With slowly increasing survival rates in pancreatic cancer and international consensus guidelines recommending surgical resection of premalignant lesions, survival post–pancreatic resection is increasing. With longer survival time, the significant comorbidities of such major surgery have far-reaching effects on the nutrition status of the survivor of pancreatic cancer. This review describes the many nutrition-related side effects of pancreatic surgery, including the development of pancreatic enzyme insufficiency, micronutrient deficiencies, diabetes, fatty liver, and metabolic bone disease. Beyond causing additional medical problems, each of these can have significant effects on quality of life and functional status. The potential mechanisms, diagnosis criteria, and potential treatments of these conditions are described. Overall, little literature exists to fully describe the effects of these comorbidities, and even less is able to guide effective treatments for this population. Clinicians caring for these patients should begin incorporating goals for promotion of long-term health and reduction of these known and reported comorbidities in patients who have undergone pancreatic surgery. Treatment plans in this population remain understudied, and clinicians may need to consider recommendations for similar disease states when developing interventions for these patients.
HowladerNNooneAKrapchoMet al, eds. Table 22.21 Cancer of the Pancreas (Invasive) Estimated United States Cancer Prevalence Counts on January 1, 2014. Bethesda, MD: National Cancer Institute; 2017.
2.
OtteryF.Supportive nutritional management of the patient with pancreatic cancer. Oncology (Williston Park). 1996;10(9)(suppl):26-32.
3.
PhillipsME.Pancreatic exocrine insufficiency following pancreatic resection. Pancreatology. 2015;15(5):449-455.
4.
DavisPFDouglasTGilbertCDet al. Side effects of cancer therapy. In: PolovichMOlsenMMLeFebvreKB, Oncology Nursing Society, eds. Chemotherapy and Biotherapy Guidelines and Recommendations for Practice. 4th ed.Pittsburgh, PA: Oncology Nursing Society; 2014:171-436.
5.
MuehlbauerPMShelburneNShieldsS. Principles of antineoplastic therapy. In: PolovichMOlsenMMLeFebvreKB, Oncology Nursing Society, eds. Chemotherapy and Biotherapy Guidelines and Recommendations for Practice. 4th ed.Pittsburgh, PA: Oncology Nursing Society; 2014:25-50.
6.
SiegelRLMillerKDJemalA.Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7-30.
KeimVKlarEPollMSchoenbergMH.Postoperative care following pancreatic surgery: surveillance and treatment. Dtsch Arztebl Int. 2009;106(48):789-794.
14.
PappasSKrzywdaEMcDowellN.Nutrition and pancreaticoduodenectomy. Nutr Clin Pract. 2010;25(3):234-243.
15.
ChristeinJDSmootRLFarnellMB.Central pancreatectomy: a technique for the resection of pancreatic neck lesions. Arch Surg. 2006;141(3):293-299.
16.
ChristeinJDFarnellMB. The role of total pancreatectomy in the treatment of pancreatic cancer. In: Von HoffDDEvansDBHrubanRH, eds. Pancreatic Cancer. Sudbury, MA: Jones & Bartlett; 2005:287-298.
17.
GallagherSFZervosEEMurrMM. Distal pancreatectomy. In: Von HoffDDEvansDBHrubanRH, eds. Pancreatic Cancer. Sudbury, MA: Jones & Bartlett; 2005:299-311.
18.
RiallTSYeoCJ. Pylorus preservation versus standard pancreaticoduodenecctomy. In: Von HoffDDEvansDBHrubanRH, eds. Pancreatic Cancer. Sudbury, MA: Jones & Bartlett; 2005:313-320.
19.
YenTWFAbdallaEKPistersPWTEvansDB. Pancreaticoduodenectomy. In: Von HoffDDEvansDBHrubanRH eds. Pancreatic Cancer. Sudbury, MA: Jones & Bartlett; 2005:265-285.
20.
KangCMLeeJH.Pathophysiology after pancreaticoduodenectomy. World J Gastroenterol. 2015;21(19):5794-5804.
21.
WastellC.Malabsorptive states after gastrointestinal surgery. Br Med J. 1968;3(5619):661-664.
22.
SullivanSAlpersDKleinS. Nutritional physiology of the alimentary tract. In: RossACCaballeroBCousinsRJTuckerKLZieglerTR eds. Modern Nutrition in Health and Disease. 11th ed.Baltimore, MD: Lippincott Williams & Wilkins; 2014:540-573.
23.
WeaverCMHeaneyRP. Calcium. In: RossACCaballeroBCousinsRJTuckerKLZieglerTR, eds. Modern Nutrition in Health and Disease. 11th ed.Philadelphia, PA: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2014:133-149.
