Diet and microbiota and Crohn’s disease pathogenesis: Insights from the First Affiliated Hospital of Sun Yat-sen University​

Professor Minhu Chen Department of Gastroenterology The First Affiliated Hospital Sun Yat-sen University Guangzhou, China

Crohn’s disease (CD) results from the complex interplay of environmental triggers, gut microbiota dysbiosis, and immune dysfunction in genetically predisposed individuals. The rapid rise of CD in urbanized countries is largely attributed to environmental changes rather than genetic drift. This study, incorporating multi-omics data from the First Affiliated Hospital of Sun Yat-sen University, explores the role of diet in CD pathogenesis by modulating gut microbiota composition and function.

Epidemiological studies have identified various nutritional components, dietary types, and dietary patterns that contribute to the risk of CD. Diet influences the gut microbiota at multiple levels, including taxonomic composition, functional capacity, and metabolic outputs, ultimately shaping host immune responses and intestinal homeostasis. Additionally, dietary shifts can drive strain-level genetic adaptations, altering microbial metabolism and host-microbe interactions, or reshape microbial guilds—functionally grouped communities that cooperate or compete within the gut ecosystem—thereby modulating key metabolic pathways and immune regulation. Our group showed that pro-inflammatory diets disrupted microbial diversity, increasing pro-inflammatory bacteria (Morganella morganii, Veillonella parvula) and microbial metabolites such as phenylacetylglutamine (PAGln), which promotes platelet activation and immune dysfunction. Sulfate-containing preservatives enhanced microbial sulfate reduction pathways, elevating hydrogen sulfide (H₂S) production, which damages epithelial integrity and drives inflammation. In contrast, polyphenol-rich diets promoted beneficial microbiota and protective metabolites, suggesting a potential dietary intervention for CD.

These studies highlight diet and gut microbial dysbiosis as key contributors to CD pathogenesis. These findings underscore the potential for precision nutrition and microbiome-based interventions in CD prevention and management.

21st century IBD landscape – lessons learnt

Professor Shu-Chen Wei Department of Internal Medicine National Taiwan University Hospital Taipei, Taiwan

Inflammatory bowel disease (IBD), which includes ulcerative colitis (UC) and Crohn’s disease (CD), has emerged as a significant health concern with substantial impact on both patients and healthcare systems. The incidence and prevalence of these diseases have increased over the past two to three decades, coinciding with advancements in diagnostic tools, a greater understanding of genetic and environmental factors, and the availability of more effective treatments. These developments have occurred around the turn of the 20th and 21st centuries. Throughout my journey to becoming an IBD specialist, I have learned many valuable lessons that I would like to share.

During my time as a resident, IBD was considered a “Western” disease, and pathologists were often hesitant to make a histologic diagnosis of IBD. At that time, it was extremely rare to diagnose CD, even in National Taiwan University Hospital (NTUH). When a CD case was diagnosed, it was often discussed at a grand round level in the Internal Medicine department. Although Professor Cheng-Yi Wang diagnosed the first IBD case (UC) in 1969, the UC to CD ratio in Taiwan during the 20th century was about 10 to 1. However, this ratio has now decreased to around 3 to 1. According to the catastrophic illness card (CIC) registration data in Taiwan, we currently have at least 8,000 IBD patients, with the incidence increasing threefold and the prevalence increasing eightfold from 2001 to 2020. In reality, we estimate that the actual number of IBD patients is 2 to 3 times higher than what is recorded in the CIC registry.

The rise in the incidence and prevalence of IBD may be related to changes in environmental factors, increased disease awareness, and advancements in diagnostic tools, though genetic factors are not easily altered within just a few decades. Recent studies have shown that serum biomarker panels can change years before an IBD diagnosis is made. This opens the possibility for disease modification or even prevention in high-risk groups. With the introduction of deep and capsule endoscopy around 2000, evaluating the small bowel has become more feasible. MR enterography and intestinal ultrasound also provide more diagnostic opportunities. Fecal calprotectin, a surrogate biomarker for endoscopic severity, became part of our daily practice in the early 21st century. These advancements have greatly improved early diagnosis and monitoring of IBD patients.

