Preoperative hypoalbuminemia as a prognostic factor in patients with gastric cancer undergoing radical gastrectomy: Construction of a nomogram

Abstract

Objective

To investigate the association of preoperative hypoalbuminemia (serum albumin <35 g/L) with clinicopathological characteristics and survival outcomes in patients with gastric cancer undergoing radical gastrectomy and to construct a nomogram based on prognostically relevant clinicopathological variables.

Methods

This retrospective cohort study included patients with gastric cancer who underwent radical gastrectomy. Clinicopathological variables and survival outcomes were compared between groups. Univariate and multivariable analyses were performed to identify variables associated with prognosis, and a nomogram was constructed based on significant predictors.

Results

Preoperative hypoalbuminemia was significantly associated with adverse clinicopathological characteristics, including anemia, lymphocyte depletion, advanced American Joint Committee on Cancer stage, vascular invasion, and perineural invasion. Kaplan–Meier analysis showed that hypoalbuminemia was associated with poorer overall survival. In multivariable Cox regression analysis, lymph node metastasis remained independently associated with overall survival, whereas preoperative hypoalbuminemia was not an independent prognostic factor.

Conclusions

Preoperative hypoalbuminemia may reflect unfavorable nutritional and inflammatory status and was associated with adverse clinicopathological characteristics and poorer survival in univariate analysis. However, it was not independently associated with overall survival after multivariable adjustment. Lymph node metastasis remained an independent prognostic factor.

Keywords

Gastric cancer hypoalbuminemia serum albumin prognosis nomogram overall survival

Introduction

Gastric cancer remains a substantial public health challenge because of its aggressive nature and high heterogeneity. According to the 2020 global cancer statistics, gastric cancer ranks fifth in incidence and fourth in mortality worldwide.¹ The disease burden is particularly heavy in East Asia. In China, it is the second most common cancer in males and the fifth most common in females in terms of incidence, and it ranks third in cancer-related mortality in both sexes.¹ Given this high prevalence, identifying reliable prognostic factors to guide individualized treatment is of paramount importance.

Nutritional depletion is a frequent complication in patients with gastric malignancy, often resulting from mechanical obstruction, metabolic derangements, and systemic inflammation. Evidence suggests that preoperative nutritional status significantly influences long-term survival in patients with gastric cancer.² Among various nutritional parameters, serum albumin is a cost-effective and readily available biomarker that reflects both visceral protein reserve and the systemic inflammatory response to the tumor. Serum albumin levels below 35 g/L, indicative of hypoalbuminemia, are associated with poor prognosis in patients with tumors.^2,3 However, in current clinical practice, the prognostic value of hypoalbuminemia is often underestimated compared with anatomical tumor characteristics.

Currently, the American Joint Committee on Cancer (AJCC) tumor–node–metastasis staging system is the gold standard for prognostication.⁴ However, patients with the same tumor–node–metastasis stage often exhibit distinct survival outcomes, suggesting that anatomical staging alone may be insufficient. Despite advances in surgical techniques and perioperative management, tumor markers and emerging approaches such as liquid biopsy have been explored to improve prognostic stratification in gastric cancer.^5,6 Therefore, incorporating host-related factors, such as nutritional status, into prognostic models may enhance predictive accuracy.

Mathematical modeling tools have emerged as powerful supplements to traditional staging systems. Nomograms integrate multiple prognostic variables to provide individualized risk prediction and have been increasingly used in gastric cancer to predict recurrence, metastasis, and overall survival (OS).^7,8 By transforming complex regression equations into visual graphs, nomograms allow clinicians to calculate a numerical probability of survival for a specific patient. This study aimed to clarify the clinicopathological associations of preoperative hypoalbuminemia and to develop a clinically applicable nomogram for individualized survival prediction. Lymph node metastasis is one of the most established prognostic determinants in gastric cancer and reflects tumor dissemination, recurrence risk, and disease burden. Therefore, prognostic assessment after radical gastrectomy should consider both tumor-related factors, particularly lymph node status, and host-related factors, such as nutritional and inflammatory status.⁸

Methods

Ethics statement

This study was conducted in accordance with the Declaration of Helsinki of 1975, as revised in 2024. The study protocol was reviewed and approved by the Research Ethics Committee of Chifeng Municipal Hospital, Chifeng, Inner Mongolia, China (Approval Number: CK20231001; Approved Date 25 October 2023). Given the retrospective nature of the study, the requirement for written informed consent was waived by the ethics committee. All patient information was anonymized and deidentified prior to analysis to protect patient privacy.

