Next Article in Journal
Potential Therapies Targeting the Metabolic Reprogramming of Diabetes-Associated Breast Cancer
Next Article in Special Issue
Screening of Differentially Expressed Genes Based on the ACRG Molecular Subtypes of Gastric Cancer and the Significance and Mechanism of AGTR1 Gene Expression
Previous Article in Journal
Maternity Blues: A Narrative Review
Previous Article in Special Issue
Gastric Cancer: Innovations in Screening, Diagnosis and Treatment
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

The Prognostic Value of the GNRI in Patients with Stomach Cancer Undergoing Surgery

Liyuan Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430062, China
Department of General Surgery, Renmin Hospital of Wuhan University, Wuhan 430060, China
Central Laboratory, Renmin Hospital of Wuhan University, Wuhan 430060, China
Department of Neurology, The First Hospital of Jilin University, Changchun 130000, China
Department of Colorectal and Anorectal Surgery, Hunan Hospital of Integrated Tradmonal Chinese and Western Medicine (Hunan Academy of Traditional Chinese Medicine Affiliated Hospital), Changsha 410006, China
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
These authors contributed equally to this work.
J. Pers. Med. 2023, 13(1), 155;
Submission received: 30 November 2022 / Revised: 5 January 2023 / Accepted: 9 January 2023 / Published: 13 January 2023
(This article belongs to the Special Issue Gastric Cancer: Innovations in Screening, Diagnosis and Treatment)


Malnutrition often induces an adverse prognosis in cancer surgery patients. The elderly nutrition risk index (GNRI) is an example of the objective indicators of nutrition-related risks. We performed a meta-analysis to thoroughly examine the evidence for the GNRI in predicting the outcomes of patients undergoing stomach cancer surgery. Eligible articles were retrieved using PubMed, the Cochrane Library, EMBASE, and Google Scholar by 24 October 2022. The clinical outcomes were overall survival (OS), cancer-specific survival (CSS), and post-operative complications. A total of 11 articles with 5593 patients were included in this meta-analysis. The combined forest plot showed that for every unit increase in the preoperative GNRI score in patients with stomach cancer, their postoperative mortality was reduced by 5.6% (HR: 0.944; 95% CI: 0.933–0.956, p < 0.001). The pooled results also demonstrated that a low GNRI was correlated with poor OS (HR: 2.052; 95% CI: 1.726–2.440, p < 0.001) and CSS (HR: 1.684; 95% CI: 1.249–2.270, p = 0.001) in patients who underwent stomach cancer surgery. Postoperative complications were more likely to occur in patients with a low GNRI, as opposed to those with a high GNRI (OR: 1.768; 95% CI: 1.445–2.163, p < 0.001). There was no evidence of significant heterogeneity, and the sensitivity analysis supported the stability and dependability of the above results. the GNRI is a valuable predictor of long-term outcomes and complications in stomach cancer patients undergoing surgery.

1. Introduction

Gastric cancer (GC) remains a particularly lethal cancer with the fourth highest fatality and the fifth highest incidence rate worldwide. East Asian countries have the highest incidence of gastric cancer, accounting for more than half of the reported patients [1]. Even after curative surgery, the prognosis of a significant number of GC patients remains poor. GC patients often have inadequate oral intake because of multiple cancer-associated symptoms, including obstruction, anorexia, nausea, and generalized fatigue [2]. Malnutrition is common in GC patients because of their increased metabolic demands, nutrient loss, and inadequate oral intake [3,4,5], which is the main risk factor that leads to perioperative complications [6,7]. Therefore, it is very important to evaluate the nutritional status of GC patients before surgery to optimize their prognosis.
The geriatric nutrition risk index (GNRI) is a nutritional parameter that involves the ratio of serum albumin level to current weight and ideal healthy weight, which is objective and simple compared with other parameters [8]. Compared with the serum albumin level or body mass index alone, the GNRI is thought to be a more accurate predictor of nutrition-related outcomes in aging populations [9]. The formula used to calculate the GNRI is as follows: GNRI = (1.489 × albumin, g/L) + (41.7 × present/ideal body weight, kg) [8]. Since the GNRI is easily applied in clinical practice, it is widely used to assess the nutritional status of various patients. A recent study suggested that a lower GNRI is associated with a poor prognosis in patients with esophageal cancer [9].
To date, several retrospective studies have analyzed the association between the GNRI and prognosis and perioperative complications in GC patients undergoing surgery. However, systematic evaluations of whether preoperative GNRI values can effectively predict the outcome of surgical treatment for GC patients have not been carried out. Therefore, in this study, we verified the impact of the GNRI on the prognosis of GC patients.

2. Methods

2.1. Literature Search Strategies

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement was used in this meta-analysis [10]. The protocol for this meta-analysis is available on PROSPERO (CRD42022369645). On 24 October 2022, PubMed, EMBASE, and Cochrane Library were searched using the following keywords: “Geriatric nutritional risk index”, “GNRI”, “Stomach Neo-plasms [Mesh]”, “Stomach Neoplasm”, “Stomach Cancer”, “Gastric Neoplasm”, “Gastric Cancer”, “Cancer of the Stomach”, “Cancer of Stomach”. The language of the studies was restricted to English. Using Google Scholar, we verified the grey documents without indexes in the above-mentioned database. In addition, we screened references that met the inclusion criteria.

2.2. Inclusion and Exclusion Criteria

The detailed inclusion criteria are as follows: patients with GC who underwent surgery, patients whose surgical prognosis was evaluated by research, and patients who supplied information on at least one of the outcomes of interest (overall survival (OS), cancer-specific survival (CSS), and postoperative complications). Reviews, conference abstracts, case reports, letters, and comments were excluded. If there was an overlap of patient groups in the study, we only chose the study with the most comprehensive data and the most rigorous method.

