Open Access

Geriatric Nutritional Risk Index Predicts Poor Prognosis of Patients After Curative Surgery for Gastric Cancer

FURUKE HIROTAKA
MATSUBARA DAIKI
KUBOTA TAKESHI
KIUCHI JUN
KUBO HIDEMASA
OHASHI TAKUMA
SHIMIZU HIROKI
ARITA TOMOHIRO
YAMAMOTO YUSUKE
KONISHI HIROTAKA
MORIMURA RYO
SHIOZAKI ATSUSHI
KURIU YOSHIAKI
IKOMA HISASHI
FUJIWARA HITOSHI
OKAMOTO KAZUMA
  &  
OTSUJI EIGO
Cancer Diagnosis & Prognosis May-June; 1(2): 43-52 DOI: 10.21873/cdp.10007
Received 12 May 2021 | Revised 07 December 2023 | Accepted 05 April 2021
Corresponding author
Takeshi Kubota, MD, PhD, Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kawaramachi-Hirokoji, Kamigyo-ku, Kyoto, 602-8566, Japan. Tel: +81 752515527, Fax: +81 752515522 tkubot@koto.kpu-m.ac.jp

Abstract

Background: The Geriatric Nutritional Risk Index (GNRI) is a nutritional measure for predicting the risk of morbidity and mortality in hospitalized patients. We evaluated the utility of the GNRI to predict the short-term and long-term outcomes after curative surgery for gastric cancer (GC). Patients and Methods: Patients who underwent curative surgery for GC between 2008 and 2016 were reviewed (n=795). We classified patients into two groups according to the GNRI (high GNRI: low and no risk; low GNRI: major and moderate risk) and compared the utility of the GNRI. Results: A low GNRI was an independent prognostic factor for poorer overall survival (hazard ratio=2.34, p<0.001). The GNRI tended to be a better prognostic indicator in elderly patients with GC. Low GNRI was associated with postoperative complications (odds ratio=2.27, p=0.002), especially in patients aged ≥75 (odds ratio=2.26, p=0.042). Conclusion: Low GNRI was associated with poor prognosis and occurrence of postoperative complications in patients with GC, especially in elderly patients.
Keywords: Geriatric Nutritional Risk Index, gastric cancer, prognostic factor, complication

Gastric cancer (GC) is the fifth most frequently diagnosed cancer and the third leading cause of cancer death worldwide (1). The prognosis in a considerable number of patients with GC is still poor even after curative surgery. Patients with GC often have insufficient oral intake due to various cancer-related symptoms such as generalized fatigue, pain, nausea, and anorexia (2). Cancer-associated obstruction directly reduces oral intake and induces malnutrition (2), which is recognized as a risk factor of perioperative complications (3-7). Furthermore, immunosuppression is induced by malnutrition (8) and is associated with poor prognosis after curative surgery (9). Therefore, it is important to evaluate nutritional status before surgery.

The Geriatric Nutritional Risk Index (GNRI) was defined by Bouillanne et al. in 2005 (10). The GNRI was a status of nutrition first used to predict the risk of morbidity and mortality in hospitalized elderly patients. It is calculated using the serum albumin and body mass index (BMI). Previous studies reported the association between the GNRI and prognosis for various types of cancer, including esophageal cancer, pancreatic ductal carcinoma, lung cancer, and renal cell carcinoma (11-17). Recently, studies reported a relationship between the GNRI and prognosis of patients with GC (18-20). Syuhei et al. reported that the GNRI was associated with postoperative complications in elderly patients with GC (18). Furthermore, the GNRI was reported as a poor prognostic factor in elderly patients with GC (19), and in elderly patients who underwent laparoscopic gastrectomy (20). However, the patients with gastric cancer that were analyzed in these studies were limited by age or operative procedure.

The present study aimed to investigate the utility of the GNRI to predict the outcome after curative surgery for GC and morbidity of postoperative complications in patients of all ages. Furthermore, we compared the utility of the GNRI between patients aged ≥75 years and those aged <75 years.

