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Digestive Diseases and Sciences
Published in: Digestive Diseases and Sciences 7/2019

Open Access 01-07-2019 | Acute Pancreatitis | Original Article

Exocrine Pancreatic Insufficiency Following Acute Pancreatitis: Systematic Review and Meta-Analysis

Authors: Wei Huang, Daniel de la Iglesia-García, Iria Baston-Rey, Cristina Calviño-Suarez, Jose Lariño-Noia, Julio Iglesias-Garcia, Na Shi, Xiaoying Zhang, Wenhao Cai, Lihui Deng, Danielle Moore, Vikesh K. Singh, Qing Xia, John A. Windsor, J. Enrique Domínguez-Muñoz, Robert Sutton

Published in: Digestive Diseases and Sciences | Issue 7/2019

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Abstract

Background/Objectives

The epidemiology of exocrine pancreatic insufficiency (EPI) after acute pancreatitis (AP) is uncertain. We sought to determine the prevalence, progression, etiology and pancreatic enzyme replacement therapy (PERT) requirements for EPI during follow-up of AP by systematic review and meta-analysis.

Methods

Scopus, Medline and Embase were searched for prospective observational studies or randomized clinical trials (RCTs) of PERT reporting EPI during the first admission (between the start of oral refeeding and before discharge) or follow-up (≥ 1 month of discharge) for AP in adults. EPI was diagnosed by direct and/or indirect laboratory exocrine pancreatic function tests.

Results

Quantitative data were analyzed from 370 patients studied during admission (10 studies) and 1795 patients during follow-up (39 studies). The pooled prevalence of EPI during admission was 62% (95% confidence interval: 39–82%), decreasing significantly during follow-up to 35% (27–43%; risk difference: − 0.34, − 0.53 to − 0.14). There was a two-fold increase in the prevalence of EPI with severe compared with mild AP, and it was higher in patients with pancreatic necrosis and those with an alcohol etiology. The prevalence decreased during recovery, but persisted in a third of patients. There was no statistically significant difference between EPI and new-onset pre-diabetes/diabetes (risk difference: 0.8, 0.7–1.1, P = 0.33) in studies reporting both. Sensitivity analysis showed fecal elastase-1 assay detected significantly fewer patients with EPI than other tests.

