Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
Citation:
Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
Citation:
Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
Objective This study aimed to estimate the incidence rate and clinical characteristics of inflammatory bowel disease (IBD) in the Chinese population, specially comparing the North and South regions.Methods We designed a questionnaire survey for patients diagnosed with IBD and conducted a systematic literature search in PubMed, China National Knowledge Internet, and Wanfang digital database, covering studies published between 2012 and 2022. Meta-analysis was performed to determine the overall incidence rate and prevalence of clinical manifestations of Crohn's disease (CD) and ulcerative colitis (UC) in mainland China. Clinical phenotypes and demographic characteristics were calculated with 95% confidence intervals (CI). A comparison between the northern and southern regions was also conducted.Results The questionnaire survey included 440 patients, and 64 publications were included for Meta-analysis. The overall incidence rates of IBD, CD, and UC were 1.36 (95% CI: 0.79-2.33) per 100,000 person-years, 0.23 (95% CI: 0.09-0.58) per 100,000 person-years, and 1.12 (95% CI: 0.69-1.80) per 100,000 person-years, respectively. The incidence rates of IBD, CD, and UC were all higher in southern China compared to the North. Clinical characteristics of 440 IBD patients from the questionnaire and 2,821 CD patients and 12,809 UC patients from the literature were analyzed. There were more male patients compared to female patients. CD cases in the North exhibited earlier disease diagnosis (P < 0.01), more upper gastrointestinal lesions (P < 0.01), and higher hospitalizations rates (P < 0.01) compared to the South. UC cases in the North had higher severity (P < 0.01), anemia rates (P < 0.01), and weight loss (P < 0.01) compared to the South.Conclusions The incidence rates of IBD, CD, and UC were higher in southern China than in the North. Northern patients exhibited more severe symptoms compared to their southern counterparts.
Inflammatory bowel disease (IBD) encompasses two distinct disorders, Crohn's disease (CD) and ulcerative colitis (UC), exhibiting variations in pathophysiology, affected gastrointestinal (GI) tract regions, symptoms, complications, disease progression, and management[1-2]. While the global incidence of IBD is generally increasing, European and North American countries show a stabilizing trend, whereas newly industrialized countries in Africa, Asia, and South America experience accelerated incidence[3]. IBD imposes a substantial economic burden worldwide due to its high incidence, prevalence, and complex phenotype, leading to recurrent episodes, persistent symptoms, frequent hospitalizations, and enormous medical costs[4]. Furthermore, IBD manifests with ethnically and regionally specific clinical features, with notable differences reported between Chinese and Caucasian patients[5-6].
Given China's status as the world's most populous country with the third largest land area, significant genetic, climatic, dietary, cultural, industrial, and urbanization differences exist between its northern and southern regions. Consequently, we hypothesize substantial disparities in the incidence and clinical features of IBD. An Asia-Pacific study has reported a rapid increase in incidence in China[7]. The Chinese Center for Disease Control and Prevention estimates that the total number of IBD cases in China will reach 1.5 million by 2025[4]. Although some studies have examined the epidemiology of specific regions in China[8-11], national representation remains limited. Numerous clinical studies have been conducted in China; however, they primarily consist of single-center investigations with small sample sizes. To fully understand the phenotypic characteristics of IBD in northern and southern China and provide targeted treatment for IBD patients, we conducted a nationwide questionnaire survey and meta-analysis to estimate the incidence rate and clinical characteristics of IBD in mainland China, with a specific focus on comparing the North and the South.
2.
Materials and methods
2.1
Data sources and patient selection
We conducted a retrospective multicenter analysis, gathering data from patients with IBD who voluntarily participated in an electronic questionnaire administered between September 15,2020 and October 8,2020. All participants had a confirmed diagnosis of IBD and received relevant treatment with long-term follow-up. Collected information encompassed demographic and clinical characteristics, including gender, IBD type, age at diagnosis, education, smoking history, annual hospitalization rate, clinical manifestations, extraintestinal manifestations, and complications (see Supplementary Table 1).
Table
1.
The phenotypic and clinical characteristics of inflammatory bowel disease from the questionnaire (N = 440).
Inclusion criteria: (1) Diagnosis of IBD based on current diagnostic criteria; (2) Volunteered participation of all individuals included in this study; (3) Participants or their families possessed the ability to comprehend and complete the questionnaire.
