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Biomarkers for Evaluating the Inflammation Status in Patients with Cancer

  • Guner, Ali (Department of Surgery, Yonsei University College of Medicine) ;
  • Kim, Hyoung-Il (Department of Surgery, Yonsei University College of Medicine)
  • Received : 2019.05.14
  • Accepted : 2019.08.14
  • Published : 2019.09.30

Abstract

Inflammation can be a causative factor for carcinogenesis or can result from a consequence of cancer progression. Moreover, cancer therapeutic interventions can also induce an inflammatory response. Various inflammatory parameters are used to assess the inflammatory status during cancer treatment. It is important to select the most optimal biomarker among these parameters. Additionally, suitable biomarkers must be examined if there are no known parameters. We briefly reviewed the published literature for the use of inflammatory parameters in the treatment of patients with cancer. Most studies on inflammation evaluated the correlation between host characteristics, effect of interventions, and clinical outcomes. Additionally, the levels of C-reactive protein, albumin, lymphocytes, and platelets were the most commonly used laboratory parameters, either independently or in combination with other laboratory parameters and clinical characteristics. Furthermore, the immune parameters are classically examined using flow cytometry, immunohistochemical staining, and enzyme-linked immunosorbent assay techniques. However, gene expression profiling can aid in assessing the overall peri-interventional immune status. The checklists of guidelines, such as STAndards for Reporting of Diagnostic accuracy and REporting recommendations for tumor MARKer prognostic studies should be considered when designing studies to investigate the inflammatory parameters. Finally, the data should be interpreted after adjusting for clinically important variables, such as age and cancer stage.

Keywords

References

  1. Hensler T, Hecker H, Heeg K, Heidecke CD, Bartels H, Barthlen W, et al. Distinct mechanisms of immunosuppression as a consequence of major surgery. Infect Immun 1997;65:2283-2291. https://doi.org/10.1128/IAI.65.6.2283-2291.1997
  2. Zeltsman M, Mayor M, Jones DR, Adusumilli PS. Surgical immune interventions for solid malignancies. Am J Surg 2016;212:682-690.e5. https://doi.org/10.1016/j.amjsurg.2016.06.008
  3. Guner A, Kim SY, Yu JE, Min IK, Roh YH, Roh C, et al. Parameters for predicting surgical outcomes for gastric cancer patients: simple is better than complex. Ann Surg Oncol 2018;25:3239-3247. https://doi.org/10.1245/s10434-018-6684-2
  4. Pennell LM, Galligan CL, Fish EN. Sex affects immunity. J Autoimmun 2012;38:J282-J291. https://doi.org/10.1016/j.jaut.2011.11.013
  5. Roved J, Westerdahl H, Hasselquist D. Sex differences in immune responses: Hormonal effects, antagonistic selection, and evolutionary consequences. Horm Behav 2017;88:95-105. https://doi.org/10.1016/j.yhbeh.2016.11.017
  6. Ono S, Tsujimoto H, Hiraki S, Takahata R, Kinoshita M, Mochizuki H. Sex differences in cytokine production and surface antigen expression of peripheral blood mononuclear cells after surgery. Am J Surg 2005;190:439-444. https://doi.org/10.1016/j.amjsurg.2005.03.031
  7. Kosuga T, Ichikawa D, Okamoto K, Komatsu S, Konishi H, Takeshita H, et al. Impact of age on early surgical outcomes of laparoscopy-assisted gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer. Anticancer Res 2015;35:2191-2198.
  8. Kudoh A, Katagai H, Takazawa T, Matsuki A. Plasma proinflammatory cytokine response to surgical stress in elderly patients. Cytokine 2001;15:270-273. https://doi.org/10.1006/cyto.2001.0927
  9. Milner JJ, Beck MA. The impact of obesity on the immune response to infection. Proc Nutr Soc 2012;71:298-306. https://doi.org/10.1017/S0029665112000158
  10. Kolb R, Sutterwala FS, Zhang W. Obesity and cancer: inflammation bridges the two. Curr Opin Pharmacol 2016;29:77-89. https://doi.org/10.1016/j.coph.2016.07.005
  11. Gunderson CC, Java J, Moore KN, Walker JL. The impact of obesity on surgical staging, complications, and survival with uterine cancer: a Gynecologic Oncology Group LAP2 ancillary data study. Gynecol Oncol 2014;133:23-27. https://doi.org/10.1016/j.ygyno.2014.01.041
  12. Khoury W, Lavery IC, Kiran RP. Effects of chronic immunosuppression on long-term oncologic outcomes for colorectal cancer patients undergoing surgery. Ann Surg 2011;253:323-327. https://doi.org/10.1097/SLA.0b013e3181fc9d36
  13. Moulin CM, Marguti I, Peron JP, Halpern A, Rizzo LV. Bariatric surgery reverses natural killer (NK) cell activity and NK-related cytokine synthesis impairment induced by morbid obesity. Obes Surg 2011;21:112-118. https://doi.org/10.1007/s11695-010-0250-8
  14. Kotani N, Hashimoto H, Sessler DI, Yoshida H, Kimura N, Okawa H, et al. Smoking decreases alveolar macrophage function during anesthesia and surgery. Anesthesiology 2000;92:1268-1277. https://doi.org/10.1097/00000542-200005000-00014
  15. Na YM, Kim MY, Kim YK, Ha YR, Yoon DS. Exercise therapy effect on natural killer cell cytotoxic activity in stomach cancer patients after curative surgery. Arch Phys Med Rehabil 2000;81:777-779. https://doi.org/10.1016/S0003-9993(00)90110-2
  16. Ukkonen M, Karlsson S, Laukkarinen J, Rantanen T, Paajanen H; Finnsepsis Study Group. Severe sepsis in elderly patients undergoing gastrointestinal surgery-a prospective multicenter follow-up study of Finnish Intensive Care Units. J Gastrointest Surg 2016;20:1028-1033. https://doi.org/10.1007/s11605-016-3076-4
  17. Solaini L, Atmaja BT, Arumugam P, Hutchins RR, Abraham AT, Bhattacharya S, et al. The role of perioperative inflammatory-based prognostic systems in patients with colorectal liver metastases undergoing surgery. A cohort study. Int J Surg 2016;36:8-12. https://doi.org/10.1016/j.ijsu.2016.10.010
  18. Kudoh A, Katagai H, Takazawa T. Plasma inflammatory cytokine response to surgical trauma in chronic depressed patients. Cytokine 2001;13:104-108. https://doi.org/10.1006/cyto.2000.0802
  19. Sutter PM, Spagnoli GC, Marx A, Gurke L, Troeger H, Fricker R, et al. Increased surface expression of CD18 and CD11b in leukocytes after tourniquet ischemia during elective hand surgery. World J Surg 1997;21:179-184. https://doi.org/10.1007/s002689900212
  20. Weighardt H, Heidecke CD, Emmanuilidis K, Maier S, Bartels H, Siewert JR, et al. Sepsis after major visceral surgery is associated with sustained and interferon-gamma-resistant defects of monocyte cytokine production. Surgery 2000;127:309-315. https://doi.org/10.1067/msy.2000.104118
  21. Sammour T, Kahokehr A, Chan S, Booth RJ, Hill AG. The humoral response after laparoscopic versus open colorectal surgery: a meta-analysis. J Surg Res 2010;164:28-37. https://doi.org/10.1016/j.jss.2010.05.046
  22. Evans C, Galustian C, Kumar D, Hagger R, Melville DM, Bodman-Smith M, et al. Impact of surgery on immunologic function: comparison between minimally invasive techniques and conventional laparotomy for surgical resection of colorectal tumors. Am J Surg 2009;197:238-245. https://doi.org/10.1016/j.amjsurg.2008.01.021
  23. Zawadzki M, Krzystek-Korpacka M, Gamian A, Witkiewicz W. Comparison of inflammatory responses following robotic and open colorectal surgery: a prospective study. Int J Colorectal Dis 2017;32:399-407. https://doi.org/10.1007/s00384-016-2697-0
  24. Pilka R, Marek R, Adam T, Kudela M, Ondrova D, Neubert D, et al. Systemic inflammatory response after open, laparoscopic and robotic surgery in endometrial cancer patients. Anticancer Res 2016;36:2909-2922.