2.3. Data Extraction and Quality Assessment

The author, publication year, study region, study period, sample size, number of male and female patients, age of patients, surgical method, cut-off, and results were the primary subjects of data extraction. The quality of the observational studies was evaluated using the Newcastle–Ottawa Scale (NOS) score [11]. High-quality literature was indicated by a score below six. Two authors double-checked each of the aforementioned processes, and a senior author resolved any discrepancies.

2.4. Statistical Methods

Stata 15.0 was used to conduct the statistical analysis. The chi-squared test was used to determine the statistical heterogeneity. A fixed effect model was utilized when p > 0.1 and I2 50% showed low heterogeneity; otherwise, the random-effect model was applied. To investigate the potential confounding factors in this meta-analysis, sub-group analyses were conducted. The tests of Egger and Begg were employed to evaluate publication bias. If there was a considerable publication bias, we changed the findings using the trim-and-fill technique [12]. To test the stability of the findings, a sensitivity analysis that separately excluded each study from the analysis was carried out. A p value of 0.05 was used to determine the significance for all the two-sided p values.

3. Results

3.1. Characteristics of Studies

A total of 11 studies that involved 5593 patients were included in this meta-analysis [13,14,15,16,17,18,19,20,21,22,23]. The PRISMA flow diagram is provided in Figure 1. Specifically, 83 irrelevant records were excluded after the screening of titles and abstracts. Following this, the full texts of the remaining 19 articles were further assessed. Three of these articles [24,25,26] were included in the multicenter study by Toya et al. [15] and were, therefore, excluded. GC patients with cachexia (with or without surgery) were included by Ruan et al. and were, therefore, excluded [27]. After excluding 2 unrelated studies and 2 conference abstracts, 11 articles were ultimately included [13,14,15,16,17,18,19,20,21,22,23].
The main characteristics of the studies included are shown in Table 1. A total of 10 studies were performed in Japan, whereas 1 study was conducted in Korea (Table 1). The details of the specific hospitals where the patients were recruited for each study can be found in Table S1 [13,14,15,16,17,18,19,20,21,22,23]. Three studies regarded GNRI scores as continuous variables, while eight studies reported the cut-off point of the GNRI to range from 85.7 to 98 (Table 1). Notably, 1551 patients underwent gastric endoscopic submucosal dissection (ESD), and 4042 patients underwent curative gastrectomy (Table 1). The NOS scores for 11 articles ranged from 6 to 8, which represented a low risk of bias (Table 1).

3.2. GNRI and Overall Survival

In total, 9 articles that involved 4948 patients explored the association between the GNRI and OS in GC patients undergoing surgery. Of these, 6 studies with 3714 patients classified patients into high and low groups using cut-off values. The pooled HR was 2.052 (95% CI: 1.726–2.440, p < 0.001), implying that a low GNRI raised the death risk by 105.2% (Figure 2A). Since there was no evidence of significant heterogeneity, a fixed-effects model was used (I2 = 0.0%, p = 0.633).
In addition, 3 articles with a total of 1234 participants considered the GNRI score as a continuous variable to explore its relationship with OS in GC patients. As shown in Figure 2B, a fixed-effects model was utilized (I2 = 45.9%, p = 0.158). The combined forest plot demonstrated that for every unit increase in the GNRI score in GC patients, their postoperative mortality was reduced by 5.6% (HR: 0.944; 95% CI: 0.933–0.956, p < 0.001).

3.3. GNRI and Cancer-Specific Survival

The relationship between the GNRI and CSS was also examined using prognostic data from 3 studies that involved 1960 participants. No significant heterogeneity was observed in the included studies (I2 = 0.0%, p = 0.953, Figure 3A), so a fixed-effects model was used. We found that patients with a low GNRI had worse CSS than those with a high GNRI (HR: 1.684, 95% CI: 1.249–2.270, p = 0.001, Figure 3A).

3.4. GNRI and Postoperative Complications

A connection between the GNRI and postoperative complications in GC patients was observed in a total of 6 studies that involved 3565 individuals. Hisada et al. assessed ESD-related complications based on the Common Terminology Criteria for Adverse Events version 5.0, with a CTCAE grade of ≥2 being considered as an adverse event [28]. In the remaining five studies, according to the Clavien Dindo classification, postoperative complications were categorized as a grade ≥ II [29]. As shown in Figure 3B, the pooled results demonstrated that postoperative complications were more likely to occur in patients with a low GNRI, as opposed to those with a high GNRI (OR: 1.768; 95% CI: 1.445–2.163, p < 0.001). No heterogeneity was found in the studies (I2 = 0.0%, p = 0.512), and a fixed-effects model was applied to this analysis.

3.5. Subgroup Analysis of OS and Postoperative Complications

We subsequently performed a subgroup analysis by correcting for the impact of publishing year, treatment, sample size, GNRI cut-off value, and definition of complications. The results revealed that the GNRI was an independent prognostic factor that affected the OS and postoperative complications of the patients in all the subgroups (Figure 4 and Figure 5 and Figure S1).

3.6. Publication Bias

The publication bias was verified by Begg’s and Egger’s tests. We confirmed that there was no evidence of publication bias for OS (Egger’s test: p = 0.825; Begg’s test: p = 0.707) or CSS (Egger’s test: p = 0.436; Begg’s test: p = 1.000) across the studies. Notably, the publication bias for postoperative complications was found by Egger’s test (Egger’s test: p = 0.004; Begg’s test: p = 0.452). Next, the trim-and-fill method was used to calculate the number of missing studies on postoperative problems. By factoring in the missing hypothesis studies, the combined OR was recalculated, but was not substantially different (HR: 1.592, 95% CI: 1.332–1.902; p < 0.001, Figure S2). As a result, the publication bias had little impact, and the outcome was quite stable.