Another significant milestone in IBD management has been the development and optimization of advanced therapies. Prior to the 21st century, our treatment options were limited to conventional therapies such as 5-ASA, steroids, and immunomodulators. The introduction of TNF-α antibodies for CD treatment in 1998 opened new possibilities for doctors and patients. Biologics have proven especially effective for patients with complicated CD, significantly increasing both clinical and endoscopic response and remission rates compared to conventional therapies. The optimization of immunomodulators or biologics has made “steroid-sparing clinical remission” an achievable goal in our daily practice. In the past, avascular necrosis of the femoral neck due to long-term steroid use was not uncommon. Therapeutic drug monitoring (TDM), whether used reactively or proactively, has played a crucial role in optimizing treatment. For TNF-α antibodies, TDM during the early treatment phase helps improve the chances of treatment success. Without proper dosage optimization, low trough levels often result in treatment failure. While the appropriate trough levels for anti-integrin and P40/P19 antibodies remain a subject of debate, TDM still offers valuable insights when deciding to shorten treatment intervals or switch to another drug class, and it helps guide discussions with patients.

In addition to biologics, small molecules represent another advancement in treatment options. As oral medications, small molecules offer more convenience for patients, although they remain contraindicated during pregnancy and lactation. It is important to inform patients about the need for birth control when taking small molecules to prevent any unintended outcomes.

In the past, surgery played a major role in managing IBD. While the advancement of medical treatments has reduced the need for surgery, it still remains an important aspect of managing IBD patients today. Indications for surgery include acute severe UC, colitis related dysplasia/cancer, CD-related fistulas, and stenosis that cannot be managed with endoscopy. Our experience has shown that “perioperative optimization” can reduce postoperative morbidity and mortality. Laparoscopic surgery is now more commonly performed compared to laparotomy, and elective surgery is always preferable to emergency surgery.

Looking back, we can appreciate the progress made in the fields of pathogenesis, medicine, surgery, and diagnostics. Looking forward, important challenges remain: how to diagnose and prevent the disease at an even earlier stage, how to successfully implement precision medicine, how to break through the therapeutic ceiling, and how to provide holistic care for our patients. These are critical tasks that lie ahead for us.

