Zhao XN, Lu J, He HY, Ge SJ. Clinical significance of preoperative nutritional status in elderly gastric cancer patients undergoing radical gastrectomy: A single-center retrospective study. World J Gastrointest Surg 2024; 16(7): 2211-2220 [PMID: 39087115 DOI: 10.4240/wjgs.v16.i7.2211]
Corresponding Author of This Article
Hong-Yong He, MD, PhD, Deputy Chief Physician, Department of General Surgery/Emergency Surgery, Zhongshan Hospital, Fudan University, No. 180 Fenglin Road, Shanghai 200032, China. he.hongyong@zs-hospital.sh.cn
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
World J Gastrointest Surg. Jul 27, 2024; 16(7): 2211-2220 Published online Jul 27, 2024. doi: 10.4240/wjgs.v16.i7.2211
Clinical significance of preoperative nutritional status in elderly gastric cancer patients undergoing radical gastrectomy: A single-center retrospective study
Co-corresponding authors: Hong-Yong He and Sheng-Jin Ge.
Author contributions: Zhao XN and Lu J collected and analyzed the data, wrote the manuscript; He HY and Ge SJ designed the study and edited the manuscript; Zhao XN and Lu J contributed equally to this work. All authors have read and approved the final manuscript. There are three main reasons for designating He HY and Ge SJ as co-corresponding authors. First, the research was a collaborative effort, and this designation accurately reflects the distribution of responsibilities and the significant time and effort each author devoted to completing the study and the resultant paper. Second, the research team comprised authors with diverse expertise and skills from different fields. The designation of co-corresponding authors best represents this diversity, promoting a comprehensive and in-depth examination of the research topic. Third, He HY and Ge SJ collaborated to design and refine the study protocol and contributed equally to reviewing and editing the manuscript. Recognizing these researchers as co-corresponding authors acknowledges and respects their equal contributions and highlights the spirit of teamwork and collaboration in this study. In summary, designating He HY and Ge SJ as co-corresponding authors accurately reflects our team's collaborative spirit, equal contributions, and diverse expertise, thereby enhancing the overall quality and reliability of the manuscript.
Supported byNational Natural Science Foundation of China, No. 82373417; Natural Science Foundation of Shanghai, No. 23ZR1409900; Clinical Research Plan of SHDC, No. SHDC2020CR3048B; and Clinical Research Fund of Zhongshan Hospital, Fudan University, No. ZSLCYJ202343.
Institutional review board statement: This study was approved by the Clinical Research Ethics Committee of Zhongshan Hospital of Fudan University (B2021-392).
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: The authors claim no conflict of interests.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Hong-Yong He, MD, PhD, Deputy Chief Physician, Department of General Surgery/Emergency Surgery, Zhongshan Hospital, Fudan University, No. 180 Fenglin Road, Shanghai 200032, China. he.hongyong@zs-hospital.sh.cn
Received: April 20, 2024 Revised: May 23, 2024 Accepted: June 12, 2024 Published online: July 27, 2024 Processing time: 92 Days and 16.1 Hours
Abstract
BACKGROUND
The population of elderly patients with gastric cancer is increasing, which is a major public health issue in China. Malnutrition is one of the greatest risk factors for adverse clinical outcomes in elderly patients with gastric cancer.
AIM
To investigate the preoperative nutritional status and its association with delayed discharge of elderly gastric cancer patients following radical gastrectomy.
METHODS
A total of 783 patients aged 65 years and older harboring gastric adenocarcinoma and following radical gastrectomy were retrospectively analyzed from the prospectively collected database of Zhongshan Hospital of Fudan University between January 2018 and May 2020.
RESULTS
The overall rate of malnutrition was 31.8%. The incidence of postoperative complications was significantly higher in the malnourished group compared to the well-nourished group (P < 0.001). Nutritional characteristics in the malnourished group, including body mass index, prognostic nutritional index (PNI), albumin, prealbumin, and hemoglobin, were all significantly lower than those in the well-nourished group. The percentage of patients who received postoperative total nutrient admixture was lower in the malnourished group compared to the well-nourished group (22.1% vs 33.5%, P = 0.001). Age ≥ 70 years (HR = 1.216, 95%CI: 1.048-1.411), PNI < 44.5 (HR = 1.792, 95%CI: 1.058-3.032), operation time ≥ 160 minutes (HR = 1.431, 95%CI: 1.237-1.656), and postoperative complications grade III or higher (HR = 2.191, 95%CI: 1.604-2.991) were all recognized as independent risk factors associated with delayed discharge.
