Exocrine Pancreatic Insufficiency Following Acute Pancreatitis: Systematic Review and Meta-Analysis.
Acute pancreatitis
Exocrine pancreatic insufficiency
Necrotizing pancreatitis
Pancreatic enzyme replacement therapy
Severe pancreatitis
Journal
Digestive diseases and sciences
ISSN: 1573-2568
Titre abrégé: Dig Dis Sci
Pays: United States
ID NLM: 7902782
Informations de publication
Date de publication:
07 2019
07 2019
Historique:
received:
23
10
2018
accepted:
26
02
2019
pubmed:
5
6
2019
medline:
24
12
2019
entrez:
5
6
2019
Statut:
ppublish
Résumé
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. 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. 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. 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.
Sections du résumé
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.
Identifiants
pubmed: 31161524
doi: 10.1007/s10620-019-05568-9
pii: 10.1007/s10620-019-05568-9
pmc: PMC6584228
doi:
Types de publication
Journal Article
Meta-Analysis
Research Support, Non-U.S. Gov't
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1985-2005Subventions
Organisme : Department of Health
ID : EME/15/20/01
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Références
Yadav D, O’Connell M, Papachristou GI. Natural history following the first attack of acute pancreatitis. Am J Gastroenterol. 2012;107:1096–1103.
doi: 10.1038/ajg.2012.126
pubmed: 22613906
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.
doi: 10.1136/gutjnl-2013-305062
pubmed: 23929695
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.
doi: 10.1097/MPA.0000000000000189
pubmed: 25333403
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.
doi: 10.1016/j.cgh.2017.05.037
pubmed: 28579182
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.
doi: 10.1053/j.gastro.2015.07.066
pubmed: 26299411
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.
doi: 10.1016/j.pan.2018.02.009
pubmed: 29482892
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.
doi: 10.7326/0003-4819-151-4-200908180-00135
pubmed: 19622511
Chowdhury RS, Forsmark CE. Review article: pancreatic function testing. Aliment Pharmacol Ther. 2003;17:733–750.
doi: 10.1046/j.1365-2036.2003.01495.x
pubmed: 12641496
Keller J, Layer P. Diagnosis of pancreatic exocrine insufficiency in chronic pancreatitis. Pancreapedia. 2015. https://doi.org/10.3998/panc.2015.37 .
doi: 10.3998/panc.2015.37
Wells G, Shea B, O’Connell D, et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp . Accessed 1 June 2018.
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.
doi: 10.1016/0197-2456(95)00134-4
pubmed: 8721797
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: 27941156
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.
doi: 10.1016/j.cgh.2014.04.035
pubmed: 24815327
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.
doi: 10.3748/wjg.v20.i45.17196
pubmed: 25493036
pmcid: 4258592
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.
doi: 10.1001/archsurg.1993.01420170122019
pubmed: 8489394
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.
doi: 10.1136/gutjnl-2012-302779
pubmed: 23100216
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.
doi: 10.1097/SLA.0000000000000264
pubmed: 24169172
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.
doi: 10.1097/SLA.0b013e3181d96c53
pubmed: 20395850
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.
doi: 10.1038/nrgastro.2016.23
pubmed: 26956064
Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560.
doi: 10.1136/bmj.327.7414.557
pubmed: 12958120
pmcid: 192859
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.
doi: 10.1136/bmj.323.7304.101
pubmed: 11451790
pmcid: 1120714
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–1101.
doi: 10.2307/2533446
pubmed: 7786990
Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.
doi: 10.1136/bmj.315.7109.629
pubmed: 9310563
pmcid: 2127453
Seligson U, Ihre T, Lundh G. Prognosis in acute haemorrhagic, necrotizing pancreatitis. Acta Chir Scand. 1982;148:423–429.
pubmed: 7180338
Mitchell CJ, Playforth MJ, Kelleher J, et al. Functional recovery of the exocrine pancreas after acute pancreatitis. Scand J Gastroenterol. 1983;18:5–8.
doi: 10.3109/00365528309181549
pubmed: 6609418
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.
doi: 10.1159/000199097
pubmed: 6500192
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: 3488572
Büchler M, Hauke A, Malfertheiner P. Follow-Up After Acute Pancreatitis: Morphology and Function. Berlin: Springer; 1987:367.
doi: 10.1007/978-3-642-83027-3_50
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.
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.
doi: 10.1007/978-3-642-76097-6_15
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.
