of parameters was better than that of using individual parameters alone.
Core Tip: To investigate the application value of multiparameter energy spectrum computed tomography (CT) imaging in the preoperative assessment of vascular and nerve infiltration in patients with gastric cancer (GC). The imaging data of GC patients were retrospectively analyzed to evaluate the accuracy and sensitivity of CT for identifying and quantifying vascular and nerve infiltration and for comparison with postoperative pathological results. The purpose of this study was to verify the clinical feasibility and potential advantages of multiparameter energy spectrum CT imaging in guiding preoperative diagnosis and treatment decision-making and to provide a new imaging basis for improving the diagnostic accuracy and prognosis of GC patients.
Citation: Wang J, Liang JC, Lin FT, Ma J. Energy spectrum computed tomography multi-parameter imaging in preoperative assessment of vascular and neuroinvasive status in gastric cancer. World J Gastrointest Surg 2024; 16(8): 2511-2520
Gastric cancer (GC) ranks second in incidence and third in mortality[1-3]. Invasion and metastasis are the main reasons for the poor prognosis of GC patients, in which GC cells with positive vascular invasion (LVI) and nerve invasion (PNI) have increased proliferative activity and invasiveness and are independent risk factors for tumor recurrence and metastasis[4]. Therefore, the effective prediction of LVI and PNI status before surgery is of great value for treatment decisions and prognosis assessments in GC patients[5]. At present, the status of LVI and PNI can only be obtained through postoperative pathology, so it is urgent to explore a noninvasive and effective preoperative examination method for evaluation[6-8]. With the rapid development of energy spectrum computed tomography (CT) imaging, multiparameter imaging, such as the energy spectrum curve, base substance concentration, and single energy image, provides more quantitative information in tumor evaluation and has shown good application value in the diagnosis, classification, and staging evaluation of GC. However, there are few domestic or other studies[9-11] on the ability of energy spectrum CT to predict the LVI and PNI status of patients with GC.
In recent years, with the continuous innovation and development of medical imaging technology, the preoperative evaluation of GC has become a research hotspot in the clinical medicine field[12]. GC is one of the most common malignant tumors of the digestive system in the world, and its therapeutic effect and prognosis are directly affected by accurate preoperative localization and comprehensive evaluation. In this context, energy spectrum CT multiparameter imaging has gradually become the focus of research, providing more comprehensive and in-depth information for preoperative evaluation[13]. The status of the vasculature and PNI of GC is very important for the selection of a surgical plan and the prediction of therapeutic effects. However, traditional CT imaging often has difficulty accurately depicting the blood supply and the degree of PNI of tumors, and there are limitations that cannot be ignored. Based on its different energy sensitivities to X-rays, energy spectrum CT multiparameter imaging technology can reveal the vascular density, oxygenation status, and nerve structure of tissues in a more detailed manner, providing a powerful tool for accurately evaluating the vascular and PNI status of GC patients[14]. The purpose of this study was to explore the application value of energy spectrum CT multiparameter imaging in the preoperative evaluation of GC and to provide a more comprehensive and accurate imaging basis for clinical practice. Through a comprehensive analysis of the state of vascular and PNI in GC, we will provide a scientific and reasonable basis for the formulation of a surgical plan and postoperative treatment to improve the quality of life and treatment effect of patients. However, there are still many research difficulties in this field, including the standardization of imaging parameters and the accurate interpretation of data. This study not only focused on the preoperative evaluation of GC but also aimed to promote the in-depth application of energy spectrum CT multiparameter imaging technology in clinical practice. Therefore, in this study, the energy spectrum CT imaging data of 62 patients with GC were analyzed and compared with pathological findings to explore their value in the assessment of LVI and PNI status in GC.
MATERIALS AND METHODS
Research
Subjects data from 75 patients diagnosed with gastric adenocarcinoma by postoperative pathology at our hospital between September 2022 and September 2023 were retrospectively collected.