3.7. Sensitivity Analysis

We used the leave-one-out method to perform a sensitivity analysis to determine how each study might affect the meta-analysis. As shown in Figure 6A, the pooled HR for OS did not significantly change after excluding one study at a time and ranged from 1.999 (95% CI: 1.611–2.481, after omitting the study by Sugawara et al. 2021) to 2.137 (95% CI: 1.782–2.564, after omitting the study by Tsuchiya et al. 2022). Similarly, the pooled OR for postoperative complications was not significantly different in the sensitivity analysis (Figure 6B). The overall OR ranged from 1.700 (95% CI: 1.369–2.112, after omitting the study by Furuke et al. 2021) to 2.168 (95% CI: 1.627–2.890, after omitting the study by Sugawara et al. 2021). From the above, we can conclude that our results are stable and reliable.

4. Discussion

This study aims to verify the predictive significance of the GNRI in GC patients treated with surgery, and the pooled data demonstrated that a higher GNRI was strongly related to longer OS and CSS and lower postoperative complications in GC patients. Furthermore, our findings held stable even after the sensitivity analysis and subgroup analysis were used to detect potential confounders, suggesting that a lower preoperative GNRI is an independent indicator of a poorer prognosis for surgery in GC patients. To the best of our knowledge from a comprehensive search of the literature, this is one of the only meta-analyses to thoroughly explore the impact of the GNRI on the prognosis of GC patients undergoing surgery. As a highly accessible indicator in clinical practice, preoperative assessment of patients’ GNRI and nutritional interventions for patients with a higher GNRI (e.g., >98) can be extremely helpful in improving the prognosis of these patients.
Malnutrition is detrimental to the immune system and is associated with inflammation and cachexia, which significantly increase the risk of postoperative complications [30,31], diminish the effectiveness of chemoradiotherapy, and increase the likelihood of adjuvant therapy adverse effects [32,33,34], all of which are directly related to the patient’s prognosis. Therefore, several biomarkers were developed, including the PNI [35] and CONUT [36], to detect patients who were malnourished. However, these indices were lacking in value for older patients, due to limitations in usual weight estimation [37]. Next, the GNRI was proposed and was used as an age-specific indicator to assess the nutritional status of elderly patients. Surprisingly, recent research has suggested that the GNRI may have better predictive value than nutritional assessment in many diseases, such as heart failure [38,39], hemodialysis [40], and patients undergoing surgery for various malignancies (for example, colorectal cancer [41], pancreatic cancer [42], gallbladder cancer [43], hepatocellular carcinoma [44], and esophageal cancer [45]). A recent study by Chen et al. also revealed that the GNRI can be used as a promising alternative to the Global Leadership Initiative on Malnutrition (GLIM) and is the best option for the perioperative management of patients with rectal cancer [46]. Compared with other types of cancer, the nutritional metabolism disorder of gastric cancer patients is more serious and specialized. Because the stomach is one of the main organs for digesting food and plays an important role in the nutrition and metabolism of the body [47,48], it is necessary to study the nutrition of gastric cancer patients for the prognosis of gastric cancer [49].
Cancer cachexia is a complex pathological disorder caused by the interaction of complex factors, such as inflammation, hypermetabolism, changes in neurohormones, and metabolic disorders [50,51,52]. It is characterized by clinical symptoms such as muscle atrophy, weight loss, fatigue, and anorexia [53]. It is reported that the vast majority of patients with advanced cancer will suffer from cachexia, which is not only a common and persistent pain factor for patients with advanced cancer, but also seriously affects the quality of life of patients and the effect of radiotherapy and chemotherapy [54]. In the case of cancer cachexia, the nutrition intake and metabolism of the body are more difficult, thus leading to a vicious circle [55]. Consistent with our study, a previous study indicated that good nutritional status and nutrition-centered comprehensive treatment can help to improve patients’ health by reducing their nausea and vomiting symptoms [56].
Aging and unhealthy diet are examples of the risk factors for gastric cancer [57,58]. It has been demonstrated that a short interval between lunch and dinner and a lack of exercise after dinner are the risk factors for gastric cancer, and the synergistic effect of these two risk factors is positively related to age, so the risk of gastric cancer in people over 55 years old is high [59,60]. In addition, the research on this topic suggests that vitamin supplementation is strongly related to a decrease in the incidence rate of gastric cancer [61,62]. It may be attributed to the inhibition of redox reactions by vitamin C and E, which clear the accumulation of reactive oxygen species (ROS) induced by oxidative stress in the process of gastric cancer [63,64]. Overall, the GNRI can be a promising predictor of poor outcomes in cancer patients undergoing surgery, so we concentrated on how it affected GC. We synthesized the existing evidence to confirm that the GNRI can be a valid predictor of poor outcomes in GC patients undergoing surgery. This study offers evidence-based support for the clinical use of the GNRI in the preoperative assessment of GC patients. Additionally, the critical value range for the GNRI for most of the included studies was 92–98, which may provide some reference value for determining the critical value of the GNRI in clinical applications.
However, this analysis has several limitations. Firstly, the analysis only included retrospective cohort studies, rather than well-designed randomized controlled trials (RCTs), which possibly limited its statistical power. Secondly, there is a lack of uniformity in the cut-off values of the GNRI across the studies, and the aggregated survival results may deviate from the actual values. Finally, since no Western studies were included and the patients were all from Asia, there may have been some selection bias in the patients’ ethnicity, and the conclusions may not be practical for patients of other ethnicities. Thus, to confirm and update our conclusion, more high-quality studies with sizable sample sizes, particularly multicenter RCTs, are urgently required. At the same time, these studies should also include patients of different ethnicities and explore the optimal cut-off values to more precisely guide clinical practice for the benefit of patients.

Supplementary Materials

The following supporting information can be downloaded at:, Figure S1: Subgroup analysis of postoperative complications based on the definition of complications [14,17,19,20,21,23]; Figure S2: The picture of the trim-and-fill method; Table S1: The hospitals that carried out the 11 studies.