Study design and participants

This retrospective cohort study included 200 consecutive patients with pathologically confirmed gastric cancer who underwent radical gastrectomy at Chifeng Municipal Hospital between October 2018 and October 2023. The follow-up cutoff date was October 2025. Preoperative hypoalbuminemia was defined as a serum albumin level <35 g/L, measured within 1 week before surgery. Patients were categorized into the hypoalbuminemia group and non-hypoalbuminemia group based on the predefined serum albumin cutoff value. Tumor staging was determined according to the eighth edition of the AJCC staging system. Patients who had received neoadjuvant chemotherapy or radiotherapy were excluded.

Inclusion criteria were as follows: (a) pathologically confirmed gastric cancer; (b) underwent radical gastrectomy with curative intent; (c) available preoperative serum albumin measurement within 1 week before surgery; (d) complete clinicopathological and follow-up data, including preoperative laboratory measurements; and (e) no other concurrent malignant tumors.

Exclusion criteria were as follows: (a) other systemic tumors, severe organ dysfunction, severe acute infections, or incomplete clinicopathological, laboratory, or follow-up data; (b) loss to follow-up or unavailable follow-up data; and (c) did not undergo radical gastrectomy.

The reporting of this study conforms to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines.⁹

Statistical analysis

Statistical analyses were performed using R software (version 3.6.0; R Foundation for Statistical Computing; Vienna, Austria). Continuous variables were presented as mean ± SD or median (interquartile range), as appropriate, and categorical variables are expressed as frequencies and percentages. Categorical variables were compared using the chi-squared test or Fisher’s exact test, as appropriate.

OS was defined as the interval from the date of diagnosis to death from any cause or last follow-up. Survival curves were generated using the Kaplan–Meier method and compared using the log-rank test.

Univariate Cox proportional hazards regression analysis was first performed to identify variables associated with OS. Variables were selected for multivariable Cox proportional hazards regression analysis based on clinical relevance and prior evidence. Preoperative hypoalbuminemia, age, sex, tumor size, lymph node metastasis, and distant metastasis were included in the multivariable model to evaluate independent prognostic factors for OS. Hazard ratios (HRs) and 95% confidence intervals (CIs) were calculated. All statistical tests were two-sided, and a P-value <0.05 was considered statistically significant.

Missing data were handled using complete-case analysis. A prognostic nomogram was constructed based on the results of the multivariate Cox model. In addition, variables considered clinically relevant according to prior evidence and univariate analysis were included in the model, even if they were not statistically significant in multivariate analysis. The nomogram was developed using the ‘rms’ package in R. Model discrimination was assessed using the concordance index (C-index). Calibration was evaluated using bootstrap resampling (1000 repetitions). The predictive performance of the model was further assessed using receiver operating characteristic (ROC) curve analysis, and the area under the curve (AUC) was calculated.

Results

Relationship between hypoalbuminemia and clinicopathological features

All 200 patients with gastric cancer underwent clinicopathological evaluation and were confirmed to have gastric cancer. Among them, 51 were female and 149 were male, with a mean age of 61.9 ± 9.42 years and a median age of 63 years. OS was defined as the time from diagnosis to death or last follow-up. Patients were followed until the follow-up cutoff date of October 2025.

Hypoalbuminemia was significantly associated with ethnicity (P = 0.0421), anemia (P = 0.0002), lymphocyte depletion (P = 0.0044), AJCC stage (P = 0.0285), vascular invasion (P = 0.0011), and perineural invasion (P = 0.0094) (Table 1).

Table 1.

