Skip to main content
Log in

Identification of Risk Factors for Pancreatic Exocrine Insufficiency After Pancreaticoduodenectomy Using a 13C-Labeled Mixed Triglyceride Breath Test

  • Original Scientific Report
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Background

There are only a few reports concerning long-term exocrine function after pancreaticoduodenectomy (PD), although the number of long-term survivors has increased. We assessed pancreatic exocrine function after PD in 189 patients to identify risk factors for pancreatic exocrine insufficiency.

Methods

We evaluated patients’ exocrine function by using the 13C-labeled mixed triglyceride breath test, a noninvasive test feasible in outpatient service units. The present study included 99 patients that underwent pancreaticojejunostomy (PJ) at Wakayama Medical University Hospital and 90 patients that underwent pancreaticogastrostomy (PG) at Hiroshima University Hospital, the standard reconstruction techniques during PD at the respective hospitals. We also analyzed long-term morphological changes of remnant pancreas by computed tomography (main pancreatic duct dilation and parenchymal atrophy), nutritional status, and endocrine function.

Results

Independent risk factors for exocrine insufficiency after PD include hard pancreas (P = 0.003, odds ratio; 3.157) and PG reconstruction (P = 0.040, odds ratio; 2.321). Breath test results correlated significantly with post-operative morphological changes, nutritional status, and endocrine function. Atrophic changes of the remnant pancreas in the PG group were more severe than those in the PJ group. Furthermore, for patients with a soft pancreas, postoperative body weight changes, prognostic nutritional index, serum total protein levels as well as exocrine test were worse in the PG group, compared with the PJ group.

Conclusions

Our results showed that PJ reconstruction might be superior to PG during PD, from the viewpoint of long-term pancreatic exocrine function, although further prospective studies are needed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Rault A, SaCunha A, Klopfenstein D et al (2005) Pancreaticojejunal anastomosis is preferable to pancreaticogastrostomy after pancreaticoduodenectomy for longterm outcomes of pancreatic exocrine function. J Am Coll Surg 201:239–244

    Article  PubMed  Google Scholar 

  2. Matsumoto J, Traverso W (2006) Exocrine following the Whipple operation as assessed by stool elastase. J Gastrointest Surg 10:1225–1229

    Article  PubMed  Google Scholar 

  3. Nakamura H, Murakami Y, Uemura K et al (2009) Predictive factors for exocrine pancreatic insufficiency after pancreatoduodenectomy with pancreaticogastrostomy. J Gastrointest Surg 13:1321–1327

    Article  PubMed  Google Scholar 

  4. Park JW, Jang JY, Kim EJ et al (2013) Effects of pancreatectomy on nutritional state, pancreatic function and quality of life. Br J Surg 100:1064–1700

    Article  CAS  PubMed  Google Scholar 

  5. Yu HH, Yang TM, Shan YS et al (2011) Zinc deficiency in patients undergoing pancreatoduodenectomy for periampullarly tumors is associated with pancreatic exocrine insufficiency. World J Surg 35:2110–2117. doi:10.1007/s00268-011-1170-z

    Article  PubMed  Google Scholar 

  6. Armstrong T, Strommer L, Ruiz-Jasbon F et al (2007) Pancreaticoduodenectomy for peri-ampullarly neoplasia leads to specific micronutrient deficiencies. Pancreatology 7:37–44

    Article  CAS  PubMed  Google Scholar 

  7. Nakamura H, Morifuji M, Murakami Y et al (2009) Usefulness of a 13C-labeled mixed triglyceride breath test for assessing pancreatic exocrine function after pancreatic surgery. Surgery 145:168–175

    Article  PubMed  Google Scholar 

  8. Watkins JB, Klein PD, Scholler DA et al (1982) Diagnosis and differentiation of fat malabsorption in children using 13C-labeled lipids: trioctanoin, triolein, and palmitic acid breath tests. Gastroenterology 82:911–917

    CAS  PubMed  Google Scholar 

  9. Kawai M, Tani M, Hirono S et al (2011) Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: a prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 253:495–501

    Article  PubMed  Google Scholar 

  10. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of survey. Ann Surg 240:205–213

    Article  PubMed Central  PubMed  Google Scholar 

  11. Bassi C, Dervenis C, Butturini G et al (2005) International study group on pancreatic fistula definition. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13

    Article  PubMed  Google Scholar 

  12. Nakamura H, Murakami Y, Uemura K et al (2011) Reduced pancreatic parenchymal thickness indicates exocrine pancreatic insufficiency after pancreatoduodenectomy. J Surg Res 171:473–478

    Article  PubMed  Google Scholar 

  13. Hirono S, Tani M, Kawai M et al (2009) A central pancreatectomy for benign or low-grade malignant neoplasms. J Gastrointest Surg 13:1659–1665

    Article  PubMed  Google Scholar 

  14. Onodera T, Goseki N, Kosaki G (1984) Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nippon Geka Gakkai Zasshi 85:1001–1005 (in Japanese)