Author Contributions

Q.Z., L.Z., Y.L., H.P. and M.W. conceived and designed the study. Q.Z., L.Z., Q.J., Y.H., H.P., M.W. and Y.L. were responsible for the collection and assembly of data, data analysis, and interpretation. Q.Z., L.Z., H.P., Y.H. and Y.L. were involved in writing the manuscript. Q.Z., L.Z., H.P., Q.J., Y.L. and M.W. revised the manuscript. All the work was performed under the instruction of Y.L. and M.W., Q.Z. and L.Z. contributed equally to this work. All authors have read and agreed to the published version of the manuscript.


This work was supported by grants from the National Natural Science Foundation of China (No. 82172855; 81870442), and Natural Science Foundation of Hubei Province, China (No. 2021CFB365). The work was also supported by the Key Project of Natural Science Foundation of Hunan Province (2021JJ30419) and the Key Project of Scientific Research Foundation of Hunan Provincial Administration of Traditional Chinese Medicine (2021017).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.


The authors thank all the medical staff who contributed to the maintenance of the medical record database.

Conflicts of Interest

The authors declare that they have no competing interests.


  1. Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
  2. Fukuda, Y.; Yamamoto, K.; Hirao, M.; Nishikawa, K.; Maeda, S.; Haraguchi, N.; Miyake, M.; Hama, N.; Miyamoto, A.; Ikeda, M.; et al. Prevalence of Malnutrition Among Gastric Cancer Patients Undergoing Gastrectomy and Optimal Preoperative Nutritional Support for Preventing Surgical Site Infections. Ann. Surg. Oncol. 2015, 22 (Suppl. 3), S778–S785. [Google Scholar] [CrossRef] [PubMed]
  3. Park, S.Y.; Yoon, J.K.; Lee, S.J.; Haam, S.; Jung, J. Postoperative change of the psoas muscle area as a predictor of survival in surgically treated esophageal cancer patients. J. Thorac. Dis. 2017, 9, 355–361. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Mariette, C.; De Botton, M.L.; Piessen, G. Surgery in esophageal and gastric cancer patients: What is the role for nutrition support in your daily practice? Ann. Surg. Oncol. 2012, 19, 2128–2134. [Google Scholar] [CrossRef]
  5. Saunders, J.; Smith, T. Malnutrition: Causes and consequences. Clin. Med. 2010, 10, 624–627. [Google Scholar] [CrossRef] [PubMed]
  6. Schiesser, M.; Kirchhoff, P.; Müller, M.K.; Schäfer, M.; Clavien, P.A. The correlation of nutrition risk index, nutrition risk score, and bioimpedance analysis with postoperative complications in patients undergoing gastrointestinal surgery. Surgery 2009, 145, 519–526. [Google Scholar] [CrossRef]
  7. Kuzu, M.A.; Terzioğlu, H.; Genç, V.; Erkek, A.B.; Ozban, M.; Sonyürek, P.; Elhan, A.H.; Torun, N. Preoperative nutritional risk assessment in predicting postoperative outcome in patients undergoing major surgery. World J. Surg. 2006, 30, 378–390. [Google Scholar] [CrossRef]
  8. Bouillanne, O.; Morineau, G.; Dupont, C.; Coulombel, I.; Vincent, J.P.; 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. 2005, 82, 777–783. [Google Scholar] [CrossRef] [Green Version]
  9. Zhou, J.; Fang, P.; Li, X.; Luan, S.; Xiao, X.; Gu, Y.; Shang, Q.; Zhang, H.; Yang, Y.; Zeng, X.; et al. Prognostic Value of Geriatric Nutritional Risk Index in Esophageal Carcinoma: A Systematic Review and Meta-Analysis. Front. Nutr. 2022, 9, 831283. [Google Scholar] [CrossRef]
  10. Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med. 2009, 6, e1000100. [Google Scholar] [CrossRef]
  11. Stang, A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur. J. Epidemiol. 2010, 25, 603–605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Duval, S.; Tweedie, R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000, 56, 455–463. [Google Scholar] [CrossRef] [PubMed]
  13. Yoshikawa, T.; Yamauchi, A.; Hamasaki, R.; Mori, Y.; Osawa, K.; Ito, R.; Kawai, Y.; Nakagami, S.; Azuma, S.; Morita, T.; et al. The Safety and Clinical Validity of Endoscopic Submucosal Dissection for Early Gastric Cancer in Patients Aged More Than 85 Years. Cancers 2022, 14, 3311. [Google Scholar] [CrossRef] [PubMed]
  14. Tsuchiya, N.; Kunisaki, C.; Kondo, H.; Sato, S.; Sato, K.; Watanabe, J.; Takeda, K.; Kosaka, T.; Akiyama, H.; Endo, I. Prognostic Factors Affecting Short- and Long-Term Outcomes of Gastrectomy for Gastric Cancer in Older Patients. Dig. Surg. 2022, 39, 109–116. [Google Scholar] [CrossRef] [PubMed]
  15. Toya, Y.; Shimada, T.; Hamada, K.; Watanabe, K.; Nakamura, J.; Fukushi, D.; Hatta, W.; Shinkai, H.; Ito, H.; Matsuhashi, T.; et al. Prediction model of 3-year survival after endoscopic submucosal dissection for early gastric cancer in elderly patients aged ≥85 years: EGC-2 model. J. Cancer Res. Clin. Oncol. 2022. [Google Scholar] [CrossRef] [PubMed]
