Association between preoperative body mass index and postoperative short-term outcomes in patients undergoing pancreaticoduodenectomy: a multicenter study

Introduction

Pancreaticoduodenectomy (PD) is widely recognized as a highly intricate procedure in the field of general surgery and currently remains the sole curative treatment for cancers affecting the pancreatic head and periampullary region, although perioperative mortality and morbidity are still really high (1-3). Postoperative complications are linked to prolonged hospitalization, escalated costs, and can potentially impact long-term recurrence and survival (4,5). Investigating risk factors associated with postoperative complications is crucial for enhancing the prognosis following PD.

Factors contributing to postoperative mortality and morbidity after PD are as follows: age, sex, American Society of Anesthesiologists (ASA) score, co-morbid illness, pathology of the tumor (malignant or benign), pancreatic duct size and texture, operative time, the blood loss and transfusion, etc. (6-8). In recent years, there are increasing investigations reporting that the nutritional status of patients is closely related to the prognosis of patients with pancreatic resection (9-11). The relationship between preoperative body mass index (BMI) and postoperative morbidity after PD has been controversial (12-15). Furthermore, the majority of studies have primarily examined the impact of high BMI or obesity, neglecting the low-BMI status, which is common in patients with pancreatic and periampullary cancers (12-17). In addition, the investigation of the relationship between low BMI and the postoperative prognosis in patients undergoing PD has been limited thus far.

Therefore, this present study aimed to identify whether BMI stratified by low-BMI, normal-BMI and high-BMI can better predict the postoperative outcomes in patients undergoing PD. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-158/rc).

Methods

Patients

Patients who underwent PD from January 2016 to December 2021 at Shanghai Changzheng Hospital, Lishui Municipal Central Hospital, Chang Shu First People Hospital, People’s Hospital of Haimen City, and Lu’an People’s Hospital of Anhui Province in the Mainland of China were consecutively enrolled into this retrospective study. The following patients having these factors were excluded from the study: (I) age less than 18 years old; (II) those with acute or chronic inflammation; laboratory abnormalities and/or clinical symptoms or signs suggestive of inflammation; (III) not documented preoperative BMI level; (IV) previous major abdominal surgery (i.e., bariatric surgery, liver surgery, pancreatectomy and splenectomy); (V) minimally invasive procedures (laparoscopic or robotic); (VI) inaccurate information of postoperative 90-day mortality or 30-day morbidity. The diagnosis was confirmed by the postoperative pathological examinations. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received ethical approval from the Institutional Ethics Committee of Lishui Municipal Central Hospital [No. 2025 (I)-227-01]. Additionally, the Ethics Committees of Shanghai Changzheng Hospital, Changshu First People Hospital, People’s Hospital of Haimen City, and Lu’an People’s Hospital of Anhui Province approved the study and granted an ethical exemption for this research. Informed consent was taken from all the patients.

Data collection

Baseline characteristics were retrieved from the medical records. The demographic characteristics included sex, age at resection, ASA score, BMI, co-morbid illnesses, performance status, cigarette smoking, alcohol drinking. BMI was calculated as an individual’s weight in kilograms divided by the square of height in meters (kg/m²). In the present study, patients were classified according to BMI: low-BMI (BMI <18.5 kg/m²), normal- BMI (18.5≤ BMI <25.0 kg/m²), and high-BMI (BMI ≥25.0 kg/m²), based on World Health Organization (WHO) definitions (18). Co-morbid illnesses included hypertension, diabetes mellitus, chronic obstructive pulmonary disease, cardiovascular disease, renal dysfunction and others. Patient laboratory variables included preoperative hemoglobin level, platelets level, international normalized ratio (INR), total bilirubin (TB), creatinine level, alanine aminotransferase (ALT), aspartate transaminase (AST), albumin level, which was recorded within 1 week before surgery. Patient preoperative treatments included neoadjuvant chemotherapy and preoperative biliary drainage. Patient clinicopathologic characteristics included the presence of macroscopic vascular invasion, maximum tumor size, pathology findings and pancreatic fistula risk score (19). Additionally, operative variables included intraoperative blood transfusion, intraoperative blood loss, and operation time.