Overall, 62 patients, 46 males and 16 females aged 36 to 71 (57.5 ± 9.1) years, were included in this study. There were 33 cases of vasculature and PNI, 5 cases of vasculature invasion, and 4 cases of PNI. Patients with LVI and/or PNI (LVI/PNI) composed the positive group, with a total of 42 patients; patients without LVI and PNI composed the negative group, with a total of 20 patients. The Medical Ethics Committee of Jiangsu Provincial People's Hospital approved this study (GYZL-ZN-2023-044), and the need to obtain informed consent from the patients was waived.
The inclusion criteria
(1) The patient was pathologically confirmed to have gastric adenocarcinoma after surgery, and the status of vascular PNI was clear; (2) An enhanced energy spectrum CT scan was performed 1 week before surgery; and (3) There was no history of iodine allergy or other related contraindications.
The exclusion criteria
(1) Incomplete clinical or CT data; (2) Preoperative antitumor therapy such as radiotherapy, chemotherapy, or targeted therapy; (3) Poor stomach filling; and (4) Image quality that did not meet the diagnostic criteria.
The scanning method
Revolution CT (American GE Company) energy spectrum scanning mode was used. Before the scan, the patient had an empty stomach for at least 6 hours and drank 800-1000 mL of water to fill the stomach cavity before the examination. The patient was placed in a supine position and scanned from the top of the diaphragm to the lower poles of both kidneys. The scanning parameters were as follows: tube voltage, 80 kVp; 140 kVp, instantaneous switching; tube current, 375 mAs; detector width, 80 mm; pitch, 0.992:1; speed, 0.6-0.8 s/RPM; matrix, 512 × 512; scanning and recombination layer thickness; and layer spacing, 5 mm. Iodohexyl (320 mg/mL, Bayer AG, Germany) was injected through the cubital vein at a dose of 1.5 mL/kg and an injection rate of 3-4 mL/s.
Postprocessing methods
The images were imported into a GE AW4.7 workstation and analyzed using Energy Spectrum Scanning Viewer software. The largest tumor layer was selected to outline an oval area of interest with a diameter greater than 1/2 of the thickness of the lesion, avoiding areas such as blood vessels and necrosis. The focal CT value (CT40 keV) in the 40 keV single-energy image on the energy spectrum, the focal CT value (CT70 keV) in the 70 keV single-energy image, the iodine concentration (IC), and the focal aortic IC (ICao) at the same level were recorded. The normalized IC (NIC) (NIC = IC/ICao) was subsequently calculated. The slope of the energy spectrum curve K (40–70) was calculated using the following formula: K (40-70) = (CT40 keV-CT70 keV)/30. In the later stage, the significant parameters of each phase were combined, namely, the arterial phase combined parameter, that is, CT40 keV + CT70 keV + IC + NIC + K (40-70), the venous phase combined parameter, CT40 keV + CT70keV + IC + NIC + K (40-70), and the delay period joint parameter, CT70keV + NIC.
Statistical analysis
SPSS 25.0 statistical software was used for the analysis. Normally distributed measurement data are represented as mean ± SD, and the differences between groups were compared by an independent sample t test. Nonnormal distributions are represented by M (Q1, Q3), and the Mann-Whitney U test was used to compare the differences between the groups. Count data are presented as frequencies, and the χ2 test was used to compare differences between groups. The receiver operating characteristic (ROC) curve was drawn for the measured parameters with statistical significance. The area under the curve (AUC) was calculated to test the diagnostic efficiency of each parameter, and the optimal threshold of each parameter was determined using the Jorden index. A binary logistic regression model was used to analyze the diagnostic efficiency of the combined parameters. For the bilateral test, the test level was α = 0.05.
RESULTS
Comparison of pathological data between the two groups of GC patients
Of the 62 GCs, 16 were located in the cardia, 4 in the fundus, 19 in the body of the stomach, and 23 in the antrum. Lymph node metastasis was significantly more likely in the LVI/PNI-positive group (P < 0.001). There were no statistically significant differences in tumor site, differentiation degree, or Lauren's classification between the two groups (all P > 0.05) (Table 1, Figures 1, 2, 3, and 4).
