Gastrin and colorectal cancer: A prospective study
Open accessAbstract
BACKGROUND & AIMS: Gastrin is a putative promoter of colorectal carcinomas. The aim of this study was to evaluate the temporal relationship between gastrinemia and development of colorectal malignancy. METHODS: We conducted a nested case-control study among 128,992 subscribers to a health maintenance program who had participated in a multiphasic health checkup between 1964 and 1969. Serum had been frozen since the checkup and the cohort followed up for cancer. Of 1881 incident colorectal carcinoma cases, 250 were randomly selected; 1 control without cancer was matched to each case by age, sex, education, and date of serum collection. Stored sera were tested for Helicobacter pylori immunoglobulin G and for gastrin and glycine-extended gastrin. RESULTS: Verified cases included 166 colon cancers, 58 rectal cancers, and 9 with cancer in both locations. A mean of 15.3 years had elapsed between serum collection and diagnosis of cancer. Median gastrin levels were similar in cases and controls (41.7 vs. 40.7 pg/mL). However, a gastrin level above normal was associated with increased risk for colorectal malignancy (odds ratio, 3.9; 95% confidence interval, 1.5-9.8). If this association is causal, 8.6% of colorectal cancers could be attributed to high serum gastrin level. CONCLUSIONS: Hypergastrinemia is associated with an increased risk of colorectal carcinoma.
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Chronic hypergastrinemia, typically present during PPI use, can promote the growth of malignant colonic epithelial cells, facilitating the deleterious sequencing adenoma-carcinoma.
“Last, chronic hypergastrinemia, typically present during PPI use, can promote the growth of malignant colonic epithelial cells, facilitating the deleterious sequencing adenoma-carcinoma[151-153].”
From Proton pump inhibitors and dysbiosis: current knowledge and aspects to be clarified (2019) · cites this paper as [152]
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ResultHypergastrinemia Is Associated with Increased Risk of Distal Colon Adenomas
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“[34] showed that serum hypergastrinemia was associated with a 3.”
BackgroundHelicobacter pylori Infection and Development of Pancreatic Cancer
de Martel, C., Llosa, A. E., Friedmana, G. D., Vogelman∥, J. H., Orentreich∥, N., Stolzenberg‐Solomon, R. Z., & Parsonnet, J. (2008) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0185 · Cited by 79 · see citing works
“Gender,* n (%) Female 69 (49) 334 (46) 69 (58) 62 (34) 116 (51) 87 (43) Male 72 (51) 395 (54) 49 (42) 117 (65) 112 (49) 117 (57) Race,* n (%) Missing 1 (1) 4 (1) 0 0 3 (1) 1 (0) Black 28 (20) 103 (14) 10 (8) 35 (19) 18 (8) 40 (20) White 109 (77) 601 (82) 98 (83) 142 (79) 198 (87) 163 (80) Other 3 (2) 22 (3) 10 (8) 3 (…”
Self-citationThe Role of Gastrin and CCK Receptors in Pancreatic Cancer and other Malignancies
Smith, J. P., Fonkoua, L. A. K., & Moody, T. W. (2016) · International Journal of Biological Sciences · doi:10.7150/ijbs.14952 · Cited by 78 · see citing works
“A large study of nearly 130,000 patients with Helicobacter pylori infections reported an approximate 4-fold increase in colorectal cancers in those with elevated gastrin levels [25].”
BackgroundMortality study of 18 000 patients treated with omeprazole
Bateman, D. N., Colin-Jones, D. G., Hartz, S. C., Langman, M. J. S., Logan, R. F., Mant, J., Murphy, M., Paterson, K. R., Rowsell, R., Thomas, S., et al. (2003) · Gut · doi:10.1136/gut.52.7.942 · Cited by 78 · see citing works
Singh, P., Velasco, M. A. D., Given, R. L., Wargovich, M. J., Varró, A., & Wang, T. C. (2000) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2000.278.3.g390 · Cited by 75 · see citing works
“In a recent prospective study, amidated gastrin and Gly-gastrin were measured in the serum of a large number of patients, some of whom eventually developed colorectal carcinomas (46).”
BackgroundResultHelicobacter pylori seropositivity and colorectal cancer risk: a prospective study of male smokers.