Patients and Methods

Study population. Seven hundred and ninety-five patients who underwent curative surgery for GC between 2008 and 2016 at our Institution were reviewed retrospectively. Tumor staging and pathological findings were classified according to the 15th Japanese Classification of Gastric Carcinoma issued by the Japanese Gastric Cancer Association (21). Histopathological type was classified into two groups: Differentiated and undifferentiated. We performed surgery according to the Japanese Gastric Cancer Association guidelines for the treatment of gastric cancer (22). After curative surgery, patients were followed-up every 3-6 months for the first 2 years after surgery, and the follow-ups continued for 5 years. This study was approved by the institutional review boards of Kyoto Prefectural University of Medicine (approval number ERB-C-1327). The present study was performed in accordance with the principles of the Declaration of Helsinki. Before surgery, written informed consent was acquired from all patients.

Definition of the GNRI. The GNRI was calculated using BMI and serum albumin level measured before curative surgery as: GNRI=1.489 × albumin (g/l) + 41.7 × BMI/22.

Patients with BMI >22 kg/m2 were included as having a BMI of 22 kg/m2 according to a previous report (19). Four grades of nutrition-related risk were defined according to the GNRI (10): Major risk: GNRI <82; moderate risk: GNRI 82 to <92; low risk: GNRI 92 to ≤98; and no risk: GNRI >98. Furthermore, patients were classified into two groups: high GNRI: low and no risk; low GNRI: major and moderate risk.

Definition of postoperative complications. We analyzed the complications that occurred after surgery during hospitalization. Complications of grade II or more as assessed by the Clavien–Dindo classification were included (23). Infectious complications included surgical site infection and pneumonia.

Statistical analysis. Categorical variables were compared using the chi-squared test. Overall survival (OS) and cancer-specific survival (CSS) analyses were performed using the Kaplan–Meier method and data were compared using the log-rank test. A multivariate analysis for prognosis was performed using Cox’s proportional hazard model to identify independent prognostic factors for OS, and the hazard ratio (HR) and 95% confidence interval (CI) were subsequently calculated. All statistical tests used in this study were two-sided, and a p-value of less than 0.05 was considered statistically significant. All statistical analyses were performed using JMP 10 software (SAS institute, Cary, NC, USA).

Results

GNRI and clinicopathological factors. Clinicopathological factors of all patients are shown in Table I. Table II shows the association between the GNRI and clinicopathological factors. Low GNRI was correlated to age ≥75 years (p<0.001), tumor size ≥45 mm (p<0.001), pathological T factor 3-4 (p<0.001), the presence of lymph node metastasis (p<0.001), the presence of lymphatic invasion (p<0.001), venous invasion (p=0.012), carcinoembryonic antigen level before surgery ≥5 ng/ml (p=0.004), and pathological stage II-III (p<0.001).

Association between GNRI and prognosis of patients after curative surgery for GC. Figure 1 shows the association between the GNRI and prognosis of patients with GC. The 5-year OS and CSS in patients with stage I-III GC were stratified according to GNRI risk (Figure 1, left panel) and were found to differ signs, p<0.001. The 5-year OS and CSS were significantly worse in the group with low GNRI than those with high GNRI (Figure 1, right panel). The 5-year OS rate of the group with low GNRI was 46% and that with a high GNRI was 84% (p<0.001), whilst the corresponding CSS rates were 67% and 89%, respectively (p<0.001).

The 5-year OS and CSS stratified based on pStage are shown in Figure 2. The low GNRI group had significantly poorer 5-year OS than that with high GNRI among patients with pStage I (p<0.001), pStage II (p=0.015), and pStage III (p=0.003) (Figure 2A). Although there was no significant difference in the 5-year CSS between the two groups in patients with pStage I disease (p=0.579), the rate in the group with low GNRI tended to be worse in patients with pStage II (p=0.063) and was significantly worse in those with pStage III disease (p=0.003) (Figure 2B).