Figure 1 Abdominal energy spectrum computed tomography images of patients with positive vascular nerve invasion in gastric cancer.
A: Arterial phase 70 keV single energy image; B: Arterial phase 70 keV color map; C: Venous phase 70 keV single energy image; D: Intravenous phase 70 keV iodine color map.
Figure 2 Energy spectrum computed tomography neuroinvasion of gastric cancer.
A: Delay period 70 keV single energy image; B: Delay period 70 keV iodine color map; C: Vascular invasion under light microscope (HE × 100); D: Nerve invasion under light microscope (HE × 200).
Figure 3 Abdominal energy spectrum computed tomography images of patients with negative vascular nerve invasion in gastric cancer.
A: Arterial phase 70 keV single energy image; B: Arterial phase 70 keV iodine color map; C: Venous phase 70 keV single energy image; D: Intravenous phase 70 keV iodine color map.
Figure 4 Negative energy spectrum computed tomography image of nerve invasion in gastric cancer.
A: Delay period 70 keV single energy image; B: Delay period 70 keV iodine color map; C: No vascular invasion was observed under light microscope (HE × 100); D: No nerve invasion was observed under light microscope (HE × 200).
Table 1 Comparison of pathological data between two groups of gastric cancer patients.
Project
LVI/PNI positive group (n = 42)
LVI/PNI negative group (n = 20)
χ2
P value
Position
2.71
0.438
Cardia
9
7
Gastric fundus
2
2
Gastric body
13
6
Gastric antrum
18
5
Differentiation
5.08
0.079
High
2
3
Middle
9
8
Low
31
9
Lauren typing
2.44
0.296
Diffuse
21
6
Intestinal
12
9
Mixed type
9
5
Lymph node metastasis
37.58
< 0.001
Yes
39
3
No
3
17
Comparison of quantitative parameters of energy spectrum CT in two groups of GC patients revealed that the CT40 keV, CT70 keV, CT40-70), IC, NIC, CT70 keV, and NIC in the LVI/PNI-positive group were greater than those in the LVI/PNI-negative group [the representative parameters were the NIC in the arterial phase: 0.14 ± 0.04 vs 0.12 ± 0.04; venous phase NIC: 0.5 (0.5, 0.6) vs 0.4 (0.4, 0.5); and delayed phase NIC: 0.6 ± 0.1 vs 0.5 ± 0.1] (all P < 0.05). There were no statistically significant differences in CT40 keV, K (40-70), or IC during the delay period between the two groups (P > 0.05) (Table 2, Figures 1, 3, and 5).
Figure 5 Energy spectra of the two groups of gastric cancer patients.
A: Energy spectrum diagram of 40-140 keV in the arterial phase; B: Energy spectrum diagram of 40-140 keV in the venous phase; C: Energy spectrum diagram of the delay period from 40 to 140 keV.
Table 2 Comparison of energy spectrum computed tomography parameters between two groups of gastric cancer patients.
Project
LVI/PNI positive group (n = 42)
LVI/PNI negative group (n = 20)
T/Z
P value
Arterial phase
CT (HU)
196.5 ± 52.7
150.7 ± 33.9
3.55
0.001
CT (HU)
87.3 ± 19.2
66.4 ± 13.1
4.4
< 0.00
Ka3m)
3.6 ± 1.2
2.8 ± 0.7
2.96
0.004
IC (× 100 μg/cm³)
19.4 ± 6.1
14.9 ± 3.8
2.96
0.004
NIC
0.1 ± 0.0
0.1 ± 0.0
2.46
0.019
Venous phase
CT4 (HU)
242.6 ± 30.4
203.1 ± 27.8
5.06
< 0.001
CT (HU)
103.4 ± 13.3
81.4 ± 11.7
6.62
< 0.001
K4n.m
4.6 ± 0.6
4.1 ± 0.6
3.58
0.001
IC (× 100 μg/cm³)
23.9 (22.4, 27.1)
22.2 (18.9, 23.2)
-3.06
0.002
NIC
0.5 (0.5, 0.6)
0.4 (0.4, 0.5)
-3.10
0.002
Delay period
CT (HU)
185.0 ± 26.6
179.4 ± 23.2
0.82
0.418
CT (HU)
80.4 ± 11.2
72.8 ± 9.9
2.58
0.012
K4n.
