Pancreas| Volume 169, ISSUE 6, P1463-1470, June 2021

A presurgical prognostic stratification based on nutritional assessment and carbohydrate antigen 19-9 in pancreatic carcinoma: An approach with nonanatomic biomarkers

Published:January 07, 2021DOI:


      Nutritional status and tumor markers are important prognostic indicators for surgical decisions in pancreatic carcinoma. This study aimed to stratify the probability of surviving pancreatic carcinoma based on systematically chosen nonanatomic biomarkers.


      We included 187 consecutive patients that underwent surgical resections for pancreatic carcinoma. We performed multivariable analyses to evaluate prognostic indicators, including 4 blood-test indexes: the neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, prognostic nutritional index, and the modified Glasgow prognostic score; and 4 body-composition indexes: the normalized total psoas muscle area, the normalized total elector spine muscle area, the psoas muscle computed tomography value, and the elector spine muscle computed tomography value.


      Poor survival was associated with 2 independent risk factors: neutrophil-to-lymphocyte ratio ≥3.0 (hazard ratio, 1.54) and prognostic nutritional index <36 (hazard ratio, 1.60), and with high carbohydrate antigen 19-9 levels (≥37 IU/mL). The 2 indexes were not significantly associated with clinicopathological factors, including carbohydrate antigen 19-9. Patients with no risk factors had significantly better survival than those with 1 (P = .007) or 2 risk factors (P = .001), and survival was similar in the latter 2 groups (P = .253). A presurgical nonanatomic scoring system (range, 0−2) was constructed: 0 points for no risk factors, 1 point for 1 or 2 nutritional risk factors, and 1 point for carbohydrate antigen 19-9 ≥37 IU/mL. Survival rate at 3 years decreased with increasing scores (76% for score 0, 42% for score 1, and 21% for score 2; all P < .05).


      Neutrophil-to-lymphocyte ratio and prognostic nutritional index were independent prognostic risk factors in pancreatic carcinoma and integrating these indexes with carbohydrate antigen 19-9 levels could successfully stratify survival.
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        • Okusaka T.
        • Nakamura M.
        • Yoshida M.
        • et al.
        clinical practice guidelines for pancreatic cancer 2019 from the Japan Pancreas Society: A synopsis.
        Pancreas. 2020; 49: 326-335
        • Yamada S.
        • Fujii T.
        • Yabusaki N.
        • et al.
        Clinical implication of inflammation-based prognostic score in pancreatic cancer: Glasgow prognostic score is the most reliable parameter.
        Medicine (Baltimore). 2016; 95: e3582
        • Asari S.
        • Matsumoto I.
        • Toyama H.
        • et al.
        Preoperative independent prognostic factors in patients with borderline resectable pancreatic ductal adenocarcinoma following curative resection: The neutrophil-lymphocyte and platelet-lymphocyte ratios.
        Surg Today. 2016; 46: 583-592
        • Watanabe J.
        • Otani S.
        • Sakamoto T.
        • et al.
        Prognostic indicators based on inflammatory and nutritional factors after pancreaticoduodenectomy for pancreatic cancer.
        Surg Today. 2016; 46: 1258-1267
        • Garcea G.
        • Ladwa N.
        • Neal C.P.
        • Metcalfe M.S.
        • Dennison A.R.
        • Berry D.P.
        Preoperative neutrophil-to-lymphocyte ratio (NLR) is associated with reduced disease-free survival following curative resection of pancreatic adenocarcinoma.
        World J Surg. 2011; 35: 868-872
        • Kanda M.
        • Fujii T.
        • Kodera Y.
        • Nagai S.
        • Takeda S.
        • Nakao A.
        Nutritional predictors of postoperative outcome in pancreatic cancer.
        Br J Surg. 2011; 98: 268-274
        • Delitto D.
        • Judge S.M.
        • George Jr., T.J.
        • et al.
        A clinically applicable muscular index predicts long-term survival in resectable pancreatic cancer.
        Surgery. 2017; 161: 930-938
        • Okumura S.
        • Kaido T.
        • Hamaguchi Y.
        • et al.
        Impact of preoperative quality as well as quantity of skeletal muscle on survival after resection of pancreatic cancer.
        Surgery. 2015; 157: 1088-1098
        • Kawai M.
        • Hirono S.
        • Okada K.I.
        • et al.
        Low lymphocyte monocyte ratio after neoadjuvant therapy predicts poor survival after pancreatectomy in patients with borderline resectable pancreatic cancer.
        Surgery. 2019; 165: 1151-1160
        • Abe T.
        • Nakata K.
        • Kibe S.
        • et al.
        Prognostic value of preoperative nutritional and immunological factors in patients with pancreatic ductal adenocarcinoma.
        Ann Surg Oncol. 2018; 25: 3996-4003
        • Onoe S.
        • Maeda A.
        • Takayama Y.
        • et al.
        The prognostic impact of the lymphocyte-to-monocyte ratio in resected pancreatic head adenocarcinoma.
        Med Princ Pract. 2019; 28: 517-525
        • Pecorelli N.
        • Carrara G.
        • De Cobelli F.
        • et al.
        Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery.
        Br J Surg. 2016; 103: 434-442
        • Sandini M.
        • Bernasconi D.P.
        • Fior D.
        • et al.
        A high visceral adipose tissue-to-skeletal muscle ratio as a determinant of major complications after pancreatoduodenectomy for cancer.
        Nutrition. 2016; 32: 1231-1237
        • Pecorelli N.
        • Capretti G.
        • Sandini M.
        • et al.
        Impact of sarcopenic obesity on failure to rescue from major complications following pancreaticoduodenectomy for cancer: Results from a multicenter study.
        Ann Surg Oncol. 2018; 25: 308-317
        • Wente M.N.
        • Bassi C.
        • Dervenis C.
        • et al.
        Delayed gastric emptying (DGE) after pancreatic surgery: A suggested definition by the International Study Group of Pancreatic Surgery (ISGPS).
        Surgery. 2007; 142: 761-768
        • Bassi C.
        • Dervenis C.
        • Butturini G.
        • et al.
        Postoperative pancreatic fistula: An international study group (ISGPF) definition.
        Surgery. 2005; 138: 8-13
        • Dindo D.
        • Demartines N.
        • Clavien P.A.
        Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey.
        Ann Surg. 2004; 240: 205-213
        • Baumgartner R.N.
        • Koehler K.M.
        • Gallagher D.
        • et al.
        Epidemiology of sarcopenia among the elderly in New Mexico.
        Am J Epidemiol. 1998; 147: 755-763
        • Mourtzakis M.
        • Prado C.M.
        • Lieffers J.R.
        • Reiman T.
        • McCargar L.J.
        • Baracos V.E.
        A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care.
        Appl Physiol Nutr Metab. 2008; 33: 997-1006
        • Otsuji H.
        • Yokoyama Y.
        • Ebata T.
        • et al.
        Preoperative sarcopenia negatively impacts postoperative outcomes following major hepatectomy with extrahepatic bile duct resection.
        World J Surg. 2015; 39: 1494-1500
        • James D.B.
        • Mary K.G.
        • Christian W.
        TNM classification of malignant tumours.
        8th ed. Wiley-Blackwell, 2017
        • Oettle H.
        • Post S.
        • Neuhaus P.
        • et al.
        Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: A randomized controlled trial.
        JAMA. 2007; 297: 267-277
        • Uesaka K.
        • Boku N.
        • Fukutomi A.
        • et al.
        Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: A phase 3, open-label, randomised, non-inferiority trial (JASPAC 01).
        Lancet. 2016; 388: 248-257
        • Japan Pancreas Society
        Classification of Pancreatic Carcinoma.
        4th English ed. Kanehara, Tokyo2017
        • Humphris J.L.
        • Chang D.K.
        • Johns A.L.
        • et al.
        The prognostic and predictive value of serum CA19.9 in pancreatic cancer.
        Ann Oncol. 2012; 23: 1713-1722
        • Hartwig W.
        • Strobel O.
        • Hinz U.
        • et al.
        CA19-9 in potentially resectable pancreatic cancer: Perspective to adjust surgical and perioperative therapy.
        Ann Surg Oncol. 2013; 20: 2188-2196
        • Tsai S.
        • George B.
        • Wittmann D.
        • et al.
        Importance of normalization of CA19-9 levels following neoadjuvant therapy in patients with localized pancreatic cancer.
        Ann Surg. 2020; 271: 740-747
        • Nakajima H.
        • Yokoyama Y.
        • Inoue T.
        • et al.
        Clinical benefit of preoperative exercise and nutritional therapy for patients undergoing hepato-pancreato-biliary surgeries for malignancy.
        Ann Surg Oncol. 2019; 26: 264-272
        • Nakajima H.
        • Yokoyama Y.
        • Inoue T.
        • et al.
        How many steps per day are necessary to prevent postoperative complications following hepato-pancreato-biliary surgeries for malignancy?.
        Ann Surg Oncol. 2020; 27: 1387-1397
        • Hayashi K.
        • Yokoyama Y.
        • Nakajima H.
        • et al.
        Preoperative 6-minute walk distance accurately predicts postoperative complications after operations for hepato-pancreato-biliary cancer.
        Surgery. 2017; 161: 525-532