Abstract
Purpose
This study aimed to clarify the relationship between obesity and postoperative C-reactive protein (CRP) and assess the usefulness of obesity status-adjusted CRP levels for predicting early complications following laparoscopic gastrectomy for gastric cancer.
Methods
This study retrospectively analyzed 527 patients who underwent laparoscopic gastrectomy for gastric cancer between January 2013 and March 2019. Patients were classified into three groups according to body mass index (BMI): BMI < 20; BMI ≥ 20 to < 25; and BMI ≥ 25. The correlation between BMI and perioperative CRP was investigated in 447 patients, excluding 80 with postoperative complications. The optimal CRP cutoff value of Clavien–Dindo (CD) grade ≥ 3 for predicting severe complications for each group was determined.
Results
BMI was significantly correlated with CRP on postoperative day (POD) 3 (p < 0.001) in 447 patients without complications. According to the receiver operating characteristic curve analysis, CRP cutoff values on POD 3 for predicting severe complications were 92.4, 111.1, and 171.9 in the BMI < 20, BMI ≥ 20 to < 25, and BMI ≥ 25 groups, respectively. In multivariate analysis for CD grade ≥ 3 complications, cardiac history and POD 3 CRP levels higher than the adjusted cutoff were identified as independent factors significantly associated with severe complications (p = 0.021 and 0.015, respectively).
Conclusion
CRP cutoff values on POD 3 adjusted for BMI were useful for predicting severe complications in gastrectomy for gastric cancer.
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References
Katai H, Mizusawa J, Katayama H, Takagi M, Yoshikawa T, Fukagawa T, Terashima M, Misawa K, Teshima S, Koeda K, Nunobe S, Fukushima N, Yasuda T, Asao Y, Fujiwara Y, Sasako M (2017) Short-term surgical outcomes from a phase III study of laparoscopy-assisted versus open distal gastrectomy with nodal dissection for clinical stage IA/IB gastric cancer: Japan Clinical Oncology Group Study JCOG0912. Gastric Cancer 20(4):699–708. https://doi.org/10.1007/s10120-016-0646-9
Kim W, Kim HH, Han SU, Kim MC, Hyung WJ, Ryu SW, Cho GS, Kim CY, Yang HK, Park DJ, Song KY, Lee SI, Ryu SY, Lee JH, Lee HJ, Korean Laparo-endoscopic Gastrointestinal Surgery Study G (2016) Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric cancer: short-term outcomes from a multicenter randomized controlled trial (KLASS-01). Ann Surg 263(1):28–35. https://doi.org/10.1097/SLA.0000000000001346
Bickenbach KA, Denton B, Gonen M, Brennan MF, Coit DG, Strong VE (2013) Impact of obesity on perioperative complications and long-term survival of patients with gastric cancer. Ann Surg Oncol 20(3):780–787. https://doi.org/10.1245/s10434-012-2653-3
Inagawa S, Adachi S, Oda T, Kawamoto T, Koike N, Fukao K (2000) Effect of fat volume on postoperative complications and survival rate after D2 dissection for gastric cancer. Gastric Cancer 3(3):141–144. https://doi.org/10.1007/pl00011708
Shimada S, Sawada N, Ishiyama Y, Nakahara K, Maeda C, Mukai S, Hidaka E, Ishida F, Kudo SE (2018) Impact of obesity on short- and long-term outcomes of laparoscopy assisted distal gastrectomy for gastric cancer. Surg Endosc 32(1):358–366. https://doi.org/10.1007/s00464-017-5684-9
Sasako M, Sakuramoto S, Katai H, Kinoshita T, Furukawa H, Yamaguchi T, Nashimoto A, Fujii M, Nakajima T, Ohashi Y (2011) Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol 29(33):4387–4393. https://doi.org/10.1200/JCO.2011.36.5908
Smyth EC, Wotherspoon A, Peckitt C, Gonzalez D, Hulkki-Wilson S, Eltahir Z, Fassan M, Rugge M, Valeri N, Okines A, Hewish M, Allum W, Stenning S, Nankivell M, Langley R, Cunningham D (2017) Mismatch repair deficiency, microsatellite instability, and survival: an exploratory analysis of the Medical Research Council Adjuvant Gastric Infusional Chemotherapy (MAGIC) Trial. JAMA Oncol 3(9):1197–1203. https://doi.org/10.1001/jamaoncol.2016.6762