  16. Matsunaga, T.; Saito, H.; Osaki, T.; Takahashi, S.; Iwamoto, A.; Fukuda, K.; Taniguchi, K.; Kuroda, H.; Takeuchi, T.; Sugamura, K.; et al. Impact of geriatric nutritional risk index on outcomes after gastrectomy in elderly patients with gastric cancer: A retrospective multicenter study in Japan. BMC Cancer 2022, 22, 540. [Google Scholar] [CrossRef] [PubMed]
  17. Hisada, H.; Tsuji, Y.; Obata, M.; Cho, R.; Nagao, S.; Miura, Y.; Mizutani, H.; Ohki, D.; Yakabi, S.; Takahashi, Y.; et al. The impact of sarcopenia on short- and long-term outcomes of endoscopic submucosal dissection for early gastric cancer. J. Gastroenterol. 2022, 57, 952–961. [Google Scholar] [CrossRef]
  18. An, S.; Eo, W.; 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 2022, 13, 3348–3357. [Google Scholar] [CrossRef]
  19. Sugawara, K.; Yamashita, H.; Urabe, M.; Okumura, Y.; Yagi, K.; Aikou, S.; Seto, Y. Geriatric Nutrition Index Influences Survival Outcomes in Gastric Carcinoma Patients Undergoing Radical Surgery. JPEN J. Parenter Enter. Nutr. 2021, 45, 1042–1051. [Google Scholar] [CrossRef]
  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. 2021, 35, 1202–1209. [Google Scholar] [CrossRef]
  21. Furuke, H.; Matsubara, D.; Kubota, T.; Kiuchi, J.; Kubo, H.; Ohashi, T.; Shimizu, H.; Arita, T.; Yamamoto, Y.; Konishi, H.; et al. Geriatric Nutritional Risk Index Predicts Poor Prognosis of Patients After Curative Surgery for Gastric Cancer. Cancer Diagn. Progn. 2021, 1, 43–52. [Google Scholar] [CrossRef] [PubMed]
  22. Hirahara, N.; Matsubara, T.; Fujii, Y.; Kaji, S.; Hyakudomi, R.; Yamamoto, T.; Uchida, Y.; Miyazaki, Y.; Ishitobi, K.; Kawabata, Y.; et al. Preoperative geriatric nutritional risk index is a useful prognostic indicator in elderly patients with gastric cancer. Oncotarget 2020, 11, 2345–2356. [Google Scholar] [CrossRef]
  23. 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 2018, 32, 1667–1672. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Toya, Y.; Endo, M.; Akasaka, R.; Morishita, T.; Yanai, S.; Nakamura, S.; Eizuka, M.; Sugimoto, R.; Uesugi, N.; Sugai, T.; et al. Prognostic nutritional index is an independent prognostic factor for older patients aged ≥ 85 years treated by gastric endoscopic submucosal dissection. BMC Gastroenterol. 2021, 21, 328. [Google Scholar] [CrossRef] [PubMed]
  25. Shimada, T.; Yamagata, T.; Kanno, Y.; Ohira, T.; Harada, Y.; Koike, Y.; Tanaka, M.; Komabayashi, D.; Shimizu, T.; Okano, H.; et al. Predictive Factors for Short-Term Survival after Non-Curative Endoscopic Submucosal Dissection for Early Gastric Cancer. Digestion 2021, 102, 630–639. [Google Scholar] [CrossRef] [PubMed]
  26. Toya, Y.; Endo, M.; Nakamura, S.; Akasaka, R.; Yanai, S.; Kawasaki, K.; Koeda, K.; Eizuka, M.; Fujita, Y.; Uesugi, N.; et al. Long-term outcomes and prognostic factors with non-curative endoscopic submucosal dissection for gastric cancer in elderly patients aged ≥ 75 years. Gastric. Cancer 2019, 22, 838–844. [Google Scholar] [CrossRef] [Green Version]
  27. Ruan, G.T.; Zhang, Q.; Zhang, X.; Tang, M.; Song, M.M.; Zhang, X.W.; Li, X.R.; Zhang, K.P.; Ge, Y.Z.; Yang, M.; et al. Geriatric Nutrition Risk Index: Prognostic factor related to inflammation in elderly patients with cancer cachexia. J. Cachexia Sarcopenia Muscle 2021, 12, 1969–1982. [Google Scholar] [CrossRef]
  28. Hisada, H.; Tamura, N.; Tsuji, Y.; Nagao, S.; Fukagawa, K.; Miura, Y.; Mizutani, H.; Ohki, D.; Yakabi, S.; Minatsuki, C.; et al. The impact of sarcopenia on adverse events associated with gastric endoscopic submucosal dissection. Surg. Endosc. 2022, 36, 6387–6395. [Google Scholar] [CrossRef]
  29. Clavien, P.A.; Barkun, J.; de Oliveira, M.L.; Vauthey, J.N.; Dindo, D.; Schulick, R.D.; de Santibañes, E.; Pekolj, J.; Slankamenac, K.; Bassi, C.; et al. The Clavien-Dindo classification of surgical complications: Five-year experience. Ann. Surg. 2009, 250, 187–196. [Google Scholar] [CrossRef] [Green Version]
  30. Goins, E.C.; Weber, J.M.; Truong, T.; Moss, H.A.; Previs, R.A.; Davidson, B.A.; Havrilesky, L.J. Malnutrition as a risk factor for post-operative morbidity in gynecologic cancer: Analysis using a national surgical outcomes database. Gynecol. Oncol. 2022, 165, 309–316. [Google Scholar] [CrossRef]
  31. Li, Q.D.; Li, H.; Li, F.J.; Wang, M.S.; Li, Z.J.; Han, J.; Li, Q.H.; Ma, X.J.; Wang da, N. Nutrition deficiency increases the risk of stomach cancer mortality. BMC Cancer 2012, 12, 315. [Google Scholar]
  32. McMillan, D.C. The systemic inflammation-based Glasgow Prognostic Score: A decade of experience in patients with cancer. Cancer Treat. Rev. 2013, 39, 534–540. [Google Scholar] [CrossRef]
  33. Kono, T.; Sakamoto, K.; Shinden, S.; Ogawa, K. Pre-therapeutic nutritional assessment for predicting severe adverse events in patients with head and neck cancer treated by radiotherapy. Clin. Nutr. 2017, 36, 1681–1685. [Google Scholar] [CrossRef] [PubMed]