Exclusion criteria: (1) Difficulties understanding Chinese, intellectual disability, or dementia; (2) Presence of neurological diseases, metabolic encephalopathy, hypoxia, intracranial injury or trauma, cerebrovascular accident, brain tumor, infection, or epilepsy; (3) Conditions related to poisoning, drug addiction, or alcohol abuse; (4) Severe heart, lung, kidney or rheumatic disease.
2.2
Literature search strategy
We conducted searches on PubMed, China National Knowledge Internet, and Wanfang digital database to identify relevant studies published from 2012 to 2022 by using the search terms related to inflammatory bowel disease (Supplementary Table 2).
Table
2.
The phenotypic and clinical characteristics of Crohn's disease from the questionnaire (N = 224).
Inclusion criteria: (1) Literature was focusing on IBD, CD, or UC originating from China was examined; (2) Original data of the cases under study were accessible through the original text or corresponding authors; (3) Non-duplicated literature from the same institution was included.
Exclusion criteria: (1) Duplicated literature, incomplete or insufficient data, limited case numbers, and unverifiable cases were excluded; (2) Reviews, systematic evaluations, reviews, letters, translations, drug trials, and basic studies were not considered.
2.4
Literature screening and data extraction
Two review authors independently screened and extracted data from studies based on predefined inclusion and exclusion criteria. In cases of discrepancies, a third investigator reviewed the findings and resolved any differences through discussion. The extracted data included: (1) comprehensive details: first author, publication year, study location, and data source; (2) epidemiology aspects: sample size, case numbers, and incidence rates; (3) Clinical characteristics: male-to-female ratio, age at IBD diagnosis, clinical manifestations, complications, extraintestinal manifestations, lesion extent, severity, and disease behavior.
2.5
Statistical analysis
The data were geographically divided into southern and northern groups based on the natural Qinling-Huaihe region[12]. The north included Shanxi and Henan Provinces, while Jiangsu Province was classified as the south. Descriptive analysis was conducted using SPSS16 software. Meta-analysis was performed using STATA16 software to estimate the crude incidence rate (per 100,000 person-years) and the proportion of clinical presentation components, along with 95% confidence intervals (95% CI), employing random-effects or fixed-effect models to account for heterogeneity between studies. Heterogeneity was assessed using Q test and I2 statistic. In case of high heterogeneity (P < 0.10 or I2 > 75%), random-effect models were used for the meta-analysis; otherwise, a fixed-effect model was applied[13]. Categorical variables were compared using Chi-square test, considering P < 0.05 as statistically significant. Geographic maps were generated by ArcGIS 10.8 software.
3.
Results
3.1
Description of the questionnaire and publications
This study included 440 patients with IBD, comprising 224 CD patients and 216 UC. Data on age at diagnosis and location are enumeration data. Participants chose between three ages when completing the questionnaire and did not fill in a specific age. We used the chi-square test to compare the data between the North and South. Table 1 provides a summary of their demographic characteristics. A total of 64 Chinese publications and 6 English publications were analyzed, encompassing 2821 CD cases and 12809 UC cases (Fig. 1). The publications exhibited high homogeneity, justifying the use of a random-effects model for meta-analysis. Incidence rates of IBD were reported in five publications[7-11]. Clinical characteristics of CD and UC were documented in 27 and 52 publications, respectively. Fig. 2 displays the specific number of CD and UC cases reported in each province.
Figure
1.
PRISMA flow diagram for literature review.
3.2
The incidence rate of IBD is higher in the South than in the North
We used meta-analysis to summarize the incidence rates of IBD.
The pooled incidence rate of IBD in mainland China was 1.36 (95% CI: 0.79-2.33) per 100,000 person-years. In the northern region, the incidence rate was 1.03 (95% CI: 0.29-3.75) per 100,000 person-years, while in the southern region, it was 1.58 (95% CI: 0.92-2.72) per 100,000 person-years.
For UC, the total incidence rate was 1.12 (95% CI: 0.69-1.80) per 100,000 person-years, with 0.93 (95% CI: 0.24-3.57) per 100,000 person-years in the North and 1.28 (95% CI: 0.82-1.98) per 100,000 person-years in the South.
The total incidence rate of CD was 0.23 (95% CI: 0.09-0.58) per 100,000 person-years. In the North, it was significantly lower at 0.09 (95% CI: 0.04-0.20) per 100,000 person-years, compared to 0.34 (95% CI: 0.13-0.90) per 100,000 person-years in the South.