References

1. Ulcerative colitis. Kobayashi T, Siegmund B, Le Berre C, Wei SC, Ferrante M, Shen B, Bernstein CN, Danese S, Peyrin-Biroulet L, Hibi T. Nat Rev Dis Primers. 2020 Sep 10;6(1):74.
2. Crohn’s disease. Roda G, Ng SC, Kotze PG, Argollo M, Panaccione R, Spinelli A, Kaser A, Peyrin-Biroulet L, Danese S. Nat Rev Dis Primers. 2020 Apr 2;6(1):22.
3. Wei SC, Shieh MJ, Chang MC, Chang YT, Wang CY, Wong JM. Long-term follow-up of ulcerative colitis in Taiwan. J Chin Med Assoc. 2012 Apr;75(4):151-5.
4. Wei SC, Ni YH, Yang HI, Su YN, Chang MC, Chang YT, Shieh MJ, Wang CY, Wong JM. A Hospital-based Study of Clinical and Genetic features of Crohn’s disease. J Formos Med Assoc. 2011 Sep;110(9):600-6.
5. Lin WC, Wong JM, Tung CC, Lin CP, Chou JW, Wang HW, Shieh MJ, Chang CH, Liu HH, Wei SC*; Taiwan Society of Inflammatory Bowel Disease multicenter study. Fecal calprotectin correlated with endoscopic remission for Asian inflammatory bowel disease patients. World J Gastroenterol. 2015 Dec 28;21(48):13566-73.
6. Lin CC, Wei SC, Lin BR, Tsai WS, Chen JS, Hsu TC, Lin WC, Huang TY, Chao TH, Lin HH, Wong JM, Lin JK. A retrospective analysis of 20-year data of the surgical management of ulcerative colitis patients in Taiwan: a study of Taiwan Society of Inflammatory Bowel Disease. Intest Res. 2016 Jul;14(3):248-57.
7. Yen HH, Weng MT, Tung CC, Wang YT, Chang YT, Chang CH, Shieh MJ, Wong JM, Wei SC*. Epidemiological trend in inflammatory bowel disease in Taiwan from 2001 to 2015: A nationwide population-based study. Intest Res. 2019 Jan;17(1):54-62.
8. Lin WC, Weng MT, Tung CC, Chang YT, Leong YL, Wang YT, Wang HY, Wong JM, Wei SC*. Trends and Risk Factors of Mortality Analysis in Patients with Inflammatory Bowel Disease: A Taiwanese Nationwide Population-Based Study. J Transl Med. 2019 Dec 12;17(1):414.
9. Lin CC, Lin HH, Chen HC, Chen NC, Shih IL, Hung JS, Yueh TC, Chiang FF, Lin PW, Tsai YY, Wei SC*. Perioperative Optimization of Crohn’s Disease. Annals of Gastroenterological Surgery. Ann Gastroenterol Surg. 2022 Oct 13;7(1):10-26.
10. Lin WC, Lin CC, Hsu WH, Chiang FF, Chang CW, Hsu TC, Wu DC , Wang HY, Wong. JM, Wei SC*. Short-term and long-term outcomes of acute severe ulcerative colitis in Taiwan: a multicenter study with pre- and post- biologics comparison. Intest Res. 2025 Jan 24.

Ileoanal pouch for ulcerative colitis: What is the state of play

Mr. Janindra Warusavitarne Consultant Colorectal Surgeon St Mark’s Hospital London, UK

Ileal pouch anal-anastomosis (IPAA) surgery in the management of ulcerative colitis (UC) has improved patient quality of life, despite the challenges proctocolectomy poses.¹

Traditionally, patients with severe UC undergo a three–stage approach:

1) subtotal colectomy and end ileostomy,
2) IPAA with diverting loop ileostomy, and
3) ileostomy closure.¹

In contrast to the two-stage approach, which combines total proctocolectomy, IPAA and diverting loop ileostomy in a single operation, this multi-operational procedure is associated with extended recovery times to reduce complications that can lead to eventual pouch failure.¹

However, research supporting the three-stage approach is limited. A multivariate study revealed that perioperative complications in two-stage procedures were more closely linked with surgeon experience than to other factors such as emergency status or medications.² Furthermore, research has shown that a defunctioning ileostomy is not associated with reduced leakage rates, and even in severe cases, pouch failure rates remain relatively low.³ This suggests a potential overuse of three-stage procedures, which imposes significant patient burden for extended periods of time. Thus, shorter-staged approaches should be considered to achieve similar outcomes whilst improving patient quality of life.

Optimising surgical outcomes with a modified two-stage approach

By applying surgical principles from the traditional three-stage approach in a two-staged process, this modified procedure entails a subtotal colectomy followed by a restorative proctocolectomy 3–6 months later.¹ Furthermore, it avoids the use of a loop ileostomy altogether, which circumvents associated comorbidities and improves recovery from sepsis, immunosuppression and nutritional compromise.¹ Studies have demonstrated that the modified two-stage approach results in significantly lower post-operative complication rates compared to the traditional two-stage procedure (p<0.01),⁴ with no significant differences when compared to the three-stage approach.¹ Surgical practices within the modified two-stage procedure should focus on reducing leak complications through optimal anastomosis techniques, regular monitoring and the consideration of varying levels of surgical expertise.

Addressing pouch-related complications to optimise treatment strategies

Despite advancements in IPAA procedures, pouchitis remains a common issue in patients with UC. Pouchitis presents a broad array of clinical and endoscopic patterns, hindering the administration of effective treatment regimens. Consequently, a classification system was developed in 2022 to improve management strategies and clinical outcomes, placing an emphasis on assessing patients’ levels of inflammation.⁵ Multiple pouchoscopies should be conducted for more accurate diagnosis, particularly in patients with antibiotic resistance and chronically active pouchitis.