Investigation of prognostic factors for 5-year OS. Univariate and multivariate analysis of prognostic factors for 5-year OS are shown in Table III. Age ≥75 years (p<0.001), tumor size ≥45 mm (p<0.001), advanced pathological T- and N-stage (p<0.001), lymphatic invasion and venous invasion (p<0.001), and low GNRI (p<0.001) were significantly associated with poor prognosis. Multivariate analysis revealed that age ≥75 years (HR=1.20, 95% CI=1.02-1.41, p=0.027), lymph node metastasis (HR=1.22, 95% CI=1.01-1.46, p=0.034), and low GNRI (HR=2.34, 95% CI=1.47-3.64, p<0.001) were independent prognostic factors for poorer survival.

Association between GNRI and prognosis stratified by age. Figure 3 shows OS and CSS curves of the GNRI groups stratified based on age (cutoff=75 years). The low GNRI group had poorer prognosis the high GNRI group for those under 75 years and 75 years or older in OS (Figure 3A, both p<0.001) and in CSS (Figure 3B, p<0.001 and p=0.005, respectively). A low GNRI was associated with poorer prognosis regardless of age.

Association between GNRI and postoperative complications. Table IV shows the association between GNRI and the frequency of postoperative complications. There was a significant inverse association between GNRI and the occurrence of complications overall (p=0.002). Table V shows the associations between GNRI and the frequency of postoperative complications stratified based on age. A low GNRI was significantly associated with increased postoperative complications in patients aged ≥75 years (p=0.042). However, in patients aged <75 years, low GNRI was not significantly associated with postoperative complications (p=0.063).

Discussion

In patients with GC, malnutrition before surgery significantly contributes to postoperative mortality, morbidity, and length of total hospital stay (24,25). Previous reports mentioned that body weight loss (26), sarcopenia (27), and malnutrition before surgery (28,29) were associated with poorer prognosis after curative surgery for GC. Therefore, it is important to evaluate nutritional status before surgery. Various nutritional indices have been developed to predict the outcome of cancer, including the prognostic nutritional index (30), the Glasgow prognostic score (31), and the Controlling Nutritional Status (32). These indices were constructed using only laboratory data. The GNRI is a simple nutritional index which can be calculated using the serum albumin level and BMI (10). As the GNRI includes a physical measurement, BMI, it may reflect nutritional status better than other indices. Recent reports revealed that the GNRI was a risk factor of morbidity and mortality in elderly patients with GC (18-20). Although the GNRI was first used in elderly patients (10), it may be effective in patients of all ages. To the best of our knowledge, there are no reports that analyzed the utility of the GNRI in patients with GC of all ages. The present study analyzed the predictive ability of the GNRI for prognosis and the occurrence of complications in patients of all ages who underwent curative surgery for GC. Furthermore, we stratified patients based on age and compared the utility of the GNRI between patients aged ≥75 years and those aged <75 years.

Malnutrition is associated with various risk factors in patients with GC. Immunosuppression is induced by malnutrition (8) and is recognized as a risk factor of poor prognosis in GC after curative surgery (9). Malnutrition before surgery has also been reported to be a risk factor of postoperative complications (33,34). We previously reported that postoperative complications were correlated with poor prognosis in patients with GC (35). Postoperative complications induce systemic inflammation that is related to immunosuppression (36). In addition, Lerut et al. reported that systemic inflammation activated micro-residual tumor and led to postoperative recurrence (37). Thus, preoperative malnutrition leads to poor prognosis after curative surgery.

We demonstrated that prognosis after surgery for patients with GC was clearly stratified based on the GNRI. The group with low GNRI had a poorer prognosis than did the high GNRI group (Figure 1). We revealed that the GNRI was an independent prognostic factor in patients with GC by multivariate analysis. Low GNRI was also poor prognostic factor in patients when stratified by age (Figure 3). Patients were divided into four risk groups based on the GNRI: Major, moderate, low, and no risk. In patients aged ≥75 years, a no-risk GNRI tended to be associated with a better prognosis than low-risk GNRI (Figure 4A, p=0.082), whereas there was no difference in prognosis between no-risk GNRI and low-risk GNRI in patients aged <75 years (Figure 4B, p=0.700). Elderly patients have low reserve capacity of nutrition, so that even a slight decrease of nutritional status may affect the outcome after curative surgery. A low GNRI was significantly associated with an increased frequency of overall complications. Furthermore, the GNRI was more effective for predicting the possibility of postoperative complications in patients aged ≥75 years than in younger patients (Table V). Hence, the results suggest that the GNRI is a useful nutritional index for evaluating short- and long-term outcomes in patients with GC of all ages after curative surgery, and may be more useful for elderly patients.