3.3
IBD patients in the North are severer than in the South
3.3.1
Patients Characteristics of CD
3.3.1.1
Information from the questionnaire
In our questionnaire, we enrolled 224 patients with CD (Table 2). Male patients account for 67.86% of the total, nearly double the proportion of female patients (32.14%). In the North, a higher percentage of patients were diagnosed at the age of 16 years or younger compared to the South (30.51% in the North; 11.52% in the South; P < 0.01). Conversely, fewer patients in the North were diagnosed between 17-40 years of age compared to the South (54.24% in the South; 77.58% in the North; P < 0.01). The number of hospitalizations was significantly higher in the North than in the South (P < 0.05). The predominant clinical symptoms observed in Chinese CD patients were diarrhea (68.75%) and abdominal pain (29.02%).
3.3.1.2
Information from publications
A total of 27 publications examined the clinical characteristics of CD patients (Table 3). The male-to-female ratio was 1.67:1. Regarding the location of disease lesions, 11% of CD patients in the North experienced involvement of the upper GI, which was significantly higher than the 4% observed in the South. The pooled predominant clinical symptoms were abdominal pain (79%; 95% CI: 65%-94%), diarrhoea (58%; 95% CI: 46%-71%), weight loss (45%; 95% CI: 38%-52%), and fever (29%; 95% CI: 23%-36%). The overall prevalence of extra-intestinal manifestations and complications was 23% (95% CI: 18%-29%) and 33% (95% CI: 23%-44%), respectively.
Table
3.
The phenotypic and clinical characteristics of Crohn's disease from publications.
In our questionnaire, we included 216 UC patients (Table 4). The male-to-female ratio was 1∶1. The primary clinical symptoms reported were bloody stools (84.72%), mucus stools (81.48%), diarrhoea (75.93%), and abdominal pain (61.11%). Notably, the prevalence of weight loss was significantly greater in the North (57.65%) compared to the South (33.59%). Furthermore, the prevalence of anemia was also significantly higher in the North (43.53%) than in the South (22.90%).
Table
4.
The phenotypic and clinical characteristics of ulcerative colitis from the questionnaire.
A total of 52 publications reported the clinical characteristics of patients with UC (Table 5). The male-to-female ratio was 1.22:1. The predominant clinical symptoms observed were mucus or bloody stool (74%; 95% CI: 68%-80%), diarrhoea (72%; 95% CI: 66%-78%), and abdominal pain (61%; 95% CI: 54%-67%).
Table
5.
The phenotypic and clinical characteristics of ulcerative colitis from publications.
Consistent with the questionnaire results (Fig. 3), a higher proportion of patients experienced weight loss in the North (36% in the North; 24% in the South; P < 0.05), and a higher prevalence of anemia was also observed in the North (39% in the North; 24% in the South; P < 0.05). The overall prevalence of extra-intestinal manifestations and complications was 10% (95% CI: 6%-12%) and 10% (95% CI: 8%-11%), respectively.
Figure
3.
The prevalence of anemia and weight loss. *P < 0.05.
In this study, we investigated the incidence rate and clinical characteristics of IBD in mainland China, with a focus on the differences between the North and South regions. Our findings revealed a higher incidence of IBD in the South compared to the North. Regarding patients with CD, the majority were diagnosed between the ages of 17 and 40, with a younger age observed in the North; CD patients in the northern region exhibited a higher prevalence of upper GI lesions and a higher rate of hospitalizations compared to those in the South. On the other hand, patients with UC in the North experienced a later disease diagnosis, fewer extra-intestinal manifestations, and higher rates of anemia and weight loss compared to those in the South.
Our study demonstrated a higher proportion of male patients with both CD and UC in China, which contrasts with the predominance of women in Western countries[14-15] but aligns with findings from other Asian patients[16-17]. The UC to CD ratio was significantly higher in the North (7.33 ∶ 1) compared to the South (2.03 ∶ 1). A Pooled analysis of the publications indicated an incidence rate of IBD in mainland China of 1.36 (95% CI: 0.79-2.33) per 100,000 person-years, which was significantly lower than rates reported in Europe, North American[18-19], and some Asian countries[11]. The incidence rate of IBD, CD, and UC were higher in southern China than in the northern regions, with statistically significant differences observed in CD (P < 0.01). Similar regional differences in incidence rates have been observed in European countries, and studies have suggested a faster rate of increase in CD compared to UC in Asia[20-23].
