Advertisement

GPIHBP1 autoantibody is an independent risk factor for the recurrence of hypertriglyceridemia-induced acute pancreatitis

  • Author Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Guofu Zhang
    Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Author Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Qi Yang
    Correspondence
    Corresponding author at. Department of Critical Care Medicine, Jinling Hospital, No. 305 Zhongshan East Road, Nanjing, Jiangsu Province, China, postal code: 210000, Telephone: +86-025-860007, Fax: +86-025-80862073
    Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Author Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Wenjian Mao
    Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
    Affiliations
    Department of Critical Care Medicine, Jinling Clinical Medical College of Nanjing Medical University, Nanjing, China (Drs Mao, Deng, and Li)
    Search for articles by this author
  • Yuepeng Hu
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Na Pu
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Hongbin Deng
    Affiliations
    Department of Critical Care Medicine, Jinling Clinical Medical College of Nanjing Medical University, Nanjing, China (Drs Mao, Deng, and Li)
    Search for articles by this author
  • Xianqiang Yu
    Affiliations
    Medical School, Southeast University, Nanjing, China (Drs Yu and Li)
    Search for articles by this author
  • Jingzhu Zhang
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Jing Zhou
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Bo Ye
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Gang Li
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Baiqiang Li
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Lu Ke
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Zhihui Tong
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Masami Murakami
    Affiliations
    Department of Clinical Laboratory Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan (Drs Murakami, Kimura, and Nakajima)
    Search for articles by this author
  • Takao Kimura
    Affiliations
    Department of Clinical Laboratory Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan (Drs Murakami, Kimura, and Nakajima)
    Search for articles by this author
  • Katsuyuki Nakajima
    Affiliations
    Department of Clinical Laboratory Medicine, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan (Drs Murakami, Kimura, and Nakajima)
    Search for articles by this author
  • Wangsen Cao
    Affiliations
    Jiangsu Key Lab of Molecular Medicine, Nanjing University School of Medicine, Nanjing, China (Dr Cao)
    Search for articles by this author
  • Yuxiu Liu
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Department of Biostatistics, School of Public Health, Nanjing Medical University, Nanjing, China (Dr Liu)
    Search for articles by this author
  • Weiqin Li
    Correspondence
    Corresponding author at. Department of Critical Care Medicine, Jinling Hospital, No. 305 Zhongshan East Road, Nanjing, Jiangsu Province, China, postal code: 210000, Telephone: +86-025-860007, Fax: +86-025-80862073
    Affiliations
    Department of Critical Care Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, Nanjing, China (Drs G. Zhang, Yang, Hu, Pu, J. Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)

    Department of Critical Care Medicine, Jinling Clinical Medical College of Nanjing Medical University, Nanjing, China (Drs Mao, Deng, and Li)

    Medical School, Southeast University, Nanjing, China (Drs Yu and Li)

    Institute of Critical Care Medicine, Nanjing University, Nanjing, China (Drs Zhang, Zhou, Ye, G. Li, B. Li, Ke, Tong, Liu, and W. Li)
    Search for articles by this author
  • Author Footnotes
    1 Guofu Zhang, Qi Yang, and Wenjian Mao contributed equally to this work.
Published:August 05, 2022DOI:https://doi.org/10.1016/j.jacl.2022.08.001

      Highlights

      • HTG-AP patients had a higher rate of GPIHBP1 autoantibody than reported HTG patients.
      • The GPIHBP1 autoantibody-positive group had a high recurrence rate of HTG-AP.
      • The GPIHBP1 autoantibody was an independent risk factor for HTG-AP recurrence.

      Background

      GPIHBP1, a glycolipid-anchored protein of capillary endothelial cells, is a crucial partner for lipoprotein lipase (LPL) in plasma triglyceride metabolism. GPIHBP1 autoantibodies block LPL binding to GPIHBP1 and lead to severe hypertriglyceridemia (HTG) and HTG-induced acute pancreatitis (HTG-AP). We sought to define the incidence of GPIHBP1 autoantibodies in patients with HTG-AP.

      Objective

      We determined the incidence of GPIHBP1 autoantibody in HTG-AP patients, and compared the clinical features and long-term outcomes between GPIHBP1 autoantibody-positive and negative groups.

