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Exocrine Pancreatic Insufficiency After Pancreatectomy for Malignancy: Systematic Review and Optimal Management Recommendations

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Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background

Exocrine pancreatic insufficiency (EPI) occurs when pancreatic enzyme activity in the intestinal lumen is insufficient for normal digestion to occur. The true incidence and diagnosis of EPI after pancreatectomy has not been fully understood and optimized. The aim of this study was to present incidence and diagnostic criteria for EPI after pancreatectomy for cancer and provide a guide for management and optimal therapy in pancreatectomy patients with cancer.

Methods

A comprehensive review of the literature with publication dates from 2014 to 2019 was performed. A comprehensive diagnostic and treatment algorithm was then created based on literature review and current treatment options.

Results

In total, 30 studies were included, 19 combined both pancreaticoduodenectomy (PD) and distal pancreatectomy (DP), 9 for central pancreatectomy, and 2 others. EPI was defined subjectively without definitive testing using any of the established diagnostic studies in the majority of studies 23 (76%). Preoperative EPI was calculated to be 11.52%. Most studies assessed exocrine function at least 6 months postoperatively with four studies extending the follow-up period beyond 12 months. EPI diagnosed postoperatively at 1 month (40.27%), 3 months (30.94%), 6 months (36.06%), and 12 months (34.69%). After PD, the median prevalence of postoperative EPI was 43.14%, CP, the median prevalence was 4.85%, DP, median prevalence of postoperative EPI of 11.94%.

Conclusion

EPI is a frequent outcome that is often misdiagnosed or under-reported by the patient post-pancreatectomy. Given the increasing overall survival in pancreatectomy patients for cancer, surgeon awareness and assessment is critical to improving patients’ overall quality of life.

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References

  1. Conroy T, Hammel P, Hebbar M, et al. FOLFIRINOX or Gemcitabine as Adjuvant Therapy for Pancreatic Cancer. N Engl J Med. 2018;379(25):2395-2406.

    Article  CAS  Google Scholar 

  2. Halloran CM, Cox TF, Chauhan S, et al. Partial pancreatic resection for pancreatic malignancy is associated with sustained pancreatic exocrine failure and reduced quality of life: a prospective study. Pancreatology. 2011;11(6):535-545.

    Article  CAS  Google Scholar 

  3. Partelli S, Frulloni L, Minniti C, et al. Faecal elastase-1 is an independent predictor of survival in advanced pancreatic cancer. Dig Liver Dis. 2012;44(11):945-951.

    Article  CAS  Google Scholar 

  4. Dominguez-Munoz JE. Pancreatic enzyme therapy for pancreatic exocrine insufficiency. Curr Gastroenterol Rep. 2007;9(2):116-122.

    Article  Google Scholar 

  5. Kahl S, Malfertheiner P. Exocrine and endocrine pancreatic insufficiency after pancreatic surgery. Best Pract Res Clin Gastroenterol. 2004;18(5):947-955.

    Article  Google Scholar 

  6. Friess H, Michalski CW. Diagnosing exocrine pancreatic insufficiency after surgery: when and which patients to treat. HPB (Oxford). 2009;11 Suppl 3:7-10.

    Article  Google Scholar 

  7. Sikkens EC, Cahen DL, de Wit J, Looman CW, van Eijck C, Bruno MJ. Prospective assessment of the influence of pancreatic cancer resection on exocrine pancreatic function. Br J Surg. 2014;101(2):109-113.

    Article  CAS  Google Scholar 

  8. Scholten L, Stoop TF, Del Chiaro M, et al. Systematic review of functional outcome and quality of life after total pancreatectomy. Br J Surg. 2019;106(13):1735-1746.

    Article  CAS  Google Scholar 

  9. Stoop TF, Ateeb Z, Ghorbani P, et al. Impact of Endocrine and Exocrine Insufficiency on Quality of Life After Total Pancreatectomy. Ann Surg Oncol. 2019.

  10. Capurso G, Traini M, Piciucchi M, Signoretti M, Arcidiacono PG. Exocrine pancreatic insufficiency: prevalence, diagnosis, and management. Clin Exp Gastroenterol. 2019;12:129-139.

    Article  Google Scholar 

  11. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1-34.

    Article  Google Scholar 

  12. Tseng DS, Molenaar IQ, Besselink MG, van Eijck CH, Borel Rinkes IH, van Santvoort HC. Pancreatic Exocrine Insufficiency in Patients With Pancreatic or Periampullary Cancer: A Systematic Review. Pancreas. 2016;45(3):325-330.

    Article  CAS  Google Scholar 

  13. Agency for Healthcare Research and Quality. National Guideline C. Practicing Chiropractors’ Committee on Radiology Protocols (PCCRP) for biomechanical assessment of spinal subluxation in chiropractic clinical practice. https://www.ahrq.gov/gam/index.html. Published 2014. Accessed 8/11/2014.

  14. Keller J, Meier V, Wolfram KU, Rosien U, Layer P. Sensitivity and specificity of an abbreviated (13)C-mixed triglyceride breath test for measurement of pancreatic exocrine function. United European Gastroenterol J. 2014;2(4):288-294.

    Article  Google Scholar 

  15. Steinberg WM, Anderson KK. Serum trypsinogen in diagnosis of chronic pancreatitis. Dig Dis Sci. 1984;29(11):988-993.

    Article  CAS  Google Scholar 

  16. Tjaden C, Hassenpflug M, Hinz U, et al. Outcome and prognosis after pancreatectomy in patients with solid pseudopapillary neoplasms. Pancreatology. 2019;19(5):699-709.

    Article  Google Scholar 

  17. Shi Y, Wang Y, Wang J, et al. Learning curve of robot-assisted middle pancreatectomy (RMP): experience of the first 100 cases from a high-volume pancreatic center in China. Surg Endosc. 2019.

