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(FUT2) Non-Secretor Status and Blood Group B Are Associated With Downloaded from gut.bmj.com on September 29, 2014 - Published by group.bmj.com Gut Online First, published on July 15, 2014 as 10.1136/gutjnl-2014-306930 Pancreas ORIGINAL ARTICLE Fucosyltransferase 2 (FUT2) non-secretor status and blood group B are associated with elevated serum lipase activity in asymptomatic subjects, and an increased risk for chronic pancreatitis: a genetic association study Frank Ulrich Weiss,1 Claudia Schurmann,2,3 Annett Guenther,1 Florian Ernst,2 Alexander Teumer,2 Julia Mayerle,1 Peter Simon,1 Henry Völzke,4 Dörte Radke,4 Andreas Greinacher,5 Jens-Peter Kuehn,6 Martin Zenker,7 Uwe Völker,2 Georg Homuth,2 Markus M Lerch1 ▸ Additional material is ABSTRACT published online only. To view Objective Serum lipase activities above the threefold Significance of this study please visit the journal online (http://dx.doi.org/10.1136/ upper reference limit indicate acute pancreatitis. We gutjnl-2014-306930). investigated whether high lipase activity—within the reference range and in the absence of pancreatitis—are What is already known on this subject? For numbered affiliations see ▸ The definition of acute pancreatitis includes end of article. associated with genetic single nucleotide polymorphisms (SNP), and whether these identified SNPs are also characteristic clinical symptoms in combination Correspondence to associated with clinical pancreatitis. with elevated serum enzyme activities (amylase Professor Markus M Lerch, or lipase) above three times the upper Methods Genome-wide association studies (GWAS) on 1 Department of Medicine A, ‘ ’ ‘ reference limit. Elevated lipase levels below University Medicine Greifswald, phenotypes serum lipase activity and high serum lipase activity’ were conducted including 3966 German this cut-off are not considered diagnostic for Fleischmannstrasse 41, pancreatitis, and can be observed in a number 17475 Greifswald, Germany; volunteers from the population-based Study-of-Health-in- [email protected] of non-pancreatic conditions. Pomerania (SHIP). Lead SNPs associated on a genome- ▸ wide significance level were replicated in two cohorts, No serum biomarker presently exists for chronic FUW and CS are equally pancreatitis contributing first authors. 1444 blood donors and 1042 pancreatitis patients. GH and MML are equally Results Initial discovery GWAS detected SNPs within or What are the new findings? contributing senior authors. near genes encoding the ABO blood group specifying ▸ In asymptomatic volunteers from a transferases A/B (ABO), Fucosyltransferase-2 (FUT2), and population-based study (N=3966) and healthy Received 4 February 2014 fi Revised 20 June 2014 Chymotrypsinogen-B2 (CTRB2), to be signi cantly blood donors (N=1444), genetic polymorphisms Accepted 23 June 2014 associated with lipase activity levels in asymptomatic that determine the so-called subjects. Replication analyses in blood donors confirmed Fucosyltransferase-2 non-secretor status and the association of FUT-2 non-secretor status (OR=1.49; the ABO blood-type B, were significantly p=0.012) and ABO blood-type-B (OR=2.48; associated with increased serum lipase −8 p=7.29×10 ) with high lipase activity levels. In activities. pancreatitis patients, significant associations were found ▸ This study is the first to identify Lewis and AB0 −4 for FUT-2 non-secretor status (OR=1.53; p=8.56×10 ) blood group systems as disease- relevant for −4 and ABO-B (OR=1.69, p=1.0×10 ) with chronic the development of pancreatitis. FUT2 pancreatitis, but not with acute pancreatitis. Conversely, non-secretors and blood group B carriers carriers of blood group O were less frequently affected by displayed 1.53-fold and 1.69-fold odds of −05) chronic pancreatitis (OR=0.62; p=1.22×10 and less developing chronic pancreatitis, whereas in likely to have high lipase activity levels (OR=0.59; blood type 0 carriers, the odds were clearly −05 p=8.14×10 ). reduced (0.62-fold). Conclusions These are the first results indicating that ▸ FUT2 non-secretor status and blood group ABO blood type-B as well as FUT2 non-secretor status are represent genetic cofactors in the development common population-wide risk factors for developing of alcoholic as well as idiopathic chronic chronic pancreatitis. They also imply that, even within the pancreatitis, but apparently do not influence reference range, elevated lipase activities may indicate the risk for acute pancreatitis. subclinical pancreatic injury in asymptomatic subjects. To cite: Weiss FU, Schurmann C, Guenther A, et al. Gut Published Online pancreatic duct system and into the duodenum. First: [please include Day INTRODUCTION Here, it has a major role in breaking down dietary Month Year] doi:10.1136/ Human pancreatic lipase (PNLIP, OMIM 246600) lipids such as