Research ArticleClinical Studies

The Clinical Influence of Geriatric Nutritional Risk Index in Patients With Gastric Cancer Who Receive Curative Treatment

TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, KENTARO HARA, KEISUKE KAZAMA, MASAKATSU NUMATA, SHO SAWAZAKI, HIROSHI TAMAGAWA, AYAKO TAMAGAWA, MASATO NAKAZONO, KENKI SEGAMI, HARUHIKO CHO, MINORI TATEISHI, TOMOYUKI MINAMI, SHINSUKE NAGASAWA, KEISUKE KOMORI, AYA KATO, KAZUKI OTANI, SHINNOSUKE KAWAHARA, TAKASHI OSHIMA, NORIO YUKAWA, AYA SAITO and YASUSHI RINO
Anticancer Research December 2023, 43 (12) 5605-5612; DOI: https://doi.org/10.21873/anticanres.16763

Abstract

Background/Aim: We evaluated the clinical impact of the Geriatric Nutritional Risk Index (GNRI) in patients who received curative treatment and perioperative adjuvant treatment. We also investigated the association between the GNRI and the clinicopathological features of patients with GC. Patients and Methods: This study included 280 patients who underwent curative treatment for GC between 2005 and 2020. The prognosis and clinicopathological parameters of the high-GNRI and low-GNRI groups were compared. Results: In the GNRI-high group, the overall survival (OS) rates at 3 and 5 years after surgery were significantly lower (82.7% and 77.9%, respectively) than those in the GNRI-low group (56.4% and 40.8%). The GNRI was selected for the final multivariate analysis model for OS. The GNRI was also a significant prognostic factor for recurrence-free survival (RFS). The RFS rates at 3 and 5 years after surgery were 79.1% and 74.8%, respectively, in the GNRI-high group, and 48.0% and 38.6% in the GNRI-low group. The GNRI was selected for the final multivariate analysis model for RFS. The GNRI was also found to affect the postoperative clinical course, including postoperative surgical complications and postoperative adjuvant chemotherapy. Conclusion: The GNRI may be a promising prognostic and predictive factor for gastric cancer. In the future, the GNRI may be used to select optimal treatment strategies.

Key Words:

Gastric cancer (GC) is the fifth most prevalent cancer and the fourth leading cause of cancer-related death in the world (1, 2). The standard treatment for resectable GC is curative gastrectomy with perioperative adjuvant treatment (3-5). The prognosis of patients with resectable GC is gradually improving due to the introduction of minimally invasive surgery, enhanced recovery after surgery programs, and perioperative nutritional care. However, the prognosis after the development of recurrent disease remains poor. The median survival time after recurrence is 12-14 months (6, 7). Therefore, it is necessary to identify prognostic and/or predictive factors for GC treatment.

Recently, the perioperative nutritional status has been shown to affect short-term oncological outcomes (e.g., the occurrence of postoperative surgical complications, physical activity after surgery, and the introduction of adjuvant treatment) (8-10). In addition, the perioperative nutritional status strongly affects long-term oncological outcomes. Various nutritional assessment tools, including the Glasgow Prognostic Score, Prognostic Nutritional Index, and Controlling Nutritional Status, have been used to evaluate the clinical impact of oncological treatment and have demonstrated a significant relationship between nutritional assessment tools and oncological outcomes (11-13). Among these nutritional assessment tools, the Geriatric Nutritional Risk Index (GNRI) is a promising nutritional assessment tool for gastrointestinal cancer treatment (14, 15). The GNRI is calculated using serum albumin level and the actual body weight/ideal body weight. Thus, the GNRI is readily available, easy to calculate, and useful for the selection of optimal treatment strategies. However, few studies have evaluated the clinical impact of the GNRI in gastric cancer treatment.

This study evaluated the clinical impact of the GNRI for the patients who received curative treatment and perioperative adjuvant treatment, and the association between the GNRI and the clinicopathological factors of patients with GC.

Patients and Methods

Patients. Patients were chosen based on their medical records from consecutive cases of curative resection for GC performed at Yokohama City University from 2005 to 2020. The following inclusion criteria were applied: 1) histologically confirmed adenocarcinoma; 2) clinical stage I-III disease according to the 15th edition of the Japanese Gastric Cancer Association’s general rules for GC (16); 3) curative gastrectomy was performed as the primary treatment for GC; and 4) complete resection (defined as R0 resection) of GC, including radical lymph node dissection.