Conclusions

The prevalence of EPI during admission and follow-up is substantial in patients with a first attack of AP. Unanswered questions remain about the way this is managed, and further RCTs are indicated.
Appendix
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Literature
1.
Yadav D, O’Connell M, Papachristou GI. Natural history following the first attack of acute pancreatitis. Am J Gastroenterol. 2012;107:1096–1103.CrossRefPubMed
2.
Das SL, Singh PP, Phillips AR, et al. Newly diagnosed diabetes mellitus after acute pancreatitis: a systematic review and meta-analysis. Gut. 2014;63:818–831.CrossRefPubMed
3.
Pendharkar SA, Salt K, Plank LD, et al. Quality of life after acute pancreatitis: a systematic review and meta-analysis. Pancreas. 2014;43:1194–1200.CrossRefPubMed
4.
Machicado JD, Gougol A, Stello K, et al. Acute pancreatitis has a long-term deleterious effect on physical health related quality of life. Clin Gastroenterol Hepatol. 2017;15:1435–1443.CrossRefPubMed
5.
Sankaran SJ, Xiao AY, Wu LM, et al. Frequency of progression from acute to chronic pancreatitis and risk factors: a meta-analysis. Gastroenterology. 2015;149:1490–1500.CrossRefPubMed
6.
Hollemans RA, Hallensleben NDL, Mager DJ, et al. Pancreatic exocrine insufficiency following acute pancreatitis: systematic review and study level meta-analysis. Pancreatology. 2018;18:253–262.CrossRefPubMed
7.
Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–269.CrossRefPubMed
8.
Chowdhury RS, Forsmark CE. Review article: pancreatic function testing. Aliment Pharmacol Ther. 2003;17:733–750.CrossRefPubMed
9.
10.
11.
Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: Is blinding necessary? Control Clin Trials. 1996;17:1–12.CrossRefPubMed
12.
de la Iglesia-Garcia D, Huang W, Szatmary P, et al. Efficacy of pancreatic enzyme replacement therapy in chronic pancreatitis: systematic review and meta-analysis. Gut. 2017;66:1354–1355.PubMed
13.
Vipperla K, Papachristou GI, Easler J, et al. Risk of and factors associated with readmission after a sentinel attack of acute pancreatitis. Clin Gastroenterol Hepatol. 2014;12:1911–1919.CrossRefPubMed
14.
Das SL, Kennedy JI, Murphy R, et al. Relationship between the exocrine and endocrine pancreas after acute pancreatitis. World J Gastroenterol. 2014;20:17196–17205.CrossRefPubMedPubMedCentral
15.
Bradley EL 3rd. A clinically based classification system for acute pancreatitis. Summary of the International Symposium on Acute Pancreatitis, Atlanta, Ga, September 11 through 13, 1992. Arch Surg. 1993;128:586–590.CrossRefPubMed
16.
Banks PA, Bollen TL, Dervenis C, et al. Classification of acute pancreatitis–2012: revision of the Atlanta classification and definitions by international consensus. Gut. 2013;62:102–111.CrossRefPubMed
17.
Guo Q, Li A, Xia Q, et al. The role of organ failure and infection in necrotizing pancreatitis: a prospective study. Ann Surg. 2014;259:1201–1207.CrossRefPubMed
18.
Raraty MG, Halloran CM, Dodd S, et al. Minimal access retroperitoneal pancreatic necrosectomy: improvement in morbidity and mortality with a less invasive approach. Ann Surg. 2010;251:787–793.CrossRefPubMed
19.
van Grinsven J, van Santvoort HC, Boermeester MA, et al. Timing of catheter drainage in infected necrotizing pancreatitis. Nat Rev Gastroenterol Hepatol. 2016;13:306–312.CrossRefPubMed
20.
21.
Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. BMJ. 2001;323:101–105.CrossRefPubMedPubMedCentral
22.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–1101.CrossRefPubMed
23.
24.
Seligson U, Ihre T, Lundh G. Prognosis in acute haemorrhagic, necrotizing pancreatitis. Acta Chir Scand. 1982;148:423–429.PubMed
25.
Mitchell CJ, Playforth MJ, Kelleher J, et al. Functional recovery of the exocrine pancreas after acute pancreatitis. Scand J Gastroenterol. 1983;18:5–8.CrossRefPubMed
26.
Angelini G, Pederzoli P, Caliari S, et al. Long-term outcome of acute necrohemorrhagic pancreatitis. A 4-year follow-up. Digestion. 1984;30:131–137.CrossRefPubMed
27.
Arenas M, Perez-Mateo M, Graells ML, et al. Evaluation of exocrine pancreatic function by the PABA test in patients with acute pancreatitis. Rev Esp Enferm Apar Dig. 1986;70:43–48.PubMed
28.
Büchler M, Hauke A, Malfertheiner P. Follow-Up After Acute Pancreatitis: Morphology and Function. Berlin: Springer; 1987:367.CrossRef
29.