Association between preoperative hypoalbuminemia and clinicopathological characteristics in patients with gastric cancer undergoing radical gastrectomy.

Clinicopathological feature	Category	Total	Hypoalbuminemia				X2	P
Clinicopathological feature	Category	Total	Yes		No		X2	P
		200
Sex	Female	51	13	25.49%	38	74.51%	3.28	0.0700
	Male	149	59	39.60%	90	60.40%
Age	<40	4	2	50.00%	2	50.00%	4.83	0.4369
	40–49	22	8	36.36%	14	63.64%
	50–59	62	27	43.55%	35	56.45%
	60–69	90	31	34.44%	59	65.56%
	70–79	37	20	54.05%	17	45.95%
	≥80	4	2	50.00%	2	50.00%
Ethnicity	Mongolian	26	14	53.85%	12	46.15%	4.13	0.0421	*
	Han	174	58	33.33%	116	66.67%
Anemia	Yes	64	35	54.69%	29	45.31%	14.27	0.0002	***
	No	136	37	27.21%	99	72.79%
Lymphocyte depletion	Yes	16	11	68.75%	5	31.25%	8.10	0.0044	**
	No	184	61	33.15%	123	66.85%
Neutrophil elevation	Yes	22	12	54.55%	10	45.45%	3.69	0.0547
	No	178	60	33.71%	118	66.29%
AJCC	AJCC Stage I	62	15	24.19%	47	75.81%	9.06	0.0285	*
	AJCC Stage II	61	21	34.43%	40	65.57%
	AJCC Stage III	60	26	43.33%	34	56.67%
	AJCC Stage IV	17	10	58.82%	7	41.18%
Vascular invasion	Yes	114	52	45.61%	62	54.39%	10.64	0.0011	**
	No	86	20	23.26%	66	76.74%
Perineural invasion	Yes	95	43	45.26%	52	54.74%	6.74	0.0094	**
	No	105	29	27.62%	76	72.38%
Elevated aspartate aminotransferase	Yes	13	7	53.85%	6	46.15%	1.92	0.1656
Elevated aspartate aminotransferase	No	187	65	34.76%	122	65.24%
Elevated alanine aminotransferase	Yes	8	4	50.00%	4	50.00%	0.71	0.3998
Elevated alanine aminotransferase	No	192	68	35.42%	124	64.58%
AFP elevated	Yes	11	6	54.55%	5	45.45%	1.74	0.1874
	No	189	66	34.92%	123	65.08%
CEA elevated	Yes	48	20	41.67%	28	58.33%	0.88	0.3481
	No	152	52	34.21%	100	65.79%
CA199 elevated	Yes	49	15	30.61%	34	69.39%	0.82	0.3659
	No	151	57	37.75%	94	62.25%
Maximum diameter of tumor	<2 cm	49	14	28.57%	35	71.43%	2.44	0.2959
Maximum diameter of tumor	2–5 cm	98	35	35.71%	63	64.29%
	>5 cm	53	23	43.40%	30	56.60%
Lymph node metastasis	Yes	118	49	41.53%	69	58.47%	3.81	0.0508
	No	82	23	28.05%	59	71.95%
Distant metastasis	Yes	17	10	58.82%	7	41.18%	3.19	0.0742
	No	183	62	33.88%	121	66.12%
Status	Alive	112	39	34.82%	73	65.18%	0.15	0.6953
	Dead	88	33	37.50%	55	62.50%

AJCC: American Joint Committee on Cancer; AFP: alpha-fetoprotein; CEA: carcinoembryonic antigen; CA19-9: carbohydrate antigen 19-9.

Univariate Cox regression analysis

Univariate Cox proportional hazards regression analysis demonstrated that lymph node metastasis (HR = 2.45, 95% CI: 1.43–4.18, P = 0.001), distant metastasis (HR = 2.69, 95% CI: 1.26–5.72, P = 0.010), vascular invasion (HR = 1.82, 95% CI: 1.08–3.09, P = 0.025), perineural invasion (HR = 2.20, 95% CI: 1.31–3.70, P = 0.003), elevated carcinoembryonic antigen (CEA) (HR = 1.85, 95% CI: 1.11–3.09, P = 0.018), and elevated carbohydrate antigen 19-9 (CA19-9) (HR = 1.87, 95% CI: 1.10–3.17, P = 0.020) were significantly associated with OS (Table 2).