Looking forward, the EARNEST trial revealed that vedolizumab significantly improves remission rates following IPAA, highlighting the potential applications of biologics in long-term UC management.⁶ Ongoing research aims to improve patient quality of life, including the impact of diet on pouch performance and fatigue management strategies.⁷ Shifting towards these patient-centric practices during and after surgery is essential to reduce patient burden and maximise long-term outcomes.

References

1. Clement E, et al. Am J Surg 2024;231:96-99
2. Hicks CW, et al. JAMA Surg 2013;148:658
3. Sahami S, et al. J Crohns Colitis 2016;10:779-785
4. Zittan E, et al. J Crohns Colitis 2016;10:766-772
5. Akiyama S, et al. Clin Gastroenterol Hepatol 2022;20:293-302.e9
6. Travis S, et al. N Engl J Med 2023;388:1191-1200
7. Gold S, et al. Inflamm Bowel Dis 2025;31:246-258.

Latest updates on endohepatology

Dr. Raymond Shing-Yan Tang Assistant Professor Department of Medicine and Therapeutics, The Chinese University of Hong Kong Hong Kong

Endohepatology is an emerging field with significant potential for improving the management of chronic liver disease.¹ A growing body of endoscopic ultrasound (EUS)-guided techniques is being developed to address the limitations of current standards of care (SOC) (Figure).^2-5

Figure. Some applications of EUS in endohepatology. A) EUS-guided variceal intervention, B) EUS-guided liver biopsy, C) EUS-guided portal pressure gradient measurement, D) EUS-guided shear-wave elastography.

Images provided by Dr Tang with permission.
EUS, endoscopic ultrasound; FNB, fine-needle biopsy.

EUS-guided variceal intervention is precise and effective^2,6-8

Variceal bleeding is a serious complication of portal hypertension.² Direct EUS-guided variceal interventions allow physicians to ensure the precise delivery of intravariceal therapy, monitor variceal obliteration in real time, and provide injection therapy even when the endoluminal view is obscured.^2,6,7 Common agents in EUS-guided variceal interventions include cyanoacrylate glue, coil, or a combination of both.^2,6,7  The combination approach may be preferable, as studies utilising this method have reported high rates of gastric variceal obliteration and low rates of post-treatment bleeding.^6,8

EUS-guided LB yields better quality specimens³

EUS-guided liver biopsy (LB) has been shown to yield comparable specimen quality than that obtained through both percutaneous and transjugular LB, in terms of both total specimen length and the completeness of the portal triad.³ When selecting needles, fine-needle biopsy (FNB) needles demonstrate better efficacy and safety compared with fine-needle aspiration (FNA) needles.⁹ Additionally, 19-gauge (19G) needles produce less fragmented specimens than 22G needles, while Franseen needles produce longer specimens and more intact cores than fork-tip needles.^10,11 Despite the benefits of EUS-guided LB, physicians should consider the increased costs and procedural duration compared to alternative methods.¹²

EUS-guided PPG measurement is feasible but warrants research^1,4,13

Multiple studies have demonstrated the technical feasibility of EUS-guided portal pressure gradient (PPG) measurement, a valuable parameter for diagnosing and quantifying portal hypertension.^4,13 When using this method, physicians should be careful to avoid intervening varices when performing the needle puncture.¹ Further research is needed to determine the potential effects of deep sedation on PPG measurements and to validate EUS-guided PPG against hepatic venous pressure gradient.¹

EUS-guided shear wave elastography matches VCTE in accuracy⁵

Vibration-controlled transient elastography (VCTE) is commonly used for assessing liver fibrosis but can be unreliable, especially in patients with obesity.⁵ A study comparing VCTE and EUS-guided shear wave elastography indicated that the EUS method is well tolerated and offers comparable accuracy to VCTE for assessing liver fibrosis.⁵