Garnacho JM, Aznar AM, Corrochano MDD, et al. Evolucion de la funcion exocrina del pancreas tras la pancreatitis aguda. Factores pronosticos. Rev Esp Enferm Apar Dig. 1989;76:19–24.
30.
Airey MC, McMahon MJ. The influence of granular pancreatin upon endocrine and exocrine pancreatic function during convalescence from acute pancreatitis. In: Lankisch PG (ed). Pancreatic Enzymes in Health and Disease. Berlin: Springer;1991:131–138.CrossRef
31.
Glasbrenner B, Büchler M, Uhl W, et al. Exocrine pancreatic function in the early recovery phase of acute oedematous pancreatitis. Eur J Gastroenterol Hepatol. 1992;4:563–567.
32.
Bozkurt T, Maroske D, Adler G. Exocrine pancreatic function after recovery from necrotizing pancreatitis. Hepatogastroenterology. 1995;42:55–58.PubMed
33.
Seidensticker F, Otto J, Lankisch PG. Recovery of the pancreas after acute pancreatitis is not necessarily complete. Int J Pancreatol. 1995;17:225–229.PubMed
34.
Malecka-Panas E, Juszynski A, Wilamski E. Acute alcoholic pancreatitis does not lead to complete recovery. Mater Med Pol. 1996;28:64–68.PubMed
35.
Malecka-Panas E, Juszynski A, Wilamski E. The natural course of acute gallstone pancreatitis. Mater Med Pol. 1996;28:8–12.PubMed
36.
John KD, Segal I, Hassan H, et al. Acute pancreatitis in Sowetan Africans. A disease with high mortality and morbidity. Int J Pancreatol. 1997;21:149–155.PubMed
37.
Tsiotos GG, Luque-de Leon E, Sarr MG. Long-term outcome of necrotizing pancreatitis treated by necrosectomy. Br J Surg. 1998;85:1650–1653.CrossRefPubMed
38.
Appelros S, Lindgren S, Borgstrom A. Short and long term outcome of severe acute pancreatitis. Eur J Surg. 2001;167:281–286.CrossRefPubMed
39.
Ibars EP, Sanchez de Rojas EA, Quereda LA, et al. Pancreatic function after acute biliary pancreatitis: Does it change? World J Surg. 2002;26:479–486.CrossRefPubMed
40.
Boreham B, Ammori BJ. A prospective evaluation of pancreatic exocrine function in patients with acute pancreatitis: correlation with extent of necrosis and pancreatic endocrine insufficiency. Pancreatology. 2003;3:303–308.CrossRefPubMed
41.
Napolitano L, Di Donato E, Faricelli R, et al. Experience on the pancreatic function after an episode of acute biliary oedematous pancreatitis. Ann Ital Chir. 2003;74:695–697.PubMed
42.
Sabater L, Pareja E, Aparisi L, et al. Pancreatic function after severe acute biliary pancreatitis: the role of necrosectomy. Pancreas. 2004;28:65–68.CrossRefPubMed
43.
Migliori M, Pezzilli R, Tomassetti P, et al. Exocrine pancreatic function after alcoholic or biliary acute pancreatitis. Pancreas. 2004;28:359–363.CrossRefPubMed
44.
Bavare C, Prabhu R, Supe A. Early morphological and functional changes in pancreas following necrosectomy for acute severe necrotizing pancreatitis. Indian J Gastroenterol. 2004;23:203–205.PubMed
45.
Symersky T, van Hoorn B, Masclee AA. The outcome of a long-term follow-up of pancreatic function after recovery from acute pancreatitis. JOP. 2006;7:447–453.PubMed
46.
Reszetow J, Hac S, Dobrowolski S, et al. Biliary versus alcohol-related infected pancreatic necrosis: similarities and differences in the follow-up. Pancreas. 2007;35:267–272.CrossRefPubMed
47.
Reddy MS, Singh S, Singh R, et al. Morphological and functional outcome after pancreatic necrosectomy and lesser sac lavage for necrotizing pancreatitis. Indian J Gastroenterol. 2007;26:217–220.PubMed
48.
Pelli H, Lappalainen-Lehto R, Piironen A, et al. Pancreatic damage after the first episode of acute alcoholic pancreatitis and its association with the later recurrence rate. Pancreatology. 2009;9:245–251.CrossRefPubMed
49.
Pezzilli R, Simoni P, Casadei R, et al. Exocrine pancreatic function during the early recovery phase of acute pancreatitis. Hepatobiliary Pancreat Dis Int. 2009;8:316–319.PubMed
50.
Gupta R, Wig JD, Bhasin DK, et al. Severe acute pancreatitis: the life after. J Gastrointest Surg. 2009;13:1328–1336.CrossRefPubMed
51.
Uomo G, Gallucci F, Madrid E, et al. Pancreatic functional impairment following acute necrotizing pancreatitis: long-term outcome of a non-surgically treated series. Dig Liver Dis. 2010;42:149–152.CrossRefPubMed
52.
Andersson B, Pendse ML, Andersson R. Pancreatic function, quality of life and costs at long-term follow-up after acute pancreatitis. World J Gastroenterol. 2010;16:4944–4951.CrossRefPubMedPubMedCentral
53.
Xu Y, Wu D, Zeng Y, et al. Pancreatic exocrine function and morphology following an episode of acute pancreatitis. Pancreas. 2012;41:922–927.CrossRefPubMed