Surgical procedure and adjuvant treatment. Each patient underwent gastrectomy with either D1+ or D2 nodal dissection. S-1-based adjuvant chemotherapy was administered for pathological stage II and III disease (13-15).

Measurement of the GNRI. GNRI was calculated using the following formula: GNRI=[1.487× serum albumin (g/l)]+[41.7× actual/usual body weight) (kg)]. The ideal body weight was determined using the following formula: ideal body weight (kg)= 22× square of height (m2). In cases in which the patient’s actual body weight exceeded the ideal body weight, the ratio of the actual body weight to the ideal body weight was considered to be “1” (17).

Evaluations and statistical analyses. The chi-squared test was employed to assess the significance of variances between the GNRI and clinicopathological factors. Overall survival (OS) and recurrence-free survival (RFS) curves were computed using the Kaplan–Meier method. Univariate and multivariate survival analyses were conducted using a Cox proportional hazards model. p-Values of <0.05 were considered to indicate statistical significance. All statistical analyses were conducted using the SPSS software program (v27.0 J Win; IBM, Armonk, NY, USA). The present study received IRB approval from Yokohama City University.

Results

Patients. The present study included 280 patients (male, n=197; female, n=83; median age, 70 years (range=32-89 years)). The surgical treatments included distal gastrectomy (n=190) and total or proximal gastrectomy (n=90). We set the cutoff value of the GNRI at 98 according to previous studies, and the OS stratified by each clinical factor was compared by a log-rank test (Table I). There were significant differences in the median age, pathological T status, and pathological background between the GNRI-high (GNRI ≥98) and GNRI-low (GNRI <98) groups. The GNRI-high group included elderly patients with advanced-stage GC. In addition, the degree of preoperative inflammation, as reflected by the preoperative neutrophil and C-reactive protein levels, was significantly higher in the GNRI-high group than that in the GNRI-low group.

View this table:
Table I.

Comparison of survival rates stratified according to patient characteristics.

Survival analysis. Each clinicopathological factor was categorized (Table II) and analyzed for prognostic significance. Univariate and multivariate analyses of OS showed that age, pathological T status, pathological N factor, vascular invasion, lymphatic invasion, postoperative surgical complications, and the GNRI were significant prognostic factors. Therefore, the GNRI was selected for the final multivariate analysis model. In the GNRI-high group, the OS rates at 3 and 5 years after surgery (82.7% and 77.9%, respectively) were significantly lower than those in the GNRI-low group (56.4% and 40.8%). The OS curves are shown in Figure 1. The GNRI was also identified as a significant prognostic factor for RFS. In the GNRI-high group, the RFS rates at 3 and 5 years after surgery were 79.1% and 74.8%, whereas those in the GNRI-low group were 48.0% and 38.6%. The GNRI was selected for the final multivariate analysis model for RFS (Table III). RFS curves are shown in Figure 2. In addition, when the first recurrence sites were compared between the two groups, there were significant differences in the rates of peritoneal, lymph node, and hematological recurrence (Table IV).

View this table:
Table II.

Uni- and multivariate Cox proportional hazards analysis of clinicopathological factors for overall survival.

Figure 1.
Figure 1.

Overall survival in patients with gastric cancer in the Geriatric Nutritional Risk Index (GNRI)-high (≥98) and GNRI-low (<98) groups.

View this table:
Table III.

Uni- and multivariate Cox proportional hazards analysis of clinicopathological factors for recurrence-free survival.

Figure 2.
Figure 2.

Recurrence-free survival in patients with gastric cancer in the Geriatric Nutritional Risk Index (GNRI)-high (≥98) and GNRI-low (<98) groups.

View this table:
Table IV.

Patterns of recurrence according to Geriatric Nutritional Risk Index.

The postoperative course of the high- and low-GNRI groups. The comparison of the postoperative clinical courses of the GNRI-high and GNRI-low groups revealed differences in postoperative complications and adjuvant chemotherapy. The incidence of anastomotic leakage was higher in GNRI-low group (GNRI-low vs. GNRI-high: 12.6% vs. 6.7%, p=0.102). In contrast, the two groups had similar incidence rates of any-grade postoperative complications, pneumonia, abdominal abscess, and pancreatic fistula.

