Abstract
Introduction
Gastrointestinal symptoms such as diarrhea, bloating, abdominal pain, and nausea are common after bariatric surgery (BS) and can lead to significant morbidity. While many diagnoses can explain these symptoms, post-bariatric exocrine pancreatic insufficiency (EPI) is becoming increasingly recognized as contributor to gastrointestinal symptoms. The frequency and outcomes of EPI after BS are not well understood. We investigated the prevalence and outcomes of EPI over 18 years at a tertiary bariatric referral center.
Methods
A retrospective review of patients who underwent primary or revisional BS from 2002 to 2020 was performed. Patients were included if they were suspected of having EPI or underwent fecal elastase testing (FE-1). EPI diagnosis was defined as positive FE-1 testing or improvement with empiric pancreatic enzyme replacement therapy (PERT).
Results
EPI was suspected in 261 patients, and 190 were tested via FE-1 (89.5%) or empirically treated (10.5%). EPI was diagnosed in 79 (41.6%) patients and was associated with older age and lower BMI. Therapeutic PERT was given to 65 patients diagnosed with EPI, and 56 (86.2%) patients reported improved symptoms. Patients who underwent RYGB and BPD-DS were more likely to have EPI than those after SG (47.9% and 70.0% vs 17.4%, p < 0.01). EPI diagnosis was associated with a history chronic pancreatitis. While diarrhea and abdominal pain were the most common symptoms prompting FE-1 testing, no symptoms were significantly associated with EPI. EPI was also associated with abnormal fecal fat results and treatment with bile acid sequestrants, but not small intestinal bacterial overgrowth.
Conclusion
This study highlights that exocrine pancreatic insufficiency can account to for previously unexplained GI complaints after bariatric surgery. Therefore, bariatric surgery programs should consider this diagnosis in symptomatic patients, especially following RYGB and BPD-DS. Further work to define patient factors that should prompt evaluation, optimal treatment, and prevention is necessary.





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References
Hales CM, Carroll MD, Fryar CD, Ogden CL (2020) Prevalence of obesity and severe obesity among adults: United States, 2017–2018. NCHS Data Brief (360):1–8. https://www.cdc.gov/nchs/data/databriefs/db360-h.pdf
Dewberry LC, Khoury JC, Ehrlich S, Jenkins TM, Beamish AJ, Kalkwarf HJ, Xanthakos SA, Inge T (2019) Change in gastrointestinal symptoms over the first 5 years after bariatric surgery in a multicenter cohort of adolescents. J Pediatr Surg 54:1220–1225
Ballem N, Yellumahanthi K, Wolfe M, Wesley MM, Clements RH (2009) Gastrointestinal symptom improvement after Roux-en-Y gastric bypass: long-term analysis. Surg Obes Relat Dis 5:553–558
Petereit R, Jonaitis L, Kupčinskas L, Maleckas A (2014) Gastrointestinal symptoms and eating behavior among morbidly obese patients undergoing Roux-en-Y gastric bypass. Medicina 50:118–123
Sollier C, Barsamian C, Bretault M, Poghosyan T, Rahmi G, Chevallier J-M, Bouillot J-L, Carette C, Czernichow S, Rives-Lange C (2020) Diagnostic and therapeutic management of post-gastric bypass chronic diarrhea: a systematic review. Obes Surg 30:1102–1111
Potoczna N, Harfmann S, Steffen R, Briggs R, Bieri N, Horber FF (2008) Bowel habits after bariatric surgery. Obes Surg 18:1287–1296
Edholm D, Svensson F, Näslund I, Karlsson FA, Rask E, Sundbom M (2013) Long-term results 11 years after primary gastric bypass in 384 patients. Surg Obes Relat Dis 9:708–713
El Labban S, Safadi B, Olabi A (2015) The effect of Roux-en-Y gastric bypass and sleeve gastrectomy surgery on dietary intake, food preferences, and gastrointestinal symptoms in post-surgical morbidly obese Lebanese subjects: a Cross-Sectional Pilot Study. Obes Surg 25:2393–2399