54.
Garip G, Sarandol E, Kaya E. Effects of disease severity and necrosis on pancreatic dysfunction after acute pancreatitis. World J Gastroenterol. 2013;19:8065–8070.CrossRefPubMedPubMedCentral
55.
Kahl S, Schutte K, Glasbrenner B, et al. The effect of oral pancreatic enzyme supplementation on the course and outcome of acute pancreatitis: a randomized, double-blind parallel-group study. JOP. 2014;15:165–174.PubMed
56.
Vujasinovic M, Tepes B, Makuc J, et al. Pancreatic exocrine insufficiency, diabetes mellitus and serum nutritional markers after acute pancreatitis. World J Gastroenterol. 2014;20:18432–18438.CrossRefPubMedPubMedCentral
57.
Winter Gasparoto RC, Racy Mde C, De Campos T. Long-term outcomes after acute necrotizing pancreatitis: What happens to the pancreas and to the patient? JOP. 2015;16:159–166.PubMed
58.
Chandrasekaran P, Gupta R, Shenvi S, et al. Prospective comparison of long term outcomes in patients with severe acute pancreatitis managed by operative and non operative measures. Pancreatology. 2015;15:478–484.CrossRefPubMed
59.
Ermolov AS, Blagovestnov DA, Rogal ML, et al. Long-term results of severe acute pancreatitis management. Khirurgiia (Mosk) 2016;10:11–15.
60.
Nikkola J, Laukkarinen J, Lahtela J, et al. The long-term prospective follow-up of pancreatic function after the first episode of acute alcoholic pancreatitis: recurrence predisposes one to pancreatic dysfunction and pancreatogenic diabetes. J Clin Gastroenterol. 2017;51:183–190.CrossRefPubMed
61.
Koziel D, Suliga E, Grabowska U, et al. Morphological and functional consequences and quality of life following severe acute pancreatitis. Ann Ital Chir. 2017;6:403–411.PubMed
62.
Tu J, Zhang J, Ke L, et al. Endocrine and exocrine pancreatic insufficiency after acute pancreatitis: long-term follow-up study. BMC Gastroenterol. 2017;17:114.CrossRefPubMedPubMedCentral
63.
Braganza J, Critchley M, Howat HT, et al. An evaluation of 75 Se selenomethionine scanning as a test of pancreatic function compared with the secretin-pancreozymin test. Gut. 1973;14:383–389.CrossRefPubMedPubMedCentral
64.
van Brunschot S, van Grinsven J, van Santvoort HC, et al. Endoscopic or surgical step-up approach for infected necrotising pancreatitis: a multicentre randomised trial. Lancet. 2018;391:51–58.CrossRefPubMed
65.
Murtaugh LC, Keefe MD. Regeneration and repair of the exocrine pancreas. Annu Rev Physiol. 2015;77:229–249.CrossRefPubMed
66.
Ho TW, Wu JM, Kuo TC, et al. Change of both endocrine and exocrine insufficiencies after acute pancreatitis in non-diabetic patients: a nationwide population-based study. Medicine (Baltimore). 2015;94:e1123.CrossRef
67.
Umapathy C, Raina A, Saligram S, et al. Natural History after acute necrotizing pancreatitis: a large US tertiary care experience. J Gastrointest Surg. 2016;20:1844–1853.CrossRefPubMed
68.
Castoldi L, De Rai P, Zerbi A, et al. Long term outcome of acute pancreatitis in Italy: results of a multicentre study. Dig Liver Dis. 2013;45:827–832.CrossRefPubMed
69.
Li J, Zhou C, Wang R, et al. Irreversible exocrine pancreatic insufficiency in alcoholic rats without chronic pancreatitis after alcohol withdrawal. Alcohol Clin Exp Res. 2010;34:1843–1848.CrossRefPubMed
70.
71.
Yadav D, Whitcomb DC. The role of alcohol and smoking in pancreatitis. Nat Rev Gastroenterol Hepatol. 2010;7:131–145.CrossRefPubMed
72.
Cote GA, Yadav D, Slivka A, et al. Alcohol and smoking as risk factors in an epidemiology study of patients with chronic pancreatitis. Clin Gastroenterol Hepatol. 2011;9:266–273. (quiz e27).CrossRefPubMed
73.
Nikkola J, Raty S, Laukkarinen J, et al. Abstinence after first acute alcohol-associated pancreatitis protects against recurrent pancreatitis and minimizes the risk of pancreatic dysfunction. Alcohol Alcohol. 2013;48:483–486.CrossRefPubMed
74.
Metadata
Title
Exocrine Pancreatic Insufficiency Following Acute Pancreatitis: Systematic Review and Meta-Analysis
Authors
Wei Huang
Daniel de la Iglesia-García
Iria Baston-Rey
Cristina Calviño-Suarez
Jose Lariño-Noia
Julio Iglesias-Garcia
Na Shi
Xiaoying Zhang
Wenhao Cai
Lihui Deng
Danielle Moore
Vikesh K. Singh
Qing Xia
John A. Windsor
J. Enrique Domínguez-Muñoz
Robert Sutton
Publication date
01-07-2019
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 7/2019
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-019-05568-9

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