Moreover, there was a difference in the percentage of patients who required postoperative adjuvant chemotherapy (GNRI-low vs. GNRI-high: 58.6% vs. 31.1%; p=0.001). However, in contrast to the percentage of patients who required postoperative adjuvant chemotherapy, the percentage of who received postoperative adjuvant chemotherapy was 54.9% in the GNRI-low group and 78.3% in the GNRI-high group (p=0.009).

Discussion

The present study aimed to clarify the prognostic impact of the GNRI in patients who received curative treatment. The major finding was that the GNRI affected both OS and RFS in patients with GC. In addition, the GNRI affects the postoperative clinical course (e.g., postoperative surgical complications and postoperative adjuvant chemotherapy). The GNRI may be a promising prognostic and predictive factor for patients with GC that physicians can apply when selecting optimal treatment strategies.

In the present study, the hazard ratio of the GNRI was 1.913 for OS and 2.576 for RFS. Although a limited number of studies have investigated the GNRI as a prognostic factor, similar results were observed in the previous studies. Hirahara et al. evaluated the clinical relationship between the GNRI and long-term oncological outcomes in 297 elderly patients with GC who underwent laparoscopic gastrectomy (18). They set the cutoff value of the GNRI at 94.8 for OS and 90.9 for cancer-specific survival (CSS) according to their ROC curves. They categorized 200 patients into the GNRI-high group and 97 into the GNRI-low group. The 5-year OS and CSS rates were 78.9% and 88.4%, respectively in the GNRI-high group and 52.2% and 73.2% in the GNRI-low group (p=0.001 and p=0.004, respectively). They also demonstrated that the GNRI was a significant prognostic factor for OS (HR=2.350; 95%CI=1.436-3.847; p<0.001). Moreover, Sugawara et al. clarified the clinical impact of the GNRI in 1,166 patients with GC who underwent curative gastrectomy (19). They set the cutoff value of the GNRI at 98. Four-hundred forty-seven patients were categorized into the GNRI-low group, and 719 patients were categorized into the high GNRI group. When the background factors of the patients were compared, the GNRI-low group had a more advanced tumor stage and older patients in comparison to the GNRI-high group. There was a significant difference in the OS of the two groups, regardless of tumor stage. They also demonstrated that the GNRI was a significant prognostic factor for OS (HR=2.15; 95%CI=1.61-2.87; p<0.001). Considering the results of the present and previous studies, the preoperative GNRI has an impact on the survival of patients with GC and might be a promising nutritional and inflammation biomarker (20-22).

Preoperative GNRI affected the long-term oncological outcomes. There are two possible explanations for this observation. The first possible explanation is that the GNRI affects postoperative surgical complications. In the present study, although the overall postoperative complication rates were similar between the two groups, the incidence of anastomotic leakage in the GNRI-low group tended to be higher than that in the GNRI-high group. Similar results have been reported in a previous study. Miao et al. evaluated the clinical relationship between the GNRI and total complications in 582 elderly patients with GC who underwent gastrectomy (23). They defined total complications as Clavien-Dindo classification grade ≥2. They found that the GNRI was one of the predictors of total complications (odds ratio=0.921, 95%CI=0.895-0.949, p<0.001). Recent studies demonstrated that postoperative complications affect for the long-term oncological outcomes in various malignancies (24, 25). Thus, a low GNRI may result in postoperative complications and, consequently, a poor prognosis. The second possible explanation is that GNRI affects the introduction of adjuvant chemotherapy. In the present study, the number of patients who required postoperative adjuvant chemotherapy was significantly higher in the low GNRI group than that in the high GNRI group. However, the number of patients who received postoperative adjuvant chemotherapy was significantly higher in the high GNRI group than that in the low GNRI group. These results suggest that patients with low GNRI are unlikely to benefit from adjuvant chemotherapy. In future studies on GNRI and adjuvant chemotherapy, we will evaluate the clinical relationship between the GNRI status and adverse events due to chemotherapy or the continuation of adjuvant chemotherapy.