      Methods

      An enzyme-linked immunosorbent assay was used to screen for GPIHBP1 autoantibody in 116 HTG-AP patients hospitalized from Jan 1, 2015 to Aug 31, 2019. All patients were followed up for 24 months. The primary outcome was the recurrence rate of HTG-AP during the two-year follow-up period. The incidence of recurrent episodes was analyzed by the Kaplan-Meier method and multivariable Cox regression was used to identify risk factors.

      Results

      GPIHBP1 autoantibodies were present in 17 of 116 study patients (14.66%). The 2-year recurrence rate of HTG-AP was much higher in the GPIHBP1 autoantibody-positive group (35%, 6 in 17) than in the negative group (4%, 4 in 99). The multivariable Cox regression analysis showed that GPIHBP1 autoantibody was an independent risk factor for HTG-AP recurrence in two years.

      Conclusions

      The presence of GPIHBP1 autoantibody is common in patients with HTG-AP, and is an independent risk factor for two-year recurrence of HTG-AP.

      Keywords

      Abbreviations:

      AP (acute pancreatitis), APACHE II (acute physiology and chronic health evaluation II), AUC (area under the ROC), BMI (body mass index), DM (diabetes mellitus), FFAs (free fatty acids), GPIHBP1 (Glycosylphosphatidylinositol-anchored high-density lipoprotein–binding protein 1), GPIHBP1 Autoantibody (GPIHBP1 Ab), HTG (hypertriglyceridemia), HTG-AP (HTG-induced acute pancreatitis), LPL (lipoprotein lipase), RAP (recurrent acute pancreatitis), ROC (receiver operating characteristic), TG (Triglycerides), TRLs (triglyceride-rich lipoproteins)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Clinical Lipidology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Pedersen SB
        • Langsted A
        • Nordestgaard BG
        Nonfasting mild-to-moderate hypertriglyceridemia and risk of acute pancreatitis.
        JAMA Intern Med. 2016; 176: 1834-1842
        • Murphy MJ
        • Sheng X
        • MacDonald TM
        • Wei L
        Hypertriglyceridemia and acute pancreatitis.
        JAMA Intern Med. 2013; 173: 162-164
        • Mosztbacher D
        • Hanak L
        • Farkas N
        • Szentesi A
        • Miko A
        • Bajor J
        • Sarlos P
        • Czimmer J
        • Vincze A
        • Hegyi PJ
        • et al.
        Hypertriglyceridemia-induced acute pancreatitis: A prospective, multicenter, international cohort analysis of 716 acute pancreatitis cases.
        Pancreatology. 2020; 20: 608-616
        • Adiamah A
        • Psaltis E
        • Crook M
        • Lobo DN
        A systematic review of the epidemiology, pathophysiology and current management of hyperlipidaemic pancreatitis.
        Clin Nutr. 2018; 37: 1810-1822
        • Yin G
        • Cang X
        • Yu G
        • Hu G
        • Ni J
        • Xiong J
        • Hu Y
        • Xing M
        • Chen C
        • Huang Y
        • et al.
        Different clinical presentations of hyperlipidemic acute pancreatitis: a Retrospective Study.
        Pancreas. 2015; 44: 1105-1110
        • Yu B
        • Li J
        • Li N
        • Zhu Y
        • Chen Y
        • He W
        • Lu N
        Progression to recurrent acute pancreatitis after a first attack of acute pancreatitis in adults.
        Pancreatology. 2020; 20: 1340-1346
        • Zafrir B
        • Saliba W
        • Jubran A
        • Hijazi R
        • Shapira C
        Severe hypertriglyceridemia-related pancreatitis: characteristics and predictors of recurrence.
        Pancreas. 2019; 48: 182-186
        • Davies BS
        • Beigneux AP
        • Barnes 2nd, RH
        • Tu Y
        • Gin P
        • Weinstein MM
        • Nobumori C
        • Nyren R
        • Goldberg I
        • Olivecrona G
        • et al.
        GPIHBP1 is responsible for the entry of lipoprotein lipase into capillaries.
        Cell Metab. 2010; 12: 42-52
        • Beigneux AP
        • Davies BS
        • Gin P
        • Weinstein MM
        • Farber E
        • Qiao X
        • Peale F
        • Bunting S
        • Walzem RL
        • Wong JS
        • et al.
        Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons.