Søvik TT, Karlsson J, Aasheim ET, Fagerland MW, Björkman S, Engström M, Kristinsson J, Olbers T, Mala T (2013) Gastrointestinal function and eating behavior after gastric bypass and duodenal switch. Surg Obes Relat Dis 9:641–647
Skogar MLSM (2017) Duodenal switch is superior to gastric bypass in patients with super obesity when evaluated with the bariatric analysis and reporting outcome system (BAROS). Obes Surg 27:08–16
Bond DS, Thomas JG, Jones DB, Schumacher LM, Webster J, Evans EW, Goldschmidt AB, Vithiananthan S (2021) Ecological momentary assessment of gastrointestinal symptoms and risky eating behaviors in Roux-en-Y gastric bypass and sleeve gastrectomy patients. Surg Obes Relat Dis 17:475–483
Uribarri-Gonzalez L, Nieto-García L, Martis-Sueiro A, Dominguez-Muñoz JE (2021) Exocrine pancreatic function and dynamic of digestion after restrictive and malabsorptive bariatric surgery: a prospective, cross-sectional, and comparative study. Surg Obes Relat Dis. https://doi.org/10.1016/j.soard.2021.06.019
Borbely Y, Plebani A, Kroll D, Ghisla S, Nett PC (2016) Exocrine pancreatic insufficiency after Roux-en-Y gastric bypass. Surg Obes Relat Dis 12:790–794
Brunet E, Caixas A, Puig V (2020) Review of the management of diarrhea syndrome after a bariatric surgery. Endocrinol Diabetes Nutr (Engl Ed) 67:401–407
Domínguez-Muñoz JE (2011) Pancreatic exocrine insufficiency: diagnosis and treatment. J Gastroenterol Hepatol 26:12–16
Löhr JM, Oliver MR, Frulloni L (2013) Synopsis of recent guidelines on pancreatic exocrine insufficiency. United Eur Gastroenterol J 1:79–83
Keller J (2005) Human pancreatic exocrine response to nutrients in health and disease. Gut 54:1–28
Domínguez-Muñoz JE (2007) Pancreatic enzyme therapy for pancreatic exocrine insufficiency. Curr Gastroenterol Rep 9:116–122
Forsmark CE (2018) Diagnosis and management of exocrine pancreatic insufficiency. Curr Treat Options Gastroenterol 16:306–315
Vanga RR, Tansel A, Sidiq S, El-Serag HB, Othman MO (2018) Diagnostic performance of measurement of fecal elastase-1 in detection of exocrine pancreatic insufficiency: systematic review and meta-analysis. Clin Gastroenterol Hepatol 16:1220-1228.e1224
Naruse S, Ishiguro H, Ko SBH, Yoshikawa T, Yamamoto T, Yamamoto A, Futakuchi S, Goto H, Saito Y, Takahashi S (2006) Fecal pancreatic elastase: a reproducible marker for severe exocrine pancreatic insufficiency. J Gastroenterol 41:901–908
Capurso G, Traini M, Piciucchi M, Signoretti M, Arcidiacono PG (2019) Exocrine pancreatic insufficiency: prevalence, diagnosis, and management. Clin Exp Gastroenterol 12:129–139
Loser C, Mollgaard A, Folsch UR (1996) Faecal elastase 1: a novel, highly sensitive, and specific tubeless pancreatic function test. Gut 39:580–586
Quercia I, Dutia R, Kotler DP, Belsley S, Laferrere B (2014) Gastrointestinal changes after bariatric surgery. Diabetes Metab 40:87–94
Meek CL, Lewis HB, Reimann F, Gribble FM, Park AJ (2016) The effect of bariatric surgery on gastrointestinal and pancreatic peptide hormones. Peptides 77:28–37
Vujasinovic M, Valente R, Thorell A, Rutkowski W, Haas SL, Arnelo U, Martin L, Lohr JM (2017) Pancreatic exocrine insufficiency after bariatric surgery. Nutrients 9:1241
Miroslav VGK, Brane B, Barbara R, Bojan T, Sasa R, Andreja K (2016) Is pancreatic exocrine insuffiency a cause of malabsorption in patients after bariatric surgery? J Pancreas 17:402–405
Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. https://doi.org/10.1016/j.jbi.2008.08.010
Vujasinovic M, Valente R, Thorell A, Rutkowski W, Haas S, Arnelo U, Martin L, Löhr JM (2017) Pancreatic exocrine insufficiency after bariatric surgery. Nutrients 9:1241
Ozmen MM, Gundogdu E, Guldogan CE, Ozmen F (2021) The effect of bariatric surgery on exocrine pancreatic function. Obes Surg 31:580–587
Domínguez-Muñoz JE (2009) Pancreatic enzyme replacement therapy: exocrine pancreatic insufficiency after gastrointestinal surgery. HPB 11:3–6