To optimize the clinical use of the GNRI in general practice, it is necessary to clarify the optimal cutoff value and evaluation methods of the GNRI for GC treatment. In the present study, we set the cutoff value of the GNRI at 98 according to previous studies and the 3- and 5- year survival rate. In contrast, previous studies reported the cutoff value of the GNRI as 92 to 98 (17-21). There are a number of reasons for the differences in the cutoff value of the GNRI. First, the patient background factors differed. In the present study, we evaluated patients with resectable GC who underwent gastrectomy, whereas some studies evaluated patients with early GC who underwent endoscopic submucosal dissection. In addition, no reports have evaluated patients with unresectable GC who underwent chemotherapy or radiation therapy. Thus, an optimal GNRI cutoff value is needed for each treatment setting. Second, the methods used to set the cutoff value of the GNRI were different. We set the cutoff value according to the survival rate, whereas some previous studies set the cutoff value of the GNRI according to ROC curves. An optimal method for setting the cutoff value is needed. Therefore, further studies are needed to clarify the optimal cutoff value of the GNRI and the optimal method for determining the GNRI.

Study limitations. First, this was a retrospective study conducted at a single institution between 2005 and 2020. Accordingly, it involved various selection and time biases. With regard to the selection bias, our institution is a university hospital; thus, our cohort of patients may be older and have more comorbidities in comparison to patients managed at other general hospitals. As for the time bias, the standard adjuvant treatment changed during the study period. Thus, changes in adjuvant treatment may have affected our study results. Second, we only analyzed patients who underwent gastrectomy. It is unclear whether the present study results could also be generalized to patients with early GC or patients with unresectable GC who underwent palliative treatment. Considering these findings, the results of the present study should be validated in a large study population.

In conclusion, the GNRI affected both the OS and RFS in patients with GC who underwent gastrectomy. The GNRI also affects postoperative surgical complications and postoperative adjuvant chemotherapy, and it may therefore be a promising prognostic and predictive factor for patients with GC that physicians can apply to select the optimal treatment strategies.

Acknowledgements

This study was supported in part by the nonprofit organization Yokoyama Surgical Research Group (YSRG).

Footnotes

  • Authors’ Contributions

    TA and IH substantially contributed to this concept and design. TA, MT, TM, YM, KH, KK1 (Keisuke Kazama), KK2 (Keisuke Komori) and MN made substantial contributions to the acquisition, analysis, and interpretation of data. TA, AT, HC, TO, AS, NY, and YR were involved in drafting the article and revising it critically for important intellectual content. TA, YM, and IH approved the final version to be published.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in association with the present study.

  • Received September 23, 2023.
  • Revision received October 16, 2023.
  • Accepted October 17, 2023.