triglycerides, oils and fats. In healthy gutjnl-2014-306930 is secreted by the exocrine pancreas through the individuals, only little lipase activity is found in the CopyrightWeiss FU, et Article al. Gut 2014; author0:1–11. doi:10.1136/gutjnl-2014-306930(or their employer) 2014. Produced by BMJ Publishing Group Ltd (& BSG) under licence.1 Downloaded from gut.bmj.com on September 29, 2014 - Published by group.bmj.com Pancreas 4308 volunteer participants (2008 males, aged 20–81 years) Significance of this study with German citizenship, European ancestry and principal resi- dence in the study area. Participants with a history of pancrea- titis or renal insufficiency, due to estimated glomerular filtration How might it impact on clinical practice in the rate (eGFR CKD-EPI) <30 mL/min per 1.73 m2)13 were foreseeable future? excluded from further analysis. For our study population of ▸ Blood group B (12–15% in a Western population) and FUT2 3966 participants, serum lipase activity was determined, and non-secretor status (20%) are common genetic traits genome-wide SNP-typing was performed. Approval was associated with serum lipase activities and the risk of obtained by the local ethic committee, and informed consent developing chronic pancreatitis. was given by all participants. ▸ Future studies investigating genetic or environmental risk factors for pancreatitis will have to correct for these factors Blood donors and pancreatitis patients in their cohorts because they vary greatly between The replication cohort consisted of 1500 blood donors (18–68 populations (eg, blood group B among Kashmiris 32%, years, mean age 32.4 years, 58.2% male) who were recruited Norwegians 8%). for the study in 2010 at University Medicine Greifswald. ▸ Elevated serum lipase activities in asymptomatic subjects Written consent and information on alcohol and tobacco con- may indicate, even when within the reference range, sumption, as well as a history of pancreatic disease was subclinical pancreatic injury. recorded. Subjects with a self-reported history of pancreatitis (N=9) were excluded from further analysis. To test the disease relevance of the identified SNPs we performed a second replica- blood, the source of which is either basolateral exocytosis of tion in 1042 German pancreatitis patients (5–97 years, mean 2 pancreatic secretory enzymes , or physiological turnover of age 46.6 years, 62.3% male) that had been enrolled in an obser- 3 acinar cells. vational study (ProZyt) between 2003 and 2011. This cohort – Almost a century ago it was recognised that high serum levels included patients with AP (n=505) and CP ( n=537).14 16 All of pancreatic secretory enzymes (initially amylase and later individuals gave their written informed consent for participation 4 lipase) indicate acute injury of the pancreas. Today, all current and genotyping, and the local ethics committee approved the guidelines require for the diagnosis of acute pancreatitis (AP), in study protocol. Definition for AP was abdominal pain in com- addition to characteristic abdominal symptoms, an elevation of bination with a greater than three-fold elevation of serum amylase or lipase of three times the upper limit of normal or amylase or lipase activity. Diagnosis of CP included the presence 15 higher. Conversely, for the diagnosis of chronic pancreatitis of unequivocal morphological evidence on computed tomog- (CP) no such serum marker exists, and neither elevated nor raphy (CT) and/or endoscopic retrograde cholangio pancrreato- fi reduced lipase activity levels are of suf cient diagnostic accuracy graphy (ERCP) and was labelled idiopathic (ICP (idiopathic 67 to be of clinical use. High subthreshold serum lipase activity chronic pancreatitis); n=229) in subjects in whom no known is common in patients with critical illness of any kind, cholecyst- risk factors, including gallstones, hyperlipidaemia or hypercal- itis, gastric ulcer disease, bowel obstruction, viral gastroenteritis caemia could be identified. Alcoholic aetiology (ACP (alcoholic and renal failure, so that an underlying pancreatic disorder chronic pancreatitis); n=214) was assumed in subjects with a 8 could so far not safely be assumed in symptomatic patients. history of regular alcohol consumption (more than two drinks In a previous population-based study, subthreshold elevated or 20 g/day). serum lipase activities were found to be associated with renal impairment, advanced age, or the use of various medications Phenotype determination that modulate the immune system,9 all of which can occasion- Serum lipase activities in the SHIP-cohort were measured using ally be associated with subclinical pancreatic damage, or overt a turbidometric assay on a Hitachi 717 analyser (Roche pancreatic disease.6 However, lipase elevations in this range are Diagnostics GmbH, Mannheim,
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