24.
MohammedSVan Buren IiGMcElhanyASilberfeinEJFisherWE.Delayed gastric emptying following pancreaticoduodenectomy: incidence, risk factors, and healthcare utilization. World J Gastrointest Surg. 2017;9(3):73-81.
25.
BeaneJDHouseMGMillerAet al. Optimal management of delayed gastric emptying after pancreatectomy: an analysis of 1,089 patients. Surgery. 2014;156(4):939-946.
26.
SabaterLAusaniaFBakkerOJet al. Evidence-based guidelines for the management of exocrine pancreatic insufficiency after pancreatic surgery. Ann Surg. 2016;264(6):949-958.
BartelMJAsbunHStaufferJRaimondoM.Pancreatic exocrine insufficiency in pancreatic cancer: a review of the literature. Dig Liver Dis. 2015;47(12):1013-1020.
33.
MatsumotoJTraversoLW.Exocrine function following the whipple operation as assessed by stool elastase. J Gastrointest Surg. 2006;10(9):1225-1229.
34.
MunizCKdos SantosJSPfrimerKet al. Nutritional status, fecal elastase-1, and 13C-labeled mixed triglyceride breath test in the long-term after pancreaticoduodenectomy. Pancreas. 2014;43(3):445-450.
35.
NordbackIParviainenMPiironenARatySSandJ.Obstructed pancreaticojejunostomy partly explains exocrine insufficiency after pancreatic head resection. Scand J Gastroenterol. 2007;42(2):263-270.
36.
SpeicherJETraversoLW.Pancreatic exocrine function is preserved after distal pancreatectomy. J Gastrointest Surg. 2010;14(6):1006-1011.
37.
WrayCJAhmadSAMatthewsJBLowyAM.Surgery for pancreatic cancer: recent controversies and current practice. Gastroenterology. 2005;128(6):1626-1641.
38.
Morera-OconFJSabater-OrtiLMunoz-FornerEPerez-GrieraJOrtega-SerranoJ.Considerations on pancreatic exocrine function after pancreaticoduodenectomy. World J Gastrointest Oncol. 2014;6(9):325-329.
39.
MaJPPengLQinTet al. Meta-analysis of pancreaticoduodenectomy prospective controlled trials: pancreaticogastrostomy versus pancreaticojejunostomy reconstruction. Chin Med J (Engl). 2012;125(21):3891-3897.
40.
MakniABediouiHJouiniMet al. Pancreaticojejunostomy vs pancreaticogastrostomy following pancreaticoduodenectomy: results of comparative study. Minerva Chir. 2011;66(4):295-302.
41.
SarnerM.Treatment of pancreatic exocrine deficiency. World J Surg. 2003;27(11):1192-1195.
42.
EllisonNMChevlenEStillCDDubaguntaS.Supportive care for patients with pancreatic adenocarcinoma: symptom control and nutrition. Hematol Oncol Clin North Am. 2002;16(1):105-121.
43.
DiMagnoEPReberHATemperoMA; American Gastroenterological Association. AGA technical review on the epidemiology, diagnosis, and treatment of pancreatic ductal adenocarcinoma. Gastroenterology. 1999;117(6):1464-1484.
44.
BabayanVK.Medium chain triglycerides and structured lipids. Lipids. 1987;22(6):417-420.
45.
ArmstrongTStrommerLRuiz-JasbonFet al. Pancreaticoduodenectomy for peri-ampullary neoplasia leads to specific micronutrient deficiencies. Pancreatology. 2007;7(1):37-44.
46.
ArmstrongTWaltersEVarshneySJohnsonCD.Deficiencies of micronutrients, altered bowel function, and quality of life during late follow-up after pancreaticoduodenectomy for malignancy. Pancreatology. 2002;2(6):528-534.
47.
AppaswamySDe SilvaDTyagiAGrocottLEHeathPDGillowT.Reversible night blindness in a patient with neuroendocrine tumour of pancreas. Eye (Lond). 2005;19(6):720-722.
48.
TiangSWarneR.Nyctalopia: the sequelae of hypovitaminosis A. BMJ Case Rep. 2010;2010:bcr0520102965.
49.
DuttaSKBustinMPRussellRMCostaBS.Deficiency of fat-soluble vitamins in treated patients with pancreatic insufficiency. Ann Intern Med. 1982;97(4):549-552.
50.
DreslerCMFortnerJGMcDermottKBajorunasDR.Metabolic consequences of (regional) total pancreatectomy. Ann Surg. 1991;214(2):131-140.
51.
ParrishCRBaumgartnerMRGoodinBJ. Small intestine malabsorptive disorders. In: MaltareseLEMullinGERaymondJL, eds. The Health Professional’s Guide to Gastrointestinal Nutrition. Chicago, IL: Academy of Nutrition and Dietetics; 2015:47-62.