The GNRI was associated with prognosis for each stage of GC (Figure 2). In patients with pStage I GC, the GNRI was not a prognosis factor for 5-year CSS (p=0.579), and was associated with poor 5-year OS (p<0.001). Hence, the GNRI may be a suitable index to predict mortality from other diseases in patients with pStage I GC. Previous studies reported that a lower GNRI was a poor prognostic factor in patients with pneumonia (38), heart failure (39), and chronic kidney disease (40). Various conditions, including immunosuppression, cardiac dysfunction, and protein energy wasting were induced by malnutrition and lead to poor prognosis (38-40). Patients with early-stage cancer may be more strongly affected by these factors than by cancer progression. These findings suggest that the GNRI was a prognostic factor even in patients with early-stage cancer. Therefore, patients with a low GNRI need strict follow-up not only for oncology but also for other systemic diseases, especially those with pStage I GC.

Our study had several limitations that need to be considered. This was a retrospective study performed at a single institution; therefore, a large-scale, multicenter study may be necessary for further analysis. In addition, an interventional study with preoperative nutrition treatment is needed to confirm this result.

In conclusion, we investigated the utility of the GNRI in predicting the outcome after curative surgery for GC and occurrence of postoperative complications. The GNRI was identified as an independent prognostic factor of 5-year OS and CSS. A low GNRI was a risk factor of postoperative complications, especially in elderly patients with GC. Thus, the GNRI may be an effective nutritional index for evaluating short- and long-term outcomes in patients of all ages after curative surgery for GC.

Conflicts of Interest

The Authors declare that they have no conflicts of interest to disclose.

Authors’ Contributions

This study was designed by H.F., D.M., T.K., and E.O.; H.F. and D.M. performed statistical analyses. The clinical information and materials were collected and kept by H.F., D.M., T.K., J.K., H.K., T.O., H.S., T.A., Y.Y., H.K., R.M., A.S., Y.K., H.I., H.F., and K.O.; H.F., D.M., and T.K. drafted the manuscript. T.K. edited and revised the manuscript. E.O. approved the final version of the manuscript.