  34. Tashiro, M.; Yamada, S.; Sonohara, F.; Takami, H.; Suenaga, M.; Hayashi, M.; Niwa, Y.; Tanaka, C.; Kobayashi, D.; Nakayama, G.; et al. Clinical Impact of Neoadjuvant Therapy on Nutritional Status in Pancreatic Cancer. Ann. Surg. Oncol. 2018, 25, 3365–3371. [Google Scholar] [CrossRef] [PubMed]
  35. Onodera, T.; Goseki, N.; Kosaki, G. [Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients]. Nihon Geka Gakkai Zasshi 1984, 85, 1001–1005. [Google Scholar]
  36. Ignacio de Ulíbarri, J.; González-Madroño, A.; de Villar, N.G.; González, P.; González, B.; Mancha, A.; Rodríguez, F.; Fernández, G. CONUT: A tool for controlling nutritional status. First validation in a hospital population. Nutr. Hosp. 2005, 20, 38–45. [Google Scholar] [PubMed]
  37. Wang, H.; Li, C.; Yang, R.; Jin, J.; Liu, D.; Li, W. Prognostic Value of the Geriatric Nutritional Risk Index in Non-Small Cell Lung Cancer Patients: A Systematic Review and Meta-Analysis. Front. Oncol. 2021, 11, 794862. [Google Scholar] [CrossRef]
  38. Nishi, I.; Seo, Y.; Hamada-Harimura, Y.; Yamamoto, M.; Ishizu, T.; Sugano, A.; Sato, K.; Sai, S.; Obara, K.; Suzuki, S.; et al. Geriatric nutritional risk index predicts all-cause deaths in heart failure with preserved ejection fraction. ESC Heart Fail. 2019, 6, 396–405. [Google Scholar] [CrossRef] [Green Version]
  39. Yasumura, K.; Abe, H.; Iida, Y.; Kato, T.; Nakamura, M.; Toriyama, C.; Nishida, H.; Idemoto, A.; Shinouchi, K.; Mishima, T.; et al. Prognostic impact of nutritional status and physical capacity in elderly patients with acute decompensated heart failure. ESC Heart Fail. 2020, 7, 1801–1808. [Google Scholar] [CrossRef]
  40. Yamada, S.; Yamamoto, S.; Fukuma, S.; Nakano, T.; Tsuruya, K.; Inaba, M. Geriatric Nutritional Risk Index (GNRI) and Creatinine Index Equally Predict the Risk of Mortality in Hemodialysis Patients: J-DOPPS. Sci. Rep. 2020, 10, 5756. [Google Scholar] [CrossRef] [Green Version]
  41. Hayama, T.; Hashiguchi, Y.; Ozawa, T.; Watanabe, M.; Fukushima, Y.; Shimada, R.; Nozawa, K.; Matsuda, K.; Fujii, S.; Fukagawa, T. The preoperative geriatric nutritional risk index (GNRI) is an independent prognostic factor in elderly patients underwent curative resection for colorectal cancer. Sci. Rep. 2022, 12, 3682. [Google Scholar] [CrossRef] [PubMed]
  42. Funamizu, N.; Sakamoto, A.; Utsunomiya, T.; Uraoka, M.; Nagaoka, T.; Iwata, M.; Ito, C.; Tamura, K.; Sakamoto, K.; Ogawa, K.; et al. Geriatric nutritional risk index as a potential prognostic marker for patients with resectable pancreatic cancer: A single-center, retrospective cohort study. Sci. Rep. 2022, 12, 13644. [Google Scholar] [CrossRef] [PubMed]
  43. Dai, H.; Xu, J. Preoperative geriatric nutritional risk index is an independent prognostic factor for postoperative survival after gallbladder cancer radical surgery. BMC Surg. 2022, 22, 133. [Google Scholar]
  44. Kanno, H.; Goto, Y.; Sasaki, S.; Fukutomi, S.; Hisaka, T.; Fujita, F.; Akagi, Y.; Okuda, K. Geriatric nutritional risk index predicts prognosis in hepatocellular carcinoma after hepatectomy: A propensity score matching analysis. Sci. Rep. 2021, 11, 9038. [Google Scholar] [CrossRef]
  45. Yamana, I.; Takeno, S.; Shibata, R.; Shiwaku, H.; Maki, K.; Hashimoto, T.; Shiraishi, T.; Iwasaki, A.; Yamashita, Y. Is the Geriatric Nutritional Risk Index a Significant Predictor of Postoperative Complications in Patients with Esophageal Cancer Undergoing Esophagectomy? Eur. Surg. Res. 2015, 55, 35–42. [Google Scholar] [CrossRef]
  46. Chen, X.Y.; Lin, Y.; Yin, S.Y.; Shen, Y.T.; Zhang, X.C.; Chen, K.K.; Zhou, C.J.; Zheng, C.G. The geriatric nutritional risk index is an effective tool to detect GLIM-defined malnutrition in rectal cancer patients. Front. Nutr. 2022, 9, 1061944. [Google Scholar] [CrossRef]
  47. Minnella, E.M.; Awasthi, R.; Loiselle, S.E.; Agnihotram, R.V.; Ferri, L.; Carli, F. Effect of Exercise and Nutrition Prehabilitation on Functional Capacity in Esophagogastric Cancer Surgery: A Randomized Clinical Trial. JAMA Surg. 2018, 153, 1081–1089. [Google Scholar] [CrossRef] [Green Version]
  48. Miranti, E.H.; Stolzenberg-Solomon, R.; Weinstein, S.J.; Selhub, J.; Männistö, S.; Taylor, P.; Freedman, N.; Albanes, D.; Abnet, C.; Murphy, G. Low vitamin B(12) increases risk of gastric cancer: A prospective study of one-carbon metabolism nutrients and risk of upper gastrointestinal tract cancer. Int. J. Cancer 2017, 141, 1120–1129. [Google Scholar] [CrossRef] [Green Version]
  49. Meng, Q.; Tan, S.; Jiang, Y.; Han, J.; Xi, Q.; Zhuang, Q.; Wu, G. Post-discharge oral nutritional supplements with dietary advice in patients at nutritional risk after surgery for gastric cancer: A randomized clinical trial. Clin. Nutr. 2021, 40, 40–46. [Google Scholar] [CrossRef]