In summary, various EUS-guided techniques are being developed to enhance the management of chronic liver disease.^2-5 However, considerations such as cost, procedural duration and validation compared to SOC should be carefully evaluated before implementing these methods.^1,12

Reference

1. Laleman W, et al. Best Pract Res Clin Gastroenterol 2022;60-61:101811.
2. Fujii-Lau LL, et al. Surg Endosc 2016;30:1396-1404.
3. Pineda JJ, et al. Gastrointest Endosc 2016;83:360-365.
4. Samarasena JB, et al. VideoGIE 2018;3:361-363.
5. Kohli DR, et al. Gastrointest Endosc 2023;97:35-41.e1.
6. Binmoeller KF, et al. Gastrointest Endosc 2011;74:1019-1025.
7. Tang RS, et al. Gastrointest Endosc 2016;83:1032-1033.
8. Bhat YM, et al. Gastrointest Endosc 2016;83:1164-1172.
9. Mohan BP, et al. Gastrointest Endosc 2019;89:238-246.e3.
10. Diehl DL, et al. Gastrointest Endosc 2024;99:931-937.
11. Aggarwal SN, et al. Gastrointest Endosc 2021;93:1133-1138.
12. Bang JY, et al. Gut 2021;70:2224-2226.
13. Choi AY, et al. J Gastroenterol Hepatol 2022;37:1373-1379.
14. Laleman W, et al. J Hepatol 2024;80:124-139.

Prevalence of gastric intestinal metaplasia
(Summary of thesis 2024)

Dr. Anthony Chun-Ling Lau Department of Medicine and Geriatrics United Christian Hospital Hong Kong

Introduction

Gastric cancer ranks sixth in both incidence and mortality in Hong Kong, accounting for 3% of new cancer cases and 4% of cancer deaths. The median age of diagnosis and death is 71 and 74, respectively. The survival rate remains low, with a 5-year relative survival rate of 35.7% in the United States. Early gastric cancer is often asymptomatic; thus, less than one-third of cases are diagnosed early. The 5-year survival rates for localized, regional, and metastatic gastric cancer are 74.7%, 34.6%, and 6.6%, respectively.¹ Japan has a significantly better overall survival rate, attributed to a higher proportion of localized disease at diagnosis due to a robust screening program.

To improve early detection and survival rates, awareness of gastric intestinal metaplasia (GIM) is rising. GIM is a known risk factor for gastric cancer, particularly non-cardia gastric cancer. Evidence suggests GIM is linked to future gastric cancer development.² Countries like Japan and South Korea, with high gastric cancer incidence, have implemented population-based screening programs for over 20 years, leading to increased early diagnoses and survival rates.³

Conversely, in Hong Kong, GIM is detected opportunistically, with no established screening guidelines. A retrospective study found local GIM prevalence at 13.9% in H. pylori-positive and 5.9% in negative patients.⁴ This study aims to evaluate GIM prevalence and distribution in a local population undergoing gastroscopy, providing insight for health policy amendments. We will also identify risk factors associated with GIM to inform preventive and surveillance strategies.

Methodology

This prospective cross-sectional study was conducted in a secondary referral center in Hong Kong.

Sample Size Calculation

Sample size was estimated using a formula for cross-sectional studies. The estimated GIM prevalence in Hong Kong is 30%, based on studies from Singaporean Chinese, Japan, and Korea. The assumption included a 5% type I error chance and a precision of 0.06, resulting in a required sample size of 224.

Patient Selection

Patients undergoing upper gastrointestinal endoscopy from September to December 2023 at the United Christian Hospital were enrolled. Inclusion criteria included both inpatients and outpatients referred for elective gastroscopy. Exclusion criteria encompassed a history of gastrectomy, active gastrointestinal bleeding, prior gastric dysplasia or cancer, and high bleeding risk conditions such as on dual antiplatelet therapy, anticoagulant, end stage renal failure and Childs C cirrhosis.