3.5 ± 0.5
3.6 ± 0.5
-0.44
0.658
IC (× 100 μg/cm³)
18.5 ± 2.8
18.9 ± 2.8
-0.45
0.652
NIC
0.6 ± 0.
0.5 ± 0.1
2.80
0.007
Quantitative parameters of the energy spectrum CT in the diagnosis of LVI/PHI in GC The ROC curve of the energy spectrum CT parameters of the GC LVI/PNI-positive group and negative group showed that the diagnostic efficiency of the CT40 keV, CT70 keV, K (40-70), IC, NIC, CT70 keV and NIC in the arterial and venous phases was good (the AUC value was 0.725-0.907). The diagnostic efficiency of the combined parameters of dynamic and static pulse stages was good (the AUC values were 0.845 and 0.931, respectively) (Table 3, Figure 6).
Figure 6 Receiver operating characteristic curve of each parameter for predicting the status of gastric cancer vascular nerve invasion.
A: Arterial phase parameter; B: Venous stage parameter; C: Delay period parameter. CT: Computed tomography; IC: Iodine concentration; NIC: Normalized iodine concentration.
Table 3 Prediction efficacy of spectral computed tomography parameters for vascular nerve invasion status in gastric cancer.
Project
AUC (95%CI)
Youden index
Optimal threshold
Sensitivity (%)
Specificity (%)
Arterial phase
CT (HU)
0.755 (0.637-0.873)
0.498
196.0
54.76
95.00
CT (HU)
0.793 (0.837-0.977)
0.545
84.5
59.52
95.00
K (₄n)
0.725 (0.602-0.848)
0.450
3.7
50.00
95.00
IC (× 100 μg/cm³)
0.726 (0.602-0.849)
0.450
19.5
50.00
95.00
NIC
0.727 (0.593-0.862)
0.517
0.1
66.67
85.00
AP-all
0.845 (0.747-0.943)
0.548
0.9
54.76
100.00
Venous phase
CTk (HU)
0.830 (0.720-0.941)
0.633
217.6
83.33
80.00
CT (HU)
0.907 (0.837-0.977)
0.710
92.4
80.95
90.00
K
0.740 (0.606-0.875)
0.405
4.1
90.48
50.00
IC (× 100μg/cm³)
0.742 (0.607-0.876)
0.405
21.8
90.48
50.00
NIC
0.745 (0.604-0.886)
462
0.5
76.19
70.00
VP-all
0.931 (0.872-0.990)
0.760
0.7
80.95
95.00
Delay period
CT (HU)
0.560 (0.406-0.713)
0.179
155.9
92.86
25.00
CT (HU)
0.708 (0.573-0.843)
0.386
74.3
78.57
60.00
K
0.529 (0.371-0.686)
0.105
3.0
90.48
20.00
IC (× 100 μg/cm³)
0.532 (0.375-0.690)
0.081
15.9
88.10
20.00
NIC
0.702 (0.560-0.845)
0.412
0.5
76.19
65.00
DP-all
0.719 (0.584-0.854)
0.374
0.7
52.38
85.00
DISCUSSION
With the development of individualized treatment for GC, it is urgent to evaluate biological characteristics such as LVI and PNI status before surgery to guide treatment[15]. LVI and PNI are important pathways for the spread and metastasis of cancer cells, and the guidelines of the National Comprehensive Cancer Network in the United States recommend that positive LVI and PNI are indications for postoperative adjuvant therapy and for neoadjuvant chemotherapy[16-18]. Therefore, accurate preoperative assessment of the LVI and PNI status of patients with GC is very important for risk stratification and individualized treatment.