MaskellCDanielsPJohnsonCD.Dietary intake after pancreatectomy. Br J Surg. 1999;86(3):323-326.
54.
HaaberABRosenfalckAMHansenBHilstedJLarsenS.Bone mineral metabolism, bone mineral density, and body composition in patients with chronic pancreatitis and pancreatic exocrine insufficiency. Int J Pancreatol. 2000;27(1):21-27.
55.
ChristensenATOstergardTAndersenV.Severe impaired deambulation in a patient with vitamin D and mineral deficiency due to exocrine pancreatic insufficiency. JOP. 2011;12(5):482-484.
56.
KlapdorSRichterEKlapdorR.Vitamin D status and per-oral vitamin D supplementation in patients suffering from chronic pancreatitis and pancreatic cancer disease. Anticancer Res. 2012;32(5):1991-1998.
57.
HolickMFBinkleyNCBischoff-FerrariHAet al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2011;96(7):1911-1930.
OngHSNgEHHengGSooKC.Pancreaticoduodenectomy with pancreaticogastrostomy: assessment of patients’ nutritional status, quality of life and pancreatic exocrine function. Aust N Z J Surg. 2000;70(3):199-203.
60.
FinkASDeSouzaLRMayerEAHawkinsRLongmireWPJr.Long-term evaluation of pylorus preservation during pancreaticoduodenectomy. World J Surg. 1988;12(5):663-670.
61.
CarmelR. Cobalamin (vitamin B12). In: RossACCaballeroBCousinsRJTuckerKLZieglerTR, eds. Modern Nutrition in Health and Disease. 11th ed.Baltimore, MD: Lippincott Williams & Wilkins; 2014:369-389.
62.
Bang JorgensenBThorsgaard PedersenNWorningH. Short report: lipid and vitamin B12 malassimilation in pancreatic insufficiency. Aliment Pharmacol Ther. 1991;5(2):207-210.
63.
ShambergerRCHendrenWHLeichtnerAM.Long-term nutritional and metabolic consequences of pancreaticoduodenectomy in children. Surgery. 1994;115(3):382-388.
64.
KimJHBaeYJJunKHChinHM.Long-term trends in hematological and nutritional status after gastrectomy for gastric cancer. J Gastrointest Surg. 2017;21(8):1212-1219.
65.
JunJHYooJELeeJAet al. Anemia after gastrectomy in long-term survivors of gastric cancer: a retrospective cohort study. Int J Surg. 2016;28:162-168.
66.
CarmelR.How I treat cobalamin (vitamin B12) deficiency. Blood. 2008;112(6):2214-2221.
67.
KingJCCousinsRJ. Zinc. In: RossACCaballeroBCousinsRJTuckerKLZieglerTR, eds. Modern Nutrition in Health and Disease. 11th ed.Baltimore MD: Lippincott Williams & Wilkins; 2014:189-205.
68.
YazbeckNMuwakkitSAbboudMSaabR.Zinc and biotin deficiencies after pancreaticoduodenectomy. Acta Gastroenterol Belg. 2010;73(2):283-286.
69.
YasudaHFujiwaraNIshizakiYKomatsuN.Anemia attributed to vitamin B6 deficiency in post-pancreaticoduodenectomy patients. Pancreatology. 2015;15(1):81-83.
70.
YuHHYangTMShanYSLinPW.Zinc deficiency in patients undergoing pancreatoduodenectomy for periampullary tumors is associated with pancreatic exocrine insufficiency. World J Surg. 2011;35(9):2110-2117.
71.
YuHHShanYSLinPW.Zinc deficiency with acrodermatitis enteropathica-like eruption after pancreaticoduodenectomy. J Formos Med Assoc. 2007;106(10):864-868.
72.
LamMAdelsteinDJ.Hypomagnesemia and renal magnesium wasting in patients treated with cisplatin. Am J Kidney Dis. 1986;8(3):164-169.
73.
SaifMW.Management of hypomagnesemia in cancer patients receiving chemotherapy. J Support Oncol. 2008;6(5):243-248.
74.
SchilskyRLAndersonT.Hypomagnesemia and renal magnesium wasting in patients receiving cisplatin. Ann Intern Med. 1979;90(6):929-931.
75.
SuttonRAWalkerVRHalabeASwenertonKCoppinCM.Chronic hypomagnesemia caused by cisplatin: effect of calcitriol. J Lab Clin Med. 1991;117(1):40-43.
76.