  25. Schneider C, von Aulock S, Zedler S, Schinkel C, Hartung T, Faist E. Perioperative recombinant human granulocyte colony-stimulating factor (Filgrastim) treatment prevents immunoinflammatory dysfunction associated with major surgery. Ann Surg 2004;239:75-81. https://doi.org/10.1097/01.sla.0000103062.21049.82
  26. Crozier JE, Leitch EF, McKee RF, Anderson JH, Horgan PG, McMillan DC. Relationship between emergency presentation, systemic inflammatory response, and cancer-specific survival in patients undergoing potentially curative surgery for colon cancer. Am J Surg 2009;197:544-549. https://doi.org/10.1016/j.amjsurg.2007.12.052
  27. Kimura A, Ono S, Hiraki S, Takahata R, Tsujimoto H, Miyazaki H, et al. The postoperative serum interleukin-15 concentration correlates with organ dysfunction and the prognosis of septic patients following emergency gastrointestinal surgery. J Surg Res 2012;175:e83-e88. https://doi.org/10.1016/j.jss.2011.12.003
  28. Aosasa S, Ono S, Mochizuki H, Tsujimoto H, Osada S, Takayama E, et al. Activation of monocytes and endothelial cells depends on the severity of surgical stress. World J Surg 2000;24:10-16. https://doi.org/10.1007/s002689910003
  29. Flohe S, Lendemans S, Schade FU, Kreuzfelder E, Waydhas C. Influence of surgical intervention in the immune response of severely injured patients. Intensive Care Med 2004;30:96-102. https://doi.org/10.1007/s00134-003-2041-3
  30. Gu CY, Zhang J, Qian YN, Tang QF. Effects of epidural anesthesia and postoperative epidural analgesia on immune function in esophageal carcinoma patients undergoing thoracic surgery. Mol Clin Oncol 2015;3:190-196. https://doi.org/10.3892/mco.2014.405
  31. Chen WK, Ren L, Wei Y, Zhu DX, Miao CH, Xu JM. General anesthesia combined with epidural anesthesia ameliorates the effect of fast-track surgery by mitigating immunosuppression and facilitating intestinal functional recovery in colon cancer patients. Int J Colorectal Dis 2015;30:475-481. https://doi.org/10.1007/s00384-014-2098-1
  32. Sacerdote P, Bianchi M, Gaspani L, Manfredi B, Maucione A, Terno G, et al. The effects of tramadol and morphine on immune responses and pain after surgery in cancer patients. Anesth Analg 2000;90:1411-1414. https://doi.org/10.1097/00000539-200006000-00028
  33. Martinez AB, Longas J, Ramirez JM. A model for lymphocyte activation in open versus laparoscopic surgery in colorectal cancer patients in enhanced recovery after surgery (ERAS) protocols. Int J Colorectal Dis 2017;32:913-916. https://doi.org/10.1007/s00384-016-2731-2
  34. Veenhof AA, Vlug MS, van der Pas MH, Sietses C, van der Peet DL, de Lange-de Klerk ES, et al. Surgical stress response and postoperative immune function after laparoscopy or open surgery with fast track or standard perioperative care: a randomized trial. Ann Surg 2012;255:216-221. https://doi.org/10.1097/SLA.0b013e31824336e2
  35. Yang D, He W, Zhang S, Chen H, Zhang C, He Y. Fast-track surgery improves postoperative clinical recovery and immunity after elective surgery for colorectal carcinoma: randomized controlled clinical trial. World J Surg 2012;36:1874-1880. https://doi.org/10.1007/s00268-012-1606-0
  36. Heiss MM, Fasol-Merten K, Allgayer H, Strohlein MA, Tarabichi A, Wallner S, et al. Influence of autologous blood transfusion on natural killer and lymphokine-activated killer cell activities in cancer surgery. Vox Sang 1997;73:237-245. https://doi.org/10.1159/000461939
  37. Theodoraki K, Markatou M, Rizos D, Fassoulaki A. The impact of two different transfusion strategies on patient immune response during major abdominal surgery: a preliminary report. J Immunol Res 2014;2014:945829.