CONCLUSION
Malnutrition is relatively common in elderly patients undergoing gastrectomy. Low PNI is an independent risk factor associated with delay discharge. More strategies are needed to improve the clinical outcome of these patients.
Core Tip: Malnutrition is a significant risk factor for adverse clinical outcomes in elderly gastric cancer patients. In our investigation of the nutritional status and perioperative nutritional support of elderly surgical patients with gastric cancer, we discovered that the overall frequency of malnutrition was 31.8%. The incidence of postoperative complications in the malnourished group was significantly higher than that in the well-nourished group. Nutritional characteristics of patients in the malnourished group were recognized as independent risk factors associated with delayed discharge.
Citation: Zhao XN, Lu J, He HY, Ge SJ. Clinical significance of preoperative nutritional status in elderly gastric cancer patients undergoing radical gastrectomy: A single-center retrospective study. World J Gastrointest Surg 2024; 16(7): 2211-2220
Gastric cancer remains the fifth most common malignant cancer and the fourth leading cause of cancer-related mortality[1,2]. Due to economic development and increased life expectancy, the population of elderly patients with gastric cancer is increasing, which is a major public health issue in China[3]. Currently, radical gastrectomy is recognized as the standard treatment for managing resectable gastric cancer[4]. Elderly patients with gastric cancer encounter numerous treatment challenges, including immunosuppression, comorbidities, organ dysfunction, and delayed recovery[5]. Advanced age is linked to a higher incidence of postoperative complications shortly after surgery and lower 5-year overall survival rate as long-term outcomes[6,7].
In China, the prevalence of malnutrition among hospitalized patients ranges from approximately 12.6% to 46.19%[8]. Malnutrition is a significant risk factor for adverse clinical outcomes in elderly gastric cancer patients[9]. At the time of diagnosis, nutritional status is independently linked to postoperative complications, disease-free survival, and overall survival[10,11]. This condition may arise from mechanical partial or complete obstruction of the digestive tract and cancer anorexia-cachexia syndrome, resulting in insufficient intake of energy or protein and disorders of absorption. Effective nutritional management involves three key steps: Screening, assessment, and intervention.
Most previous studies have concentrated on hospitalized internal medical patients[12], with only a few addressing surgical patients regardless of age[13]. Thus, in this retrospective study, we aim to investigate the nutritional status and perioperative nutritional support of elderly surgical gastric cancer patients, providing a basis for implementing effective nutritional interventions.
MATERIALS AND METHODS
Study design and patients
We prospectively recruited consecutive patients with gastric cancer, collected their clinicopathological data, and retrospectively analyzed their clinicopathological features. The records of elderly gastric cancer patients aged 65 years and older who underwent radical surgical resection of gastric adenocarcinoma between January 2018 and May 2010 were retrospectively identified, based on the database of patients with gastric cancer in the Department of General Surgery of Zhongshan Hospital of Fudan University (Shanghai, China). Patients with other malignancies, emergency surgery, previous gastrointestinal surgery, and incomplete clinical or pathological records were excluded. As a result, a total of 783 patients were included in the final analysis (Figure 1). A retrospective review of prospectively collected data was performed, and the clinicopathological features, including demographic information, medical history, laboratory tests, postoperative complications, length of stay (LOS), and cost of hospitalization, were collected and analyzed. The variables which reflected the nutritional status including albumin, prealbumin, hemoglobin, and total lymphocyte count were recorded from laboratory tests performed within one week prior to surgery. The cut-off value for albumin, prealbumin, and hemoglobin were defined using the lower limit of normal reference value of Zhongshan Hospital (albumin 30 g/L, prealbumin 180 mg/L, and hemoglobin 90 g/L). Clavien-Dindo complication grading criteria was used to grade surgical complications[14]. The research was conducted in accordance with the Declaration of Helsinki, and ethical approval (B2021-392) was granted by the Clinical Research Ethics Committee of Zhongshan Hospital of Fudan University (Shanghai, China). Signed informed consent was obtained from all patients for the acquisition and use of anonymized clinical data.
Figure 1 Flowchart of the inclusion process of patients.
Definition and assessment of malnutrition
Malnutrition is a serious condition that occurs when the diet does not contain the right amount of nutrients. It means "poor nutrition" and can refer to undernutrition and overnutrition[15]. In this study, we focus on undernutrition in elderly gastric cancer patients. According to the European Society for Clinical Nutrition and Metabolism (ESPEN) diagnostic criteria, malnutrition is defined as unintentional weight loss of more than 5% over the last 3 months and a body mass index (BMI) less than 20 kg/m2 for patients under 70 years old, or less than 22 kg/m2 for those age 70 and older or more than 10% (regardless of time frame)[16]. Nutritional assessment is conducted using the prognostic nutritional index (PNI), a readily accessible tool widely used to evaluate the nutritional status of gastric cancer patients[17]. The PNI is calculated based on the following equation: [(0.005 × total lymphocyte count (/mm3)) + (10 × serum albumin (g/dL))]. The cut-off value for PNI was defined using the median value. The composition and duration of nutritional management were recorded and analyzed.
