Skip to main content
SpringerLink
Log in

Impact of stress hyperglycemia on long-term prognosis in acute pancreatitis without diabetes

  • IM - ORIGINAL
  • Published:
Internal and Emergency Medicine Aims and scope Submit manuscript

Abstract

Stress hyperglycemia has been confirmed as a strong predictor of poor short-term prognosis in acute pancreatitis. However, whether stress hyperglycemia affects the long-term prognosis of patients with acute pancreatitis is unclear. We aimed to investigate the effect of stress hyperglycemia on the long-term prognosis of non-diabetic patients with acute pancreatitis. This retrospective observational study was conducted on 4055 patients with acute pancreatitis from 1 January 2016 to 31 October 2020. The association between stress hyperglycemia and the prognosis was evaluated using regression modeling. There were 935(71.5%) normoglycemic and 373(28.5%) stress hyperglycemia patients. 46(12.3%) patients with stress hyperglycemia had evidence of diabetes compared with 33(3.5%) patients without stress hyperglycemia (P < 0.001). After multivariate adjustment, patients with stress hyperglycemia were more likely to have evidence of diabetes (OR 2.905, 95% CI 1.688–4.999) compared with normoglycemic. However, stress hyperglycemia is not associated with the recurrence of pancreatitis and progression to chronic pancreatitis. Stress hyperglycemia was independently associated with diabetes secondary to acute pancreatitis. Accordingly, a follow-up diabetes-screening program for AP with stress hyperglycemia is an important part of identifying the disease as soon as possible, delaying islet damage, and improving the prognosis of post-acute pancreatitis diabetes mellitus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

All the data are available upon request to the corresponding author.

References

  1. Losser MR, Damoisel C, Payen D (2010) Bench-to-bedside review: glucose and stress conditions in the intensive care unit. Crit Care 4:231. https://doi.org/10.1186/cc9100

    Article  Google Scholar 

  2. Ishihara M, Inoue I, Kawagoe T, Shimatani Y, Kurisu S, Hata T et al (2006) Is admission hyperglycaemia in non-diabetic patients with acute myocardial infarction a surrogate for previously undiagnosed abnormal glucose tolerance? Eur Heart J 20:2413–2419. https://doi.org/10.1093/eurheartj/ehl271

    Article  Google Scholar 

  3. Di Luzio R, Dusi R, Barbanti FA, Calogero P, Marchesini G, Bianchi G (2022) Prognostic value of stress hyperglycemia in patients admitted to medical/geriatric departments for acute medical illness. Diabetes Ther 1:145–159. https://doi.org/10.1007/s13300-021-01183-y

    Article  CAS  Google Scholar 

  4. Capes SE, Hunt D, Malmberg K, Gerstein HC (2000) Stress hyperglycaemia and increased risk of death after myocardial infarction in patients with and without diabetes: a systematic overview. Lancet 9206:773–778. https://doi.org/10.1016/s0140-6736(99)08415-9

    Article  Google Scholar 

  5. Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC (2001) Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke 10:2426–2432. https://doi.org/10.1161/hs1001.096194

    Article  Google Scholar 

  6. Kotagal M, Symons R, Hirsch I, Umpierrez G, Dellinger E, Farrokhi E et al (2015) Perioperative hyperglycemia and risk of adverse events among patients with and without diabetes. Ann Surg 1:97–103. https://doi.org/10.1097/sla.0000000000000688

    Article  Google Scholar 

  7. Mederos MA, Reber HA, Girgis MD (2021) Acute pancreatitis: a review. JAMA 4:382–390. https://doi.org/10.1001/jama.2020.20317

    Article  CAS  Google Scholar 

  8. Lee PJ, Papachristou GI (2019) New insights into acute pancreatitis. Nat Rev Gastroenterol Hepatol 8:479–496. https://doi.org/10.1038/s41575-019-0158-2

    Article  Google Scholar 

  9. Iannuzzi JP, King JA, Leong JH, Quan J, Windsor JW, Tanyingoh D et al (2022) Global incidence of acute pancreatitis is increasing over time: a systematic review and meta-analysis. Gastroenterology 1:122–134. https://doi.org/10.1053/j.gastro.2021.09.043

    Article  Google Scholar 

  10. Das SL, Singh PP, Phillips AR, Murphy R, Windsor JA, Petrov MS (2014) Newly diagnosed diabetes mellitus after acute pancreatitis: a systematic review and meta-analysis. Gut 5:818–831. https://doi.org/10.1136/gutjnl-2013-305062

