Kim M, Han KD, Ko SH, Woo Y, Han JH. Effect of smoking on the risk of gastrointestinal cancer after cholecystectomy: A national population-based cohort study. World J Gastrointest Surg 2024; 16(9): 2796-2807 [DOI: 10.4240/wjgs.v16.i9.2796]
Corresponding Author of This Article
Jae Hyun Han, MD, PhD, Associate Professor, Division of Hepatobiliary-Pancreas Surgery and Liver Transplantation, Department of Surgery, St Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Joongbudae-ro 93, Paldal-gu, Suwon 16247, South Korea. gelasius@catholic.ac.kr
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Cohort 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/
Minseob Kim, Department of Surgery, Graduate School of Medicine, The Catholic University of Korea, Seoul 06591, South Korea
Kyung-Do Han, Department of Statistics and Actuarial Science, Soongsil University, Seoul 06978, South Korea
Seung-Hyun Ko, Division of Endocrinology and Metabolism, Department of Internal Medicine, St Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Suwon 16247, South Korea
Yoonkyung Woo, Jae Hyun Han, Division of Hepatobiliary-Pancreas Surgery and Liver Transplantation, Department of Surgery, St Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Suwon 16247, South Korea
Author contributions: Kim M, Han KD, Ko SH, Woo Y, and Han JH contributed to the conception and design of the study, acquisition of data, drafting of the article, and making critical revisions related to the important intellectual content of the manuscript; All authors approved the final version of the article to be published; Kim M and Han KD are designated as co-first authors in recognition of their equal and substantial contributions to the study; They both played key roles in conception of the study, data acquisition and analysis, and drafting the article.
Supported bythe Clinical Research Invigoration Project of the St Vincent’s Hospital, The Catholic University of Korea, No. VC22ZASI0080.
Institutional review board statement: The study was approved by both the Korean National Health Insurance Service and the Institutional Review Board of the Catholic University of Korea (Approval No. VIRB-20220420-001).
Informed consent statement: Because this was a retrospective analysis of medical claims data, the need for informed consent was waived.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: The original anonymous dataset is available on request from the corresponding author at gelasius@catholic.ac.kr.
STROBE statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
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: Jae Hyun Han, MD, PhD, Associate Professor, Division of Hepatobiliary-Pancreas Surgery and Liver Transplantation, Department of Surgery, St Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Joongbudae-ro 93, Paldal-gu, Suwon 16247, South Korea. gelasius@catholic.ac.kr
Received: April 1, 2024 Revised: July 4, 2024 Accepted: July 31, 2024 Published online: September 27, 2024 Processing time: 170 Days and 3.1 Hours
Abstract
BACKGROUND
The role of smoking in the incidence of colorectal cancer (CRC) or gastric cancer (GC) in populations undergoing cholecystectomy has not been investigated.
AIM
To evaluate the effect of smoking on CRC or GC development in cholecystectomy patients.
METHODS
A total of 174874 patients who underwent cholecystectomy between January 1, 2010 and December 31, 2017 were identified using the Korean National Health Insurance Service claims database. These patients were matched 1:1 with members of a healthy population according to age and sex. CRC or GC risk after cholecystectomy and the association between smoking and CRC or GC risk in cholecystectomy patients were evaluated using adjusted hazard ratios (HRs) and 95%CIs.
RESULTS
The risks of CRC (adjusted HR: 1.15; 95%CI: 1.06-1.25; P = 0.0013) and GC (adjusted HR: 1.11; 95%CI: 1.01-1.22; P = 0.0027) were significantly higher in cholecystectomy patients. In the population who underwent cholecystectomy, both CRC and GC risk were higher in those who had smoked compared to those who had never smoked. For both cancers, the risk tended to increase in the order of non-smokers, ex-smokers, and current smokers. In addition, a positive correlation was observed between the amount of smoking and the risks of both CRC and GC.
CONCLUSION
Careful follow-up and screening should be performed, focusing on the increased risk of gastrointestinal cancer in the cholecystectomy group, particularly considering the individual smoking habits.