        Cell Metab. 2007; 5: 279-291
        • Goulbourne CN
        • Gin P
        • Tatar A
        • Nobumori C
        • Hoenger A
        • Jiang H
        • Grovenor CR
        • Adeyo O
        • Esko JD
        • Goldberg IJ
        • et al.
        The GPIHBP1-LPL complex is responsible for the margination of triglyceride-rich lipoproteins in capillaries.
        Cell Metab. 2014; 19: 849-860
        • Beigneux AP
        • Franssen R
        • Bensadoun A
        • Gin P
        • Melford K
        • Peter J
        • Walzem RL
        • Weinstein MM
        • Davies BS
        • Kuivenhoven JA
        • et al.
        Chylomicronemia with a mutant GPIHBP1 (Q115P) that cannot bind lipoprotein lipase.
        Arterioscler Thromb Vasc Biol. 2009; 29: 956-962
        • Franssen R
        • Young SG
        • Peelman F
        • Hertecant J
        • Sierts JA
        • Schimmel AW
        • Bensadoun A
        • Kastelein JJ
        • Fong LG
        • Dallinga-Thie GM
        • Beigneux AP
        Chylomicronemia with low postheparin lipoprotein lipase levels in the setting of GPIHBP1 defects.
        Circ Cardiovasc Genet. 2010; 3: 169-178
        • Olivecrona G
        • Ehrenborg E
        • Semb H
        • Makoveichuk E
        • Lindberg A
        • Hayden MR
        • Gin P
        • Davies BS
        • Weinstein MM
        • Fong LG
        • et al.
        Mutation of conserved cysteines in the Ly6 domain of GPIHBP1 in familial chylomicronemia.
        J Lipid Res. 2010; 51: 1535-1545
        • Coca-Prieto I
        • Kroupa O
        • Gonzalez-Santos P
        • Magne J
        • Olivecrona G
        • Ehrenborg E
        • Valdivielso P
        Childhood-onset chylomicronaemia with reduced plasma lipoprotein lipase activity and mass: identification of a novel GPIHBP1 mutation.
        J Intern Med. 2011; 270: 224-228
        • Rios JJ
        • Shastry S
        • Jasso J
        • Hauser N
        • Garg A
        • Bensadoun A
        • Cohen JC
        • Hobbs HH
        Deletion of GPIHBP1 causing severe chylomicronemia.
        J Inherit Metab Dis. 2012; 35: 531-540
        • Plengpanich W
        • Young SG
        • Khovidhunkit W
        • Bensadoun A
        • Karnman H
        • Ploug M
        • Gardsvoll H
        • Leung CS
        • Adeyo O
        • Larsson M
        • et al.
        Multimerization of glycosylphosphatidylinositol-anchored high density lipoprotein-binding protein 1 (GPIHBP1) and familial chylomicronemia from a serine-to-cysteine substitution in GPIHBP1 Ly6 domain.
        J Biol Chem. 2014; 289: 19491-19499
        • Ariza MJ
        • Martinez-Hernandez PL
        • Ibarretxe D
        • Rabacchi C
        • Rioja J
        • Grande-Aragon C
        • Plana N
        • Tarugi P
        • Olivecrona G
        • Calandra S
        • Valdivielso P
        Novel mutations in the GPIHBP1 gene identified in 2 patients with recurrent acute pancreatitis.
        J Clin Lipidol. 2016; 10 (e101): 92-100
        • Rabacchi C
        • D'Addato S
        • Palmisano S
        • Lucchi T
        • Bertolini S
        • Calandra S
        • Tarugi P
        Clinical and genetic features of 3 patients with familial chylomicronemia due to mutations in GPIHBP1 gene.
        J Clin Lipidol. 2016; 10 (e914): 915-921
        • Lin MH
        • Tian XH
        • Hao XL
        • Fei H
        • Yin JL
        • Yan DD
        • Li T
        Management of a pregnant patient with chylomicronemia from a novel mutation in GPIHBP1: a case report.
        BMC Pregnancy Childbirth. 2020; 20: 272
        • Beigneux AP
        • Miyashita K
        • Ploug M
        • Blom DJ
        • Ai M
        • Linton MF
        • Khovidhunkit W
        • Dufour R
        • Garg A
        • McMahon MA
        • et al.
        Autoantibodies against GPIHBP1 as a Cause of Hypertriglyceridemia.
        N Engl J Med. 2017; 376: 1647-1658
        • Miyashita K
        • Lutz J
        • Hudgins LC
        • Toib D
        • Ashraf AP
        • Song W
        • Murakami M
        • Nakajima K
        • Ploug M
        • Fong LG
        • et al.