  38. Fukuda T, Seto Y, Yamada K, Hiki N, Fukunaga T, Oyama S, et al. Can immune-enhancing nutrients reduce postoperative complications in patients undergoing esophageal surgery? Dis Esophagus 2008;21:708-711. https://doi.org/10.1111/j.1442-2050.2008.00861.x
  39. Giger U, Buchler M, Farhadi J, Berger D, Husler J, Schneider H, et al. Preoperative immunonutrition suppresses perioperative inflammatory response in patients with major abdominal surgery-a randomized controlled pilot study. Ann Surg Oncol 2007;14:2798-2806. https://doi.org/10.1245/s10434-007-9407-7
  40. Arumugam S, Lau CS, Chamberlain RS. Probiotics and Synbiotics Decrease Postoperative Sepsis in Elective Gastrointestinal Surgical Patients: a Meta-Analysis. J Gastrointest Surg 2016;20:1123-1131. https://doi.org/10.1007/s11605-016-3142-y
  41. Liu Z, Li C, Huang M, Tong C, Zhang X, Wang L, et al. Positive regulatory effects of perioperative probiotic treatment on postoperative liver complications after colorectal liver metastases surgery: a double-center and double-blind randomized clinical trial. BMC Gastroenterol 2015;15:34. https://doi.org/10.1186/s12876-015-0260-z
  42. Braga M, Gianotti L, Vignali A, Di Carlo V. Immunonutrition in gastric cancer surgical patients. Nutrition 1998;14:831-835. https://doi.org/10.1016/S0899-9007(98)00103-8
  43. Furukawa K, Tashiro T, Yamamori H, Takagi K, Morishima Y, Sugiura T, et al. Effects of soybean oil emulsion and eicosapentaenoic acid on stress response and immune function after a severely stressful operation. Ann Surg 1999;229:255-261. https://doi.org/10.1097/00000658-199902000-00014
  44. Wang WP, Yan XL, Ni YF, Guo K, Ke CK, Cheng QS, et al. Effects of lipid emulsions in parenteral nutrition of esophageal cancer surgical patients receiving enteral nutrition: a comparative analysis. Nutrients 2013;6:111-123. https://doi.org/10.3390/nu6010111
  45. Schmidt SC, Hamann S, Langrehr JM, Hoflich C, Mittler J, Jacob D, et al. Preoperative high-dose steroid administration attenuates the surgical stress response following liver resection: results of a prospective randomized study. J Hepatobiliary Pancreat Surg 2007;14:484-492. https://doi.org/10.1007/s00534-006-1200-7
  46. Pratschke S, von Dossow-Hanfstingl V, Dietz J, Schneider CP, Tufman A, Albertsmeier M, et al. Dehydroepiandrosterone modulates T-cell response after major abdominal surgery. J Surg Res 2014;189:117-125. https://doi.org/10.1016/j.jss.2014.02.002
  47. Li H, Wang C, Yu J, Cao S, Wei F, Zhang W, et al. Dendritic cell-activated cytokine-induced killer cells enhance the anti-tumor effect of chemotherapy on non-small cell lung cancer in patients after surgery. Cytotherapy 2009;11:1076-1083. https://doi.org/10.3109/14653240903121252
  48. Brivio F, Lissoni P, Gilardi R, Ferrante R, Vigore L, Curzi L, et al. Abrogation of surgery-induced decline in circulating dendritic cells by subcutaneous preoperative administration of IL-2 in operable cancer patients. J Biol Regul Homeost Agents 2000;14:200-203.
  49. Nishiyama J, Matsuda M, Ando S, Hirasawa M, Suzuki T, Makuuchi H. The effects of the early administration of sivelestat sodium, a selective neutrophil elastase inhibitor, on the postoperative course after radical surgery for esophageal cancer. Surg Today 2012;42:659-665. https://doi.org/10.1007/s00595-011-0105-5
  50. Ono S, Aosasa S, Mochizuki H. Effects of a protease inhibitor on reduction of surgical stress in esophagectomy. Am J Surg 1999;177:78-82. https://doi.org/10.1016/S0002-9610(98)00300-6
  51. Kerr SF, Klonizakis M, Glynne-Jones R. Suppression of the postoperative neutrophil leucocytosis following neoadjuvant chemoradiotherapy for rectal cancer and implications for surgical morbidity. Colorectal Dis 2010;12:549-554. https://doi.org/10.1111/j.1463-1318.2009.01858.x
  52. Tanis E, Julie C, Emile JF, Mauer M, Nordlinger B, Aust D, et al. Prognostic impact of immune response in resectable colorectal liver metastases treated by surgery alone or surgery with perioperative FOLFOX in the randomised EORTC study 40983. Eur J Cancer 2015;51:2708-2717. https://doi.org/10.1016/j.ejca.2015.08.014
  53. Westerterp M, Boermeester MA, Omloo JM, Hulshof MC, Vervenne WL, Lutter R, et al. Differential responses of cellular immunity in patients undergoing neoadjuvant therapy followed by surgery for carcinoma of the oesophagus. Cancer Immunol Immunother 2008;57:1837-1847. https://doi.org/10.1007/s00262-008-0511-8
  54. Wang D, Yang XL, Chai XQ, Shu SH, Zhang XL, Xie YH, et al. A short-term increase of the postoperative naturally circulating dendritic cells subsets in flurbiprofen-treated patients with esophageal carcinoma undergoing thoracic surgery. Oncotarget 2016;7:18705-18712. https://doi.org/10.18632/oncotarget.7669
  55. Liakopoulos OJ, Dorge H, Schmitto JD, Nagorsnik U, Grabedunkel J, Schoendube FA. Effects of preoperative statin therapy on cytokines after cardiac surgery. Thorac Cardiovasc Surg 2006;54:250-254. https://doi.org/10.1055/s-2006-923836
  56. Amar D, Zhang H, Park B, Heerdt PM, Fleisher M, Thaler HT. Inflammation and outcome after general thoracic surgery. Eur J Cardiothorac Surg 2007;32:431-434. https://doi.org/10.1016/j.ejcts.2007.06.017
  57. De Lorenzo A, Pittella F, Rocha A. Increased preoperative C-reactive protein levels are associated with inhospital death after coronary artery bypass surgery. Inflammation 2012;35:1179-1183. https://doi.org/10.1007/s10753-011-9426-1
  58. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Usefulness of a modified inflammationbased prognostic system for predicting postoperative mortality of patients undergoing surgery for primary hepatocellular carcinoma. J Surg Oncol 2011;103:801-806. https://doi.org/10.1002/jso.21857
  59. Josse JM, Cleghorn MC, Ramji KM, Jiang H, Elnahas A, Jackson TD, et al. The neutrophil-to-lymphocyte ratio predicts major perioperative complications in patients undergoing colorectal surgery. Colorectal Dis 2016;18:O236-O242. https://doi.org/10.1111/codi.13373