OlsenMDavisPFDouglasTTet al. Side effects of cancer therapy. In: PolovichMOlsenMMLeFebvreKB, Oncology Nursing Society, eds. Chemotherapy and Biotherapy Guidelines and Recommendations for Practice. 4th ed.Pittsburgh, PA: Oncology Nursing Society; 2014:171-390.
77.
BurkhartRAGerberSMTholeyRMet al. Incidence and severity of pancreatogenic diabetes after pancreatic resection. J Gastrointest Surg. 2015;19(2):217-225.
78.
CuiYAndersenDK.Pancreatogenic diabetes: special considerations for management. Pancreatology. 2011;11(3):279-294.
79.
MaedaHHanazakiK.Pancreatogenic diabetes after pancreatic resection. Pancreatology. 2011;11(2):268-276.
80.
HataTIshidaMMotoiFet al. Clinical characteristics and risk factors for the development of postoperative hepatic steatosis after total pancreatectomy. Pancreas. 2016;45(3):362-369.
81.
OhgiKOkamuraYYamamotoYet al. Perioperative computed tomography assessments of the pancreas predict nonalcoholic fatty liver disease after pancreaticoduodenectomy. Medicine (Baltimore). 2016;95(6):e2535.
82.
TakemuraNSaiuraAKogaRYamamotoJYamaguchiT. Risk factors for and management of postpancreatectomy hepatic steatosis [published online September 20, 2016]. Scand J Surg.
83.
ItoYKenmochiTShibutaniSet al. Evaluation of predictive factors in patients with nonalcoholic fatty liver disease after pancreaticoduodenectomy. Am Surg. 2014;80(5):500-504.
84.
KatoHIsajiSAzumiYet al. Development of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH) after pancreaticoduodenectomy: proposal of a postoperative NAFLD scoring system. J Hepatobiliary Pancreat Sci. 2010;17(3):296-304.
85.
KishiYShimadaKNaraSEsakiMKosugeT.Administration of pancrelipase as effective treatment for hepatic steatosis after pancreatectomy. Pancreas. 2015;44(6):983-987.
86.
NagayaTTanakaNKimuraTet al. Mechanism of the development of nonalcoholic steatohepatitis after pancreaticoduodenectomy. BBA Clin. 2015;3:168-174.
87.
NakagawaNMurakamiYUemuraKet al. Nonalcoholic fatty liver disease after pancreatoduodenectomy is closely associated with postoperative pancreatic exocrine insufficiency. J Surg Oncol. 2014;110(6):720-726.
88.
NomuraRIshizakiYSuzukiKKawasakiS.Development of hepatic steatosis after pancreatoduodenectomy. AJR Am J Roentgenol. 2007;189(6):1484-1488.
89.
OkamuraYSugimotoHYamadaSet al. Risk factors for hepatic steatosis after pancreatectomy: a retrospective observational cohort study of the importance of nutritional management. Pancreas. 2012;41(7):1067-1072.
90.
SatoRKishiwadaMKuriyamaNet al. Paradoxical impact of the remnant pancreatic volume and infectious complications on the development of nonalcoholic fatty liver disease after pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci. 2014;21(8):562-572.
91.
SongSCChoiSHChoiDWHeoJSKimWSKimMJ.Potential risk factors for nonalcoholic steatohepatitis related to pancreatic secretions following pancreaticoduodenectomy. World J Gastroenterol. 2011;17(32):3716-3723.
92.
TanakaNHoriuchiAYokoyamaTet al. Clinical characteristics of de novo nonalcoholic fatty liver disease following pancreaticoduodenectomy. J Gastroenterol. 2011;46(6):758-768.
93.
YooDGJungBHHwangSet al. Prevalence analysis of de novo hepatic steatosis following pylorus-preserving pancreaticoduodenectomy. Dig Surg. 2014;31(4-5):359-365.
NagaiMShoMSatoiSet al. Effects of pancrelipase on nonalcoholic fatty liver disease after pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci. 2014;21(3):186-192.
96.
SatoiSShoMYanagimotoHet al. Do pancrelipase delayed-release capsules have a protective role against nonalcoholic fatty liver disease after pancreatoduodenectomy in patients with pancreatic cancer? A randomized controlled trial. J Hepatobiliary Pancreat Sci. 2016;23(3):167-173.
97.
YamazakiSTakayamaTHigakiTet al. Pancrelipase with branched-chain amino acids for preventing nonalcoholic fatty liver disease after pancreaticoduodenectomy. J Gastroenterol. 2016;51(1):55-62.
98.
RaoofMNaslundIRaskESzaboE.Effect of gastric bypass on bone mineral density, parathyroid hormone and vitamin D: 5 years follow-up. Obes Surg. 2016;26(5):1141-1145.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