Core Tip: The study found that patients who underwent cholecystectomy, especially those who were smokers, had a higher risk of developing colorectal and gastric cancers. The analysis of Korean National Health Insurance data revealed increased risks of gastrointestinal cancer following cholecystectomy, with an association with smoking habits. This emphasizes the need for thorough screening and follow-up in these patients.
Citation: Kim M, Han KD, Ko SH, Woo Y, Han JH. Effect of smoking on the risk of gastrointestinal cancer after cholecystectomy: A national population-based cohort study. World J Gastrointest Surg 2024; 16(9): 2796-2807
Cholecystectomy is the third most commonly performed abdominal surgery in both the United States and South Korea[1,2]. Over the last two decades, the number of cholecystectomies has increased significantly in South Korea[3], and approximately 115 patients per 100000 people worldwide undergo cholecystectomy each year[4]. This increase is due to several factors, including increases in gallbladder disease associated with Western lifestyles[5-7], standardization of laparoscopic cholecystectomy[8-10], and increased availability of this procedure in hospitals of various sizes[3].
As cholecystectomy has become more common, several studies have investigated the association between cholecystectomy and the risk of developing various cancers[5,11-16], including colorectal cancer (CRC)[17-21] and gastric cancer (GC)[22,23]. Changes in bile flow, increased exposure to bile salts, carcinogenic effects of secondary bile acids due to changes in bile acid concentrations, and hormonal effects have been proposed as basic mechanisms that increase the risk of cancer after cholecystectomy[5,15]. Previous reports tended to show a positive association between cholecystectomy and the risk of CRC or GC; however, one systematic review[15] concluded that the association was not clearly significant. These inconsistent results highlight the need for high-quality studies and further consideration of the factors that may affect the incidence of cancer.
Tobacco smoking is an important preventable factor that increases the risk of cancer globally[24,25]. Smoking alone contributes to the development of gastrointestinal cancers, including CRC and GC[25-28], and affects several stages of carcinogenesis[29,30]. Several studies have shown that smoke components cause cancer through synergistic interactions with various other environmental and chemical carcinogens[30]. Although smoking plays an important and synergistic role in cancer development, it has never been investigated as an important factor in the association between cholecystectomy and CRC or GC.
This study aimed to examine the epidemiological evidence to clarify the association between cholecystectomy and CRC or GC according to smoking status in a nationwide population-based cohort using the Korean National Health Insurance Service (NHIS) claims database.
MATERIALS AND METHODS
Study population
Medical insurance in South Korea is managed by the South Korean government as a single system, and approximately 97% of the South Korean population is covered by this service. The Korean NHIS provides routine health screening every 2 years to all registered adults and collects the population’s health data through this screening. This nationwide database includes demographic factors, medical resource utilization, and regular medical health examinations. Our study was approved by both the NHIS and the Institutional Review Board of the Catholic University of Korea. Because this was a retrospective analysis of medical claims data, the need for informed consent was waived.
Between January 1, 2010 and December 31, 2017, a total of 491131 subjects aged 20 years and older who underwent cholecystectomy were screened for study eligibility. We excluded participants who did not receive regular health check-ups within 2 years after cholecystectomy (n = 280810), and participants were followed until December 31, 2017 (or were censored at CRC or GC). We also excluded participants with a history of cancer before cholecystectomy (n = 21176) and with missing data on at least one variable (n = 9348) as well as those who were diagnosed with CRC or GC within 1 year after enrollment (n = 2733) to reduce bias in the analysis of the association between cholecystectomy and CRC or GC. After exclusion, 174874 patients in the study group were matched 1:1 with a control group of members of the general population who did not undergo cholecystectomy, considering age and sex (Figure 1).
Figure 1 Flow diagram of study inclusion and exclusion.
We identified CRC or GC cases using specific international classification of disease (ICD)-10 codes. CRC was identified using the ICD-10 codes for colon (C18) and rectum (C19-20), and GC was identified using ICD-10 codes for stomach (C16). Cholecystectomy was identified using insurance claim codes (Q7380).