The southern regions of mainland China exhibited a more Westernized lifestyle, including diet, urbanization, and overall development, compared to the North. Urbanization has been associated with an increased risk of UC and CD, particularly CD[24]. Additionally, a Western-style diet has been considered a risk factor for IBD[25-26]. The northern region experiences a warm temperate semi-humid climate with severe winters, while the southern region has a humid subtropical climate with abundant rainfall. Moreover, the more advanced medical infrastructure in the South yields more comprehensive disease screening capabilities, which may contribute to the observed differences in incidence rates between the North and South in China.
Regarding the demographic and clinical characteristics of CD patients, the majority were diagnosed at the ages of 17-40 years, with a younger age at diagnosis in the North. Patients from the South generally had higher educational qualifications, likely reflecting the overall level of education in that region. Interestingly, smoking, which is considered an independent risk factor for CD[27], was not prevalent among the majority of Chinese patients. Disease location data from publications indicated that 48% of Chinese CD patients had lesions in the ileocolon, with only 5% involving the upper GI. In contrast, Western population demonstrated a more even distribution of disease locations, with 1-6% of patients presenting with upper GI involvement[28]. Significantly more patients with upper GI lesions were observed in the North (11%) than in the South (4%), indicating a higher disease severity in the northern region[29-31]. Disease behavior analysis showed that 57% of Chinese CD patients had stricturing or penetrating disease, which is much higher than the rate of 13-35% in European patients[32]. The number of hospitalizations was significantly higher in the North than in the South, probably due to more advanced medical facilities and a shift towards outpatient management in the South. Clinical symptoms, including abdominal pain, diarrhea, fever, and weight loss, were consistent across both regions.
In terms of the demographic and clinical characteristics of UC patients, Chinese patients had later disease diagnoses, with a peak age of 17-40 years, consistent with previous studies[33]. Left hemicolonic lesions were more common, and the majority of patients had never smoked. The severity of UC patients appeared to be more severe than in developed countries, with a higher prevalence of moderate severity in the North and mild severity in the South[34]. The main symptoms reported were mucus or bloody stool, abdominal pain, and diarrhea. The prevalence of anemia in China was higher than Europe[35], and lower than 36.3% in Korea[36]. Both questionnaire and literature data showed significantly higher prevalence of anemia and weight loss in patients in the North than in the South. Moderate disease activity was identified as an independent risk factor for anemia development in patients with IBD[37]. Patients with moderate or severe disease may suffer from dietary restriction due to worsening clinical symptoms or deficiencies in essential nutrients, including iron, folic acid, and vitamin B12, resulting from mucosal disorders and malabsorption. The prevalence of extraintestinal manifestations in Chinese UC patients was lower compared to Swiss[38] and Spain[39].
5.
Conclusions
In conclusion, our study provides insights into the incidence rate and clinical characteristics of IBD in mainland China, highlighting regional differences between the North and South. These disparities may be influenced by various factors, including lifestyle, climate, and medical infrastructure. Understanding these differences is crucial for developing tailored approaches to the management and treatment of IBD in different regions of China. By recognizing and addressing these regional nuances, healthcare policy makers and providers can better serve the needs of IBD patients across the country.
Acknowledgments:
We would like to thank the authors of the included studies for publishing their data for secondary analysis.
Roda G, Chien Ng S, Kotze P G, et al. Crohn's disease. Nat Rev Dis Primers, 2020; 6(1): 22. doi: 10.1038/s41572-020-0156-2
[2]
Ungaro R, Mehandru S, Allen P B, et al. Ulcerative colitis. Lancet, 2017; 389(10080): 1756-1770. doi: 10.1016/S0140-6736(16)32126-2
[3]
Ng S C, Shi H Y, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet, 2017; 390(10114): 2769-2778. doi: 10.1016/S0140-6736(17)32448-0
[4]
Kaplan G G. The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol, 2015; 12(12): 720-727. doi: 10.1038/nrgastro.2015.150
[5]
Clinical characteristics and treatment of inflammatory bowel disease: a comparison of Eastern and Western perspectives - PubMed[EB/OL]. /2023-03-25. https://pubmed.ncbi.nlm.nih.gov/25206259/.
[6]
The differences between American and Chinese patients with Crohn's disease - PubMed[EB/OL]. /2023-03-25. https://pubmed.ncbi.nlm.nih.gov/19878519/.