Bozkurt T, Maroske D, Adler G. Exocrine pancreatic function after recovery from necrotizing pancreatitis. Hepatogastroenterology. 1995;42:55–58.
pubmed: 7782037
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: 7642969
Malecka-Panas E, Juszynski A, Wilamski E. Acute alcoholic pancreatitis does not lead to complete recovery. Mater Med Pol. 1996;28:64–68.
pubmed: 9088129
Malecka-Panas E, Juszynski A, Wilamski E. The natural course of acute gallstone pancreatitis. Mater Med Pol. 1996;28:8–12.
pubmed: 9088119
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: 9209956
Tsiotos GG, Luque-de Leon E, Sarr MG. Long-term outcome of necrotizing pancreatitis treated by necrosectomy. Br J Surg. 1998;85:1650–1653.
doi: 10.1046/j.1365-2168.1998.00950.x
pubmed: 9876068
Appelros S, Lindgren S, Borgstrom A. Short and long term outcome of severe acute pancreatitis. Eur J Surg. 2001;167:281–286.
doi: 10.1080/110241501300091462
pubmed: 11354320
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.
doi: 10.1007/s00268-001-0253-7
pubmed: 11910484
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.
doi: 10.1159/000071768
pubmed: 12890992
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: 15206812
Sabater L, Pareja E, Aparisi L, et al. Pancreatic function after severe acute biliary pancreatitis: the role of necrosectomy. Pancreas. 2004;28:65–68.
doi: 10.1097/00006676-200401000-00010
pubmed: 14707732
Migliori M, Pezzilli R, Tomassetti P, et al. Exocrine pancreatic function after alcoholic or biliary acute pancreatitis. Pancreas. 2004;28:359–363.
doi: 10.1097/00006676-200405000-00001
pubmed: 15097850
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: 15627657
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: 16998241
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.
doi: 10.1097/MPA.0b013e31805b8319
pubmed: 17895849
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: 18227571
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.
doi: 10.1159/000212089
pubmed: 19407478
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: 19502175
Gupta R, Wig JD, Bhasin DK, et al. Severe acute pancreatitis: the life after. J Gastrointest Surg. 2009;13:1328–1336.
doi: 10.1007/s11605-009-0901-z
pubmed: 19415400
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.
doi: 10.1016/j.dld.2009.08.007
pubmed: 19836318
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.
doi: 10.3748/wjg.v16.i39.4944
pubmed: 20954281
pmcid: 2957603
Xu Y, Wu D, Zeng Y, et al. Pancreatic exocrine function and morphology following an episode of acute pancreatitis. Pancreas. 2012;41:922–927.
doi: 10.1097/MPA.0b013e31823d7f2d
pubmed: 22481293
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.
doi: 10.3748/wjg.v19.i44.8065
pubmed: 24307801
pmcid: 3848155
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: 24618443
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.
doi: 10.3748/wjg.v20.i48.18432
pubmed: 25561813
pmcid: 4277983
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: 25791549
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.
doi: 10.1016/j.pan.2015.08.006
pubmed: 26364168
Ermolov AS, Blagovestnov DA, Rogal ML, et al. Long-term results of severe acute pancreatitis management. Khirurgiia (Mosk) 2016;10:11–15.
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.
doi: 10.1097/MCG.0000000000000564
pubmed: 28060789
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: 28768898
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.
doi: 10.1186/s12876-017-0663-0
pubmed: 29078749
pmcid: 5658961
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.
doi: 10.1136/gut.14.5.383
pubmed: 4716507
pmcid: 1412691
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.
doi: 10.1016/S0140-6736(17)32404-2
pubmed: 29108721
Murtaugh LC, Keefe MD. Regeneration and repair of the exocrine pancreas. Annu Rev Physiol. 2015;77:229–249.
doi: 10.1146/annurev-physiol-021014-071727
pubmed: 25386992
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.
doi: 10.1097/MD.0000000000001123
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.
doi: 10.1007/s11605-016-3264-2
pubmed: 27619808
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.
doi: 10.1016/j.dld.2013.03.012
pubmed: 23831129
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.
doi: 10.1111/j.1530-0277.2010.01272.x
pubmed: 20662806
Maisonneuve P, Lowenfels AB, Mullhaupt B, et al. Cigarette smoking accelerates progression of alcoholic chronic pancreatitis. Gut. 2005;54:510–514.
doi: 10.1136/gut.2004.039263
pubmed: 15753536
pmcid: 1774435
Yadav D, Whitcomb DC. The role of alcohol and smoking in pancreatitis. Nat Rev Gastroenterol Hepatol. 2010;7:131–145.
doi: 10.1038/nrgastro.2010.6
pubmed: 20125091
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).
doi: 10.1016/j.cgh.2010.10.015
pubmed: 21029787
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.
doi: 10.1093/alcalc/agt019
pubmed: 23538610
Domínguez-Muñoz JE, Hardt PD, Lerch MM, et al. Potential for screening for pancreatic exocrine insufficiency using the fecal elastase-1 test. Dig Dis Sci. 2017;62:1119–1130. https://doi.org/10.1007/s10620-017-4524 .
doi: 10.1007/s10620-017-4524-z
pubmed: 28315028