Covariates
Participants were classified into three age groups as follows: 20-39 years; 40-64 years; and 65 years or older. Income status was classified into four groups based on health insurance contributions. Information on lifestyle factors (smoking status, alcohol consumption, and regular physical activity) was based on responses to self-reported health questionnaires. Lifestyle factors included smoking (non-smoker, ex-smoker, or current smoker), alcohol consumption (none, moderate: < 30 g/day, or heavy: ≥ 30 g/day), and regular physical activity (yes or no). Body mass index (BMI) was divided into five groups as follows: < 18.5 kg/m2; 18.5-23.0 kg/m2; 23.0-25.0 kg/m2; 25.0-30.0 kg/m2; and ≥ 30.0 kg/m2.
Diabetes mellitus (DM) was identified by ICD-10 codes E11-E14 with claims for antidiabetic medications or a fasting blood glucose level of ≥ 7 mmol/L[31]. Hypertension was identified using ICD-10 codes I10-I13 or I15 with claims for antihypertensive medications or systolic/diastolic blood pressure of ≥ 40/90 mmHg[32]. Dyslipidemia was identified using the ICD-10 code E78 with claims for lipid-lowering medications or fasting total cholesterol of ≥ 40 mg/dL[32]. Estimated glomerular filtration rate (eGFR) was calculated from serum creatinine and several factors using the Modification of Diet in Renal Disease Study equation[33], and chronic kidney disease was defined by eGFR of < 60 mL/min/1.73 m2. Blood laboratory test results included fasting glucose, total cholesterol, high-density lipoprotein cholesterol, and low-density lipoprotein cholesterol.
Outcomes
The primary outcomes were the risk of CRC or GC after cholecystectomy in the nationwide adult population. We also investigated the risk of CRC or GC according to smoking status in patients who underwent cholecystectomy as the primary outcomes. The secondary outcomes were the amount of smoking (pack-years) in patients who underwent cholecystectomy.
Statistical analysis
Baseline characteristics were described using numbers and percentages for categorical variables and means ± SD for continuous variables. Differences between groups were compared using χ2 tests for categorical variables and Student’s t-tests for continuous variables.
The incidence rate (IR) of CRC or GC after cholecystectomy was calculated per 1000 person-years. The hazard ratio (HR) and 95%CI of CRC or GC after cholecystectomy were estimated using Cox proportional hazards regression. Three different HR models were evaluated according to adjustment factors as follows: no adjustment in model 1; adjustment for age and sex in model 2; and age, sex, smoking status, alcohol consumption, regular physical activity, hypertension, DM, dyslipidemia, BMI, and eGFR in model 3.
IR, HR, and CI were also analyzed in patients who underwent cholecystectomy according to smoking status and amount of smoking. Three HR models were obtained after adjustments. HR model 1 and model 2 were adjusted in the same way as in the previous calculation, and HR model 3 was adjusted in the same way as in the previous calculation except for smoking status. In the subgroup analysis according to several factors, IR and adjusted HR model 3 were also estimated.
All statistical analyses were performed with SAS version 9.4 (SAS Institute, Cary, NC, United States). A two-sided P < 0.05 was considered statistically significant.
RESULTS
Baseline characteristics
Of the 174874 patients in the study group, the mean age was 55.7 years, and 51.6% were male. In the cholecystectomy group, 61.6% were non-smokers and 18.8% were current smokers (which was lower than the rate in the control group), while 19.7% were ex-smokers (higher than in the control group). Compared to the matched control group, the cholecystectomy group had higher rates of BMI > 25 kg/m2, DM, hypertension, dyslipidemia, and chronic kidney disease and lower rates of income level, moderate-to-heavy alcoholic consumption behavior, and regular physical activity (Table 1).
Table 1 Baseline characteristics and comparison of demographics between the cholecystectomy group and matched control group.
Risk of CRC and GC after cholecystectomy compared with the matched control group
The IR of CRC in the cholecystectomy group was 1.60 per 1000 person-years compared to 1.38 per 1000 person-years in the control group. After adjusting for age, sex, smoking status, alcohol consumption, regular physical activity, hypertension, DM, dyslipidemia, BMI, and eGFR, the adjusted HR for CRC in the cholecystectomy group vs the control group was 1.15 (95%CI: 1.06-1.25; P = 0.0013).