        Chylomicronemia from GPIHBP1 autoantibodies.
        J Lipid Res. 2020; 61: 1365-1376
        • Lutz J
        • Dunaj-Kazmierowska M
        • Arcan S
        • Kassner U
        • Miyashita K
        • Murakami M
        • Ploug M
        • Fong LG
        • Young SG
        • Nakajima K
        • Beigneux AP
        Chylomicronemia from GPIHBP1 autoantibodies successfully treated with rituximab: a case report.
        Ann Intern Med. 2020; 173: 764-765
        • Hu X
        • Dallinga-Thie GM
        • Hovingh GK
        • Chang SY
        • Sandoval NP
        • Dang TLP
        • Fukamachi I
        • Miyashita K
        • Nakajima K
        • Murakami M
        • et al.
        GPIHBP1 autoantibodies in a patient with unexplained chylomicronemia.
        J Clin Lipidol. 2017; 11: 964-971
        • Ashraf AP
        • Miyashita K
        • Nakajima K
        • Murakami M
        • Hegele RA
        • Ploug M
        • Fong LG
        • Young SG
        • Beigneux AP
        Intermittent chylomicronemia caused by intermittent GPIHBP1 autoantibodies.
        J Clin Lipidol. 2020; 14: 197-200
        • Eguchi J
        • Miyashita K
        • Fukamachi I
        • Nakajima K
        • Murakami M
        • Kawahara Y
        • Yamashita T
        • Ohta Y
        • Abe K
        • Nakatsuka A
        • et al.
        GPIHBP1 autoantibody syndrome during interferon beta1a treatment.
        J Clin Lipidol. 2019; 13: 62-69
        • Banks PA
        • Bollen TL
        • Dervenis C
        • Gooszen HG
        • Johnson CD
        • Sarr MG
        • Tsiotos GG
        • Vege SS
        Acute pancreatitis classification working G: classification of acute pancreatitis–2012: revision of the Atlanta classification and definitions by international consensus.
        Gut. 2013; 62: 102-111
        • Yang Q
        • Pu N
        • Li XY
        • Shi XL
        • Chen WW
        • Zhang GF
        • Hu YP
        • Zhou J
        • Chen FX
        • Li BQ
        • et al.
        Digenic inheritance and gene-environment interaction in a patient with hypertriglyceridemia and acute pancreatitis.
        Front Genet. 2021; 12640859
        • Al-Haddad M
        • Wallace MB
        Diagnostic approach to patients with acute idiopathic and recurrent pancreatitis, what should be done?.
        World J Gastroenterol. 2008; 14: 1007-1010
        • Romagnuolo J
        • Guda N
        • Freeman M
        • Durkalski V
        Preferred designs, outcomes, and analysis strategies for treatment trials in idiopathic recurrent acute pancreatitis.
        Gastrointest Endosc. 2008; 68: 966-974
        • Cote GA
        • Imperiale TF
        • Schmidt SE
        • Fogel E
        • Lehman G
        • McHenry L
        • Watkins J
        • Sherman S
        Similar efficacies of biliary, with or without pancreatic, sphincterotomy in treatment of idiopathic recurrent acute pancreatitis.
        Gastroenterology. 2012; 143 (e1501): 1502-1509
        • Shi XL
        • Yang Q
        • Pu N
        • Li XY
        • Chen WW
        • Zhou J
        • Li G
        • Tong ZH
        • Ferec C
        • Cooper DN
        • et al.
        Identification and functional characterization of a novel heterozygous missense variant in the LPL associated with recurrent hypertriglyceridemia-induced acute pancreatitis in pregnancy.
        Mol Genet Genomic Med. 2020; 8: e1048
        • Tu J
        • Zhang J
        • Ke L
        • Yang Y
        • Yang Q
        • Lu G
        • Li B
        • Tong Z
        • Li W
        • Li J
        Endocrine and exocrine pancreatic insufficiency after acute pancreatitis: long-term follow-up study.
        BMC Gastroenterol. 2017; 17: 114
        • Miyashita K
        • Fukamachi I
        • Machida T
        • Nakajima K
        • Young SG
        • Murakami M
        • Beigneux AP
        • Nakajima K
        An ELISA for quantifying GPIHBP1 autoantibodies and making a diagnosis of the GPIHBP1 autoantibody syndrome.
        Clin Chim Acta. 2018; 487: 174-178
        • Leth JM
        • Leth-Espensen KZ
        • Kristensen KK
        • Kumari A