In this study, CT40 keV, CT70 keV, IC, NIC, CT70 keV and the NIC in the arterial and venous phases were greater in the LVI/PNI-positive group than in the negative group. The main vector in the blood vessels after an enhanced scan is iodine, and the IC and single-energy CT values of the energy spectrum CT are highly sensitive to iodine[19]. Studies[20-22] have shown that positive LVI and PNI are significantly related to the angiogenesis of GC, and positive patients have more active angiogenesis and an increased blood supply of cancerous tumors. Therefore, the CT40 keV, CT70 keV, IC, and NIC can reflect the blood supply and angiogenesis of GC patients to determine the risk of LVI and PNI. Previous studies[23-25] have shown that the IC and NIC of the arterial phase in patients with vascular cancer-positive thrombi are greater than those in vascular cancer-negative patients, which is consistent with some of the results of this study. Energy spectrum CT can be used for substance composition analysis, and the difference in the energy spectrum curve reflects the different compositions of the tumor. In this study, K (40-70) in the arterial and venous phases was greater in the LVI/PNI-positive group than in the LVI/PNI-negative group[26]. LVI-positive patients often form local microvascular cancer suppositories, and cancer suppositories are tumor cells that aggregate with each other or with white blood cells, platelets, etc. Cancer suppositories increase their material mass, which leads to enhanced X-ray attenuation, so the positive group K (40-70) is larger, indicating that K (40-70) can be used to evaluate the status of LVI and PNI[27-29].
The ROC curve results showed that the AUC values of CT40 keV, CT70 keV, K (40-70), IC, NIC, and CT70 keV and the NIC in the dynamic and static phases were all > 0.7, and the diagnostic efficiency of the venous phase was better than that of the arterial phase and the delayed phase. The arterial stage of the tumor often reflects the strengthening of larger blood vessels, while the contrast agent in the tissue in the delayed stage is clear, and only the venous stage can reflect the tumor microcirculation and better represent the tumor neovascularization and blood supply[30]. As a result, only a few of the parameters in the delayed stage are significant, and the venous stage's prediction effect is superior to that of the arterial stage's. During the study, to eliminate the differences in the use of contrast agents and scanning time for different lesions during scanning, the IC of the aorta at the same level of the lesions was selected as a reference, and the NIC was used for further comparison[31-33]. The results showed that the AUCs of both the arterial and venous NIC were greater than those of the IC. Further analysis revealed that the diagnostic efficacy of the combined parameters in the third stage was superior to that of the single parameters, and the AUC values were all > 0.8, among which the AUC, sensitivity, and specificity were 0.931, 80.95%, and 95.00%, respectively[34-36]. When the venous phase association parameters was > 0.68 in patients, the diagnostic efficacy of the combined parameters was greater than that of the single parameters[37]. The probability of an LVI/PNI positive state is greater. The high specificity is beneficial for accurately screening patients with true-positive LVI and PNI invasion before surgery and preventing overdiagnosis and treatment caused by the inclusion of false-positive patients in the application of neoadjuvant therapy and intraoperative resection scope decisions[38-40]. Therefore, the combined parameters of the venous phase have important value in predicting the status of LVI and PNI.
There are several limitations in this study. The radiation dose of energy spectrum CT is greater than that of conventional enhanced CT, but the patients have obvious benefits. This was a single-center study with a small sample size, and the sample size needs to be expanded for further stratified research.
CONCLUSION
In summary, CT40 keV, CT70 keV, K (40-70), IC, NIC, and CT70 keV and the NIC in the delayed stage of the dynamic and static pulse phase of spectral CT have certain clinical value in the preoperative assessment of the LVI and PNI status of GC patients. These findings can provide a certain imaging basis for clinical treatment decisions and prognostic judgments in patients with GC.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B
Novelty: Grade B
Creativity or Innovation: Grade B
Scientific Significance: Grade B
P-Reviewer: Moshref L S-Editor: Qu XL L-Editor: A P-Editor: Che XX
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