Using the same method as for CRC development, IR and HR were also analyzed for GC development after cholecystectomy compared with the control population. The IR of GC was 1.34 per 1000 person-years in the cholecystectomy group and 1.20 per 1000 person-years in the control group. When adjusted for the same confounders of CRC development, the adjusted HR was 1.11 (95%CI: 1.01-1.22; P = 0.027) in the cholecystectomy group compared with the control group (Table 2, HR model 3).
Table 2 Incidence rate and hazard ratio for the risk of colorectal cancer and gastric cancer after cholecystectomy.
Risk of CRC and GC according to smoking status and quantity in patients who underwent cholecystectomy
In patients who underwent cholecystectomy, the risks of CRC and GC were analyzed according to smoking status and quantity. There was a significantly increased risk of CRC after cholecystectomy in ex-smokers and current smokers compared to non-smokers when adjusted for several demographic and comorbid factors. In addition, the risk of CRC increased in the order of non-smokers, ex-smokers, and current smokers. (Figure 2A). A tendency for the risk of CRC to increase was observed according to the amount of smoking as well as smoking status. In particular, compared to non-smokers, the risk of CRC significantly increased for those who smoked more than 20 pack-years (Figure 2B).
Figure 2 Risk of colorectal and gastric cancer according to smoking status and quantity in cholecystectomy patients.
The hazard ratios were adjusted for age, sex, alcohol consumption, regular physical activity, hypertension, diabetes mellitus, dyslipidemia, body mass index and estimated glomerular filtration rate. A: Colorectal cancer (CRC) risk after cholecystectomy according to smoking status; B: CRC risk after cholecystectomy according to smoking quantity; C: Gastric cancer (GC) risk after cholecystectomy according to smoking status; D: GC risk after cholecystectomy according to smoking quantity. HR: Hazard ratio.
The risk of GC according to smoking status and amount showed a pattern similar to that of the risk of CRC occurrence. Compared with non-smokers, ex-smokers and current smokers had a significantly higher risk of GC (Figure 2C). The risk of GC increased significantly in cases of patients smoking for more than 20 pack-years (Figure 2D). The estimated HRs were 1.37 (95%CI: 1.09-1.72; P = 0.001) in the 20 pack-years to 30 pack-years group and 1.43 (95%CI: 1.19-1.73; P = 0.001) in the 30 pack-years or more group (Table 3).
Table 3 Incidence rate and hazard ratio for the risk of colorectal cancer and gastric cancer after cholecystectomy according to smoking habits.
Subgroup analysis according to smoking status and quantity in patients who underwent cholecystectomy
We further analyzed the adjusted HR of CRC and GC according to smoking status and rate in the cholecystectomy group by age (over or under 65-years-old) and sex. The risk of CRC was significantly higher in elderly patients who underwent cholecystectomy at age 65 years or older with a smoking history compared to non-smokers. In particular, the HR was 1.87 (95%CI: 1.44-2.42) for current smokers compared to non-smokers. In patients older than 65 years, a tendency for an increased risk of CRC was observed with increased amount of smoking. In patients younger than 65 years, the risk increased only when smoking more than 30 pack-years. Among male patients, the risk of CRC significantly increased for smokers and tended to increase with the amount of smoking. In female patients, the risk of CRC increased for current smoking and those smoking for more than 30 pack-years (Table 4).
Table 4 Subgroup analysis according to smoking status and quantity in patients who underwent cholecystectomy.
The risk of GC also significantly increased among current smokers in both age groups (≥ 65 years or < 65 years) in the cholecystectomy population. Based on the amount of smoking, the risk of GC was higher in smokers aged 65 years or older with 20 pack-years or more and in those younger than 65 years with 30 pack-years or more. In addition, compared to non-smokers, the risk of GC increased in the male cholecystectomy group with a smoking history or those who smoked more than 20 pack-years (Table 4).