References

  1. ↵
    1. Rajappa S,
    2. Singh M,
    3. Uehara R,
    4. Schachterle SE,
    5. Setia S
    : Cancer incidence and mortality trends in Asia based on regions and human development index levels: an analyses from GLOBOCAN 2020. Curr Med Res Opin 39(8): 1127-1137, 2023. DOI: 10.1080/03007995.2023.2231761
    OpenUrlCrossRefPubMed
  2. ↵
    1. Li J,
    2. Kuang XH,
    3. Zhang Y,
    4. Hu DM,
    5. Liu K
    : Global burden of gastric cancer in adolescents and young adults: estimates from GLOBOCAN 2020. Public Health 210: 58-64, 2022. DOI: 10.1016/j.puhe.2022.06.010
    OpenUrlCrossRefPubMed
  3. ↵
    1. Lordick F,
    2. Carneiro F,
    3. Cascinu S,
    4. Fleitas T,
    5. Haustermans K,
    6. Piessen G,
    7. Vogel A,
    8. Smyth E, ESMO Guidelines Committee
    : Gastric cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up. Ann Oncol 33(10): 1005-1020, 2022. DOI: 10.1016/j.annonc.2022.07.004
    OpenUrlCrossRefPubMed
    1. Ajani JA,
    2. D’Amico TA,
    3. Bentrem DJ,
    4. Chao J,
    5. Cooke D,
    6. Corvera C,
    7. Das P,
    8. Enzinger PC,
    9. Enzler T,
    10. Fanta P,
    11. Farjah F,
    12. Gerdes H,
    13. Gibson MK,
    14. Hochwald S,
    15. Hofstetter WL,
    16. Ilson DH,
    17. Keswani RN,
    18. Kim S,
    19. Kleinberg LR,
    20. Klempner SJ,
    21. Lacy J,
    22. Ly QP,
    23. Matkowskyj KA,
    24. McNamara M,
    25. Mulcahy MF,
    26. Outlaw D,
    27. Park H,
    28. Perry KA,
    29. Pimiento J,
    30. Poultsides GA,
    31. Reznik S,
    32. Roses RE,
    33. Strong VE,
    34. Su S,
    35. Wang HL,
    36. Wiesner G,
    37. Willett CG,
    38. Yakoub D,
    39. Yoon H,
    40. McMillian N,
    41. Pluchino LA
    : Gastric Cancer, Version 2.2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 20(2): 167-192, 2022. DOI: 10.6004/jnccn.2022.0008
    OpenUrlCrossRefPubMed
  5. ↵
    1. Japanese Gastric Cancer Association
    : Japanese Gastric Cancer Treatment Guidelines 2021 (6th edition). Gastric Cancer 26(1): 1-25, 2023. DOI: 10.1007/s10120-022-01331-8
    OpenUrlCrossRefPubMed
  6. ↵
    1. Kang YK,
    2. Chen LT,
    3. Ryu MH,
    4. Oh DY,
    5. Oh SC,
    6. Chung HC,
    7. Lee KW,
    8. Omori T,
    9. Shitara K,
    10. Sakuramoto S,
    11. Chung IJ,
    12. Yamaguchi K,
    13. Kato K,
    14. Sym SJ,
    15. Kadowaki S,
    16. Tsuji K,
    17. Chen JS,
    18. Bai LY,
    19. Oh SY,
    20. Choda Y,
    21. Yasui H,
    22. Takeuchi K,
    23. Hirashima Y,
    24. Hagihara S,
    25. Boku N
    : Nivolumab plus chemotherapy versus placebo plus chemotherapy in patients with HER2-negative, untreated, unresectable advanced or recurrent gastric or gastro-oesophageal junction cancer (ATTRACTION-4): a randomised, multicentre, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol 23(2): 234-247, 2022. DOI: 10.1016/S1470-2045(21)00692-6
    OpenUrlCrossRefPubMed
  7. ↵
    1. Smyth EC,
    2. Nilsson M,
    3. Grabsch HI,
    4. Van Grieken NC,
    5. Lordick F
    : Gastric cancer. Lancet 396(10251): 635-648, 2020. DOI: 10.1016/S0140-6736(20)31288-5
    OpenUrlCrossRefPubMed
  8. ↵
    1. Aoyama T
    : Perioperative body composition changes in the multimodal treatment of gastrointestinal cancer. Surg Today 50(3): 217-222, 2020. DOI: 10.1007/s00595-019-01815-8
    OpenUrlCrossRefPubMed
    1. Aoyama T,
    2. Hara K,
    3. Kazama K,
    4. Maezawa Y
    : Clinical impact of nutrition and inflammation assessment tools in gastric cancer treatment. Anticancer Res 42(11): 5167-5180, 2022. DOI: 10.21873/anticanres.16023