References

1 Bray F Ferlay J Soerjomataram I Siegel RL Torre LA & Jemal A Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68(6) 394 - 424 2018. PMID: 30207593. DOI: 10.3322/caac.21492
2 Fukuda Y Yamamoto K Hirao M Nishikawa K Maeda S Haraguchi N Miyake M Hama N Miyamoto A Ikeda M Nakamori S Sekimoto M Fujitani K & Tsujinaka T Prevalence of malnutrition among gastric cancer patients undergoing gastrectomy and optimal preoperative nutritional support for preventing surgical site infections. Ann Surg Oncol. 22(Suppl 3) S778 - S785 2015. PMID: 26286199. DOI: 10.1245/s10434-015-4820-9
3 Rey-Ferro M Castaño R Orozco O Serna A & Moreno A Nutritional and immunologic evaluation of patients with gastric cancer before and after surgery. Nutrition. 13(10) 878 - 881 1997. PMID: 9357024. DOI: 10.1016/s0899-9007(97)00269-4
4 Sungurtekin H Sungurtekin U Balci C Zencir M & Erdem E The influence of nutritional status on complications after major intraabdominal surgery. J Am Coll Nutr. 23(3) 227 - 232 2004. PMID: 15190047. DOI: 10.1080/07315724.2004.10719365
5 Kuzu MA Terzioğlu H Genç V Erkek AB Ozban M Sonyürek P Elhan AH & Torun N Preoperative nutritional risk assessment in predicting postoperative outcome in patients undergoing major surgery. World J Surg. 30(3) 378 - 390 2006. PMID: 16479353. DOI: 10.1007/s00268-005-0163-1
6 Schiesser M Kirchhoff P Müller MK Schäfer M & Clavien PA The correlation of nutrition risk index, nutrition risk score, and bioimpedance analysis with postoperative complications in patients undergoing gastrointestinal surgery. Surgery. 145(5) 519 - 526 2009. PMID: 19375611. DOI: 10.1016/j.surg.2009.02.001
7 Correia MI Caiaffa WT da Silva AL & Waitzberg DL Risk factors for malnutrition in patients undergoing gastroentero-logical and hernia surgery: an analysis of 374 patients. Nutr Hosp. 16(2) 59 - 64 2001. PMID: 11443835.
Pubmed |
8 Bourke CD Berkley JA & Prendergast AJ Immune dysfunction as a cause and consequence of malnutrition. Trends Immunol. 37(6) 386 - 398 2016. PMID: 27237815. DOI: 10.1016/j.it.2016.04.003
9 Urakawa S Yamasaki M Goto K Haruna M Hirata M Morimoto-Okazawa A Kawashima A Iwahori K Makino T Kurokawa Y Yamada T Mori M Doki Y & Wada H Peri-operative monocyte count is a marker of poor prognosis in gastric cancer: increased monocytes are a characteristic of myeloid-derived suppressor cells. Cancer Immunol Immunother. 68(8) 1341 - 1350 2019. PMID: 31324947. DOI: 10.1007/s00262-019-02366-0
10 Bouillanne O Morineau G Dupont C Coulombel I Vincent JP Nicolis I Benazeth S Cynober L & Aussel C Geriatric Nutritional Risk Index: a new index for evaluating at-risk elderly medical patients. Am J Clin Nutr. 82(4) 777 - 783 2005. PMID: 16210706. DOI: 10.1093/ajcn/82.4.777
11 Yamana I Takeno S Shimaoka H Yamashita K Yamada T Shiwaku H Hashimoto T Yamashita Y & Hasegawa S Geriatric Nutritional Risk Index as a prognostic factor in patients with esophageal squamous cell carcinoma -retrospective cohort study. Int J Surg. 56 44 - 48 2018. PMID: 29602015. DOI: 10.1016/j.ijsu.2018.03.052
12 Migita K Matsumoto S Wakatsuki K Ito M Kunishige T Nakade H & Sho M The Prognostic significance of the Geriatric Nutritional Risk Index in patients with esophageal squamous cell carcinoma. Nutr Cancer. 70(8) 1237 - 1245 2018. PMID: 30235009. DOI: 10.1080/01635581.2018.1512640
13 Kubo N Sakurai K Tamura T Toyokawa T Tanaka H Muguruma K Yashiro M & Ohira M The impact of geriatric nutritional risk index on surgical outcomes after esophagectomy in patients with esophageal cancer. Esophagus. 16(2) 147 - 154 2019. PMID: 30311102. DOI: 10.1007/s10388-018-0644-6