Written informed consent was obtained, and 233 patients were recruited. Six were excluded due to intolerance or need for endoscopic hemostasis due to alternative pathologies, resulting in 226 participants.

The study was approved by the research ethics committee of the Hospital Authority of Hong Kong.

Clinical Characteristics

Demographic data were collected during recruitment interviews and through the Clinical Management System.

Endoscopy

Endoscopies were performed by gastroenterology fellows, following the Sydney protocol for gastric mapping, which included biopsies from gastric antrum, incisura and body. Samples were fixed in buffered 10% formalin.

Histologic Assessment

Specimens were processed, embedded, and stained using H&E stain. Modified Giemsa stain was utilized if H. pylori status was suspicious. Histological findings were recorded according to the updated Sydney System, grading GIM and H. pylori colonization by visual analog scale.

Evaluation of GIM

Extensive GIM was defined as GIM present in both the antrum and body, while focal GIM was defined as GIM in either location.

Statistical Analysis

Pearson’s chi-square test analyzed the association between GIM and categorical variables. The association with age was analyzed using the Student’s t-test. Logistic regression was performed, expressing results as odds ratios (OR) with 95% confidence intervals (CI). Statistical significance was set at 5%.

Results

Baseline Characteristics of Participants

Table 1 summarizes the baseline characteristics of the participants. The mean age of participants was 64.13 ± 12.83. Only 5 (2.2%) had a first-degree family history of gastric cancer. Table 2 summarizes the indications of gastroscopy. The most common endoscopy indications were epigastric pain (24.3%), anemia (19.5%), and acid reflux (14.6%).

Table 1.  Baseline characteristics of the 226 subjects

S.D., standard deviation

Table 2. Indications for endoscopy

*Others include: Vitamin B12 deficiency, follow-up for Barrett’s esophagus, weight loss, follow-up for duodenal polyp, vomiting, dysphagia, globus sensation.

Prevalence of Gastric Intestinal Metaplasia

GIM was found in 78 (34.5%) of participants, with an equal gender distribution. Active H. pylori infection was identified in 36 (15.9%) participants.

Table 3 summarizes the distribution of GIM.

Table 3. Patterns of GIM distribution

Univariate and Logistic Regression Analysis

Significant differences in GIM prevalence were found based on gender (p=0.018), smoking history (p=0.025), active H. pylori status (p=0.012), and BMI (p=0.043). Age was associated with GIM (p<0.001). Logistic regression identified older age (OR 1.045; 95% CI 1.017–1.075; p=0.002) and active H. pylori (OR 2.787; 95% CI 1.275–6.090; p=0.010) as significant independent risk factors.

Discussion

This study found a GIM prevalence of 34.5% among patients referred for gastroscopy, aligning with global prevalence rates.^5-7 H. pylori infection (OR 2.787; 95% CI 1.275–6.090; p=0.010) and older age (OR 1.045; 95% CI 1.017–1.075; p=0.002) were independently associated with GIM. While local consensus recommends against population screening of H. pylori due to declining local gastric cancer incidence, a “Test and Treat” strategy is suggested for asymptomatic high-risk individuals, such as those with a family history of gastric cancer.⁸

Our study had identified 14 (6.2%) and 2 (0.88%) patients who require further surveillance due to extensive GIM and focal GIM with family history of gastric cancer respectively, in accordance with the European guideline.⁹ Further cost-effectiveness analysis will be necessary to determine if a population screening strategy is worthwhile in Hong Kong. Systematic review suggested that endoscopic screening in high gastric cancer incidence countries, like Japan and South Korea, was cost-effective while in low to moderate incidence countries, a targeted screening of high-risk populations was more cost-effective.¹⁰

Our findings indicate the necessity for awareness and management of GIM due to its prevalence and potential progression to gastric malignancy. A targeted approach for high-risk populations in Hong Kong is likely more appropriate than broad population screening.