Table 2.

Univariate Cox regression analysis of overall survival in gastric cancer patients.

Variable	HR	CI_Lower	CI_Upper	P_Value
Age	1.002913	0.976246	1.030308	0.832469
Sex	1.193007	0.703075	2.024346	0.513021
Tumor size	1.004748	0.933431	1.081513	0.899664
Lymph node metastasis	2.447542	1.433534	4.178805	0.00104
Distant metastasis	2.685105	1.260583	5.719408	0.010461
Vascular invasion	1.824921	1.078035	3.089264	0.025108
Perineural invasion	2.198888	1.3068	3.699962	0.002999
High AFP	1.637752	0.705736	3.800617	0.250739
High CEA	1.851748	1.111189	3.085857	0.01805
High CA199	1.868827	1.101193	3.171573	0.020495

HR: hazard ratio; CI: confidence interval; AFP: alpha-fetoprotein; CEA: carcinoembryonic antigen; CA19-9: carbohydrate antigen 19-9.

Multivariate Cox regression analysis

Clinically relevant variables, including preoperative hypoalbuminemia, age, sex, tumor size, lymph node metastasis, and distant metastasis, were included in the multivariable Cox proportional hazards regression model. In this model, lymph node metastasis remained independently associated with OS (HR = 2.48, 95% CI: 1.37–4.46, P = 0.003), whereas preoperative hypoalbuminemia was not independently associated with OS (HR = 1.13, 95% CI: 0.63–2.03, P = 0.692) (Table 3).

Table 3.

Multivariate Cox regression analysis of overall survival in patients with gastric cancer.

Variable	HR	95% CI	P-value
Preoperative hypoalbuminemia	1.13	0.63–2.03	0.692
Age	1.01	0.98–1.04	0.483
Sex	1.16	0.67–1.99	0.598
Tumor size	0.99	0.91–1.07	0.729
Lymph node metastasis	2.48	1.37–4.46	0.003
Distant metastasis	1.89	0.86–4.17	0.114

HR: hazard ratio; CI: confidence interval.

Nomogram construction and validation

A prognostic nomogram was constructed using clinically relevant variables and Cox regression results, including preoperative hypoalbuminemia and established tumor-related factors (Figure 1). Calibration curves indicated good agreement between predicted and observed outcomes (Figure 2). ROC analysis showed an AUC of 0.879 (Figure 3). Kaplan–Meier survival analysis showed that preoperative hypoalbuminemia, maximum tumor diameter, lymph node metastasis, and perineural invasion were significantly associated with OS (Figure 4).

Figure 1.

Nomogram for predicting 3-year and 5-year overall survival in patients with gastric cancer.

Figure 2.

Calibration curves for the nomogram. The x-axis represents the predicted survival probability, and the y-axis represents the actual observed survival. The diagonal dashed line represents the ideal prediction. The curves indicate good consistency for (a) 3-year and (b) 5-year OS. OS: overall survival.

Figure 3.

Receiver operating characteristic (ROC) curve of the nomogram model. The area under the curve (AUC) is 0.879, indicating satisfactory discriminative ability.

Figure 4.

Kaplan–Meier survival curves for overall survival according to preoperative hypoalbuminemia status, maximum tumor diameter, lymph node metastasis, and perineural invasion. (a) Patients with preoperative hypoalbuminemia had significantly poorer overall survival than those without hypoalbuminemia (P = 0.01381). (b) Patients with lymph node metastasis had poorer overall survival than those without lymph node metastasis. (c) Overall survival differed significantly according to maximum tumor diameter (<2 cm, 2–5 cm, and >5 cm; P = 0.0047). (d) Patients with perineural invasion had poorer overall survival than those without perineural invasion (P = 0.0052).