14 Wang Y Wang L Fang M Li J Song T Zhan W & Xu H Prognostic Value of the Geriatric Nutritional Risk Index in patients exceeding 70 years old with esophageal squamous cell carcinoma. Nutr Cancer. 72(4) 620 - 626 2020. PMID: 31390885. DOI: 10.1080/01635581.2019.1650189
15 Hu SP Chen L Lin CY Lin WH Fang FQ & Tu MY The Prognostic Value of preoperative Geriatric Nutritional Risk Index in patients with pancreatic ductal adenocarcinoma. Cancer Manag Res. 12 385 - 395 2020. PMID: 32021451. DOI: 10.2147/CMAR.S229341
16 Shoji F Matsubara T Kozuma Y Haratake N Akamine T Takamori S Katsura M Toyokawa G Okamoto T & Maehara Y Preoperative Geriatric Nutritional Risk Index: A predictive and prognostic factor in patients with pathological stage I non-small cell lung cancer. Surg Oncol. 26(4) 483 - 488 2017. PMID: 29113668. DOI: 10.1016/j.suronc.2017.09.006
17 Miyake H Tei H & Fujisawa M Geriatric Nutrition Risk Index is an important predictor of cancer-specific survival, but not recurrence-free survival, in patients undergoing surgical resection for non-metastatic renal cell carcinoma. Curr Urol. 10(1) 26 - 31 2017. PMID: 28559774. DOI: 10.1159/000447147
18 Kushiyama S Sakurai K Kubo N Tamamori Y Nishii T Tachimori A Inoue T & Maeda K The Preoperative Geriatric Nutritional Risk Index predicts postoperative complications in elderly patients with gastric cancer undergoing gastrectomy. In Vivo. 32(6) 1667 - 1672 2018. PMID: 30348732. DOI: 10.21873/invivo.11430
19 Hirahara N Matsubara T Fujii Y Kaji S Hyakudomi R Yamamoto T Uchida Y Miyazaki Y Ishitobi K Kawabata Y & Tajima Y Preoperative geriatric nutritional risk index is a useful prognostic indicator in elderly patients with gastric cancer. Oncotarget. 11(24) 2345 - 2356 2020. PMID: 32595832. DOI: 10.18632/oncotarget.27635
20 Hirahara N Tajima Y Fujii Y Kaji S Kawabata Y Hyakudomi R Yamamoto T & Taniura T Prediction of postoperative complications and survival after laparoscopic gastrectomy using preoperative Geriatric Nutritional Risk Index in elderly gastric cancer patients. Surg Endosc. 35(3) 1202 - 1209 2021. PMID: 32152675. DOI: 10.1007/s00464-020-07487-7
21 Japanese Gastric Cancer Association Japanese Classification of Gastric Carcinoma, 15th Edition.. Kanehara & Co., Ltd., Tokyo.
22 Japanese Gastric Cancer Association Japanese Gastric Cancer Treatment Guidelines, 5th Edition.. Kanehara & Co., Ltd., Tokyo.
23 Clavien PA Barkun J de Oliveira ML Vauthey JN Dindo D Schulick RD de Santibañes E Pekolj J Slankamenac K Bassi C Graf R Vonlanthen R Padbury R Cameron JL & Makuuchi M The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 250(2) 187 - 196 2009. PMID: 19638912. DOI: 10.1097/SLA.0b013e3181b13ca2
24 Hu WH Cajas-Monson LC Eisenstein S Parry L Cosman B & Ramamoorthy S Preoperative malnutrition assessments as predictors of postoperative mortality and morbidity in colorectal cancer: an analysis of ACS-NSQIP. Nutr J. 14 91 2015. PMID: 26345703. DOI: 10.1186/s12937-015-0081-5
25 Garth AK Newsome CM Simmance N & Crowe TC Nutritional status, nutrition practices and post-operative complications in patients with gastrointestinal cancer. J Hum Nutr Diet. 23(4) 393 - 401 2010. PMID: 20337847. DOI: 10.1111/j.1365-277X.2010.01058.x
26 Loh KW Vriens MR Gerritsen A Borel Rinkes IH van Hillegersberg R Schippers C Steenhagen E Ong TA Moy FM & Molenaar IQ Unintentional weight loss is the most important indicator of malnutrition among surgical cancer patients. Neth J Med. 70(8) 365 - 369 2012. PMID: 23065984.
Pubmed |
27 Yamamoto K Hirao M Nishikawa K Omori T Yanagimoto Y Shinno N Sugimura K Miyata H Wada H Takahashi H Yasui M Ohue M Yano M Fujitani K & Tsujinaka T Sarcopenia is associated with impaired overall survival after gastrectomy for elderly gastric cancer. Anticancer Res. 39(8) 4297 - 4303 2019. PMID: 31366521. DOI: 10.21873/anticanres.13595