    Article  Google Scholar 

  11. Shen HN, Yang CC, Chang YH, Lu CL, Li CY (2015) Risk of diabetes mellitus after first-attack acute pancreatitis: a national population-based study. Am J Gastroenterol 12:1698–1706. https://doi.org/10.1038/ajg.2015.356

    Article  Google Scholar 

  12. Lee YK, Huang MY, Hsu CY, Su YC (2016) Bidirectional relationship between diabetes and acute pancreatitis: a population-based cohort study in Taiwan. Medicine (Baltimore) 2:e2448. https://doi.org/10.1097/md.0000000000002448

    Article  Google Scholar 

  13. Banks PA, Bollen TL, Dervenis C, Gooszen HG, Johnson CD, Sarr MG et al (2013) Classification of acute pancreatitis–2012: revision of the Atlanta classification and definitions by international consensus. Gut 1:102–111. https://doi.org/10.1136/gutjnl-2012-302779

    Article  Google Scholar 

  14. Petrov MS (2021) Diagnosis of endocrine disease: post-pancreatitis diabetes mellitus: prime time for secondary disease. Eur J Endocrinol 4:R137-r149. https://doi.org/10.1530/eje-20-0468

    Article  CAS  Google Scholar 

  15. Petrov MS, Basina M (2021) Diagnosis of endocrine disease: diagnosing and classifying diabetes in diseases of the exocrine pancreas. Eur J Endocrinol 4:R151-r163. https://doi.org/10.1530/eje-20-0974

    Article  CAS  Google Scholar 

  16. American Diabetes Association (2021) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2021. Diabetes Care 1:S15–S33. https://doi.org/10.2337/dc21-S002

    Article  Google Scholar 

  17. Dungan KM, Braithwaite SS, Preiser JC (2009) Stress hyperglycaemia. Lancet 9677:1798–1807. https://doi.org/10.1016/s0140-6736(09)60553-5

    Article  Google Scholar 

  18. Schneider A, Löhr JM, Singer MV (2007) The M-ANNHEIM classification of chronic pancreatitis: introduction of a unifying classification system based on a review of previous classifications of the disease. J Gastroenterol 2:101–119. https://doi.org/10.1007/s00535-006-1945-4

    Article  Google Scholar 

  19. Yang X, Zhang R, Jin T, Zhu P, Yao L, Li L et al (2022) Stress hyperglycemia is independently associated with persistent organ failure in acute pancreatitis. Dig Dis Sci 5:1879–1889. https://doi.org/10.1007/s10620-021-06982-8

    Article  CAS  Google Scholar 

  20. Shore S, Borgerding JA, Gylys-Colwell I, McDermott K, Ho PM, Tillquist MN et al (2014) Association between hyperglycemia at admission during hospitalization for acute myocardial infarction and subsequent diabetes: insights from the veterans administration cardiac care follow-up clinical study. Diabetes Care 2:409–418. https://doi.org/10.2337/dc13-1125

    Article  Google Scholar 

  21. Gornik I, Vujaklija-Brajkovic A, Renar IP, Gasparovic V (2010) A prospective observational study of the relationship of critical illness associated hyperglycaemia in medical ICU patients and subsequent development of type 2 diabetes. Crit Care 4:R130. https://doi.org/10.1186/cc9101

    Article  Google Scholar 

  22. MacIntyre EJ, Majumdar SR, Gamble JM, Minhas-Sandhu JK, Marrie TJ, Eurich DT (2012) Stress hyperglycemia and newly diagnosed diabetes in 2124 patients hospitalized with pneumonia. Am J Med 10:1036.e1017–1023. https://doi.org/10.1016/j.amjmed.2012.01.026

    Article  Google Scholar 

  23. Wang X, Cheng FTF, Lam TYT, Liu Y, Huang D, Liu X et al (2022) Stress hyperglycemia is associated with an increased risk of subsequent development of diabetes among bacteremic and nonbacteremic patients. Diabetes Care 6:1438–1444. https://doi.org/10.2337/dc21-1682

    Article  CAS  Google Scholar 

  24. Petrov MS, Yadav D (2019) Global epidemiology and holistic prevention of pancreatitis. Nat Rev Gastroenterol Hepatol 3:175–184. https://doi.org/10.1038/s41575-018-0087-5

    Article  Google Scholar 

  25. Cho J, Scragg R, Petrov MS (2019) Risk of mortality and hospitalization after post-pancreatitis diabetes mellitus vs type 2 diabetes mellitus: a population-based matched cohort study. Am J Gastroenterol 5:804–812. https://doi.org/10.14309/ajg.0000000000000225