        • Lund Winther AM
        • Young SG
        • Ploug M
        Evolution and Medical Significance of LU Domain-Containing Proteins.
        Int J Mol Sci. 2019; : 20
        • Kristensen KK
        • Midtgaard SR
        • Mysling S
        • Kovrov O
        • Hansen LB
        • Skar-Gislinge N
        • Beigneux AP
        • Kragelund BB
        • Olivecrona G
        • Young SG
        • et al.
        A disordered acidic domain in GPIHBP1 harboring a sulfated tyrosine regulates lipoprotein lipase.
        Proc Natl Acad Sci U S A. 2018; 115: E6020-E6029
        • Garg R
        • Rustagi T
        Management of hypertriglyceridemia induced acute pancreatitis.
        Biomed Res Int. 2018; 20184721357
        • Forsmark CE
        • Vege SS
        • Wilcox CM
        Acute pancreatitis.
        N Engl J Med. 2016; 375: 1972-1981
        • Zheng Y
        • Zhou Z
        • Li H
        • Li J
        • Li A
        • Ma B
        • Zhang T
        • Liao Q
        • Ye Y
        • Zhang Z
        • et al.
        A multicenter study on etiology of acute pancreatitis in Beijing during 5 years.
        Pancreas. 2015; 44: 409-414
        • Zhu Y
        • Pan X
        • Zeng H
        • He W
        • Xia L
        • Liu P
        • Zhu Y
        • Chen Y
        • Lv N
        A study on the etiology, severity, and mortality of 3260 patients with acute pancreatitis according to the revised Atlanta classification in Jiangxi, China over an 8-year period.
        Pancreas. 2017; 46: 504-509
        • Li X
        • Ke L
        • Dong J
        • Ye B
        • Meng L
        • Mao W
        • Yang Q
        • Li W
        • Li J
        Significantly different clinical features between hypertriglyceridemia and biliary acute pancreatitis: a retrospective study of 730 patients from a tertiary center.
        BMC Gastroenterol. 2018; 18: 89
        • Tian X
        • Huang Y
        • Wang H
        Deviation of Chinese adults' diet from the Chinese Food Pagoda 2016 and its association with adiposity.
        Nutrients. 2017; : 9
        • Li XY
        • Pu N
        • Chen WW
        • Shi XL
        • Zhang GF
        • Ke L
        • Ye B
        • Tong ZH
        • Wang YH
        • Liu G
        • et al.
        Identification of a novel LPL nonsense variant and further insights into the complex etiology and expression of hypertriglyceridemia-induced acute pancreatitis.
        Lipids Health Dis. 2020; 19: 63
        • Pu N
        • Yang Q
        • Shi XL
        • Chen WW
        • Li XY
        • Zhang GF
        • Li G
        • Li BQ
        • Ke L
        • Tong ZH
        • et al.
        Gene-environment interaction between APOA5 c.553G>T and pregnancy in hypertriglyceridemia-induced acute pancreatitis.
        J Clin Lipidol. 2020; 14: 498-506
        • Doubilet H
        • Mulholland JH
        Recurrent acute pancreatitis: observations on etiology and surgical treatment.
        Ann Surg. 1948; 128: 609-636
        • Wehrmann T
        Long-term results (>/= 10 years) of endoscopic therapy for sphincter of Oddi dysfunction in patients with acute recurrent pancreatitis.
        Endoscopy. 2011; 43: 202-207
        • Bertilsson S
        • Sward P
        • Kalaitzakis E
        Factors that affect disease progression after first attack of acute pancreatitis.
        Clin Gastroenterol Hepatol. 2015; 13 (e1663): 1662-1669
        • Vipperla K
        • Papachristou GI
        • Easler J
        • Muddana V
        • Slivka A
        • Whitcomb DC
        • Yadav D
        Risk of and factors associated with readmission after a sentinel attack of acute pancreatitis.
        Clin Gastroenterol Hepatol. 2014; 12: 1911-1919
        • Penn AH
        • Schmid-Schonbein GW
        The intestine as source of cytotoxic mediators in shock: free fatty acids and degradation of lipid-binding proteins.
        Am J Physiol Heart Circ Physiol. 2008; 294: H1779-H1792
        • Gan SI
        • Edwards AL
        • Symonds CJ
        • Beck PL
        Hypertriglyceridemia-induced pancreatitis: a case-based review.
        World J Gastroenterol. 2006; 12: 7197-7202