Statistical analysis
Statistical analysis was performed with SPSS Software (version 25.0; SPSS Inc., Chicago, IL, United States). Normal distribution measurement data were expressed as mean ± SD, and t test was used to compare the differences between the groups. The measurement data of skewed distribution were expressed as median (interquartile range), and the categorical variables were expressed as counts and percentages and compared using the χ2 test or Fisher’s exact test. Univariate and multivariate analyses were conducted using the Cox proportional hazards regression model. Differences were considered statistically significant at values of P < 0.05.
RESULTS
General characteristics
Table 1 summarizes the clinical characteristics of elderly gastric cancer patients enrolled in this study, and their relationships with nutritional status. Most patients were male (74.6%) and the median age was 70 years at diagnosis, ranging from 65 to 86 years. 9.7% (76/783) of the patients suffered from 3 or more comorbidities, such as coronary heart disease, hypertension, chronic obstructive pulmonary disease, etc. Of these patients, 132 (16.9%) received preoperative consultation due to comorbidities. The overall frequency of malnutrition in the patients was 31.8% (249/783). The patients in the malnourished group were older than those in the well-nourished group (P < 0.001), and the incidence of postoperative complications in the malnourished group was significantly higher compared to that in the well-nourished group (grade I-II: 10.8% vs 6.9%; grade III and higher: 11.7% vs 4.0%; P < 0.001). While, the gender, comorbidity, anesthesia type, surgery type, operation time, preoperative consultation, neoadjuvant chemotherapy, TNM stage, cost of hospitalization, and unplanned readmission rate within 30 days were not statistically different between the two groups.
Table 1 Clinical characteristics of malnourished and well-nourished elderly patients.
Factor
Malnourished
Well-nourished
P value
Total
All patients
249
100
534
100
783
100
Age (years)
< 0.001
Median (IQR)
72 (69, 76)
69 (67, 73)
70 (67, 74)
Gender
0.762
Female
65
26.1
134
25.1
199
25.4
Male
184
73.9
400
74.9
584
74.6
Comorbidity
0.321
0-2
221
88.8
486
91.0
707
90.3
≥ 3
28
11.2
48
9.0
76
9.7
Type of anesthesia
0.073
GA
35
14.1
52
9.7
87
11.1
TEA
214
85.9
482
90.3
696
88.9
Type of surgery
0.721
Total gastrectomy
112
45.0
247
46.3
359
45.8
Distal gastrectomy
130
52.2
267
50.0
397
50.7
Proximal gastrectomy
7
2.8
20
3.7
27
3.5
Operation time (min)
0.082
Median (IQR)
160 (126, 189)
160 (129, 191)
160 (123, 189)
Preoperative consultation
0.303
No
202
81.1
449
84.1
651
83.1
Yes
47
18.9
85
15.9
132
16.9
Neoadjuvant chemotherapy
0.647
No
240
96.4
518
97.0
758
96.8
Yes
9
3.6
16
3.0
25
3.2
TNM stage
0.059
I
32
12.9
87
16.3
126
16.1
II
53
21.3
133
24.9
150
19.2
III
164
65.8
314
58.8
507
64.7
Clavien-Dindo classification
< 0.001
None
193
77.5
476
89.1
669
85.4
I + II
27
10.8
37
6.9
64
8.2
III or higher
29
11.7
21
4.0
50
6.4
Cost of hospitalization (× 103 RMB)
0.293
Median (IQR)
55.3 (47.4, 66.6)
54.7 (47.8, 63.2)
54.8 (47.7, 64.7)
Re-admission within 30 days
11
4.4
4
0.7
0.790
15
1.9
Perioperative nutritional characteristics
As shown in Table 2, nutritional characteristics of patients in the malnourished group, including BMI, PNI, albumin, prealbumin, and hemoglobin, were all significantly lower than those in the well-nourished group. However, the total lymphocyte count did not differ significantly between the two groups. To solve the problem of malnutrition in the 783 elderly gastric cancer patients enrolled in this study, 424 (54.1%) received preoperative nutritional support, and the nutritional support primarily consisted of carbohydrates derived from the diet. In the malnourished group, 30.8% (77/249) of the patients received a single nutritional transfusion and 12.4% (31/249) received total parenteral nutrition (TPN). In the well-nourished group, 55.4% (296/534) received a single nutritional transfusion and 3.7% (20/534) received TPN. The rate of preoperative TPN support was significantly higher in the malnourished group compared to the well-nourished group (P < 0.001) (Table 3).