Berstad A, Erchinger F, Hjartholm A-S (2010) Fecal fat determination with a modified titration method. Scand J Gastroenterol 45:603–607
VdK JH (1953) Quantitative determination of the saturated and unsaturated higher fatty acids in fecal fat. Scand J Clin Lab Invest 5:30–36
Rezaie A, Buresi M, Lembo A, Lin H, McCallum R, Rao S, Schmulson M, Valdovinos M, Zakko S, Pimentel M (2017) Hydrogen and methane-based breath testing in gastrointestinal disorders: the north American consensus. Am J Gastroenterol 112:775–784
Barkun AN, Love J, Gould M, Pluta H, Steinhart H (2013) Bile acid malabsorption in chronic diarrhea: pathophysiology and treatment. Can J Gastroenterol 27:653–659
Williams AJ, Merrick MV, Eastwood MA (1991) Idiopathic bile acid malabsorption–a review of clinical presentation, diagnosis, and response to treatment. Gut 32:1004–1006
Jacobsen SH, Olesen SC, Dirksen C, Jorgensen NB, Bojsen-Moller KN, Kielgast U, Worm D, Almdal T, Naver LS, Hvolris LE, Rehfeld JF, Wulff BS, Clausen TR, Hansen DL, Holst JJ, Madsbad S (2012) Changes in gastrointestinal hormone responses, insulin sensitivity, and beta-cell function within 2 weeks after gastric bypass in non-diabetic subjects. Obes Surg 22:1084–1096
Chaudhary A, Dominguez-Munoz JE, Layer P, Lerch MM (2020) Pancreatic exocrine insufficiency as a complication of gastrointestinal surgery and the impact of pancreatic enzyme replacement therapy. Dig Dis 38:53–68
Hill PG (2001) Faecal fat: time to give it up. Ann Clin Biochem 38:164–167
Rothenbacher D, Löw M, Hardt PD, Klör HU, Ziegler H, Brenner H (2005) Prevalence and determinants of exocrine pancreatic insufficiency among older adults: results of a population-based study. Scand J Gastroenterol 40:697–704
James Toouli AVB, Oliver MR, Pearce CB, Wilson JS, Wray NH (2010) Management of pancreatic exocrine insufficiency: Australasian Pancreatic Club recommendations. Med J Aust 193:461–467
Kunovský L, Dítě P, Jabandžiev P, Eid M, Poredská K, Vaculová J, Sochorová D, Janeček P, Tesaříková P, Blaho M, Trna J, Hlavsa J, Kala Z (2021) Causes of exocrine pancreatic insufficiency other than chronic pancreatitis. J Clin Med 10:5779
Lohr JM, Oliver MR, Frulloni L (2013) Synopsis of recent guidelines on pancreatic exocrine insufficiency. United Eur Gastroenterol J 1:79–83
Dominguez-Munoz JE (2017) Potential for screening for pancreatic exocrine insufficiency using the fecal elastase-1 test. Dig Dis Sci 62:1119–1130
Borbély YM, Osterwalder A, Kröll D, Nett PC, Inglin RA (2017) Diarrhea after bariatric procedures: diagnosis and therapy. World J Gastroenterol 23:4689
Uribarri-Gonzalez L, Nieto-García L, Librero-López J, Martis-Sueiro A, Dominguez-Muñoz JE (2018) Factors associated with pancreatic exocrine insufficiency (PEI) in patients after restrictive and malabsorptive bariatric surgery. Pancreatology 18:S125–S126
Acknowledgements
We would like to thank Jeffrey Flack for assistance with electronic medical record data gathering. The project described used RedCAP, which was supported by the National Center for Advancing Translation Sciences (NCATS), National Institutes of Health (NIH), through grand UL1 TR001860.
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This was an unfunded project.
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Drs. Nicole Moore, Trevor Plescia, Shushmita Ahmed, Barbara Jachniewicz, Mohamed Ali, Alexis R. Chirco, Ganesh Rajasekar and Victoria Lyo have no interests or financial ties to disclose.
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Moore, H.N., Chirco, A.R., Plescia, T. et al. Exocrine pancreatic insufficiency after bariatric surgery: a bariatric surgery center of excellence experience. Surg Endosc 37, 1466–1475 (2023). https://doi.org/10.1007/s00464-022-09388-3
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DOI: https://doi.org/10.1007/s00464-022-09388-3