    CAS  PubMed  Google Scholar 

  15. Kanda M, Fujii T, Kodera S et al (2011) Nutritional predictors of postoperative outcome in pancreatic cancer. Br J Surg 98:268–274

    Article  CAS  PubMed  Google Scholar 

  16. Schiesser M, Kirchhoff P, Müller MK et al (2009) The correlation of nutrition risk index, nutrition risk score, and bioimpedance analysis with postoperative complications in patients undergoing gastrointestinal surgery. Surgery 145:519–526

    Article  PubMed  Google Scholar 

  17. Murakami Y, Uemura K, Hayashidani Y et al (2008) Long-term pancreatic endocrine function following pancreatoduodenectomy with pancreaticogastrostomy. J Surg Oncol 97:519–522

    Article  PubMed  Google Scholar 

  18. Ishikawa O, Ohigashi H, Eguchi H et al (2004) Long-term follow-up of glucose tolerance function after Pancreaticoduodenectomy: comparison between pancreaticogastrostomy and pancreaticojejunostomy. Surgery 136:617–623

    Article  PubMed  Google Scholar 

  19. Lankisch PG, Lembcke B, Wemgen G et al (1986) Functional reserve capacity of the exocrine pancreas. Digestion 35:175–181

    Article  CAS  PubMed  Google Scholar 

  20. Miyakawa S, Niwamoto N, Horiguchi A et al (2000) Fat absorption after pylorus-preserving pancreatoduodenectomy reconstructed with Billroth II pancreaticojejunostomy or Billroth I pancreaticogastrostomy. Hepatogastroenterology 47:264–268

    CAS  PubMed  Google Scholar 

  21. Hyunh H, Couper RTL (2000) Pancreatic function tests. In: Walker WA (ed) Pediatric gastrointestinal disease: pathophysiology, diagnosis, management, 3rd edn. Decker, Ontario, pp 1515–1528

    Google Scholar 

  22. Loser C, Mollgaard A, Folsch UR (1996) Faecal elastase 1: a novel, highly sensitive and specific tubeless pancreatic function test. Gut 39:580–586

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Sziegoleit A, Linder D (1991) Studies on the sterol-binding capacity of human pancreatic elastase 1. Gastroenterology 100:768–774

    CAS  PubMed  Google Scholar 

  24. Fischer B, Hoh S, Wehler M et al (2001) Fecal elastase-1: lyophilization of stool samples prevents false low results in diarrhea. Scand J Gastroenterol 36:771–774

    Article  CAS  PubMed  Google Scholar 

  25. Yeo CJ, Cameron JL, Maher MM et al (1995) A prospective randomized trial of pancreaticogastrostomy versus pancreaticojejunostomy after Pancreaticoduodenectomy. Ann Surg 222:580–592

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Bassi C, Falconi M, Molinari E et al (2005) Reconstruction by pancreaticojejunostomy versus pancreaticogastrostomy following pancreatectomy. Results of a comparative study. Ann Surg 242:767–773

    Article  PubMed Central  PubMed  Google Scholar 

  27. Duffas JP, Suc B, Msika S et al (2005) A controlled randomized multicenter trial of pancreatogastrostomy or pancreaticojejunostomy after pancreatoduodenectomy. Am J Surg 189:720–729

    Article  PubMed  Google Scholar 

  28. Fernández-Cruz L, Cosa R, Blanco L et al (2008) Pancreatogastrostomy with gastric partition after pylorus-preserving pancreatoduodenectomy versus conventional pancreatojejunostomy. A prospective randomized study. Ann Surg 248:930–938

    Article  PubMed  Google Scholar 

  29. Wellner UF, Sick O, Olschewski M et al (2012) Randomized controlled single-center trial compairing pancreatogastrostomy versus pancreaticojejunostomy after partial pancreatoduodenectomy. J Gastrointest Surg 16:1686–1695

    Article  PubMed  Google Scholar 

  30. Topal B, Fieuws S, Aerts R et al (2013) Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after Pancreaticoduodenectomy for pancreatic or periampullary tumours: a multicentre randomized trial. Lancet Oncol 14:655–662

    Article  PubMed  Google Scholar 

  31. Ishiwatari H, Sato Y, Murase K et al (2013) Treatment of pancreatic fibrosis with siRNA against a collagen-specific chaperone in vitamin A coupled liposomes. Gut 62:1328–1339

    Article  CAS  PubMed  Google Scholar 

  32. Fang WL, Su CH, Shyr YM et al (2007) Functional and morphological changes in pancreatic remnant after pancreaticoduodenectomy. Pancreas 35:361–365

    Article  PubMed  Google Scholar 

  33. Tomimaru Y, Takeda Y, Kobayashi S et al (2009) Comparison of postoperative morphological changes in remnant pancreas between pancreaticojejunostomy and pancreaticogastrostomy after Pancreaticoduodenectomy. Pancreas 38:203–207

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoshiaki Murakami.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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 39, 516–525 (2015). https://doi.org/10.1007/s00268-014-2832-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-014-2832-4

Keywords

Navigation