Limitations

This study’s participant selection may limit the generalizability of findings, as it only includes symptomatic patients. Exclusion of high-bleeding risk individuals further skews the data. Additionally, there may be interobserver variability in histological assessments.

Conclusion

The 34.5% GIM prevalence suggests it is common in Hong Kong, with older age and active H. pylori status identified as significant risk factors. These insights can guide local authorities in developing strategies to address GIM and gastric cancer. Future research should evaluate histological subtyping of GIM and cost-effectiveness of surveillance strategies.

Reference

1. Surveillance Research Program, National Cancer Institute. (2023). SEERExplorer: An interactive website for SEER cancer statistics*. Available from: https://seer.cancer.gov/statistics-network/explorer/. Data source: SEER Incidence Data, November 2022 Submission.
2. Choi, A. Y., Strate, L. L., Fix, M. C., Schmidt, R. A., Ende, A. R., Yeh, M. M., Inadomi, J. M., & Hwang, J. H. (2018). Association of gastric intestinal metaplasia and East Asian ethnicity with the risk of gastric adenocarcinoma in a U.S. population. Gastrointestinal Endoscopy, 87(4), 1023-1028.
3. Choi, K. S., Jun, J. K., Suh, M., Park, B., Noh, D. K., Song, S. H., Jung, K. W., Lee, H. Y., Choi, I. J., & Park, E. C. (2015). Effect of endoscopy screening on stage at gastric cancer diagnosis: Results of the National Cancer Screening Programme in Korea. British Journal of Cancer, 112(3), 608-612.
4. Yee, Y. K., Wong, K. W., Hui, C. K., Chan, C. K., Chan, A. O. O., Lam, S. K., Fung, F. M. Y., Hung, I., & Wong, B. C. Y. (2009). Prevalence and time trend of intestinal metaplasia in Hong Kong. Journal of Gastroenterology and Hepatology, 24, 896-899.
5. Asaka, M., Sugiyama, T., Nobuta, A., Kato, M., Takeda, H., & Graham, D. Y. (2001). Atrophic gastritis and intestinal metaplasia in Japan: Results of a large multicenter study. Helicobacter, 6(4), 294-299.
6. Kim, N., Park, Y. S., Cho, S. I., Lee, H. S., Choe, G., Kim, I. W., Won, Y. D., Park, J. H., Kim, J. S., Jung, H. C., & Song, I. S. (2008). Prevalence and risk factors of atrophic gastritis and intestinal metaplasia in a Korean population without significant gastroduodenal disease. Helicobacter, 13(4), 245-255.
7. Eriksson, N. K., Kärkkäinen, P. A., Färkkilä, M. A., & Arkkila, P. E. (2008). Prevalence and distribution of gastric intestinal metaplasia and its subtypes. Digestive and Liver Disease, 40(5), 355-360.
8. Pimentel-Nunes, P., Libânio, D., Marcos-Pinto, R., Areia, M., Leja, M., Esposito, G., Garrido, M., Kikuste, I., Megraud, F., Matysiak-Budnik, T., Annibale, B., Dumonceau, J. M., Barros, R., Fléjou, J. F., Carneiro, F., van Hooft, J. E., Kuipers, E. J., & Dinis-Ribeiro, M. (2019). Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): Guideline update 2019. Endoscopy, 51(4), 365-388.
9. Leung, W. K., Cheung, K. S., Sham, P. C. O., Tang, R. S. Y., Loo, C. K., Hsu, A. S. J., Cheung, T. K., Lam, L. Y., Chiu, B. C. F., & Wu, J. C. Y. (2023). Consensus recommendations for the screening, diagnosis, and management of Helicobacter pylori infection in Hong Kong. Hong Kong Medical Journal, 29(6), 532-541.
10. Canakis, A., Pani, E., Saumoy, M., & Shah, S. C. (2020). Decision model analyses of upper endoscopy for gastric cancer screening and preneoplasia surveillance: A systematic review. Therapeutic Advances in Gastroenterology, 13, 1756284820941662.

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