Nagasako Y, Satoh S, Isogaki J, Inaba K, Taniguchi K, Uyama I (2012) Impact of anastomotic complications on outcome after laparoscopic gastrectomy for early gastric cancer. Br J Surg 99(6):849–854. https://doi.org/10.1002/bjs.8730
Li Z, Bai B, Zhao Y, Yu D, Lian B, Liu Y, Zhao Q (2018) Severity of complications and long-term survival after laparoscopic total gastrectomy with D2 lymph node dissection for advanced gastric cancer: a propensity score-matched, case-control study. Int J Surg 54(Pt A):62–69. https://doi.org/10.1016/j.ijsu.2018.04.034
Matsunaga T, Saito H, Murakami Y, Kuroda H, Fukumoto Y, Osaki T (2017) Serum level of C-reactive protein on postoperative day 3 is a predictive indicator of postoperative pancreatic fistula after laparoscopic gastrectomy for gastric cancer. Asian J Endosc Surg 10(4):382–387. https://doi.org/10.1111/ases.12374
Tanaka H, Tamura T, Toyokawa T, Muguruma K, Kubo N, Sakurai K, Ohira M (2019) C-reactive protein elevation ratio as an early predictor of postoperative severe complications after laparoscopic gastrectomy for gastric cancer: a retrospective study. BMC Surg 19(1):114. https://doi.org/10.1186/s12893-019-0582-9
Sun F, Ge X, Liu Z, Du S, Ai S, Guan W (2017) Postoperative C-reactive protein/albumin ratio as a novel predictor for short-term complications following gastrectomy of gastric cancer. World J Surg Oncol 15(1):191. https://doi.org/10.1186/s12957-017-1258-5
Okamura A, Watanabe M, Fukudome I, Yamashita K, Yuda M, Hayami M, Imamura Y, Mine S (2018) Relationship between visceral obesity and postoperative inflammatory response following minimally invasive esophagectomy. World J Surg 42(11):3651–3657. https://doi.org/10.1007/s00268-018-4675-x
Paepegaey AC, Genser L, Bouillot JL, Oppert JM, Clement K, Poitou C (2015) High levels of CRP in morbid obesity: the central role of adipose tissue and lessons for clinical practice before and after bariatric surgery. Surg Obes Relat Dis 11(1):148–154. https://doi.org/10.1016/j.soard.2014.06.010
Mori T, Kimura T, Kitajima M (2010) Skill accreditation system for laparoscopic gastroenterologic surgeons in Japan. Minim Invasive Ther Allied Technol 19(1):18–23. https://doi.org/10.3109/13645700903492969
Lee JH, Park B, Joo J, Kook MC, Kim YI, Lee JY, Kim CG, Choi IJ, Eom BW, Yoon HM, Ryu KW, Kim YW, Cho SJ (2018) Body mass index and mortality in patients with gastric cancer: a large cohort study. Gastric Cancer 21(6):913–924. https://doi.org/10.1007/s10120-018-0818-x
Brierley J, Gospodarowicz MK, Wittekind C (2017) TNM classification of malignant tumours. Eighth edition. edn. John Wiley & Sons, Inc., Chichester, West Sussex, UK ; Hoboken, NJ
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 a survey. Ann Surg 240(2):205–213. https://doi.org/10.1097/01.sla.0000133083.54934.ae
Katai H, Sasako M, Fukuda H, Nakamura K, Hiki N, Saka M, Yamaue H, Yoshikawa T, Kojima K, Group JGCSS (2010) Safety and feasibility of laparoscopy-assisted distal gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer: a multicenter phase II trial (JCOG 0703). Gastric Cancer 13(4):238–244. https://doi.org/10.1007/s10120-010-0565-0
Tsujimoto H, Ichikura T, Ono S, Sugasawa H, Hiraki S, Sakamoto N, Yaguchi Y, Yoshida K, Matsumoto Y, Hase K (2009) Impact of postoperative infection on long-term survival after potentially curative resection for gastric cancer. Ann Surg Oncol 16(2):311–318. https://doi.org/10.1245/s10434-008-0249-8
Wang S, Xu L, Wang Q, Li J, Bai B, Li Z, Wu X, Yu P, Li X, Yin J (2019) Postoperative complications and prognosis after radical gastrectomy for gastric cancer: a systematic review and meta-analysis of observational studies. World J Surg Oncol 17(1):52. https://doi.org/10.1186/s12957-019-1593-9