    Article  Google Scholar 

  26. Woodmansey C, McGovern AP, McCullough KA, Whyte MB, Munro NM, Correa AC et al (2017) Incidence, demographics, and clinical characteristics of diabetes of the exocrine pancreas (type 3c): a retrospective cohort study. Diabetes Care 11:1486–1493. https://doi.org/10.2337/dc17-0542

    Article  Google Scholar 

  27. Zhi M, Zhu X, Lugea A, Waldron RT, Pandol SJ, Li L (2019) Incidence of new onset diabetes mellitus secondary to acute pancreatitis: a systematic review and meta-analysis. Front Physiol. https://doi.org/10.3389/fphys.2019.00637

    Article  PubMed  PubMed Central  Google Scholar 

  28. Winter Gasparoto RC, Racy Mde C, De Campos T (2015) Long-term outcomes after acute necrotizing pancreatitis: what happens to the pancreas and to the patient? Jop 2:159–166. https://doi.org/10.6092/1590-8577/2958

    Article  Google Scholar 

  29. Umapathy C, Raina A, Saligram S, Tang G, Papachristou GI, Rabinovitz M et al (2016) Natural history after acute necrotizing pancreatitis: a large US tertiary care experience. J Gastrointest Surg 11:1844–1853. https://doi.org/10.1007/s11605-016-3264-2

    Article  Google Scholar 

  30. Tu J, Zhang J, Ke L, Yang Y, Yang Q, Lu G et al (2017) Endocrine and exocrine pancreatic insufficiency after acute pancreatitis: long-term follow-up study. BMC Gastroenterol 1:114. https://doi.org/10.1186/s12876-017-0663-0

    Article  CAS  Google Scholar 

  31. Barth E, Albuszies G, Baumgart K, Matejovic M, Wachter U, Vogt J et al (2007) Glucose metabolism and catecholamines. Crit Care Med 9(Suppl):S508-518. https://doi.org/10.1097/01.Ccm.0000278047.06965.20

    Article  Google Scholar 

  32. Andrews RC, Walker BR (1999) Glucocorticoids and insulin resistance: old hormones, new targets. Clin Sci (Lond) 5:513–523. https://doi.org/10.1042/cs0960513

    Article  Google Scholar 

  33. Qing H, Desrouleaux R, Israni-Winger K, Mineur YS, Fogelman N, Zhang C et al (2020) Origin and function of stress-induced IL-6 in murine models. Cell 2:372-387.e314. https://doi.org/10.1016/j.cell.2020.05.054

    Article  CAS  Google Scholar 

  34. Stentz FB, Umpierrez GE, Cuervo R, Kitabchi AE (2004) Proinflammatory cytokines, markers of cardiovascular risks, oxidative stress, and lipid peroxidation in patients with hyperglycemic crises. Diabetes 8:2079–2086. https://doi.org/10.2337/diabetes.53.8.2079

    Article  Google Scholar 

  35. Liu C, Feng X, Li Q, Wang Y, Li Q, Hua M (2016) Adiponectin, TNF-α and inflammatory cytokines and risk of type 2 diabetes: a systematic review and meta-analysis. Cytokine. https://doi.org/10.1016/j.cyto.2016.06.028

    Article  PubMed  PubMed Central  Google Scholar 

  36. Gillies N, Pendharkar SA, Asrani VM, Mathew J, Windsor JA, Petrov MS (2016) Interleukin-6 is associated with chronic hyperglycemia and insulin resistance in patients after acute pancreatitis. Pancreatology 5:748–755. https://doi.org/10.1016/j.pan.2016.06.661

    Article  CAS  Google Scholar 

  37. Xu E, Pereira MMA, Karakasilioti I, Theurich S, Al-Maarri M, Rappl G et al (2017) Temporal and tissue-specific requirements for T-lymphocyte IL-6 signalling in obesity-associated inflammation and insulin resistance. Nat Commun. https://doi.org/10.1038/ncomms14803

    Article  PubMed  PubMed Central  Google Scholar 

  38. Miranda PJ, DeFronzo RA, Califf RM, Guyton JR (2005) Metabolic syndrome: definition, pathophysiology, and mechanisms. Am Heart J 1:33–45. https://doi.org/10.1016/j.ahj.2004.07.013

    Article  CAS  Google Scholar 

  39. Gehrke N, Schattenberg JM (2020) Metabolic inflammation-a role for hepatic inflammatory pathways as drivers of comorbidities in nonalcoholic fatty liver disease? Gastroenterology 7:1929-1947.e1926. https://doi.org/10.1053/j.gastro.2020.02.020