Postoperative outcomes

Postoperative mortality was defined as death occurring within 90 days of the operation or during the same hospital stay. Postoperative morbidity was defined as complications occurring within 30 days after surgery and graded according to the classification proposed by Dindo and colleagues (20). Minor and major morbidity were defined as Clavien-Dindo grades I–II and III–V, respectively. Postoperative complications after PD included postoperative pancreatic fistula (POPF), delayed gastric emptying (DGE), postpancreatectomy hemorrhage (PPH), biliary leakage, surgical site infection (SSI), ascites, biliary tract infection and other complications. POPF and clinically relevant POPF (CR-POPF) (grade B–C) were defined based on the International Study Group of Pancreatic Surgery (ISGPS) definition (21,22). DGE was defined as the requirement of a nasogastric tube for more than 7 days, reinsertion of the tube after postoperative day 7, or inability to tolerate a solid diet by postoperative day 14, based on the ISGPS definition (23). PPH was defined as a decrease in hemoglobin level of greater than 3 g/dL after PD compared to the postoperative baseline level, along with postoperative transfusion due to falling hemoglobin, and/or the requirement for radiological intervention (e.g., embolization) and/or reoperation to control bleeding (24). Chyle leak was defined as the presence of milky-colored fluid from a drain, drain site, or wound on or after postoperative day 3, with a triglyceride content equal to or greater than 110 mg/dL (1.2 mmol/L) (25). SSI was defined as superficial and/or deep incisional SSI (defined by the guidelines for prevention of SSI) occurring within 30 days after surgery (26). Biliary leakage was defined as either a drain fluid bilirubin concentration more than 3 times higher than the serum concentration on or after postoperative day 3, or the requirement for radiologic or operative intervention due to the presence of biliary collections or bile peritonitis (27). In addition, the presence of pleural effusion and ascites necessitating the use of diuretics or paracentesis was considered as morbidity. Other complications encompassed hepatic insufficiency, pulmonary infection, renal dysfunction, urinary infection, and cardiocerebrovascular accident. The database was closed as of December 2021.

Statistical analysis

Baseline characteristics of the patients were presented as the number (percentage) for categorical variables and as median (range) or mean ± standard deviation (SD) for continuous variables. Continuous variables were compared using either the Student’s t-test or the Mann-Whitney U test, while categorical variables were compared using either the χ² test or the Fisher’s exact test. The parameters of the enrolled patients in this study were selected to investigate the potential relationship with short-term outcomes after PD, based on the results reported in previous studies. The cut-off values for the continuous variables were determined based on commonly used thresholds in previous studies. The incidences of mortality and morbidity were compared among the low-BMI, high-BMI, and normal-BMI group. Only variables that showed significance with a P value <0.1 in the univariate analysis were included in the subsequent multivariate analysis, conducted using logistic regression analyses. All P values were calculated using a two-sided test, and a significance level of P<0.05 was applied. Statistical analyses were conducted using SPSS software version 25.0 (SPSS, Chicago, IL, USA).

Results

Clinical and pathological characteristics

Our database enrolled 836 patients who underwent PD during the study period. Based on the inclusion and exclusion criteria, 658 patients were included in this study. Of all the 658 patients in the present study, 399 (60.6%) were male and 259 (39.4%) were female, with a median age of 62.0 years (range, 18–85 years). By using 18.5 and 25.0 kg/m² as the cut-off values of BMI, 64 patients (9.7%) were low-BMI, 475 patients (72.2%) were normal-BMI and 119 patients (18.1%) were high-BMI. Patient characteristics are presented in Table 1. There were no significant differences in age, sex, ASA score, Eastern Cooperative Oncology Group (ECOG) performance status, preoperative treatments, most laboratory findings, tumor-pathologic parameters, or operative findings among the low-BMI, high-BMI, and normal-BMI groups. However, compared with the normal-BMI group, the low-BMI group had significantly lower hemoglobin level (P=0.045), TB (P=0.02), and ALT level (P=0.005). Additionally, the high-BMI group had a significantly higher rate of co-morbid illness (55.5% vs. 41.3%, P=0.005), as well as higher hemoglobin levels (P=0.02) and albumin levels (P=0.006) compared to the normal-BMI group.

Comparisons of postoperative mortality and morbidity

Comparisons of postoperative short-term outcomes in patients among low-BMI, normal-BMI, and high-BMI groups are presented in Table 2. The results of univariable and multivariable analyses of postoperative mortality after PD are presented in Table 3. Univariate analyses and multivariate analyses for prognostic factors of postoperative morbidity, major morbidity after PD are shown in Tables 4,5. Table 6 displays the results of univariate and multivariate logistic regression analyses for CR-POPF following PD. Compared with the normal-BMI group, multivariable analyses demonstrated that low-BMI was independent associated with postoperative mortality [odds ratio (OR) 4.220, 95% confidence interval (CI): 1.133–15.712, P=0.03], overall morbidity (OR 2.084, 95% CI: 1.135–3.827, P=0.02), and CR-POPF (OR 3.422, 95% CI: 1.895–6.177, P<0.001). In addition, multivariable analyses identified that high-BMI was independent risk factor for postoperative mortality (OR 4.046, 95% CI: 1.262–12.976, P=0.02), overall morbidity (OR 2.364, 95% CI: 1.462–3.822, P<0.001), major morbidity (OR 2.249, 95% CI: 1.181–4.283, P=0.01), and CR-POPF (OR 1.995, 95% CI: 1.210–3.287, P=0.007).