Forest plots were generated to visually summarize the HRs and 95% CIs from the univariate and multivariable Cox regression analyses (Figure 5). In the univariate analysis, lymph node metastasis, distant metastasis, vascular invasion, perineural invasion, elevated CEA, and elevated CA19-9 were associated with poorer OS. In the multivariable analysis, lymph node metastasis remained independently associated with OS, whereas preoperative hypoalbuminemia was not an independent prognostic factor.

Figure 5.

Forest plots showing hazard ratios (HRs) with 95% confidence intervals (CIs) derived from Cox proportional hazards regression analyses. (a) Univariate analysis showing significant prognostic factors. (b) Multivariate analysis including preoperative hypoalbuminemia and clinically relevant variables. Lymph node metastasis remained independently associated with overall survival, whereas preoperative hypoalbuminemia was not an independent prognostic factor. Squares represent HRs, horizontal lines represent 95% CIs, and the vertical dashed line indicates an HR of 1.0.

Discussion

This study integrated clinicopathological parameters and laboratory indicators to construct a prognostic nomogram for patients with gastric cancer who underwent radical gastrectomy. Nomogram-based models have been increasingly applied in gastric cancer to improve individualized prognostic assessment beyond conventional staging systems.^7,8 Compared with the traditional tumor–node–metastasis staging system, which primarily reflects the anatomical extent of disease, our nomogram also incorporates host-related clinical variables, thereby providing a more comprehensive prognostic evaluation.⁴ The model demonstrated moderate discrimination (C-index = 0.70) and a satisfactory area under the ROC curve, suggesting potential utility for individualized survival prediction.

In recent gastric cancer research, prognostic models that integrate host-related factors, including nutritional and systemic inflammatory indicators, have shown additional predictive value.¹⁰ Preoperative serum albumin is a readily available and cost-effective biomarker reflecting nutritional reserve and systemic inflammatory status.² The association between hypoalbuminemia and adverse oncologic outcomes has been reported in gastric cancer cohorts.³ The mechanism linking hypoalbuminemia to poor survival is likely multifactorial and may involve tumor-related systemic inflammation and impaired immune function.³

Composite immune–nutritional indicators incorporating albumin, such as the Prognostic Immune and Nutritional Index, have also demonstrated prognostic significance in gastric cancer cohorts undergoing curative surgery.¹¹ In addition, systemic inflammatory and coagulation markers, including preoperative plasma fibrinogen, have been associated with long-term survival, further supporting the influence of host systemic condition on tumor progression.¹²

Consistent with previous reports, abnormal tumor markers (CEA, CA19-9, and alpha-fetoprotein) and adverse pathological factors such as perineural invasion were associated with worse prognosis.¹³ These findings emphasize that gastric cancer prognosis reflects the interaction between tumor aggressiveness and host biological status.^2,5

From a clinical perspective, integrating tumor burden indicators with modifiable host factors such as hypoalbuminemia may improve risk stratification and help guide perioperative management.⁷ Our findings support considering hypoalbuminemia as a component of multivariable prognostic assessment rather than relying solely on tumor characteristics.²

Perioperative nutritional assessment and intervention have been recommended in major gastrointestinal cancer surgery, particularly for patients at high nutritional risk.¹⁴ Structured nutritional support strategies, including oral nutritional supplementation and enteral nutrition, may improve postoperative recovery and treatment tolerance.¹⁴ Recent gastric cancer treatment guidelines also emphasize the importance of comprehensive perioperative management, including nutritional evaluation.¹⁵

This study has limitations, including its single-center retrospective design and moderate sample size, which may introduce selection bias. External validation in independent multicenter cohorts is required to confirm the generalizability of this model. Future prospective research should determine whether targeted nutritional optimization in hypoproteinemic patients can improve long-term survival outcomes.¹⁴

Unlike many fixed pathological characteristics, preoperative hypoalbuminemia represents a potentially modifiable risk factor. Timely nutritional assessment and targeted perioperative nutritional intervention may improve postoperative recovery and reduce complication rates in patients undergoing major gastrointestinal cancer surgery.^16,17 Early identification of high-risk individuals using objective biomarkers such as serum albumin may therefore enable clinicians to initiate structured nutritional support before surgery, thereby optimizing physiological reserve and potentially improving tolerance to adjuvant treatment.¹⁶