Tu RH, Lin JX, Li P, Xie JW, Wang JB, Lu J, Chen QY, Cao LL, Lin M, Zheng CH, Huang CM (2018) Comprehensive complication index predicts cancer-specific survival of patients with postoperative complications after curative resection of gastric cancer. Gastroenterol Res Pract 2018:4396018–4396018. https://doi.org/10.1155/2018/4396018
Kim EY, Yim HW, Park CH, Song KY (2017) C-reactive protein can be an early predictor of postoperative complications after gastrectomy for gastric cancer. Surg Endosc 31(1):445–454. https://doi.org/10.1007/s00464-016-5272-4
Mortensen K, Nilsson M, Slim K, Schafer M, Mariette C, Braga M, Carli F, Demartines N, Griffin SM, Lassen K, Enhanced Recovery After Surgery G (2014) Consensus guidelines for enhanced recovery after gastrectomy: Enhanced Recovery After Surgery (ERAS(R)) Society recommendations. Br J Surg 101(10):1209–1229. https://doi.org/10.1002/bjs.9582
Doyle SL, Mongan AM, Donohoe CL, Pidgeon GP, Sherlock M, Reynolds JV, Lysaght J (2017) Impact of visceral obesity and metabolic syndrome on the postoperative immune, inflammatory, and endocrine response following surgery for esophageal adenocarcinoma. Dis Esophagus 30(6):1–11. https://doi.org/10.1093/dote/dox008
Kim ES, Kim SY, Koh M, Lee HM, Kim K, Jung J, Kim HS, Moon WK, Hwang S, Moon A (2018) C-reactive protein binds to integrin alpha2 and Fcgamma receptor I, leading to breast cell adhesion and breast cancer progression. Oncogene 37(1):28–38. https://doi.org/10.1038/onc.2017.298
Secchiero P, Rimondi E, di Iasio MG, Agnoletto C, Melloni E, Volpi I, Zauli G (2013) C-Reactive protein downregulates TRAIL expression in human peripheral monocytes via an Egr-1-dependent pathway. Clin Cancer Res 19(8):1949–1959. https://doi.org/10.1158/1078-0432.CCR-12-3027
Tsujiura M, Hiki N, Ohashi M, Nunobe S, Kumagai K, Ida S, Okumura Y, Sano T, Yamaguchi T (2017) “Pancreas-compressionless gastrectomy”: a novel laparoscopic approach for suprapancreatic lymph node dissection. Ann Surg Oncol 24(11):3331–3337. https://doi.org/10.1245/s10434-017-5974-4
Kawabata R, Takiguchi S, Kimura Y, Imamura H, Fujita J, Tamura S, Fujitani K, Kishi K, Yamamoto K, Fujiwara S, Kurokawa Y, Mori M, Doki Y (2016) A randomized phase II study of the clinical effects of ultrasonically activated coagulating shears (Harmonic scalpel) in open gastrectomy for gastric cancer. Surg Today 46(5):561–568. https://doi.org/10.1007/s00595-015-1213-4
Acknowledgements
The authors thank Yayoi Hongo, a staff member at the Department of Gastroenterological Surgery in Saitama Medical University International Medical Center, for help in preparing the manuscript.
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Data are not available because of ethical restrictions. Due to the nature of this research, the study participants did not agree for their data to be shared publicly, so supporting data is not available.
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Study conception and design: Kazuaki Matsui, Shinichi Sakuramoto, Hirofumi Sugita, Keishi Yamashita. Acquisition of data: Kazuaki Matsui, Kenji Nishibeppu, Gen Ebara, Shohei Fujita, Shiro Fujihata, Shuichiro Oya. Analysis and interpretation of data: Kazuaki Matsui, Yutaka Miyawaki, Hiroshi Sato. Drafting of manuscript: Kazuaki Matsui. Critical revision of manuscript: Shinichi Sakuramoto, Shigeshi Yamaguchi, Keishi Yamashita
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the Independent Ethics Committee of Saitama Medical University International Medical Center (19-226).
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Matsui, K., Sakuramoto, S., Sugita, H. et al. C-reactive protein adjusted for body mass index as a predictor of postoperative complications following laparoscopic gastrectomy for gastric cancer. Langenbecks Arch Surg 406, 1875–1884 (2021). https://doi.org/10.1007/s00423-021-02200-1
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DOI: https://doi.org/10.1007/s00423-021-02200-1