[7]
Ng S C, Kaplan G G, Tang W, et al. Population density and risk of inflammatory bowel disease: a prospective population-based study in 13 countries or regions in Asia-Pacific. Am J Gastroenterol, 2019; 114(1): 107-115. doi: 10.1038/s41395-018-0233-2
[8]
Zhao J, Ng S C, Lei Y, et al. First prospective, population-based inflammatory bowel disease incidence study in mainland of China: the emergence of "western" disease. Inflamm Bowel Dis, 2013; 19(9): 1839-1845. doi: 10.1097/MIB.0b013e31828a6551
[9]
Zeng Z, Zhu Z, Yang Y, et al. Incidence and clinical characteristics of inflammatory bowel disease in a developed region of Guangdong Province, China: A prospective population-based study: incidence of inflammatory bowel disease. J Gastroenterol Hepatol, 2013; 28(7): 1148-1153. doi: 10.1111/jgh.12164
[10]
Yang H, Li Y, Wu W, et al. The incidence of inflammatory bowel disease in northern China: a prospective population-based study. PLoS ONE, 2014; 9(7): e101296. doi: 10.1371/journal.pone.0101296
[11]
Ng S C, Tang W, Ching J Y, et al. Incidence and phenotype of inflammatory bowel disease based on results from the Asia-pacific Crohn's and colitis epidemiology study. Gastroenterology, 2013; 145(1): 158-165. e2. doi: 10.1053/j.gastro.2013.04.007
[12]
Baiping Zhang. Ten scientific issues in the study of north-south transition zone in China. Advances in Geographical Sciences, 2019; 38(3): 305-311.
[13]
Borenstein M, Hedges L V, Higgins J P T, et al. A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods, 2010; 1(2): 97-111. doi: 10.1002/jrsm.12
[14]
Kaplan G G, Ng S C. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology, 2017; 152(2): 313-321. e2. doi: 10.1053/j.gastro.2016.10.020
[15]
Goodman W A, Erkkila I P, Pizarro T T. Sex matters: impact on pathogenesis, presentation and treatment of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol, 2020; 17(12): 740-754. doi: 10.1038/s41575-020-0354-0
[16]
Park S-K, Wong Z, Park S H, et al. Extraintestinal manifestation of inflammatory bowel disease in Asian patients: A multinational study. Dig Liver Dis, 2021; 53(2): 196-201. doi: 10.1016/j.dld.2020.06.046
[17]
Park S H, Kim Y-J, Rhee K H, et al. A 30-year trend analysis in the epidemiology of inflammatory bowel disease in the Songpa-Kangdong District of Seoul, Korea in 1986-2015. J Crohns Colitis, 2019; 13(11): 1410-1417. doi: 10.1093/ecco-jcc/jjz081
[18]
Nguyen G C, Chong C A, Chong R Y. National estimates of the burden of inflammatory bowel disease among racial and ethnic groups in the United States. J Crohns Colitis, 2014; 8(4): 288-295. doi: 10.1016/j.crohns.2013.09.001
[19]
Zhao M, Gönczi L, Lakatos P L, et al. The burden of inflammatory bowel disease in europe in 2020. J Crohns Colitis, 2021; 15(9): 1573-1587.
[20]
Jones G R, Lyons M, Plevris N, et al. IBD prevalence in Lothian, Scotland, derived by capture-recapture methodology. Gut, 2019; 68(11): 1953-1960. doi: 10.1136/gutjnl-2019-318936
[21]
Nerich V, Monnet E, Weill A, et al. Fine-scale geographic variations of inflammatory bowel disease in France: correlation with socioeconomic and house equipment variables. Inflamm Bowel Dis, 2010; 16(5): 813-821. doi: 10.1002/ibd.21122
[22]
Nerich V, Monnet E, Etienne A, et al. Geographical variations of inflammatory bowel disease in France: a study based on national health insurance data. Inflamm Bowel Dis, 2006; 12(3): 218-226. doi: 10.1097/01.MIB.0000206540.38834.8c
[23]
Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut, 1996; 39(5): 690-697. doi: 10.1136/gut.39.5.690
[24]
Soon I S, Molodecky N A, Rabi D M, et al. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC gastroenterol, 2012; 12: 51. doi: 10.1186/1471-230X-12-51
[25]
Prideaux L, Kamm M A, De Cruz P P, et al. Inflammatory bowel disease in Asia: a systematic review. J Gastroenterol Hepatol, 2012; 27(8): 1266-1280. doi: 10.1111/j.1440-1746.2012.07150.x
[26]
Myles I A. Fast food fever: reviewing the impacts of the Western diet on immunity. Nutr J, 2014; 13: 61. doi: 10.1186/1475-2891-13-61
[27]
Cabré E, Domènech E. Impact of environmental and dietary factors on the course of inflammatory bowel disease. World J Gastroenterol, 2012; 18(29): 3814-3822. doi: 10.3748/wjg.v18.i29.3814
[28]
Mak W Y, Zhao M, Ng S C, et al. The epidemiology of inflammatory bowel disease: East meets west. J Gastroenterol Hepatol, 2020; 35(3): 380-389. doi: 10.1111/jgh.14872
[29]
Crohn's disease of esophagus, stomach and duodenum - PubMed[EB/OL]. /2023-03-26. https://pubmed.ncbi.nlm.nih.gov/30891327/.