  50. Solheim, T.S.; Laird, B.; Balstad, T.R.; Stene, G.B.; Bye, A.; Johns, N.; Pettersen, C.H.; Fallon, M.; Fayers, P.; Fearon, K.; et al. A randomized phase II feasibility trial of a multimodal intervention for the management of cachexia in lung and pancreatic cancer. J. Cachexia Sarcopenia Muscle 2017, 8, 778–788. [Google Scholar] [CrossRef]
  51. Fearon, K.; Strasser, F.; Anker, S.D.; Bosaeus, I.; Bruera, E.; Fainsinger, R.L.; Jatoi, A.; Loprinzi, C.; MacDonald, N.; Mantovani, G.; et al. Definition and classification of cancer cachexia: An international consensus. Lancet Oncol. 2011, 12, 489–495. [Google Scholar] [CrossRef] [PubMed]
  52. Fearon, K.C.; Glass, D.J.; Guttridge, D.C. Cancer cachexia: Mediators, signaling, and metabolic pathways. Cell Metab. 2012, 16, 153–166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Jendretzki, J.; Henniger, D.; Schiffmann, L.; Wolz, C.; Kollikowski, A.; Meining, A.; Einsele, H.; Winkler, M.; Löffler, C. Every fifth patient suffered a high nutritional risk-Results of a prospective patient survey in an oncological outpatient center. Front. Nutr. 2022, 9, 1033265. [Google Scholar] [CrossRef]
  54. Teunissen, S.C.C.M.; Wesker, W.; Kruitwagen, C.; de Haes, H.C.J.M.; Voest, E.E.; de Graeff, A. Symptom prevalence in patients with incurable cancer: A systematic review. J. Pain Symptom Manag. 2007, 34, 94–104. [Google Scholar] [CrossRef]
  55. Bozzetti, F. Nutritional intervention is indicated in malnourished cancer patients. Clin. Nutr. 2019, 38, 477. [Google Scholar] [CrossRef]
  56. Uster, A.; Ruehlin, M.; Mey, S.; Gisi, D.; Knols, R.; Imoberdorf, R.; Pless, M.; Ballmer, P.E. Effects of nutrition and physical exercise intervention in palliative cancer patients: A randomized controlled trial. Clin. Nutr. 2018, 37, 1202–1209. [Google Scholar] [CrossRef]
  57. Guo, Y.; Li, Z.X.; Zhang, J.Y.; Ma, J.-L.; Zhang, L.; Zhang, Y.; Zhou, T.; Liu, W.-D.; Han, Z.-X.; Li, W.-Q.; et al. Association Between Lifestyle Factors, Vitamin and Garlic Supplementation, and Gastric Cancer Outcomes: A Secondary Analysis of a Randomized Clinical Trial. JAMA Netw. Open 2020, 3, e206628. [Google Scholar] [CrossRef]
  58. Adiamah, A.; Rollins, K.E.; Kapeleris, A.; Welch, N.T.; Iftikhar, S.Y.; Allison, S.P.; Lobo, D.N. Postoperative arginine-enriched immune modulating nutrition: Long-term survival results from a randomised clinical trial in patients with oesophagogastric and pancreaticobiliary cancer. Clin. Nutr. 2021, 40, 5482–5485. [Google Scholar] [CrossRef]
  59. Xu, L.; Zhang, X.; Lu, J.; Dai, J.-X.; Lin, R.-Q.; Tian, F.-X.; Liang, B.; Guo, Y.-N.; Luo, H.-Y.; Li, N.; et al. The Effects of Dinner-to-Bed Time and Post-Dinner Walk on Gastric Cancer Across Different Age Groups: A Multicenter Case-Control Study in Southeast China. Medicine 2016, 95, e3397. [Google Scholar] [CrossRef]
  60. Song, Q.; Wang, J.; Jia, Y.; Wang, C.; Wang, N.; Tan, B.; Ma, W.; Guan, S.; Jiang, D.; Cheng, Y. Shorter dinner-to-bed time is associated with gastric cardia adenocarcinoma risk partly in a reflux-dependent manner. Ann. Surg. Oncol. 2014, 21, 2615–2619. [Google Scholar] [CrossRef] [PubMed]
  61. Li, W.Q.; Zhang, J.Y.; Ma, J.L.; Li, Z.-X.; Zhang, L.; Zhang, Y.; Guo, Y.; Zhou, T.; Li, J.-Y.; Shen, L.; et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: Follow-up of a randomized intervention trial. BMJ 2019, 366, l5016. [Google Scholar] [CrossRef] [Green Version]
  62. Ma, J.L.; Zhang, L.; Brown, L.M.; Li, J.-Y.; Shen, L.; Pan, K.-F.; Liu, W.-D.; Hu, Y.; Han, Z.-X.; Crystal-Mansour, S.; et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J. Natl. Cancer Inst. 2012, 104, 488–492. [Google Scholar] [CrossRef] [PubMed]
  63. Amini, L.; Chekini, R.; Nateghi, M.R.; Haghani, H.; Jamialahmadi, T.; Sathyapalan, T.; Sahebkar, A. The Effect of Combined Vitamin C and Vitamin E Supplementation on Oxidative Stress Markers in Women with Endometriosis: A Randomized, Triple-Blind Placebo-Controlled Clinical Trial. Pain Res. Manag. 2021, 2021, 5529741. [Google Scholar] [CrossRef] [PubMed]
  64. Rozemeijer, S.; de Grooth, H.J.; Elbers, P.; Girbes, A.R.J.; den Uil, C.A.; Dubois, E.A.; Wils, E.-J.; Rettig, T.C.D.; van Zanten, A.R.H.; Vink, R.; et al. Early high-dose vitamin C in post-cardiac arrest syndrome (VITaCCA): Study protocol for a randomized, double-blind, multi-center, placebo-controlled trial. Trials 2021, 22, 546. [Google Scholar] [CrossRef] [PubMed]
Figure 1. The flow diagram of identifying eligible studies.
Figure 1. The flow diagram of identifying eligible studies.
Jpm 13 00155 g001
Figure 2. Meta-analysis of overall survival. Forest plot of the GNRI (dichotomous variable) in relation to overall survival (A). Forest plot of GNRI (continuous variable) in relation to overall survival (B). HR, hazard ratio; CL, confidence interval; GNRI, geriatric nutrition risk index [13,14,15,16,17,18,19,20,21].