    Article  CAS  Google Scholar 

  40. Ballestri S, Zona S, Targher G, Romagnoli D, Baldelli E, Nascimbeni F et al (2016) Nonalcoholic fatty liver disease is associated with an almost twofold increased risk of incident type 2 diabetes and metabolic syndrome. Evidence from a systematic review and meta-analysis. J Gastroenterol Hepatol 5:936–944. https://doi.org/10.1111/jgh.13264

    Article  CAS  Google Scholar 

  41. Kotronen A, Juurinen L, Hakkarainen A, Westerbacka J, Cornér A, Bergholm R et al (2008) Liver fat is increased in type 2 diabetic patients and underestimated by serum alanine aminotransferase compared with equally obese nondiabetic subjects. Diabetes Care 1:165–169. https://doi.org/10.2337/dc07-1463

    Article  CAS  Google Scholar 

  42. Speelman T, Dale L, Louw A, Verhoog NJD (2022) The association of acute phase proteins in stress and inflammation-induced T2D. Cells. https://doi.org/10.3390/cells11142163

    Article  PubMed  PubMed Central  Google Scholar 

  43. Gillies NA, Pendharkar SA, Singh RG, Asrani VM, Petrov MS (2017) Lipid metabolism in patients with chronic hyperglycemia after an episode of acute pancreatitis. Diabetes Metab Syndr. https://doi.org/10.1016/j.dsx.2016.12.037

    Article  PubMed  Google Scholar 

  44. Pendharkar SA, Asrani VM, Murphy R, Cutfield R, Windsor JA, Petrov MS (2017) The role of gut-brain axis in regulating glucose metabolism after acute pancreatitis. Clin Transl Gastroenterol 1:e210. https://doi.org/10.1038/ctg.2016.63

    Article  CAS  Google Scholar 

  45. Sand J, Nordback I (2009) Acute pancreatitis: risk of recurrence and late consequences of the disease. Nat Rev Gastroenterol Hepatol 8:470–477. https://doi.org/10.1038/nrgastro.2009.106

    Article  Google Scholar 

  46. Lin YC, Kor CT, Su WW, Hsu YC (2018) Risk factors and prediction score for chronic pancreatitis: a nationwide population-based cohort study. World J Gastroenterol 44:5034–5045. https://doi.org/10.3748/wjg.v24.i44.5034

    Article  Google Scholar 

  47. Sankaran SJ, Xiao AY, Wu LM, Windsor JA, Forsmark CE, Petrov MS (2015) Frequency of progression from acute to chronic pancreatitis and risk factors: a meta-analysis. Gastroenterology 6:1490-1500.e1491. https://doi.org/10.1053/j.gastro.2015.07.066

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank all staffs for their support.

Funding

This work was supported by National Natural Science Foundation of China (81970717 and 82170845).

Author information

Author notes

  1. Jun Zhang and Xiaoyuan Wang have contributed equally to this work.

Authors and Affiliations

  1. Department of Endocrinology, Zhongda Hospital, School of Medicine, Southeast University, Nanjing, China

    Jun Zhang, Xiaoyuan Wang, Yingqi Lv & Ling Li

  2. Institute of Glucose and Lipid Metabolism, Southeast University, Nanjing, China

    Jun Zhang, Xiaoyuan Wang, Yingqi Lv & Ling Li

  3. Department of Endocrinology, Changji Branch, First Affiliated Hospital of Xinjiang Medical University, Xinjiang, China

    Jiaying Hou & Xianghui Su

  4. Department of Endocrinology, Hunan Provincial People’s Hospital, First Affiliated Hospital of Hunan Normal University, Changsha, Hunan, China

    Chi Zhang

Authors
  1. Jun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoyuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingqi Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiaying Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xianghui Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ling Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JZ: Conceptualization, Data curation, and writing—original draft preparation. XW: Formal analysis and investigation; JH, YL, CZ, and XS: data collection and writing—review; LL: contributed to the design of the study, discussion, reviewed and edited the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ling Li.

Ethics declarations

Competing interests

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of this study.

Ethical statements

The study has been approved by the Ethics Committee of Zhongda Hospital, Southeast University (Approval No: 2022ZDSYLL017-P01). The study protocol conformed to the tenets of the Declaration of Helsinki; informed consent was obtained from all patients enrolled.

Human and animal rights statement and Informed consent

Informed consent was obtained from all patients enrolled; animals have not been included in the present study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Wang, X., Lv, Y. et al. Impact of stress hyperglycemia on long-term prognosis in acute pancreatitis without diabetes. Intern Emerg Med 19, 681–688 (2024). https://doi.org/10.1007/s11739-023-03524-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11739-023-03524-0

Keywords

Search

Navigation