    OpenUrlAbstract/FREE Full Text
  10. ↵
    1. Aoyama T,
    2. Kazama K,
    3. Maezawa Y,
    4. Hara K
    : Usefulness of nutrition and inflammation assessment tools in esophageal cancer treatment. In Vivo 37(1): 22-35, 2023. DOI: 10.21873/invivo.13051
    OpenUrlAbstract/FREE Full Text
  11. ↵
    1. Pikuła A,
    2. Skórzewska M,
    3. Pelc Z,
    4. Mlak R,
    5. Gęca K,
    6. Sędłak K,
    7. Ciseł B,
    8. Kwietniewska M,
    9. Rawicz-Pruszyński K,
    10. Polkowski WP
    : Prognostic value of systemic inflammatory response markers in patients undergoing neoadjuvant chemotherapy and gastrectomy for advanced gastric cancer in the eastern European population. Cancers (Basel) 14(8): 1997, 2022. DOI: 10.3390/cancers14081997
    OpenUrlCrossRefPubMed
    1. Yu Q,
    2. Li KZ,
    3. Fu YJ,
    4. Tang Y,
    5. Liang XQ,
    6. Liang ZQ,
    7. Bai JH
    : Clinical significance and prognostic value of C-reactive protein/albumin ratio in gastric cancer. Ann Surg Treat Res 100(6): 338-346, 2021. DOI: 10.4174/astr.2021.100.6.338
    OpenUrlCrossRefPubMed
  13. ↵
    1. Huang D,
    2. Gao Y
    : The value of the systematic inflammation-based Glasgow Prognostic Score in patients with gastric cancer: A literature review. J Cancer Res Ther 10(4): 799, 2014. DOI: 10.4103/0973-1482.146054
    OpenUrlCrossRefPubMed
  14. ↵
    1. Lu W,
    2. Shen J,
    3. Zou D,
    4. Li P,
    5. Liu X,
    6. Jian Y
    : Predictive role of preoperative geriatric nutritional risk index for clinical outcomes in surgical gastric cancer patients: A meta-analysis. Front Surg 9: 1020482, 2022. DOI: 10.3389/fsurg.2022.1020482
    OpenUrlCrossRefPubMed
  15. ↵
    1. He L,
    2. Li Y,
    3. Qu L,
    4. Zhang F
    : Prognostic and clinicopathological value of the geriatric nutritional risk index in gastric cancer: A meta-analysis of 5,834 patients. Front Surg 9: 1087298, 2023. DOI: 10.3389/fsurg.2022.1087298
    OpenUrlCrossRefPubMed
  16. ↵
    1. Japanese Gastric Cancer Association
    : Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 24(1): 1-21, 2021. DOI: 10.1007/s10120-020-01042-y
    OpenUrlCrossRefPubMed
  17. ↵
    1. Kato M,
    2. Hayashi Y,
    3. Fukuda H,
    4. Yamaguchi S,
    5. Inoue T,
    6. Ogiyama H,
    7. Kitamura S,
    8. Komori M,
    9. Yamamoto K,
    10. Yamamoto M,
    11. Nagai K,
    12. Nakahara M,
    13. Egawa S,
    14. Yamada T,
    15. Sasakawa A,
    16. Kizu T,
    17. Nishiyama O,
    18. Shichijo S,
    19. Yoshii S,
    20. Tsujii Y,
    21. Shinzaki S,
    22. Iijima H,
    23. Takehara T
    : Geriatric nutritional risk index as a prognostic indicator in elderly patients with early colorectal cancer undergoing endoscopic submucosal dissection. Dig Endosc 34(3): 569-578, 2022. DOI: 10.1111/den.14090
    OpenUrlCrossRefPubMed
  18. ↵
    1. Hirahara N,
    2. Matsubara T,
    3. Fujii Y,
    4. Kaji S,
    5. Hyakudomi R,
    6. Yamamoto T,
    7. Uchida Y,
    8. Miyazaki Y,
    9. Ishitobi K,
    10. Kawabata Y,
    11. Tajima Y
    : Preoperative geriatric nutritional risk index is a useful prognostic indicator in elderly patients with gastric cancer. Oncotarget 11(24): 2345-2356, 2020. DOI: 10.18632/oncotarget.27635
    OpenUrlCrossRefPubMed
  19. ↵
    1. Sugawara K,
    2. Yamashita H,
    3. Urabe M,
    4. Okumura Y,
    5. Yagi K,
    6. Aikou S,
    7. Seto Y