  18. Xiao W, Zhu J, Peng L, Hong L, Sun G, Li Y. The role of central pancreatectomy in pancreatic surgery: a systematic review and meta-analysis. HPB (Oxford). 2018;20(10):896-904.

    Article  Google Scholar 

  19. Senthilnathan P, Gul SI, Gurumurthy SS, et al. Laparoscopic central pancreatectomy: Our technique and long-term results in 14 patients. J Minim Access Surg. 2015;11(3):167-171.

    Article  Google Scholar 

  20. Goudard Y, Gaujoux S, Dokmak S, et al. Reappraisal of central pancreatectomy a 12-year single-center experience. JAMA Surg. 2014;149(4):356-363.

    Article  Google Scholar 

  21. Zhang T, Wang X, Huo Z, et al. Robot-Assisted Middle Pancreatectomy for Elderly Patients: Our Initial Experience. Med Sci Monit. 2015;21:2851-2860.

    Article  Google Scholar 

  22. Kang P, Wang Z, Leng K, et al. Binding pancreaticogastrostomy anastomosis in central pancreatectomy: A single center experience. Medicine (Baltimore). 2017;96(45):e8354.

    Article  Google Scholar 

  23. Hong D, Liu Y, Peng S, et al. Binding pancreaticogastrostomy in laparoscopic central pancreatectomy: a novel technique in laparoscopic pancreatic surgery. Surg Endosc. 2016;30(2):715-720.

    Article  Google Scholar 

  24. Jiang CY, Wang W. Initial experience in total laparoscopic central pancreatectomy with pancreatogastrostomy. Cell Biochem Biophys. 2015;71(2):1023-1028.

    Article  CAS  Google Scholar 

  25. Jilesen AP, van Eijck CH, Busch OR, van Gulik TM, Gouma DJ, van Dijkum EJ. Postoperative Outcomes of Enucleation and Standard Resections in Patients with a Pancreatic Neuroendocrine Tumor. World J Surg. 2016;40(3):715-728.

    Article  Google Scholar 

  26. Lim PW, Dinh KH, Sullivan M, et al. Thirty-day outcomes underestimate endocrine and exocrine insufficiency after pancreatic resection. HPB (Oxford). 2016;18(4):360-366.

    Article  Google Scholar 

  27. Neophytou H, Wangermez M, Gand E, Carretier M, Danion J, Richer JP. Predictive factors of endocrine and exocrine insufficiency after resection of a benign tumour of the pancreas. Ann Endocrinol (Paris). 2018;79(2):53-61.

    Article  Google Scholar 

  28. Wang X, Chen YH, Tan CL, et al. Enucleation of pancreatic solid pseudopapillary neoplasm: Short-term and long-term outcomes from a 7-year large single-center experience. Eur J Surg Oncol. 2018;44(5):644-650.

    Article  Google Scholar 

  29. Maignan A, Ouaissi M, Turrini O, et al. Risk factors of exocrine and endocrine pancreatic insufficiency after pancreatic resection: A multi-center prospective study. J Visc Surg. 2018;155(3):173-181.

    Article  CAS  Google Scholar 

  30. Hirono S, Murakami Y, Tani M, et al. Identification of risk factors for pancreatic exocrine insufficiency after pancreaticoduodenectomy using a 13C-labeled mixed triglyceride breath test. World J Surg. 2015;39(2):516-525.

    Article  Google Scholar 

  31. Okano K, Murakami Y, Nakagawa N, et al. Remnant pancreatic parenchymal volume predicts postoperative pancreatic exocrine insufficiency after pancreatectomy. Surgery. 2016;159(3):885-892.

    Article  Google Scholar 

  32. Li Y, Li Y. Central versus Distal Pancreatectomy for Benign or Low-Grade Malignant Lesions in the Pancreatic Neck and Proximal Body. Am Surg. 2019;85(11):1239-1245.

    Article  Google Scholar 

  33. Hallac A, Aleassa EM, Rogers M, Falk GA, Morris-Stiff G. Exocrine pancreatic insufficiency in distal pancreatectomy: incidence and risk factors. HPB (Oxford). 2020;22(2):275-281.

    Article  Google Scholar 

  34. Roberts KJ, Bannister CA, Schrem H. Enzyme replacement improves survival among patients with pancreatic cancer: Results of a population based study. Pancreatology. 2019;19(1):114-121.

    Article  CAS  Google Scholar 

  35. Kusakabe J, Anderson B, Liu J, et al. Long-Term Endocrine and Exocrine Insufficiency After Pancreatectomy. J Gastrointest Surg. 2019;23(8):1604-1613.

    Article  Google Scholar 

  36. Othman MO, Harb D, Barkin JA. Introduction and practical approach to exocrine pancreatic insufficiency for the practicing clinician. Int J Clin Pract. 2018;72(2).

  37. Borowitz DS, Grand RJ, Durie PR. Use of pancreatic enzyme supplements for patients with cystic fibrosis in the context of fibrosing colonopathy. Consensus Committee. J Pediatr. 1995;127(5):681-684.

    Article  CAS  Google Scholar 

  38. Southern WN, Rahmani R, Aroniadis O, et al. Postoperative Clostridium difficile-associated diarrhea. Surgery. 2010;148(1):24-30.

    Article  Google Scholar 

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Correspondence to Robert C. G. Martin II.

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Moore, J.V., Tom, S., Scoggins, C.R. et al. Exocrine Pancreatic Insufficiency After Pancreatectomy for Malignancy: Systematic Review and Optimal Management Recommendations. J Gastrointest Surg 25, 2317–2327 (2021). https://doi.org/10.1007/s11605-020-04883-1

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