Current international guidelines emphasize routine screening for malnutrition in patients with cancer and recommend individualized perioperative nutritional strategies for those at high nutritional risk.¹⁸ In gastric cancer specifically, multimodal perioperative management, including nutritional optimization, has been increasingly recognized as an integral component of enhanced recovery pathways and comprehensive oncologic care.¹⁹ Risk-adapted strategies based on integrated prognostic models may facilitate closer surveillance in high-risk patients and more informed clinical decision making in gastric cancer management.²⁰ Preoperative hypoalbuminemia has also been associated with poorer outcomes in patients with gastric cancer undergoing gastrectomy, supporting its clinical relevance as a host-related risk marker.²¹

Serum albumin is not only a marker of nutritional reserve but also a well-recognized negative acute-phase reactant. Therefore, preoperative hypoalbuminemia in patients with gastric cancer may reflect both impaired nutritional status and tumor-related systemic inflammation. Preoperative albumin has been reported to be associated with prognosis in gastric cancer, and inflammation- or nutrition-based composite indices such as the Prognostic Immune and Nutritional Index may provide additional prognostic information.^14,15

Nutritional status in gastric cancer is inherently multidimensional and cannot be fully captured by a single biochemical parameter. In addition to serum albumin, body composition, skeletal muscle depletion, and cachexia-related indicators may provide complementary prognostic information. A recent study showed that a low preoperative Cachexia Index was associated with severe postoperative morbidity in patients undergoing gastrectomy for gastric cancer.²²

Another issue that warrants consideration is that the study period overlapped with the coronavirus disease 2019 (COVID-19) pandemic. Pandemic-related delays in diagnosis, changes in healthcare access, and deterioration in nutritional status may have influenced disease stage at presentation and perioperative outcomes. A recent study specifically reported that the COVID-19 pandemic affected gastric cancer stage and nutritional status, which should be taken into account when interpreting our findings.^2,3 These findings support the importance of comprehensive perioperative assessment, including nutritional status.

In addition, inflammatory markers such as C-reactive protein, the modified Glasgow Prognostic Score, the neutrophil-to-lymphocyte ratio, the platelet-to-lymphocyte ratio, and the systemic immune-inflammation index were not routinely available in this retrospective cohort. Therefore, we were unable to evaluate whether these inflammatory indices modified the association between preoperative hypoalbuminemia and survival outcomes. Future studies should integrate albumin with systemic inflammatory markers to provide a more comprehensive assessment of the nutritional and inflammatory status of patients with gastric cancer.

Conclusion

Preoperative hypoalbuminemia (serum albumin <35 g/L) was significantly associated with adverse clinicopathological characteristics in patients with gastric cancer undergoing radical gastrectomy and showed an association with poorer outcomes. However, it was not identified as an independent prognostic factor in multivariable analysis. Hypoalbuminemia should be interpreted as a marker of unfavorable preoperative condition rather than a standalone determinant of prognosis. Combined assessment with established prognostic variables, particularly lymph node status, may provide more meaningful risk stratification.

Footnotes

Acknowledgments

None.

Author contributions

Zhen-Wu Qu and Yang Zhang contributed to data collection and statistical analysis. Ming-Yue Guo contributed to study conception and design and drafted the manuscript. All authors critically revised the manuscript, approved the final version, and agree to be accountable for all aspects of the work.

Animal studies

Not applicable.

Data availability statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Declaration of conflicting interests

The authors declare that there is no conflict of interest.

Ethics approval

The study protocol was reviewed and approved by the Research Ethics Committee of Chifeng Municipal Hospital, Chifeng, Inner Mongolia, China (Approval No. CK20231001; approved on 25 October 2023).

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Informed consent

Given the retrospective nature of the study, the requirement for written informed consent was waived by the Research Ethics Committee of Chifeng Municipal Hospital.

Trial registration

Not applicable (retrospective observational study).

ORCID iD

Ming-Yue Guo

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