    : Geriatric Nutrition Index influences survival outcomes in gastric carcinoma patients undergoing radical surgery. JPEN J Parenter Enteral Nutr 45(5): 1042-1051, 2021. DOI: 10.1002/jpen.1978
    OpenUrlCrossRefPubMed
  20. ↵
    1. Furuke H,
    2. Matsubara D,
    3. Kubota T,
    4. Kiuchi J,
    5. Kubo H,
    6. Ohashi T,
    7. Shimizu H,
    8. Arita T,
    9. Yamamoto Y,
    10. Konishi H,
    11. Morimura R,
    12. Shiozaki A,
    13. Kuriu Y,
    14. Ikoma H,
    15. Fujiwara H,
    16. Okamoto K,
    17. Otsuji E
    : Geriatric Nutritional Risk Index predicts poor prognosis of patients after curative surgery for gastric cancer. Cancer Diagn Progn 1(2): 43-52, 2021. DOI: 10.21873/cdp.10007
    OpenUrlCrossRefPubMed
  21. ↵
    1. Shimada T,
    2. Yamagata T,
    3. Kanno Y,
    4. Ohira T,
    5. Harada Y,
    6. Koike Y,
    7. Tanaka M,
    8. Komabayashi D,
    9. Shimizu T,
    10. Okano H,
    11. Suzuki S,
    12. Ito K
    : Predictive factors for short-term survival after non-curative endoscopic submucosal dissection for early gastric Cancer. Digestion 102(4): 630-639, 2021. DOI: 10.1159/000510165
    OpenUrlCrossRefPubMed
  22. ↵
    1. An S,
    2. Eo W,
    3. Lee S
    : Comparison of the clinical value of the Geriatric Nutritional Risk Index and Prognostic Nutritional Index as determinants of survival outcome in patients with gastric cancer. J Cancer 13(12): 3348-3357, 2022. DOI: 10.7150/jca.77397
    OpenUrlCrossRefPubMed
  23. ↵
    1. Miao X,
    2. Ding L,
    3. Hu J,
    4. Zhu H,
    5. Zhao K,
    6. Lu J,
    7. Jiang X,
    8. Xu Q,
    9. Zhu S
    : A web-based calculator combining Geriatric Nutritional Risk Index (GNRI) and Tilburg Frailty Indicator (TFI) predicts postoperative complications among young elderly patients with gastric cancer. Geriatr Gerontol Int 23: 205-212, 2023. DOI: 10.1111/ggi.14544
    OpenUrlCrossRefPubMed
  24. ↵
    1. Aoyama T,
    2. Murakawa M,
    3. Katayama Y,
    4. Yamaoku K,
    5. Kanazawa A,
    6. Higuchi A,
    7. Shiozawa M,
    8. Morimoto M,
    9. Yoshikawa T,
    10. Yamamoto N,
    11. Rino Y,
    12. Masuda M,
    13. Morinaga S
    : Impact of postoperative complications on survival and recurrence in pancreatic cancer. Anticancer Res 35: 2401-2409, 2015.
    OpenUrlAbstract/FREE Full Text
  25. ↵
    1. Tamagawa A,
    2. Aoyama T,
    3. Tamagawa H,
    4. Ju M,
    5. Komori K,
    6. Maezawa Y,
    7. Kano K,
    8. Kazama K,
    9. Murakawa M,
    10. Atsumi Y,
    11. Sawazaki S,
    12. Hara K,
    13. Numata M,
    14. Sato T,
    15. Yukawa N,
    16. Masuda M,
    17. Rino Y
    : Influence of postoperative pneumonia on esophageal cancer survival and recurrence. Anticancer Res 39(5): 2671-2678, 2019. DOI: 10.21873/anticanres.13392
    OpenUrlAbstract/FREE Full Text
Back to top

In this issue

Print
Download PDF
Article Alerts
Email Article
Citation Tools
Reprints and Permissions
The Clinical Influence of Geriatric Nutritional Risk Index in Patients With Gastric Cancer Who Receive Curative Treatment
TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, KENTARO HARA, KEISUKE KAZAMA, MASAKATSU NUMATA, SHO SAWAZAKI, HIROSHI TAMAGAWA, AYAKO TAMAGAWA, MASATO NAKAZONO, KENKI SEGAMI, HARUHIKO CHO, MINORI TATEISHI, TOMOYUKI MINAMI, SHINSUKE NAGASAWA, KEISUKE KOMORI, AYA KATO, KAZUKI OTANI, SHINNOSUKE KAWAHARA, TAKASHI OSHIMA, NORIO YUKAWA, AYA SAITO, YASUSHI RINO
Anticancer Research Dec 2023, 43 (12) 5605-5612; DOI: 10.21873/anticanres.16763
Twitter logo Facebook logo Mendeley logo

Jump to section

Keywords