Figure 2. Meta-analysis of overall survival. Forest plot of the GNRI (dichotomous variable) in relation to overall survival (A). Forest plot of GNRI (continuous variable) in relation to overall survival (B). HR, hazard ratio; CL, confidence interval; GNRI, geriatric nutrition risk index [13,14,15,16,17,18,19,20,21].
Jpm 13 00155 g002
Figure 3. Forest plot of the GNRI in relation to cancer-specific survival (A) and postoperative complications (B). HR, hazard ratio; OR, odds ratio; CL, confidence interval; GNRI, geriatric nutrition risk index [14,16,17,19,20,21,22,23].
Figure 3. Forest plot of the GNRI in relation to cancer-specific survival (A) and postoperative complications (B). HR, hazard ratio; OR, odds ratio; CL, confidence interval; GNRI, geriatric nutrition risk index [14,16,17,19,20,21,22,23].
Jpm 13 00155 g003
Figure 4. Subgroup analysis of overall survival based on sample size (A), cut-off value (B), treatment (C), and publishing year (D). ESD, endoscopic submucosal dissection; HR, hazard ratio; CL, confidence interval [14,16,17,18,19,20,21].
Figure 4. Subgroup analysis of overall survival based on sample size (A), cut-off value (B), treatment (C), and publishing year (D). ESD, endoscopic submucosal dissection; HR, hazard ratio; CL, confidence interval [14,16,17,18,19,20,21].
Jpm 13 00155 g004
Figure 5. Subgroup analysis of postoperative complications based on sample size (A), cut-off value (B), treatment (C), and publishing year (D). ESD, endoscopic submucosal dissection; OR, odds ratio; CL, confidence interval [14,16,17,18,19,20,21].
Figure 5. Subgroup analysis of postoperative complications based on sample size (A), cut-off value (B), treatment (C), and publishing year (D). ESD, endoscopic submucosal dissection; OR, odds ratio; CL, confidence interval [14,16,17,18,19,20,21].
Jpm 13 00155 g005
Figure 6. Sensitivity analysis of overall survival (A) and postoperative complications (B). CL, confidence interval [14,16,17,19,20,21].
Figure 6. Sensitivity analysis of overall survival (A) and postoperative complications (B). CL, confidence interval [14,16,17,19,20,21].
Jpm 13 00155 g006
Table 1. Main characteristics of the studies included.
Table 1. Main characteristics of the studies included.
StudyStudy RegionStudy DesignStudy PeriodSample SizeMale/
Age (Years) TreatmentCut-OffOutcomeNOS Score
Toya et al. 2022 [15]Tohoku, JapanRJanuary 2002–December 2017740469/27186 (85–93.0) aGastric ESDContinuousOS (U)6
Matsunaga et al. 2022 [16]Multi-center, JapanRJanuary 2005–December 2015497330/16780.6 ± 4.0Curative gastrectomy97/95.8OS (M), CSS (M)8
An et al. 2022 [18]Gangdong, KoreaRJune 2006–December 2017450301/14960 (52–69) aCurative gastrectomyContinuousOS (M)7
Hisada et al. 2022 [17]Tokyo, JapanRJanuary 2009–December 2019767559/20875 (65–95) bGastric ESD92OS (M),
complications (M)
Yoshikawa et al. 2022 [13]Osaka, JapanRJanuary 2006–December 20204430/1486 (85–96) bGastric ESDContinuousOS (U)6
Tsuchiya et al. 2022 [14]Yokohama, JapanRApril 2002–December 2018186128/5882 (80–93) bCurative gastrectomy98OS (U),
complications (M)
Hirahara et al. 2021 [20]Shimane, JapanRJanuary 2010–December 2017303209/9465–91 cCurative gastrectomy85.7OS (M),
complications (M)
Sugawara et al. 2021 [19]Tokyo, JapanRApril 2001–December 20141166816/35025–91 cCurative gastrectomy98OS (M), CSS (M),
complications (U)
Furuke et al. 2021 [21]Kyoto, JapanR2008–2016795534/26168 (29–89) bCurative gastrectomy92OS (M),
complications (U)
Hirahara et al. 2020 [22]Shimane, JapanRJanuary 2010–December 2017297205/9265–91 cCurative gastrectomy90.9CSS (M)7
Kushiyama et al. 2018 [23]Osaka, JapanRJanuary 2006–December 2015348230/11879.6 ± 3.8Curative gastrectomy92Complications (M)7
R: retrospective study; ESD, endoscopic submucosal dissection; OS, overall survival; CSS, cancer-specific survival; M, multivariate analysis, U, univariate analysis, a medians with interquartile ranges; b medians with ranges; c age with ranges.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, Q.; Zhang, L.; Jin, Q.; He, Y.; Wu, M.; Peng, H.; Li, Y. The Prognostic Value of the GNRI in Patients with Stomach Cancer Undergoing Surgery. J. Pers. Med. 2023, 13, 155.

AMA Style

Zhang Q, Zhang L, Jin Q, He Y, Wu M, Peng H, Li Y. The Prognostic Value of the GNRI in Patients with Stomach Cancer Undergoing Surgery. Journal of Personalized Medicine. 2023; 13(1):155.

Chicago/Turabian Style

Zhang, Qianqian, Lilong Zhang, Qi Jin, Yongheng He, Mingsheng Wu, Hongxing Peng, and Yijin Li. 2023. "The Prognostic Value of the GNRI in Patients with Stomach Cancer Undergoing Surgery" Journal of Personalized Medicine 13, no. 1: 155.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop