Geriatric nutritional risk index predicts postoperative outcomes in elderly patients with pancreatoduodenectomy: a propensity score-matched analysis

Introduction

Pancreatic cancer (PC), with an increasing incidence of approximately 1% per year, ranks as the third leading cause of cancer-related mortality, and its five-year survival rate remains as low as 13% (1). This unfavorable prognosis is primarily due to the absence of effective early detection methods and the limited efficacy of traditional therapeutic approaches (2,3). Only 15–20% of patients are eligible for potentially curative surgery (4). Pancreaticoduodenectomy (PD), primarily used to resect tumors located in the periampullary region, most of which are PCs situated in the pancreatic head, has long been considered one of the most technically demanding and impactful surgical procedures. Despite continuous technological and medical advancements leading to a reduction in postoperative mortality rates, the associated complications still significantly impact patients’ prognosis (5). Advanced age presents a significant global public health challenge. The number of elderly patients undergoing PD for tumors continues to increase (6). Despite some researchers advocating for performing PD on elderly patients with thorough preparation (7,8), there is still an ongoing debate regarding the impact of age on postoperative complications and mortality rates (6,9). Therefore, promptly identifying and stratifying elderly patients is crucial.

Malnutrition is characterized by inadequate or excessive nutrient intake, an imbalance of essential nutrients, or the impaired utilization of nutrients by the body (10,11). Cancer-associated cachexia is a multifactorial syndrome primarily characterized by the loss of muscle mass, leading to a decline in quality of life, failure of anti-cancer therapies, and other adverse outcomes (12,13). Cachexia or weight loss is significantly associated with poorer survival rates in patients with PC (14,15).

The Geriatric Nutrition Risk Index (GNRI) serves as a valuable tool for the identification of patients at risk for nutrition-related morbidity and mortality (16). This method, which incorporates albumin levels and ideal body weight (IBW), has been widely validated and is associated with frailty and various clinical results in patients (17-19). Furthermore, a previous retrospective analysis involving 106 patients demonstrated an independent association between a GNRI <94 and surgical site infection following PD (20,21). However, there are limited available data on the relationship between preoperative malnutrition in elderly patients who undergo PD and postoperative outcomes. Our aim was to investigate the association between preoperative GNRI and postoperative complications in elderly patients. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2024-541/rc) (22).

Methods

Study design

The study retrospectively collected data from 392 patients who underwent PD at the Department of Pancreatic Surgery in West China Hospital of Sichuan University between January 2018 and March 2023. This study was approved by the institutional review board of West China Hospital of Sichuan University (No. 2024-1386) in July 2024. Individual consent for this retrospective analysis was waived. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments (23). The article data are accessible for research purposes up to 2 years following publication (from August 2024 to December 2026).

The inclusion criteria were as follows: (I) patients aged 65 years or older; (II) patients who underwent PD with pancreaticojejunostomy; (III) the perioperative data and pathological results were complete. Exclusion criteria: (I) patients who underwent PD combined with distal pancreatectomy or experienced multiple pancreatic injuries; (II) pancreaticojejunostomy with invagination pancreatojejunostomy or pancreaticogastrostomy; (III) intraoperative modifications in surgical techniques.

Data collection

Clinical data were collected using the electronic medical record system. Hemoglobin and hematocrit levels were reassessed on the 3rd to 5th day after surgery. The intraoperative blood loss of patients was estimated using formula proposed by Mercuriali, Inghilleri and Nadler (24,25). The calculation methods have been widely used and verified (26). The GNRI was used to assess the nutritional status of elderly patients. The patients were categorized into two groups: an at-risk group (GNRI ≤98) and a no-risk group (GNRI >98) (16). The GNRI was calculated using the following formula: [1.489 × serum albumin concentration (g/L)] + [41.7 × present body weight (PBW; kg)/IBW (kg)]. The IBW was determined by calculating height² (m²) ×22. If the PBW exceeded the IBW, the ratio of PBW to IBW was set to 1.

Subgroup analysis

We further stratified the at-risk group based on GNRI cutoff values into high-risk group (GNRI <82), moderate-risk group (GNRI =82–91), and low-risk group (GNRI =92–98) to investigate the significance of GNRI on postoperative outcomes (27).

End points

Based on Clavien-Dindo classification, the primary outcome of the study was defined as major morbidity (Clavien-Dindo scale with ≥ grade 3b complications) (28). The secondary outcomes encompassed clinically relevant postoperative pancreatic fistula (POPF), delayed gastric emptying (DGE), and post-pancreatectomy hemorrhage (PPH), mortality rates, and length of hospital stay (LOS). POPF, DGE, and PPH were defined and classified by the International Study Group of Pancreatic Surgery (ISGPS) (29-31), and only grade B and grade C were recorded. Postoperative mortality was defined as any death that occurred during hospitalization.

Surgical procedure

The experienced surgeons performed a standard pancreatoduodenectomy (classical Whipple procedure) using either laparoscopic or open approaches. Approximately 40% of the distal stomach, pylorus, entire length of the duodenum, common bile duct, gallbladder, pancreatic head tissue with lesions on the right side of the portal vein and adjacent section of the proximal jejunum were resected. Lymph node dissection was performed around the pylorus, pancreatic head and duodenum uncinate process region as well as hepatoduodenal ligament. The consistent implementation of internal pancreatic stenting during surgery was performed for all patients due to a higher incidence of clinically relevant POPF associated with external stenting after PD (32).

Statistical analysis

Continuous variables were presented as mean (standard deviation, SD) or median (interquartile range, IQR), as appropriate. Comparisons between groups were performed by the χ² test (categorical variables) or the Wilcoxon test (continuous variables). To control for differences between the two groups, we performed propensity score matching (PSM) (33). A conditional logistic regression model was fitted to the GNRI classification as the outcome, while age, gender, body mass index (BMI), bilirubin levels, presence of comorbidities (hypertension, diabetes, cardiac disease, pulmonary disease, and cerebral infarction), combined organ resection, type of surgical approach, and American Society of Anesthesiologists Physical Status Classification System (ASA) scores were used as covariates. Nearest-neighbor matching was performed in a 1:1 ratio with a caliper size of 0.2. Variables that showed significance at P<0.1 in univariate regression analyses underwent further evaluation through multivariate regression analyses. In this study, statistical significance was defined as P<0.05. In the subgroup analysis, we conducted analysis of variance (ANOVA) analyses for normally distributed continuous variables and Kruskal-Wallis test for non-normally distributed continuous variables across different groups. Data analysis was conducted using SPSS 26 software (SPSS Inc., Chicago, IL, USA).

Results

A total of 392 patients over 65 years of age who underwent PD were identified: 206 (52.6%) in the at-risk GNRI group and 186 (47.4%) in the no-risk GNRI group. The perioperative profiles of the two GNRI groups are described in Tables 1,2.

Before stratification, the median duration of operation was 294 (IQR, 232–330) min, and there were 316 (80.6%) open surgery. Some 55 patients (14%) had extended resection and 167 of 392 patients (42.6%) were ASA scores >2. The overall postoperative morbidity rate was 59.4% (233 patients) and the major morbidity rate was 10.2% (40 patients). The median duration of postoperative hospital stay was 9 (IQR, 7–13) days.

Comparison between at-risk and no-risk GNRI in entire unmatched cohort

Age (P=0.03), BMI (P<0.001), presence of hypertension (P=0.01), and preoperative bilirubin level (P<0.001) were all significantly different between the two unmatched GNRI groups. Patients in the at-risk GNRI group exhibited advanced age, lower BMI, a higher likelihood of experiencing jaundice, and a lower prevalence of Hypertension.

In terms of clinic outcomes, patients in the at-risk GNRI group experienced a higher rate of major morbidity (13.1% vs. 7.0%, P=0.046) and pulmonary infection (15.5% vs. 7.5%, P=0.01), but a shorter operative time [median: 289 (IQR, 234–310) vs. 300 (IQR, 231–340) min].

Comparison between at-risk and no-risk GNRI in matched cohort

After 1:1 PSM, we generated 129 matched pairs between the two GNRI groups. All covariates were well balanced, with an absolute standardized difference (ASD) <0.1 and no significant differences between the groups. Patients in the at-risk GNRI group had higher rates of major complication (13.2% vs. 5.4%, P=0.03) and pulmonary infection (17.8% vs. 9.3%, P=0.046). We did not find any significant difference in rates of total morbidity, POPF, DGE, PPH, bile leakage, chylous fistula, cardiac disease, cerebral infarction, wound infection, reoperation, LOS or 30-day mortality among the two groups.

Univariate and multivariable logistic regression analysis evaluating the relationship between GNRI and major morbidity was also performed (Table 3). Advanced age [odds ratio (OR) =1.084, 95% CI: 0.989–1.189, P=0.09], increased BMI (OR =1.167, 95% CI: 0.996–1.368, P=0.056), preoperative pulmonary disease (OR =2.265, 95% CI: 0.936–5.485, P=0.07), and at-risk GNRI (OR =2.645, 95% CI: 1.058–6.617, P=0.04) were identified as significant predictors for major morbidity. In the multivariable analysis, the at-risk GNRI group exhibited a significantly higher risk for major morbidity (OR =2.698, 95% CI: 1.062–6.856, P=0.04).

Subgroup analysis

No statistically significant differences in baseline characteristics or clinical outcomes were observed between the groups, except for BMI, preoperative bilirubin levels, and operative time. The high-risk group had the highest incidence of jaundice (81.8%) and the lowest BMI (median 17.6; IQR, 16.2–20.2). In the high-risk group, the major mobility rate was 18.2%, in the moderate-risk group, 14.7% and in the low-risk group, 11.7%; however, no statistically significant differences were observed (Table 4).

Discussion

The number of elderly patients suffering from periampullary cancer has been on the rise worldwide. A growing number of studies have explored the clinical outcomes of elderly patients after PD, and have suggested that surgical selection should be made with caution to guarantee safety and optimize patient benefits. To mitigate confounding bias, we employed the PSM method for the first time to evaluate the predictive significance of the GNRI in elderly patients. In this study, elderly individuals categorized within the at-risk GNRI group demonstrated a heightened risk of major morbidity and postoperative pneumonia following PD, both prior to and subsequent to matching.

The surgical management of elderly patients has historically presented a complex challenge, primarily due to the increased prevalence of preoperative comorbidities and the diminished physical function that often accompany aging. Nonetheless, multiple studies have illustrated the safety and feasibility of performing PD surgery in elderly patients who meet stringent selection criteria (34,35). Miyazaki et al. conducted a retrospective analysis of 205 PD patients, stratifying them by age (≤70 vs. >70 years). The results revealed no statistically significant difference in mortality (0% vs. 1%; P=0.43) or morbidity (26% vs. 20%; P=0.41) between the two groups (36). A recent clinical trial came to similar conclusions (37). However, studies investigating age-related postoperative outcomes in PD have yielded inconsistent findings (9,38). Pineño-Flores et al. enrolled a total of 79 patients in their study (9). The ASA scores were comparable between both groups. Patients aged 75 years or older required a higher number of transfusions. There were no significant differences observed in the duration of surgery, although the elderly group underwent more vascular resections (26% vs. 8.7%; P=0.04). Morbidity was found to be higher among the elderly population (61.9% vs. 46.6%). Patients aged 75 years or older experienced more non-surgical complications (33.3%, P=0.050), with pneumonia being the most frequent complication encountered. Postoperative mortality rate was significantly higher among those aged ≥75 years compared to younger patients (9% vs. 0%; P=0.02). In a study involving 300 patients with pancreatic ductal adenocarcinoma undergoing pancreatectomy, there were no significant differences observed in terms of surgery-related complications, 30-day mortality, and LOS between the two groups. However, it was found that elderly patients had a higher prevalence of preoperative morbidity, which was associated with an increased incidence of postoperative non-surgical complications (P=0.002) (6). Hence, it is essential to identify the risk factors for severe complications in elderly patients undergoing PD.

Older patients with gastrointestinal tract-related cancers face an elevated risk of malnutrition due to obstruction or digestive dysfunction caused by the tumor (39). Furthermore, the elderly population is potentially susceptible to malnutrition, which is frequently linked to physical or psychological impairment during the aging process (40). Studies have shown that malnutrition constitutes a risk factor for postoperative complications following surgery (39,41). At present, there are several methods to assess the nutritional status of elderly patients (39), such as the Mini Nutritional Assessment, and the Nutritional Risk Screening. However, these methods have limitations due to their heavy reliance on subjective interpretation of clinical history and physical examination, leading to potential bias and time-consuming procedures. The use of these methods may not be optimal in a fast-paced surgical environment. Nevertheless, the GNRI, which is derived from readily accessible indicators such as body weight and albumin levels, demonstrates remarkable practicality for routine implementation. Furthermore, its reliability has been extensively validated across diverse pathological conditions. In relation to PD, two studies have indicated a potential association between lower GNRI levels and the occurrence of surgical site infections or post-pancreatectomy hemorrhage (20,21). In this study, we observed that patients in the at-risk group exhibited a higher prevalence of pre-operative comorbidities, including pneumonia and jaundice. One study has shown that pneumonia is associated with a significantly higher 90-day mortality rate compared to those without pneumonia (29.8% vs. 2.1%, P<0.001) and has the greatest impact on mortality after PD (OR =9.6, P<0.001) (42). The research also found that a preoperative total serum bilirubin level of ≥13 mg/dL was linked to higher mortality rates within 90 days after PD (43). Moreover, a propensity-matched study revealed that direct surgery for preoperative jaundice was linked to higher overall postoperative complication rates, including PPH and POPF, in comparison to preoperative biliary drainage (44). After matching, both groups were well balanced for all variables. The at-risk GNRI group had significantly higher rates of major complications (13.2% vs. 5.4%, P=0.03) and pulmonary infections (17.8% vs. 9.3%, P=0.046). In multivariable analysis, this group also showed a significantly increased risk for major morbidity (OR =2.698, 95% CI: 1.062–6.856, P=0.04). These results have significant implications for clinical practice, emphasizing the need to identify and address malnutrition risk factors before surgery to improve outcomes. Subsequent subgroup analysis revealed a gradual increase in the incidence of major mobility deterioration with rising risk levels; however, our study did not demonstrate a significant difference. Clinical practice often indicates that populations at higher nutritional risk are more susceptible to developing postoperative complications. This condition may be attributed to the limitations in sample size and the variations in baseline information prior to surgery. Further investigation is necessary to explore the phenomenon.

This naturally brings attention to the vital contributions of various healthcare professionals specializing in nutrition. Examples range from clinicians with advanced nutrition training to clinical nurse specialists specializing in nutrition. Clinical evidence has revealed that clinical nurse specialists in nutrition is equipped to provide expert assistance, guaranteeing superior safety, effectiveness, and care quality (45). To date, the adoption of nurse nutrition specialists remains limited globally. Training programs tailored to this profession are highly necessary(45 46).

There are certain limitations in this study. Firstly, being a retrospective study inherently introduces information and selection biases that cannot be entirely eliminated despite our utilization of the PSM method as a means to alleviate them. However, complete elimination of these biases can only be achieved through prospective randomized controlled trials. Secondly, in order to fully comprehend the influence of long-term outcomes on elderly individuals, further exploration utilizing supplementary real-world data is imperative.

Conclusions

GNRI is a standardized nutritional screening tool that can be used to preoperatively assess the risk of postoperative complications in older patients undergoing pancreatoduodenectomy. It is an independent predictor of major morbidity after pancreatoduodenectomy. The postoperative morbidity and mortality rates in elderly patients within the high-risk group appear to be comparable to those in the moderate or low-risk group. To further verify this conclusion, large-scale and prospective trials research is still needed.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2024-541/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2024-541/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2024-541/prf

Funding: This study was supported by the Sichuan Provincial Science and Technology Department Project (No. 23NSFSC0850) and Sichuan Province Cadres Health Research Project(Sichuan Ganyan 2023-117).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2024-541/coif). All authors report that this study was supported by the Sichuan Provincial Science and Technology Department Project (No. 23NSFSC0850) and Sichuan Province Cadres Health Research Project (Sichuan Ganyan 2023-117). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was approved by the institutional review board of West China Hospital of Sichuan University (No. 2024-1386) in July 2024. Individual consent for this retrospective analysis was waived. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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