Limburg, P. J., Stolzenberg‐Solomon, R. Z., Colbert, L. H., Perez-Perez, G. I., Blaser, M. J., Taylor, P. R., Virtamo, J. R. K., & Albanes, D. (2002) · PubMed · Cited by 74 · see citing works
CCK‐B/gastrin receptors in human colorectal cancer
Schmitz, F., Otte, J. ‐., Stechele, H. U., Reimann, B., Banasiewicz, T., Fölsch, U. R., Schmidt, W. E., & Herzig, K. (2001) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.2001.00870.x · Cited by 74 · see citing works
Dockray, G. J. (2004) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2004.07.003 · Cited by 73 · see citing works
Potential adverse effects of proton pump inhibitors
Coté, G. A., & Howden, C. W. (2008) · Current Gastroenterology Reports · doi:10.1007/s11894-008-0045-4 · Cited by 69 · see citing works
Glycine-Extended Gastrin Exerts Growth-Promoting Effects on Human Colon Cancer Cells
Stepan, V. M., Sawada, M., Todisco, A., & Dickinson, C. J. (1999) · Molecular Medicine · doi:10.1007/bf03402058 · Cited by 69 · see citing works
Self-citationColucci, R., Blandizzi, C., Tanini, M., Vassalle, C., Breschi, M. C., & Tacca, M. D. (2005) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706053 · Cited by 68 · see citing works
“…cancer, and it has been proposed that CCK-2 receptors may mediate direct inhibitory or growth factor-dependent stimulant actions on cell growth (Varro et al., 2002); (3) some models of intestinal epithelial cells do not express CCK-2 receptors and need to be transfected to examine the effects…”
BackgroundHelicobacter pylori but not gastrin is associated with the development of colonic neoplasms
Selgrad, M., Bornschein, J., Kandulski, A., Hille, C., Weigt, J., Roessner, A., Wex, T., & Malfertheiner, P. (2014) · International Journal of Cancer · doi:10.1002/ijc.28758 · Cited by 68 · see citing works
“Gastrin is capable of stimulating growth factor dependent signaling pathways and therefore hypergastrinemia may act as a putative promoter of colorectal neoplasia in humans.(15) In vitro, high gastrin levels have been shown to be associated with growth and proliferation of colon cancer cells.”
BackgroundChen, X.-Z., Schöttker, B., Castro, F. A., Chen, H., Zhang, Y., Holleczek, B., & Brenner, H. (2016) · Oncotarget · doi:10.18632/oncotarget.7946 · Cited by 69 · see citing works
Proton Pump Inhibitors: Risks and Rewards and Emerging Consequences to the Gut Microbiome
Singh, A., Cresci, G., & Kirby, D. F. (2018) · Nutrition in Clinical Practice · doi:10.1002/ncp.10181 · Cited by 68 · see citing works
Jensen, R. T. (2002) · Pharmacology & Toxicology · doi:10.1034/j.1600-0773.2002.910611.x · Cited by 68 · see citing works
Sarri, B., Canonge, R., Audier, X., Simon, E., Wojak, J., Caillol, F., Cador, C., Marguet, D., Poizat, F., Giovannini, M. F., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-46489-x · Cited by 67 · see citing works
Inoue, I., Mukoubayashi, C., Yoshimura, N., Niwa, T., Deguchi, H., Watanabe, M., Enomoto, S., Maekita, T., Ueda, K., Iguchi, M., et al. (2011) · International Journal of Cancer · doi:10.1002/ijc.25931 · Cited by 67 · see citing works
Subramaniam, D., Ramalingam, S., May, R. J., Dieckgraefe, B. K., Berg, D. E., Pothoulakis, C., Houchen, C. W., Wang, T. C., & Anant, S. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.01.040 · Cited by 67 · see citing works
Association between Helicobacter pylori infection and the risk of colorectal cancer
Zuo, Y., Zhao, J., Bie, M., Xu, C., Hao, X., & Wang, B. (2020) · Medicine · doi:10.1097/md.0000000000021832 · Cited by 64 · see citing works
Kim, T. J., Kim, E. R., Chang, D. K., Kim, Y., Baek, S., Kim, K., & Hong, S. N. (2017) · Helicobacter · doi:10.1111/hel.12377 · Cited by 64 · see citing works
Chronic Hypergastrinemia: Causes and Consequences
Orlando, L. A., Lenard, L. G., & Orlando, R. C. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9419-3 · Cited by 63 · see citing works
“I carcinogen by the World Health Organization [64].”
BackgroundHelicobacter pyloriand colorectal neoplasia: Is there a causal link?
Papastergiou, V. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i2.649 · Cited by 62 · see citing works
Atrophic Gastritis, Helicobacter pylori , and Colorectal Cancer Risk: A Case‐Control Study
Montani, A., Sasazuki, S., Inoue, M., Natsukawa, S., Shaura, K., Koizumi, Y., Kasuga, Y., Hanaoka, T., & Tsugane, S. (2007) · Helicobacter · doi:10.1111/j.1523-5378.2007.00513.x · Cited by 61 · see citing works
Mechanism of Activation of Protein Kinase D2(PKD2) by the CCKB/Gastrin Receptor
Sturany, S., Lint, J. V., Gilchrist, A., Vandenheede, J. R., Adler, G., & Seufferlein, T. T. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200934200 · Cited by 61 · see citing works
Elevated Serum Gastrin Is Associated With a History of Advanced Neoplasia in Barrett's Esophagus
Wang, J. S., Varró, A., Lightdale, C. J., Lertkowit, N., Slack, K. N., Fingerhood, M., Tsai, W. Y., Wang, T. C., & Abrams, J. A. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.629 · Cited by 58 · see citing works
Mizuno, S., Morita, Y., Inui, T., Asakawa, A., Ueno, N., Ando, T., Kato, H., Uchida, M., Yoshikawa, T., & Inui, A. (2005) · International Journal of Cancer · doi:10.1002/ijc.21280 · Cited by 57 · see citing works
“sae and with an increased risk of colonic malignancy in a subpopulation of patients.(6,15) The way in which H.”
BackgroundFerrand, A., Bertrand, C., Portolan, G., Cui, G., Carlson, J. E., Pradayrol, L., Fourmy, D., Dufresne, M., Wang, T. C., & Seva, C. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-0978 · Cited by 56 · see citing works
“In addition, a recent study suggests that the risk for developing colorectal carcinoma is increased in patients with hypergastrinemia (46).”
BackgroundGastrin, inflammation, and carcinogenesis
Chao, C., & Hellmich, M. R. (2010) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e328333faf8 · Cited by 56 · see citing works
Helicobacter pylori Protein–Specific Antibodies and Risk of Colorectal Cancer
Epplein, M., Pawlita, M., Michel, A., Peek, R. M., Cai, Q., & Blot, W. J. (2013) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0702 · Cited by 53 · see citing works
“An association between highgastrin levels and colorectal cancer risk has been suggested in several studies of human populations (28–30), although the association only reached significance in one study (30).”
Helicobacter pylori infection is an independent risk factor for colonic adenomatous neoplasms
Nam, J. H., Hong, C. W., Kim, B. C., Shin, A., Ryu, K. H., Park, B.-J., Kim, B., Sohn, D. K., Han, K. S., Kim, J., et al. (2016) · Cancer Causes & Control · doi:10.1007/s10552-016-0839-x · Cited by 53 · see citing works
“pylori-induced hypergastrinemia stimulates colonic carcinogenesis by cell proliferation, and some studies have supported this claim [20, 28].”
Cholecystokinin-B/gastrin receptors enhance wound healing in the rat gastric mucosa
Schmassmann, A., & Reubi, J. C. (2000) · Journal of Clinical Investigation · doi:10.1172/jci8115 · Cited by 53 · see citing works
“The growth-promoting effect of gastrin (18–20) has generated substantial interest because of potential side effects such as gastric or colorectal tumor growth during hypergastrinemia induced by long-term treatment with gastric acid-inhibitory drugs (38, 39).”
BackgroundChoi, D. S., Seo, S. I., Shin, W. G., & Park, C. H. (2020) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000127 · Cited by 51 · see citing works
“1998 Thorburn (37) Case-control USA 1964–1991 466 Community-based IgG anti-HP antibody N/A 9”
BackgroundInfluentialAssociation of Helicobacter Pylori Infection and Colon Cancer
Strofilas (2012) · Journal of Clinical Medicine Research · doi:10.4021/jocmr880w · Cited by 51 · see citing works
“differ between the two groups, in accordance to numerous previous case-control studies [30-33].”
ResultRole of gastrin peptides in carcinogenesis
Grabowska, A. M., & Watson, S. A. (2007) · Cancer Letters · doi:10.1016/j.canlet.2007.06.017 · Cited by 51 · see citing works
Association of Helicobacter pylori Infection With Colon Cancer and Adenomatous Polyps.
Teimoorian, F., Ranaei, M., Hajian‐Tilaki, K., Shokri‐Shirvani, J., & Vosough, Z. (2018) · Europe PMC (PubMed Central) · Cited by 51 · see citing works
Gastrin, Helicobacter pylori, and Colorectal Adenomas
Robertson, D. J., Sandler, R. S., Ahnen, D. J., Greenberg, E. R., Mott, L. A., Cole, B. F., & Baron, J. A. (2008) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2008.09.006 · Cited by 50 · see citing works
Cobb, S., Wood, T. G., Ceci, J. D., Varró, A., Velasco, M. A. D., & Singh, P. (2004) · Cancer · doi:10.1002/cncr.20094 · Cited by 50 · see citing works
Expression of gastrin and its receptor in human gastric cancer tissues
Hur, K., Kwak, M. K., Lee, H.-J., Park, D. J., Lee, H. K., Lee, H. S., Kim, W. H., Michaeli, D., & Yang, H. (2005) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-005-0043-y · Cited by 49 · see citing works
“However, little information is available on the expression of gastrin/CCKB receptor protein in gastric carcinoma tissues, although a previous epidemiological study demonstrated that above-normal gastrin levels are associated with an increased risk of colorectal malignancy (Thorburn et al. 1998).”
ResultPhase I/II study of G17-DT, an anti-gastrin immunogen, in advanced colorectal cancer.
Smith, A. M., Justin, T. A., Michaeli, D., & Watson, S. A. (2000) · PubMed · Cited by 49 · see citing works
Siersema, P. D., Yu, S., Sahbaie, P., Steyerberg, E. W., Simpson, P. W., Kuipers, E. J., & Triadafilopoulos, G. (2006) · Gastrointestinal Endoscopy · doi:10.1016/j.gie.2005.08.043 · Cited by 47 · see citing works
Personal review: is profound acid inhibition safe?
Waldum, H. L., & Brenna (2000) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2000.00681.x · Cited by 47 · see citing works
Gastroesophageal reflux disease
Rai, A. M., & Orlando, R. C. (2001) · Current Opinion in Gastroenterology · doi:10.1097/00001574-200107000-00011 · Cited by 47 · see citing works
Gastrin-induced gastric adenocarcinoma growth is mediated through cyclin D1
Song, D. H., Rana, B., Wolfe, J. R., Crimmins, G. M., Choi, C. J., Albanese, C., Wang, T. C., Pestell, R. G., & Wolfe, M. M. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00516.2002 · Cited by 47 · see citing works
Potential role of endocrine gastrin in the colonic adenoma carcinoma sequence
Watson, S. A., Morris, T. M., McWilliams, D. F., Harris, J. C., Evans, S. A., Smith, A. M., & Clarke, P. A. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600509 · Cited by 46 · see citing works
“…a positive temporal relationship has been observed between hyper-gastrinaemia and increased incidence of colon cancer with 8.9% of colon cancer being shown to be attributable to elevated gastrin levels (Thorburn et al, 1998), indicating a sub-group of patients exhibiting increased sensitivity.”
BackgroundMethodInfluentialThe relationship of Helicobacter pylori infection and colon neoplasia, on the basis of meta-analysis
Rokkas, T., Sechopoulos, P., Pistiolas, D., Kothonas, F., Margantinis, G., & Koukoulis, G. (2013) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0b013e328363d3cd · Cited by 42 · see citing works
Bierkamp, C., Kowalski‐Chauvel, A., Dehez, S., Fourmy, D., Pradayrol, L., & Seva, C. (2002) · Oncogene · doi:10.1038/sj.onc.1205999 · Cited by 42 · see citing works
“…that, both gastrin and CCK-2R are often upregulated in human carcinomas and precancerous lesions of the gastrointestinal tract and that in an epidemiological study increased colorectal cancer risk has been attributed to prolonged hypergastrinemia (Smith and Watson, 2000a,b; Thorburn et al., 1998).”
BackgroundAbbass, K., Gul, W., Beck, G., Markert, R. J., & Akram, S. (2011) · Southern Medical Journal · doi:10.1097/smj.0b013e31821e9009 · Cited by 41 · see citing works
Colorectal cancer risk in relation to use of acid suppressive medications
Chubak, J., Boudreau, D. M., Rulyak, S. J., & Mandelson, M. T. (2009) · Pharmacoepidemiology and Drug Safety · doi:10.1002/pds.1749 · Cited by 40 · see citing works
Hu, K., Wu, M., Chu, C., Wang, H., Lin, S., Liu, C., Su, T., Liao, W., Chen, C., Liu, C., et al. (2018) · Clinical Infectious Diseases · doi:10.1093/cid/ciy591 · Cited by 40 · see citing works
Somatostatin inhibits colon cancer cell growth through cyclooxygenase‐2 downregulation
Colucci, R., Blandizzi, C., Ghisu, N., Florio, T., & Tacca, M. D. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.268 · Cited by 40 · see citing works
“…suggest that hypergastrinaemia is associated with an increased risk of colorectal cancer, and it has been observed that most patients with colorectal cancer may present an increased expression of gastrin receptors and COX-2 in their neoplastic tissues (Thorburn et al., 1998; Hartwich et al., 2001).”
BackgroundIdentification of CCK-B/gastrin receptor splice variants in human peripheral blood mononuclear cells
Schmitz, F., Schrader, H., Otte, J., Schmitz, H., Stuber, E. R., Herzig, K., & Schmidt, W. E. (2001) · Regulatory Peptides · doi:10.1016/s0167-0115(01)00281-6 · Cited by 40 · see citing works
Chen, Y., Xu, S., Ding, Y., Huang, X., & Deng, B. (2013) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2013.14.12.7613 · Cited by 39 · see citing works
“Several studies have evaluated this hypothesis and have found increased levels of circulating gastrin in patients colonized with H. pylori who are diagnosed with colorectal cancer (Thorburn et al., 1998; A. Hartwich et al., 2001; Georgopoulos et al., 2006).”
BackgroundKhajeh, S., Tohidkia, M. R., Aghanejad, A., Mehdipour, T., Fathi, F., & Omidi, Y. (2018) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2018.1478846 · Cited by 39 · see citing works
“Different cumulative in vitro studies have shown that G17-Gly promotes proliferation of different GI cell lines including pancreatic carcinoma cell line (AR4–2J) [4], gastric carcinoma cell lines (AGS and SIIA), and colon carcinoma cell lines (HCT-116, LoVo and HT29) [5].”
BackgroundChao, C., Goluszko, E., Lee, Y.-T., Kolokoltsov, A. A., Davey, R. A., Uchida, T., Townsend, C. M., & Hellmich, M. R. (2006) · Oncogene · doi:10.1038/sj.onc.1209862 · Cited by 39 · see citing works
“%) for developing colorectal cancer (Thorburn et al., 1998).”
Role of gastrin-peptides in Barrett's and colorectal carcinogenesis
Chueca, E. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i45.6560 · Cited by 38 · see citing works
Hu, K., Wu, M., Chu, C., Wang, H., Lin, S., Liu, S.-C., Liu, C., Su, T., Chen, C., Liu, C., et al. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-00257 · Cited by 37 · see citing works
“(28) reported that hypergastrinemia may promote colorectal neoplasia in humans, because gastrin is capable of stimulating growth factor–dependent signaling pathways.”
Yang, F., Xu, Y.-L., & Zhu, R. (2019) · Minerva Medica · doi:10.23736/s0026-4806.19.05942-1 · Cited by 37 · see citing works
Zumkeller, N., Brenner, H., Chang-Claude, J. C., Hoffmeister, M., Nieters, A., & Rothenbacher, D. (2007) · European Journal of Cancer · doi:10.1016/j.ejca.2007.03.005 · Cited by 37 · see citing works
- Authors
- Thorburn*, C. M., Friedman‡, G. D., Dickinson§, C. J., Vogelman∥, J. H., Orentreich∥, N., & Parsonnet*, #.
- Affiliations
- Kaiser Permanente (US)
- Stanford University (US)
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 1998-08
- Volume
- 115
- Issue
- 2
- Pages
- 275-280
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W2029989332
- Cited by
- 267
- References
- 42
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 8 · 2022: 5 · 2021: 7 · 2020: 14 · 2019: 12 · 2018: 9 · 2017: 12 · 2016: 13 · 2015: 1 · 2014: 7 · 2013: 19 · 2012: 12
- FWCI
- 8.89
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gastroenterology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r03ca065801-01a1, DK34933)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK034933)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
- Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
- Keywords
- gastrin, hypergastrinemia, colorectal cancer, colon cancer, rectal cancer, serum gastrin, cancer risk, Helicobacter pylori, glycine-extended gastrin, temporal relations
- MeSH terms
- Colonic Neoplasms, Female, Gastrins, Humans, Male, Middle Aged, Prospective Studies, Rectal Neoplasms, Risk Factors, Colorectal Neoplasms, Cohort Studies, Incidence, Multivariate Analysis, Odds Ratio, Case-Control Studies
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