  60. Mokart D, Capo C, Blache JL, Delpero JR, Houvenaeghel G, Martin C, et al. Early postoperative compensatory anti-inflammatory response syndrome is associated with septic complications after major surgical trauma in patients with cancer. Br J Surg 2002;89:1450-1456. https://doi.org/10.1046/j.1365-2168.2002.02218.x
  61. Rettig TC, Verwijmeren L, Dijkstra IM, Boerma D, van de Garde EM, Noordzij PG. Postoperative interleukin-6 level and early detection of complications after elective major abdominal surgery. Ann Surg 2016;263:1207-1212. https://doi.org/10.1097/SLA.0000000000001342
  62. Saeed K, Dale AP, Leung E, Cusack T, Mohamed F, Lockyer G, et al. Procalcitonin levels predict infectious complications and response to treatment in patients undergoing cytoreductive surgery for peritoneal malignancy. Eur J Surg Oncol 2016;42:234-243. https://doi.org/10.1016/j.ejso.2015.10.004
  63. Weighardt H, Heidecke CD, Westerholt A, Emmanuilidis K, Maier S, Veit M, et al. Impaired monocyte IL-12 production before surgery as a predictive factor for the lethal outcome of postoperative sepsis. Ann Surg 2002;235:560-567. https://doi.org/10.1097/00000658-200204000-00015
  64. Anitei MG, Zeitoun G, Mlecnik B, Marliot F, Haicheur N, Todosi AM, et al. Prognostic and predictive values of the immunoscore in patients with rectal cancer. Clin Cancer Res 2014;20:1891-1899. https://doi.org/10.1158/1078-0432.CCR-13-2830
  65. Matsutani S, Shibutani M, Maeda K, Nagahara H, Fukuoka T, Nakao S, et al. Significance of tumor-infiltrating lymphocytes before and after neoadjuvant therapy for rectal cancer. Cancer Sci 2018;109:966-979. https://doi.org/10.1111/cas.13542
  66. Ishizuka M, Nagata H, Takagi K, Iwasaki Y, Kubota K. Systemic inflammatory response predicts perioperative central venous catheter-related bloodstream infection in patients Undergoing colorectal cancer surgery with administration of parenteral nutrition. Anticancer Res 2012;32:4045-4050.
  67. Strohmeyer JC, Blume C, Meisel C, Doecke WD, Hummel M, Hoeflich C, et al. Standardized immune monitoring for the prediction of infections after cardiopulmonary bypass surgery in risk patients. Cytometry B Clin Cytom 2003;53:54-62.
  68. Song B, Zhen S, Meng F. T cell inflammation profile after surgical resection may predict tumor recurrence in HBV-related hepatocellular carcinoma. Int Immunopharmacol 2016;41:35-41. https://doi.org/10.1016/j.intimp.2016.10.015
  69. Chan AW, Chan SL, Wong GL, Wong VW, Chong CC, Lai PB, et al. Prognostic nutritional index (PNI) predicts tumor recurrence of very early/early stage hepatocellular carcinoma after surgical resection. Ann Surg Oncol 2015;22:4138-4148. https://doi.org/10.1245/s10434-015-4516-1
  70. Lindenmann J, Fink-Neuboeck N, Avian A, Pichler M, Habitzruther M, Maier A, et al. Preoperative Glasgow prognostic score as additional independent prognostic parameter for patients with esophageal cancer after curative esophagectomy. Eur J Surg Oncol 2017;43:445-453. https://doi.org/10.1016/j.ejso.2016.10.015
  71. Toiyama Y, Inoue Y, Saigusa S, Kawamura M, Kawamoto A, Okugawa Y, et al. C-reactive protein as predictor of recurrence in patients with rectal cancer undergoing chemoradiotherapy followed by surgery. Anticancer Res 2013;33:5065-5074.
  72. Wei IH, Harmon CM, Arcerito M, Cheng DF, Minter RM, Simeone DM. Tumor-associated macrophages are a useful biomarker to predict recurrence after surgical resection of nonfunctional pancreatic neuroendocrine tumors. Ann Surg 2014;260:1088-1094. https://doi.org/10.1097/SLA.0000000000000262
  73. Galizia G, Lieto E, Auricchio A, Cardella F, Mabilia A, Podzemny V, et al. Naples prognostic score, based on nutritional and inflammatory status, is an independent predictor of long-term outcome in patients undergoing surgery for colorectal cancer. Dis Colon Rectum 2017;60:1273-1284. https://doi.org/10.1097/DCR.0000000000000961
  74. He YF, Luo HQ, Wang W, Chen J, Yao YW, Yan Y, et al. Preoperative NLR and PLR in the middle or lower ESCC patients with radical operation. Eur J Cancer Care (Engl) 2017;26:e12445. https://doi.org/10.1111/ecc.12445
  75. Ishizuka M, Nagata H, Takagi K, Iwasaki Y, Shibuya N, Kubota K. Clinical significance of the C-reactive protein to albumin ratio for survival after surgery for colorectal cancer. Ann Surg Oncol 2016;23:900-907. https://doi.org/10.1245/s10434-015-4948-7
  76. Ishizuka M, Oyama Y, Abe A, Kubota K. Combination of platelet count and neutrophil to lymphocyte ratio is a useful predictor of postoperative survival in patients undergoing surgery for gastric cancer. J Surg Oncol 2014;110:935-941. https://doi.org/10.1002/jso.23753
  77. Malietzis G, Giacometti M, Askari A, Nachiappan S, Kennedy RH, Faiz OD, et al. A preoperative neutrophil to lymphocyte ratio of 3 predicts disease-free survival after curative elective colorectal cancer surgery. Ann Surg 2014;260:287-292. https://doi.org/10.1097/SLA.0000000000000216
  78. Mimatsu K, Fukino N, Ogasawara Y, Saino Y, Oida T. Utility of inflammatory marker- and nutritional status-based prognostic factors for predicting the prognosis of stage IV gastric cancer patients undergoing non-curative surgery. Anticancer Res 2017;37:4215-4222.
  79. Watt DG, Martin JC, Park JH, Horgan PG, McMillan DC. Neutrophil count is the most important prognostic component of the differential white cell count in patients undergoing elective surgery for colorectal cancer. Am J Surg 2015;210:24-30. https://doi.org/10.1016/j.amjsurg.2014.12.031
  80. Yamamoto T, Yanagimoto H, Satoi S, Toyokawa H, Yamao J, Kim S, et al. Circulating myeloid dendritic cells as prognostic factors in patients with pancreatic cancer who have undergone surgical resection. J Surg Res 2012;173:299-308. https://doi.org/10.1016/j.jss.2010.09.027
  81. Zikos TA, Donnenberg AD, Landreneau RJ, Luketich JD, Donnenberg VS. Lung T-cell subset composition at the time of surgical resection is a prognostic indicator in non-small cell lung cancer. Cancer Immunol Immunother 2011;60:819-827. https://doi.org/10.1007/s00262-011-0996-4
  82. Jin Z, Li R, Liu J, Lin J. Long-term prognosis after cancer surgery with inhalational anesthesia and total intravenous anesthesia: a systematic review and meta-analysis. Int J Physiol Pathophysiol Pharmacol 2019;11:83-94.