DISCUSSION
As the number of cases of cholecystectomy for various indications increases, interest is increasing in whether it affects long-term prognosis before and after surgery. Previous research has demonstrated the relationship between cholecystectomy and the occurrence of gastrointestinal cancer, but controversy over the correlation between the two has continued. Focusing on the association between CRC or GC after cholecystectomy, this large nationwide population-based cohort study revealed a novel association of smoking habits and the additional risk of CRC or GC in patients undergoing cholecystectomy. Our findings also suggest that smoking history and quantity are more likely to cause CRC and GC in male or elderly patients who underwent cholecystectomy, in a dose-dependent manner. These results are significant as they are the first to demonstrate, using nationwide population data, that the risk factor of smoking has a synergistic effect with cholecystectomy, thereby increasing the incidence of gastrointestinal cancer.
Cholecystectomy, smoking, and CRC
The incidence of CRC is anticipated to rise, driven by modifiable environmental factors linked to Western lifestyles[34]. Key contributors include smoking, low physical activity, obesity, poor diet, excessive alcohol consumption, inflammatory bowel disease, and gut microbiota[34].
Our research identified cholecystectomy as a risk factor for CRC that is comparable to these other known modifiable factors. Our results revealed an association between cholecystectomy and the development of CRC (adjusted HR: 1.15; 95%CI: 1.06-1.25), and the results were consistent with a previous meta-analysis (relative risk: 1.22; 95%CI: 1.08-1.38)[21]. These significant clinical findings are explained by the pathophysiology of altered bile acid metabolism[21,35]. Alterations in bile acid metabolism not only increase secondary bile acids, which themselves act as potential tumor promoters, but increased secondary bile acids also affect the gut microbiome and cause CRC[35]. This pathophysiological mechanism is similar to those driven by known modifiable factors that cause CRC, including induction of inflammation[36], direct DNA damage[37], changes in cellular immunity[38], and changes in the microbiome[34]. Therefore, considering that the CRC risk was found to be higher in the cholecystectomy group compared to the control group, despite having milder smoking and drinking statuses, cholecystectomy can be considered as an important demographic risk factor for CRC.
Several previous studies based on medical databases found no significant association between cholecystectomy and CRC[5,14,17]. Given these inconsistent results, it was necessary to consider the additional impact of another risk factor on the population undergoing cholecystectomy to establish a clear understanding of the relationship between cholecystectomy and CRC risk. Subsequently, we selected smoking, a well-established risk factor associated with various stages of CRC development[29,34], and further investigated the association between smoking and CRC risk in patients undergoing cholecystectomy. In patients who underwent cholecystectomy, the risk of CRC was increased to 35%-40% in those who had smoked compared to non-smokers, and a tendency to increase the risk of CRC was observed as the amount of smoking increased. When the amount of smoking was 30 pack-years or more, the risk of CRC increased to 59%.
Smoking has been linked to multiple effects on the heterogeneous pathway of colorectal carcinogenesis[39,40], and a meta-analysis by Botteri et al[41] demonstrated that ever-smokers had an 18% higher risk of developing CRC compared with non-smokers. In addition, the risk of CRC reportedly increases with the amount of smoking[42,43]. Recent research demonstrated that smoking promotes CRC by altering the gut microbiota composition and inducing dysbiosis[44]. Dysbiosis of the gut microbiota has been shown to increase taurodeoxycholic acid (TDCA), which activates oncogenic pathways in the colonic epithelium and impairs intestinal barrier function[44]. TDCA is derived by a conjugate of secondary bile acid deoxycholic acid (DCA) with the amino acid taurine[45] and is a known toxic metabolite affecting both esophageal cancer and CRC[44]. An increase in TDCA metabolite concentration could therefore be induced by an increase in DCA concentration in the gut, which plays a key role in CRC development after cholecystectomy. Additionally, as the increase in TDCA is further promoted in ever-smokers or others with a higher amount of smoking, the risk of CRC is thought to be higher than the risk known from previous studies.
Cholecystectomy, smoking, and GC
GC is one of the most common cancers in East Asia, and risk factors for GC include active tobacco smoking, Helicobacter pylori infection, salted food intake, and alcohol consumption[23]. In previous studies of the role of cholecystectomy as a risk factor for GC, several conflicting results were obtained. A recent meta-analysis identified a positive association between cholecystectomy and the risk of GC (relative risk: 1.11; 95%CI: 1.03-1.20)[23]. However, another nationwide cohort study found no significant relationship between cholecystectomy and the risk of GC (adjusted HR: 1.10; 95%CI: 0.99-1.22) but revealed a significantly increased GC risk among those who underwent cholecystectomy only in male patients (adjusted HR: 1.17; 95%CI: 1.04-1.32)[5].