[30]
Oral and upper gastrointestinal Crohn's disease - PubMed[EB/OL]. /2023-03-26. https://pubmed.ncbi.nlm.nih.gov/28708248/.
[31]
Sun X W, Wei J, Yang Z, et al. Clinical Features and Prognosis of Crohn's Disease with Upper Gastrointestinal Tract Phenotype in Chinese Patients. Dig Dis Sci, 2019; 64(11): 3291-3299. doi: 10.1007/s10620-019-05651-1
[32]
Zhao M, Gönczi L, Lakatos P L, et al. The Burden of Inflammatory Bowel Disease in Europe in 2020. J Crohns Colitis, 2021; 15(9): 1573-1587. doi: 10.1093/ecco-jcc/jjab029
[33]
Wang Y, Ouyang Q, APDW 2004 Chinese IBD working group. Ulcerative colitis in China: retrospective analysis of 3100 hospitalized patients. J Gastroenterol Hepatol, 2007; 22(9): 1450-1455. doi: 10.1111/j.1440-1746.2007.04873.x
[34]
Wang Y F, Zhang H, Ouyang Q. Clinical manifestations of inflammatory bowel disease: East and West differences. J Dig Dis, 2007; 8(3): 121-127. doi: 10.1111/j.1443-9573.2007.00296.x
[35]
Filmann N, Rey J, Schneeweiss S, et al. Prevalence of Anemia in Inflammatory Bowel Diseases in European Countries: A Systematic Review and Individual Patient Data Meta-analysis. Inflamm Bowel Dis, 2014; 20(5): 936-945. doi: 10.1097/01.MIB.0000442728.74340.fd
[36]
Ds L, Kb B, Jy K, et al. The prevalence and clinical characteristics of anemia in Korean patients with inflammatory bowel disease. Intest Res, 2016; 14(1): 43-49. doi: 10.5217/ir.2016.14.1.43
[37]
Antunes C V de A, Hallack Neto A E, Nascimento C R de A, et al. Anemia in inflammatory bowel disease outpatients: prevalence, risk factors, and etiology. Biomed Res Int, 2015; 2015: 728925. doi: 10.1155/2015/728925
[38]
Vavricka S R, Rogler G, Gantenbein C, et al. Chronological order of appearance of extraintestinal manifestations relative to the time of IBD diagnosis in the swiss inflammatory bowel disease cohort. Inflamm Bowel Dis, 2015; 21(8): 1794-1800. doi: 10.1097/MIB.0000000000000429
[39]
Marin-Jimenez I, Bastida G, Forés A, et al. Impact of comorbidities on anti-TNFα response and relapse in patients with inflammatory bowel disease: the VERNE study. BMJ open gastroenterol, 2020; 7(1): e000351. doi: 10.1136/bmjgast-2019-000351
He, T., Song, L.-Q., Weng, X.-Y. et al. Clinical relevance of inflammatory markers in the evaluation of severity of ulcerative colitis: A retrospective study. Open Life Sciences, 2025, 20(1): 20251088.
2.
Di, Y., Li, H., Yang, J. et al. PPARγ/NF-κB axis contributes to cold-induced resolution of experimental colitis and preservation of intestinal barrier. Biochimica et Biophysica Acta - Molecular Basis of Disease, 2024, 1870(7): 167326.
Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
Qi Liang, Bo Qu, Chunye Li, Yue Hu, Chunyi Yang, Tingting Yang, Yuzhu Di, Hui Li. Clinical characteristics and north-south differences of inflammatory bowel disease in China: A cross-sectional study and meta-analysis[J]. Frigid Zone Medicine, 2024, 4(1): 23-30. doi: 10.2478/fzm-2024-0003
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