  83. Weng M, Chen W, Hou W, Li L, Ding M, Miao C. The effect of neuraxial anesthesia on cancer recurrence and survival after cancer surgery: an updated meta-analysis. Oncotarget 2016;7:15262-15273. https://doi.org/10.18632/oncotarget.7683
  84. Giger-Pabst U, Lange J, Maurer C, Bucher C, Schreiber V, Schlumpf R, et al. Short-term preoperative supplementation of an immunoenriched diet does not improve clinical outcome in well-nourished patients undergoing abdominal cancer surgery. Nutrition 2013;29:724-729. https://doi.org/10.1016/j.nut.2012.10.007
  85. Klek S, Sierzega M, Szybinski P, Szczepanek K, Scislo L, Walewska E, et al. The immunomodulating enteral nutrition in malnourished surgical patients - a prospective, randomized, double-blind clinical trial. Clin Nutr 2011;30:282-288. https://doi.org/10.1016/j.clnu.2010.10.001
  86. Chen L, Sun L, Lang Y, Wu J, Yao L, Ning J, et al. Fast-track surgery improves postoperative clinical recovery and cellular and humoral immunity after esophagectomy for esophageal cancer. BMC Cancer 2016;16:449. https://doi.org/10.1186/s12885-016-2506-8
  87. Liu HT, Huang YC, Cheng SB, Huang YT, Lin PT. Effects of coenzyme Q10 supplementation on antioxidant capacity and inflammation in hepatocellular carcinoma patients after surgery: a randomized, placebo-controlled trial. Nutr J 2016;15:85. https://doi.org/10.1186/s12937-016-0205-6
  88. Parolari A, Camera M, Alamanni F, Naliato M, Polvani GL, Agrifoglio M, et al. Systemic inflammation after on-pump and off-pump coronary bypass surgery: a one-month follow-up. Ann Thorac Surg 2007;84:823-828. https://doi.org/10.1016/j.athoracsur.2007.04.048
  89. Papadima A, Boutsikou M, Lagoudianakis EE, Kataki A, Konstadoulakis M, Georgiou L, et al. Lymphocyte apoptosis after major abdominal surgery is not influenced by anesthetic technique: a comparative study of general anesthesia versus combined general and epidural analgesia. J Clin Anesth 2009;21:414-421. https://doi.org/10.1016/j.jclinane.2008.10.015
  90. Reisinger KW, Derikx JP, van Vugt JL, Von Meyenfeldt MF, Hulsewe KW, Olde Damink SW, et al. Sarcopenia is associated with an increased inflammatory response to surgery in colorectal cancer. Clin Nutr 2016;35:924-927. https://doi.org/10.1016/j.clnu.2015.07.005
  91. Buttenschoen K, Schneider ME, Utz K, Kornmann M, Beger HG, Carli Buttenschoen D. Effect of major abdominal surgery on endotoxin release and expression of Toll-like receptors 2/4. Langenbecks Arch Surg 2009;394:293-302. https://doi.org/10.1007/s00423-008-0357-8
  92. Brix-Christensen V, Tonnesen E, Sorensen IJ, Bilfinger TV, Sanchez RG, Stefano GB. Effects of anaesthesia based on high versus low doses of opioids on the cytokine and acute-phase protein responses in patients undergoing cardiac surgery. Acta Anaesthesiol Scand 1998;42:63-70. https://doi.org/10.1111/j.1399-6576.1998.tb05082.x
  93. Greco F, Hoda MR, Wagner S, Reichelt O, Inferrera A, Fischer K, et al. Adipocytokine: a new family of inflammatory and immunologic markers of invasiveness in major urologic surgery. Eur Urol 2010;58:781-787. https://doi.org/10.1016/j.eururo.2010.07.022
  94. Iwasaki A, Shirakusa T, Maekawa T, Enatsu S, Maekawa S. Clinical evaluation of systemic inflammatory response syndrome (SIRS) in advanced lung cancer (T3 and T4) with surgical resection. Eur J Cardiothorac Surg 2005;27:14-18. https://doi.org/10.1016/j.ejcts.2004.09.006
  95. Bruce DM, Smith M, Walker CB, Heys SD, Binnie NR, Gough DB, et al. Minimal access surgery for cholelithiasis induces an attenuated acute phase response. Am J Surg 1999;178:232-234. https://doi.org/10.1016/S0002-9610(99)00160-9
  96. Mokart D, Merlin M, Sannini A, Brun JP, Delpero JR, Houvenaeghel G, et al. Procalcitonin, interleukin 6 and systemic inflammatory response syndrome (SIRS): early markers of postoperative sepsis after major surgery. Br J Anaesth 2005;94:767-773. https://doi.org/10.1093/bja/aei143
  97. Karth GD, Buberl A, Nikfardjam M, Meyer B, Wollenek G, Grimm M, et al. Role of amiodarone on the systemic inflammatory response induced by cardiac surgery: proinflammatory actions. Can J Anaesth 2007;54:262-268. https://doi.org/10.1007/BF03022770
  98. Ni XC, Yi Y, Fu YP, He HW, Cai XY, Wang JX, et al. Prognostic value of the modified Glasgow prognostic score in patients undergoing radical surgery for hepatocellular carcinoma. Medicine (Baltimore) 2015;94:e1486. https://doi.org/10.1097/MD.0000000000001486
  99. Ji F, Liang Y, Fu SJ, Guo ZY, Shu M, Shen SL, et al. A novel and accurate predictor of survival for patients with hepatocellular carcinoma after surgical resection: the neutrophil to lymphocyte ratio (NLR) combined with the aspartate aminotransferase/platelet count ratio index (APRI). BMC Cancer 2016;16:137. https://doi.org/10.1186/s12885-016-2189-1