The adjusted HR for GC in patients who underwent cholecystectomy in our study was 1.11 (95%CI: 1.01-1.22; P = 0.027), indicating a significant association between cholecystectomy and GC risk. Considering our large-scale national study with statistical power, along with the observation that the cholecystectomy group has higher cancer risks despite having milder smoking and drinking statuses compared to the control group, we suggest that cholecystectomy serves as a risk factor for GC.
Our analysis, which considered smoking as a major modifiable risk factor for GC, also found a significant correlation between the risk of GC and smoking habits in patients who underwent cholecystectomy. Compared with non-smokers, the risk of GC risk for ex-smokers was 1.19 times higher and in current smokers was 1.35 times higher in patients who underwent cholecystectomy. In addition, a significant increase in GC risk was observed in those who smoked more than 20 pack-years compared with non-smokers in the cholecystectomy population.
The development of GC after cholecystectomy can be explained by the increased duodenal gastric reflux of bile acid and increased exposure to secondary bile acid[15,23]. According to past studies, bile acid concentrations in gastric juice are associated with the extent of gastric atrophy and intestinal metaplasia, and GC occurs more frequently in patients with high bile acid concentrations compared to low bile acid concentrations[46]. Smoking increases the reflux of bile acids into the stomach, thereby increasing the concentration of bile acids in the stomach and altering the gut microbiome[47]. In addition, nicotine, a major factor in cigarette smoking, can increase the genotoxic effects of DCA[47,48]. Considering these results collectively, the overlapping physiological changes caused by cholecystectomy and smoking are likely the main mechanisms that increase the risk of GC.
Limitations
Our study had several limitations. First, we did not conduct a subgroup analysis of cancer risk based on CRC or GC anatomical sites. As for the association between the risk of CRC and cholecystectomy, a difference in cancer risk was reported not only in the colon and rectum but also in the proximal colon and distal colon[5,15,21]. In addition, it was found that there was a difference in the risk of cancer after cholecystectomy according to the cardia or non-cardia in GC[15,23]. Future analysis should focus on the association between cholecystectomy, smoking, and cancer risk considering the anatomical factors. Second, because the risk factors for gallbladder disease, which are indications for cholecystectomy, and the risk factors for CRC or GC overlap considerably, it is necessary to investigate the mechanism that underlie whether only the physiological changes that occur after cholecystectomy increase the risk of cancer. Third, this study was confined to the Korean adult population. Ethnic differences need to be investigated further. Last, confounding of the results may have been caused by protopathic bias. Protopathic bias, which refers to confounding by retrocausal relationships, is defined as confounding that takes place when exposure occurs in response to the early symptoms of a disease that we observe[17]. To minimize this bias, appropriate lag-time periods are required. In this study, a 1-year lag-time period was applied; however, the cancer risk might still be overestimated as no clear lag-time period exists between cholecystectomy and CRC or GC.
CONCLUSION
A significant positive association exists between cholecystectomy and CRC or GC risk, identifying cholecystectomy as a major epidemiologic risk factor. In addition, smoking exacerbates CRC or GC risk in cholecystectomy patients, indicating that the interaction between cholecystectomy and smoking is a crucial concern for those susceptible to CRC or GC. Therefore, clinicians should recognize that cholecystectomy performed for indiscriminate indications may increase cancer risk and should prioritize gastrointestinal cancer screening and careful follow-up, particularly for patients with a history of smoking who have undergone cholecystectomy. Furthermore, it is important to emphasize not only cessation but also the avoidance of initiating smoking for patients who have undergone cholecystectomy to prevent the further development of CRC or GC.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: South Korea
Peer-review report’s classification
Scientific Quality: Grade C
Novelty: Grade B
Creativity or Innovation: Grade B
Scientific Significance: Grade B
P-Reviewer: Liu C S-Editor: Li L L-Editor: A P-Editor: Yuan YY
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