Table 2 Nutritional characteristics of malnourished and well-nourished elderly gastric cancer patients.
Factor
Malnourished
Well-nourished
P value
Total
BMI (kg/m2)
19.4 ±1.8
24.5 ± 2.6
< 0.001
22.9 ± 3.4
PNI
46.7 ± 5.7
48.8 ± 5.3
< 0.001
48.1 ± 5.6
Albumin (g/L)
39.1 ± 4.6
40.7 ± 4.0
< 0.001
40.2 ± 4.3
Prealbumin (mg/L)
193.2 ± 50.6
214.6 ± 47.7
< 0.001
207.8 ± 49.6
Hemoglobin (g/L)
117.0 ± 24.1
122.8 ± 23.1
0.001
121.0 ± 23.6
TLC (× 109/L)
1.57 ± 0.55
1.60 ± 0.54
0.472
1.59 ± 0.54
Table 3 Perioperative nutritional support among elderly gastric cancer patients.
Factor
Malnourished
Well-nourished
P value
Total
Preoperative nutrition
< 0.001
Diet
141
56.6
218
40.8
359
45.9
Diet + single transfusion
77
30.8
295
55.4
373
47.6
TPN
31
12.4
20
3.7
51
6.5
Postoperative nutrition
0.001
Single transfusion
194
77.9
355
66.5
549
70.1
TNA
55
22.1
179
33.5
234
29.9
Postoperative PN period (days)
0.951
Median (IQR)
5 (4, 6)
5 (4, 6)
5 (4, 6)
Postoperative EN period (days)
0.273
Median (IQR)
2 (1, 3)
2 (1, 2)
2 (1, 2)
After surgery, all patients received parenteral nutrition support. Among those in the well-nourished group, 77.9% (194/249) received a single transfusion of carbohydrates with or without composite amino acids, while 22.1% (55/249) received total nutrient admixture (TNA). In patients with normal nutritional status, 66.5% (355/534) of the patients received a single transfusion and 33.5% (179/534) of the patients received TNA. The proportion of patients who received TNA was notably lower in the well-nourished group compared to the malnourished group (P = 0.001). However, there were no significant differences in the postoperative nutritional support rates or duration between the two groups (Table 3).
Risk factors associated with prolonged LOS
The median LOS of elderly gastric cancer patients enrolled in this study was 8 days (Table 1). A LOS of 9 days or more was defined as prolonged LOS. In order to estimate the clinical factors that might influence the LOS, univariate analyses for LOS were performed. As shown in Table 4, clinical factors such as patient age, gender, nutritional status, postoperative nutritional support, operation time, anesthesia type, surgery type, postoperative complications, comorbidity, BMI, PNI, albumin, prealbumin, and hemoglobin were all included in the univariate analysis. Patient age, PNI, prealbumin, operation time, and comorbidities were significant predictors for prolonged LOS.
Table 4 Univariate Cox regression analyses of clinical factors associated with length of stay.
To evaluate the robustness of the value of significant predictors for prolonged LOS, Cox multivariate regression analyses were performed to derive risk estimates related to prolonged LOS with the same clinical parameters that showed significance in univariate analyses to control for confounders. As depicted in Table 5, age ≥ 70 years (OR = 1.216, 95%CI: 1.048-1.411, P = 0.010), PNI < 44.5 (OR = 1.792, 95%CI: 1.058-3.032, P = 0.030), operation time ≥ 160 min (OR = 1.431, 95%CI: 1.237-1.656, P < 0.001), and postoperative complications grade III or higher (OR = 2.191, 95%CI: 1.604-2.991, P < 0.001) were recognized as independent predictors for prolonged LOS of elderly patients with gastric cancer enrolled in this study.
Table 5 Multivariate Cox regression analyses of clinical factors associated with length of stay.
Malnutrition presents a significant challenge to patient’s safety in perioperative settings, particularly among elderly patients[18]. In elderly patients with gastric cancer, perioperative malnutrition often occurs due to decreased physical activity, absorption disorders, insufficient food intake, and metabolic disruptions[19]. These malnourished patients often develop anemia, hypoproteinemia, and electrolyte abnormalities before surgery[20]. Additionally, malnourished elderly patients always experience higher rates of postoperative complications and longer hospital stays compared to well-nourished individuals[21]. Hence, it is crucial to screen and assess the nutritional status of patients before major abdominal surgery. In our research, the overall frequency of malnutrition in elderly gastric cancer patients was 31.8%, which is relatively high compared to findings from previous research. This variation can be attributed to observed differences in age distribution, measuring instruments, patient characteristics, and hospital locations.