  100. Dias Rodrigues V, Barroso de Pinho N, Abdelhay E, Viola JP, Correia MI, Brum Martucci R. Nutrition and immune-modulatory intervention in surgical patients with gastric cancer. Nutr Clin Pract 2017;32:122-129. https://doi.org/10.1177/0884533616653807
  101. Sun KY, Xu JB, Chen SL, Yuan YJ, Wu H, Peng JJ, et al. Novel immunological and nutritional-based prognostic index for gastric cancer. World J Gastroenterol 2015;21:5961-5971. https://doi.org/10.3748/wjg.v21.i19.5961
  102. Xie X, Luo KJ, Hu Y, Wang JY, Chen J. Prognostic value of preoperative platelet-lymphocyte and neutrophil-lymphocyte ratio in patients undergoing surgery for esophageal squamous cell cancer. Dis Esophagus 2016;29:79-85. https://doi.org/10.1111/dote.12296
  103. Liao R, Jiang N, Tang ZW, Li W, Huang P, Luo SQ, et al. Systemic and intratumoral balances between monocytes/macrophages and lymphocytes predict prognosis in hepatocellular carcinoma patients after surgery. Oncotarget 2016;7:30951-30961. https://doi.org/10.18632/oncotarget.9049
  104. Hyun MH, Lee CH, Kwon YJ, Cho SI, Jang YJ, Kim DH, et al. Robot versus laparoscopic gastrectomy for cancer by an experienced surgeon: comparisons of surgery, complications, and surgical stress. Ann Surg Oncol 2013;20:1258-1265. https://doi.org/10.1245/s10434-012-2679-6
  105. Hsu JT, Wang CC, Le PH, Chen TH, Kuo CJ, Lin CJ, et al. Lymphocyte-to-monocyte ratios predict gastric cancer surgical outcomes. J Surg Res 2016;202:284-290. https://doi.org/10.1016/j.jss.2016.01.005
  106. Pang S, Zhou Z, Yu X, Wei S, Chen Q, Nie S, et al. The predictive value of integrated inflammation scores in the survival of patients with resected hepatocellular carcinoma: a retrospective cohort study. Int J Surg 2017;42:170-177. https://doi.org/10.1016/j.ijsu.2017.04.018
  107. Jain S, Gautam V, Naseem S. Acute-phase proteins: As diagnostic tool. J Pharm Bioallied Sci 2011;3:118-127. https://doi.org/10.4103/0975-7406.76489
  108. Warschkow R, Tarantino I, Ukegjini K, Beutner U, Muller SA, Schmied BM, et al. Diagnostic study and meta-analysis of C-reactive protein as a predictor of postoperative inflammatory complications after gastroesophageal cancer surgery. Langenbecks Arch Surg 2012;397:727-736. https://doi.org/10.1007/s00423-012-0944-6
  109. Warschkow R, Ukegjini K, Tarantino I, Steffen T, Muller SA, Schmied BM, et al. Diagnostic study and meta-analysis of C-reactive protein as a predictor of postoperative inflammatory complications after pancreatic surgery. J Hepatobiliary Pancreat Sci 2012;19:492-500. https://doi.org/10.1007/s00534-011-0462-x
  110. Kim S, McClave SA, Martindale RG, Miller KR, Hurt RT. Hypoalbuminemia and Clinical Outcomes: What is the Mechanism behind the Relationship? Am Surg 2017;83:1220-1227. https://doi.org/10.1177/000313481708301123
  111. Iwaku A, Kinoshita A, Onoda H, Fushiya N, Nishino H, Matsushima M, et al. The Glasgow prognostic score accurately predicts survival in patients with biliary tract cancer not indicated for surgical resection. Med Oncol 2014;31:787. https://doi.org/10.1007/s12032-013-0787-1
  112. Dupre A, Malik HZ. Inflammation and cancer: what a surgical oncologist should know. Eur J Surg Oncol 2018;44:566-570. https://doi.org/10.1016/j.ejso.2018.02.209
  113. Roxburgh CS, Salmond JM, Horgan PG, Oien KA, McMillan DC. The relationship between the local and systemic inflammatory responses and survival in patients undergoing curative surgery for colon and rectal cancers. J Gastrointest Surg 2009;13:2011-2018. https://doi.org/10.1007/s11605-009-1034-0
  114. Guner A, Kim HI. ASO Author Reflections: Parameters for Predicting Surgical Outcomes for Gastric Cancer Patients: Simple Is Better Than Complex. Ann Surg Oncol 2018;25:699-700. https://doi.org/10.1245/s10434-018-6725-x
  115. Lee JY, Kim HI, Kim YN, Hong JH, Alshomimi S, An JY, et al. Clinical significance of the prognostic nutritional index for predicting short- and long-term surgical outcomes after gastrectomy: a retrospective analysis of 7781 gastric cancer patients. Medicine (Baltimore) 2016;95:e3539. https://doi.org/10.1097/MD.0000000000003539
  116. Kohira S, Oka N, Inoue N, Itatani K, Hanayama N, Kitamura T, et al. Effect of the neutrophil elastase inhibitor sivelestat on perioperative inflammatory response after pediatric heart surgery with cardiopulmonary bypass: a prospective randomized study. Artif Organs 2013;37:1027-1033. https://doi.org/10.1111/aor.12103
  117. Ng CS, Lee TW, Wan S, Wan IY, Sihoe AD, Arifi AA, et al. Thoracotomy is associated with significantly more profound suppression in lymphocytes and natural killer cells than video-assisted thoracic surgery following major lung resections for cancer. J Invest Surg 2005;18:81-88. https://doi.org/10.1080/08941930590926320
  118. Volk T, Schenk M, Voigt K, Tohtz S, Putzier M, Kox WJ. Postoperative epidural anesthesia preserves lymphocyte, but not monocyte, immune function after major spine surgery. Anesth Analg 2004;98:1086-1092.
  119. Ammendola M, Sacco R, Zuccala V, Luposella M, Patruno R, Gadaleta P, et al. Mast cells density positive to tryptase correlate with microvascular density in both primary gastric cancer tissue and loco-regional lymph node metastases from patients that have undergone radical surgery. Int J Mol Sci 2016;17:1905. https://doi.org/10.3390/ijms17111905
  120. Decker D, Tolba R, Springer W, Lauschke H, Hirner A, von Ruecker A. Abdominal surgical interventions: local and systemic consequences for the immune system--a prospective study on elective gastrointestinal surgery. J Surg Res 2005;126:12-18. https://doi.org/10.1016/j.jss.2005.01.006
  121. Leal-Noval SR, Munoz-Gomez M, Arellano V, Adsuar A, Jimenez-Sanchez M, Corcia Y, et al. Influence of red blood cell transfusion on $CD4^{+}$ T-helper cells immune response in patients undergoing cardiac surgery. J Surg Res 2010;164:43-49. https://doi.org/10.1016/j.jss.2009.03.010
  122. Matsuda A, Furukawa K, Takasaki H, Suzuki H, Kan H, Tsuruta H, et al. Preoperative oral immuneenhancing nutritional supplementation corrects Th1/Th2 imbalance in patients undergoing elective surgery for colorectal cancer. Dis Colon Rectum 2006;49:507-516. https://doi.org/10.1007/s10350-005-0292-5
  123. Kirman I, Belizon A, Balik E, Feingold D, Arnell T, Horst P, et al. Perioperative sargramostim (recombinant human GM-CSF) induces an increase in the level of soluble VEGFR1 in colon cancer patients undergoing minimally invasive surgery. Eur J Surg Oncol 2007;33:1169-1176. https://doi.org/10.1016/j.ejso.2007.03.014
  124. Crucitti A, Corbi M, Tomaiuolo PM, Fanali C, Mazzari A, Lucchetti D, et al. Laparoscopic surgery for colorectal cancer is not associated with an increase in the circulating levels of several inflammationrelated factors. Cancer Biol Ther 2015;16:671-677. https://doi.org/10.1080/15384047.2015.1026476
  125. Spittler A, Sautner T, Gornikiewicz A, Manhart N, Oehler R, Bergmann M, et al. Postoperative glycylglutamine infusion reduces immunosuppression: partial prevention of the surgery induced decrease in HLA-DR expression on monocytes. Clin Nutr 2001;20:37-42. https://doi.org/10.1054/clnu.2000.0153
  126. Welters ID, Feurer MK, Preiss V, Muller M, Scholz S, Kwapisz M, et al. Continuous S-(+)-ketamine administration during elective coronary artery bypass graft surgery attenuates pro-inflammatory cytokine response during and after cardiopulmonary bypass. Br J Anaesth 2011;106:172-179. https://doi.org/10.1093/bja/aeq341
  127. Ikuta S, Miki C, Hatada T, Inoue Y, Araki T, Tanaka K, et al. Allogenic blood transfusion is an independent risk factor for infective complications after less invasive gastrointestinal surgery. Am J Surg 2003;185:188-193. https://doi.org/10.1016/S0002-9610(02)01370-3
  128. Leijte GP, Custers H, Gerretsen J, Heijne A, Roth J, Vogl T, et al. Increased plasma levels of dangerassociated molecular patterns are associated with immune suppression and postoperative infections in patients undergoing cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Front Immunol 2018;9:663. https://doi.org/10.3389/fimmu.2018.00663
  129. Schilling T, Kozian A, Senturk M, Huth C, Reinhold A, Hedenstierna G, et al. Effects of volatile and intravenous anesthesia on the alveolar and systemic inflammatory response in thoracic surgical patients. Anesthesiology 2011;115:65-74. https://doi.org/10.1097/ALN.0b013e318214b9de
  130. Zak-Nejmark T, Jankowska R, Passowicz-Muszynska E, Malolepszy J, Marciniak M, Jonkisz A, et al. Skin reactivity to histamine and expression of histamine receptors mRNA in lymphocytes of healthy subjects and non-small-cell lung cancer patients before and after surgery. Lung Cancer 2004;45:31-38. https://doi.org/10.1016/j.lungcan.2004.01.005
  131. Leaver HA, Craig SR, Yap PL, Walker WS. Lymphocyte responses following open and minimally invasive thoracic surgery. Eur J Clin Invest 2000;30:230-238. https://doi.org/10.1046/j.1365-2362.2000.00622.x
  132. Qadan M, Battista C, Gardner SA, Anderson G, Akca O, Polk HC Jr. Oxygen and surgical site infection: a study of underlying immunologic mechanisms. Anesthesiology 2010;113:369-377. https://doi.org/10.1097/ALN.0b013e3181e19d1d
  133. Kim HI, Kim H, Cho HW, Kim SY, Song KJ, Hyung WJ, et al. The ratio of intra-tumoral regulatory T cells (Foxp3+)/helper T cells (CD4+) is a prognostic factor and associated with recurrence pattern in gastric cardia cancer. J Surg Oncol 2011;104:728-733. https://doi.org/10.1002/jso.22038
  134. Lee JY, Son T, Cheong JH, Hyung WJ, Noh SH, Kim CB, et al. Association between chemotherapyresponse assays and subsets of tumor-infiltrating lymphocytes in gastric cancer: a pilot study. J Gastric Cancer 2015;15:223-230. https://doi.org/10.5230/jgc.2015.15.4.223
  135. Lee S, Choi S, Kim SY, Yun MJ, Kim HI. Potential utility of FDG PET-CT as a non-invasive tool for monitoring local immune responses. J Gastric Cancer 2017;17:384-393. https://doi.org/10.5230/jgc.2017.17.e43
  136. Zhuang Y, Peng LS, Zhao YL, Shi Y, Mao XH, Chen W, et al. $CD8^{+}$ T cells that produce interleukin-17 regulate myeloid-derived suppressor cells and are associated with survival time of patients with gastric cancer. Gastroenterology 2012;143:951-62.e8. https://doi.org/10.1053/j.gastro.2012.06.010
  137. Gerard A, Beemiller P, Friedman RS, Jacobelli J, Krummel MF. Evolving immune circuits are generated by flexible, motile, and sequential immunological synapses. Immunol Rev 2013;251:80-96. https://doi.org/10.1111/imr.12021
  138. Xie J, Tato CM, Davis MM. How the immune system talks to itself: the varied role of synapses. Immunol Rev 2013;251:65-79. https://doi.org/10.1111/imr.12017
  139. Annunziato F, Romagnani C, Romagnani S. The 3 major types of innate and adaptive cell-mediated effector immunity. J Allergy Clin Immunol 2015;135:626-635. https://doi.org/10.1016/j.jaci.2014.11.001
  140. Romagnani S. T-cell subsets (Th1 versus Th2). Ann Allergy Asthma Immunol 2000;85:9-18. https://doi.org/10.1016/S1081-1206(10)62426-X
  141. Moraga I, Spangler J, Mendoza JL, Garcia KC. Multifarious determinants of cytokine receptor signaling specificity. Adv Immunol 2014;121:1-39. https://doi.org/10.1016/B978-0-12-800100-4.00001-5
  142. Miller MC, Mayo KH. Chemokines from a structural perspective. Int J Mol Sci 2017;18:18. https://doi.org/10.3390/ijms18010018
  143. Lin E, Calvano SE, Lowry SF. Inflammatory cytokines and cell response in surgery. Surgery 2000;127:117-126. https://doi.org/10.1067/msy.2000.101584
  144. Cavaillon JM, Singer M. Inflammation: From Molecular and Cellular Mechanisms to the Clinic. Weinheim: Wiley-VCH; 2017.