28 Almasaudi AS McSorley ST Dolan RD Edwards CA & McMillan DC The relation between Malnutrition Universal Screening Tool (MUST), computed tomography-derived body composition, systemic inflammation, and clinical outcomes in patients undergoing surgery for colorectal cancer. Am J Clin Nutr. 110(6) 1327 - 1334 2019. PMID: 31529042. DOI: 10.1093/ajcn/nqz230
29 Matsubara D Shoda K Kubota T Kosuga T Konishi H Shiozaki A Fujiwara H Okamoto K Kudou M Arita T Morimura R Murayama Y Ikoma H Kuriu Y Nakanishi M & Otsuji E Preoperative total cholesterol-lymphocyte score as a novel immunonutritional predictor of survival in gastric cancer. Langenbecks Arch Surg. 404(6) 743 - 752 2019. PMID: 31659435. DOI: 10.1007/s00423-019-01824-8
30 Hirahara N Tajima Y Fujii Y Yamamoto T Hyakudomi R Taniura T Kaji S & Kawabata Y Preoperative Prognostic Nutritional Index predicts long-term outcome in gastric cancer: a propensity score-matched analysis. Anticancer Res. 38(8) 4735 - 4746 2018. PMID: 30061243. DOI: 10.21873/anticanres.12781
31 Ikeguchi M Urushibara S Shimoda R Yamamoto M Maeta Y & Ashida K Inflammation-based prognostic scores and nutritional prognostic index in patients with locally-advanced unresectable colorectal cancer. World J Surg Oncol. 12 210 2014. PMID: 25022764. DOI: 10.1186/1477-7819-12-210
32 Suzuki S Kanaji S Yamamoto M Oshikiri T Nakamura T & Kakeji Y Controlling Nutritional status (CONUT) score predicts outcomes of curative resection for gastric cancer in the elderly. World J Surg. 43(4) 1076 - 1084 2019. PMID: 30569221. DOI: 10.1007/s00268-018-04889-6
33 Fukuda Y Yamamoto K Hirao M Nishikawa K Maeda S Haraguchi N Miyake M Hama N Miyamoto A Ikeda M Nakamori S Sekimoto M Fujitani K & Tsujinaka T Prevalence of malnutrition among gastric cancer patients undergoing gastrectomy and optimal preoperative nutritional support for preventing surgical site infections. Ann Surg Oncol. 22(Suppl 3) S778 - S785 2015. PMID: 26286199. DOI: 10.1245/s10434-015-4820-9
34 Zheng HL Lu J Li P Xie JW Wang JB Lin JX Chen QY Cao LL Lin M Tu R Huang CM & Zheng CH Effects of preoperative malnutrition on short- and long-term outcomes of patients with gastric cancer: Can we do better. Ann Surg Oncol. 24(11) 3376 - 3385 2017. PMID: 28699132. DOI: 10.1245/s10434-017-5998-9
35 Kubota T Hiki N Sano T Nomura S Nunobe S Kumagai K Aikou S Watanabe R Kosuga T & Yamaguchi T Prognostic significance of complications after curative surgery for gastric cancer. Ann Surg Oncol. 21(3) 891 - 898 2014. PMID: 24254205. DOI: 10.1245/s10434-013-3384-9
36 Mantovani A Allavena P Sica A & Balkwill F Cancer-related inflammation. Nature. 454(7203) 436 - 444 2008. PMID: 18650914. DOI: 10.1038/nature07205
37 Lerut T Moons J Coosemans W Van Raemdonck D De Leyn P Decaluwé H Decker G & Nafteux P Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification. Ann Surg. 250(5) 798 - 807 2009. PMID: 19809297. DOI: 10.1097/SLA.0b013e3181bdd5a8
38 Wei L Xie H Li J Li R Chen W Huang L Li X & Yan P The prognostic value of geriatric nutritional risk index in elderly patients with severe community-acquired pneumonia: A retrospective study. Medicine (Baltimore). 99(37) e22217 2020. PMID: 32925799. DOI: 10.1097/MD.0000000000022217
39 Li H Cen K Sun W & Feng B Prognostic value of geriatric nutritional risk index in elderly patients with heart failure: a meta-analysis.. Aging Clin Exp Res. PMID: 32766928. DOI: 10.1007/s40520-020-01656-3
40 Lin TY & Hung SC Geriatric Nutritional Risk Index Is Associated with Unique Health Conditions and Clinical Outcomes in Chronic Kidney Disease Patients. Nutrients. 11(11) 2769 2019. PMID: 31739530. DOI: 10.3390/nu11112769