Preoperative malnutrition in patients is often indicated by lower levels of hemoglobin, prealbumin, and albumin compared to well-nourished individuals[22]. Selecting appropriate assessment tools is vital for the early diagnosis and treatment of malnutrition. The PNI, determined by the concentration of serum albumin and lymphocyte count in peripheral blood, serves as an indicator of the inflammatory and nutritional status as well as patient prognosis[17]. Unlike other screening tools, PNI is advantageous as it can be swiftly and easily assessed via laboratory tests during the preoperative diagnosis. Previous studies have shown that preoperative PNI is an independent prognostic factor for disease-free survival together with the TNM stage in gastric cancer patients following surgery[23]. Recent research had identified preoperative PNI as a specific and sensitive prognostic predictor for elderly patients who underwent gastrointestinal tumor surgery[24]. Monitoring PNI indicators can help to predict malnutrition occurrence before surgery, guide prevention efforts and reduce perioperative complications in gastric cancer patients[25]. The results of this study revealed that low PNI is an independent predictor for prolonged hospital stays, suggesting that PNI predicts both short-term and long-term outcomes for elderly patients. Future research is essential to enhance the understanding and improvement of preoperative PNI.
Malnutrition, defined as a condition resulting from inadequate intake of minerals, vitamins, and other nutrients necessary for maintaining healthy tissues and organ function, requires collaborative efforts from healthcare providers, nurses, and access to nutritious food[15]. Providing nutritional support to malnourished patients can mitigate postoperative complications, such as surgical site infections and gastrointestinal issues after surgery[25]. Guidelines from the ESPEN and American Society for Parenteral and Enteral Nutrition recommend that it is preferable to use oral or enteral nutrition if at all possible[16,26]. Generally, enteral nutrition is preferred over parenteral nutrition because it is more physiological, cheaper, simpler, and less complicated. In addition, there are a large number of studies demonstrating that food in the gut has an important role in preserving normal physiology, especially that related to immune function and systemic inflammation[27]. However, in cases where a patient experiences pyloric obstruction or when enteral nutrition does not provide sufficient energy, alternative nutrition methods such as peripheral parenteral nutrition or TPN are often utilized. Our study found a significantly higher rate of preoperative TPN in malnourished patients compared to well-nourished patients, though the overall rate of preoperative parenteral nutrition support in malnourished patients was low (43.5%). Optimizing the nutritional status of elderly patients with malnutrition prior to surgery is essential for improving surgical outcomes.
Despite recommendations advocating for early initiation of oral or enteral feeding to enhance clinical outcomes and minimize surgical complications in gastric cancer patients postgastrectomy, postoperative nutritional support practices vary widely among different surgical teams. According to the Japanese Gastric Cancer Treatment Guidelines, liquids should be introduced on the first postoperative day, with solid foods starting from the second to fourth day, depending on the type of surgery[28]. In this study, the median duration of parenteral nutrition was five days. Notably, 54.8% of elderly patients received only carbohydrates, with or without composite amino acids postoperatively, several important insights and implications can be drawn regarding the nutritional management of these patients. No significant difference in duration was observed between well-nourished and malnourished patients. It may take time for malnourished patients to receive adequate care. Our study also confirmed previous findings that malnourished patients have higher overall postoperative complication rates. This underscores the need for heightened attention and individualized nutritional support for elderly patients during the postoperative period.
There are several limitations to this study. First, being a retrospective analysis, it may have selection biases despite data collection from a prospectively recruited database. Second, long-term outcomes were not considered, and the relationship between perioperative nutritional support and clinical outcomes in malnourished patients was not investigated. Third, there are many subjective factors which might affect length of hospital stay, such as the patient's subjective wishes, that were not included, and these may be as important as objective factors, particularly in China.
CONCLUSION
Malnutrition is relatively common in elderly patients undergoing gastrectomy. Low PNI is an independent risk factor associated with delayed discharge. More attention and strategies are needed to improve the clinical outcome of malnourished elderly gastric cancer patients.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade C
Novelty: Grade B
Creativity or Innovation: Grade C
Scientific Significance: Grade C
P-Reviewer: Dziegielewska-Gesiak S, Poland S-Editor: Qu XL L-Editor: Webster JR P-Editor: Che XX
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