  145. Datta J, Berk E, Xu S, Fitzpatrick E, Rosemblit C, Lowenfeld L, et al. Anti-HER2 $CD4^{+}$ T-helper type 1 response is a novel immune correlate to pathologic response following neoadjuvant therapy in HER2- positive breast cancer. Breast Cancer Res 2015;17:71. https://doi.org/10.1186/s13058-015-0584-1
  146. Kvarnstrom A, Swartling T, Kurlberg G, Bengtson JP, Bengtsson A. Pro-inflammatory cytokine release in rectal surgery: comparison between laparoscopic and open surgical techniques. Arch Immunol Ther Exp (Warsz) 2013;61:407-411. https://doi.org/10.1007/s00005-013-0239-9
  147. Wu FP, Sietses C, von Blomberg BM, van Leeuwen PA, Meijer S, Cuesta MA. Systemic and peritoneal inflammatory response after laparoscopic or conventional colon resection in cancer patients: a prospective, randomized trial. Dis Colon Rectum 2003;46:147-155. https://doi.org/10.1007/s10350-004-6516-2
  148. Leung KL, Lai PB, Ho RL, Meng WC, Yiu RY, Lee JF, et al. Systemic cytokine response after laparoscopicassisted resection of rectosigmoid carcinoma: a prospective randomized trial. Ann Surg 2000;231:506-511. https://doi.org/10.1097/00000658-200004000-00008
  149. Ahlers O, Nachtigall I, Lenze J, Goldmann A, Schulte E, Hohne C, et al. Intraoperative thoracic epidural anaesthesia attenuates stress-induced immunosuppression in patients undergoing major abdominal surgery. Br J Anaesth 2008;101:781-787. https://doi.org/10.1093/bja/aen287
  150. Sun HZ, Song YL, Wang XY. Effects of different anesthetic methods on cellular immune and neuroendocrine functions in patients with hepatocellular carcinoma before and after surgery. J Clin Lab Anal 2016;30:1175-1182. https://doi.org/10.1002/jcla.22000
  151. Yeh CN, Lee HL, Liu YY, Chiang KC, Hwang TL, Jan YY, et al. The role of parenteral glutamine supplement for surgical patient perioperatively: result of a single center, prospective and controlled study. Langenbecks Arch Surg 2008;393:849-855. https://doi.org/10.1007/s00423-008-0405-4
  152. Chen DW, Wei Fei Z, Zhang YC, Ou JM, Xu J. Role of enteral immunonutrition in patients with gastric carcinoma undergoing major surgery. Asian J Surg 2005;28:121-124. https://doi.org/10.1016/S1015-9584(09)60275-X
  153. Watt SK, Hasselbalch HC, Skov V, Kjær L, Thomassen M, Kruse TA, et al. Whole blood gene expression profiling in patients undergoing colon cancer surgery identifies differential expression of genes involved in immune surveillance, inflammation and carcinogenesis. Surg Oncol 2018;27:208-215. https://doi.org/10.1016/j.suronc.2018.03.002
  154. Allen CJ, Griswold AJ, Schulman CI, Sleeman D, Levi JU, Livingstone AS, et al. Global gene expression change induced by major thoracoabdominal surgery. Ann Surg 2017;266:981-987. https://doi.org/10.1097/SLA.0000000000001992
  155. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014;513:202-209. https://doi.org/10.1038/nature13480
  156. Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, et al. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods 2015;12:453-457. https://doi.org/10.1038/nmeth.3337
  157. Altman DG, McShane LM, Sauerbrei W, Taube SE. Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med 2012;9:e1001216. https://doi.org/10.1371/journal.pmed.1001216
  158. Cohen JF, Korevaar DA, Altman DG, Bruns DE, Gatsonis CA, Hooft L, et al. STARD 2015 guidelines for reporting diagnostic accuracy studies: explanation and elaboration. BMJ Open 2016;6:e012799. https://doi.org/10.1136/bmjopen-2016-012799
  159. Welsch T, Muller SA, Ulrich A, Kischlat A, Hinz U, Kienle P, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22:1499-1507. https://doi.org/10.1007/s00384-007-0354-3
  160. Lee K, Hwang H, Nam KT. Immune response and the tumor microenvironment: how they communicate to regulate gastric cancer. Gut Liver 2014;8:131-139. https://doi.org/10.5009/gnl.2014.8.2.131
  161. Kim CH, Park SM, Kim JJ. The impact of preoperative low body mass index on postoperative complications and long-term survival outcomes in gastric cancer patients. J Gastric Cancer 2018;18:274-286. https://doi.org/10.5230/jgc.2018.18.e30
  162. Seo HS, Jung YJ, Kim JH, Park CH, Kim IH, Lee HH. Long-term nutritional outcomes of near-total gastrectomy in gastric cancer treatment: a comparison with total gastrectomy using propensity score matching analysis. J Gastric Cancer 2018;18:189-199. https://doi.org/10.5230/jgc.2018.18.e21
  163. Lee HJ, Hyung WJ, Yang HK, Han SU, Park YK, An JY, et al. Short-term outcomes of a multicenter randomized controlled trial comparing laparoscopic distal gastrectomy with D2 lymphadenectomy to open distal gastrectomy for locally advanced gastric cancer (KLASS-02-RCT). Ann Surg. Forthcoming 2019.
  164. Kim HH, Han SU, Kim MC, Kim W, Lee HJ, Ryu SW, et al. Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with stage I gastric cancer: The KLASS-01 Randomized Clinical Trial. JAMA Oncol 2019;5:506-513. https://doi.org/10.1001/jamaoncol.2018.6727
  165. Desiderio J, Stewart CL, Sun V, Melstrom L, Warner S, Lee B, et al. Enhanced recovery after surgery for gastric cancer patients improves clinical outcomes at a US Cancer Center. J Gastric Cancer 2018;18:230-241. https://doi.org/10.5230/jgc.2018.18.e24
  166. Mortensen K, Nilsson M, Slim K, Schafer M, Mariette C, Braga M, et al. Consensus guidelines for enhanced recovery after gastrectomy: Enhanced Recovery After Surgery $(ERAS^{(R)})$ Society recommendations. Br J Surg 2014;101:1209-1229. https://doi.org/10.1002/bjs.9582

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