Discussion

This study investigated the association between preoperative BMI and postoperative short-term outcomes following PD with a multicenter, large sample cohort. The result revealed that both low-BMI and high-BMI were independently associated with postoperative mortality, overall morbidity, major morbidity, and CR-POPF. In addition, high BMI was an independent risk factor for chyle leak and the low-BMI group had a high risk of SSI. Therefore, BMI might serve as an easy-to-use and objective marker which can help surgeons refine preoperative management and select patients for PD.

Obesity has become a significant global health issue, reaching epidemic levels across the globe. In 2016, the WHO reported that over 1.9 billion adults were overweight, with more than 650 million classified as obese (WHO, n.d.). The escalating prevalence of overweight and obesity is poised to amplify the incidence of obesity-related chronic diseases, encompassing diabetes, coronary heart disease, hypertension, and various malignancies such as colorectal, prostate, breast, and pancreatic cancer (28,29). Furthermore, several recent studies have indicated a significant association between obesity and unfavorable postoperative outcomes following pancreatic surgery (30,31).

PD is one of the most complex procedures with extensive dissection and complicated reconstructions. In recent years, advancements in perioperative management, patient selection, and surgical techniques have resulted in a notable decrease in PD mortality, now standing at 3−5%. Nevertheless, postoperative morbidity following PD remains substantial, ranging from 40% to 60% (32,33). There are many severe complications such as POPF, DGE, and PPH, resulting in worse outcomes (34,35). Otherwise, another study have investigated the potential role of obesity as a predictor for postoperative short-term outcomes (13). Nonetheless, there is considerable ongoing debate surrounding the impact of obesity on postoperative morbidity following PD (36-39). Given the global rise in obesity rates and the increasing number of obese patients undergoing PD, it is crucial to elucidate the role of obesity as a preoperative predictive factor in PD. Therefore, we conducted a study to examine the influence of preoperative BMI categories on postoperative outcomes in patients who underwent PD. To the best of our knowledge, this study represents one of the largest investigations exploring the potential association between preoperative BMI categories and postoperative morbidity following PD. In this study, BMI ≥25.0 kg/m² was considered to be high-BMI. The high-BMI group exhibits a significantly higher incidence of preoperative comorbidities. Furthermore, high-BMI was independently associated with postoperative mortality, overall morbidity and major morbidity.

Preoperative low-BMI also emerged as a significant independent risk factor for heightened postoperative mortality and overall morbidity following PD. In previous studies, low-BMI was reported to be significantly associated with sarcopenia and low albumin level, indicating potential clinical manifestations of compromised immune function and malnutrition. Moreover, low-BMI patients who are more prone to presenting with sarcopenia often exhibit a diminished capacity to withstand the stress and starvation induced by surgery (40-42). In the study, low-BMI patients also had lower hemoglobin level, which also means malnutrition. These might be the reason that low-BMI patients has poor postoperative outcomes. In addition, low-BMI has been reported to have an increased risk of SSI in general surgeries (43,44), which had the same result in this study.

POPF represents the most severe complication following PD, with an incidence of up to 30%, even in high-volume centers (45). On the basis of the findings of the International Study Group of POPF (21), several factors are found to have a significant relationship with the incidence of POPF, such as duct size, the texture and pancreas, intraoperative blood loss, as well as pathologic subtype (46,47). CR-POPF are often commonly defined as category B and C fistula (22). The occurrence of POPF in patients after PD probably with severe consequences remains the most relevant clinical hazard. Therefore, it is crucial to accurately predict the occurrence of CR-POPF and identify patient risk stratification to guide surgical decision-making and clinical management (45). Although the rejection of PD in high-risk patients for POPF is unlikely, comprehending the low-risk population can lead to benefits such as reduced abdominal drainage, accelerated recovery, enteral nutrition, and shorter hospital stays (48,49). Previous studies have shown that patients with high-BMI are more likely to experience a higher incidence of both POPF and CR-POPF (39,50). In this study, both low BMI and high BMI were identified as independent risk factors for CR-POPF, while high BMI was also found to be an independent risk factor for overall POPF. The level of BMI might be an easy-to-use index to predict POPF for patients undergoing PD and refine perioperative management.

In addition, we initially categorized patients with BMI ≥25 kg/m² as the high-BMI group (N=119), which inherently included both overweight (25.0–29.9 kg/m², N=110) and obese (≥30.0 kg/m², N=9) subpopulations. To resolve potential misclassification bias raised, we conducted in-depth subgroup analyses stratifying this cohort into overweight and obesity groups. The results in Table 7 revealed that overweight was associated with a significantly higher rate of postoperative mortality, overall morbidity, major morbidity, CR-POPF and chyle leak. In addition, compared with normal group, obesity group had a significantly higher rate of postoperative mortality and CR-POPF. Compared with the overweight group, the obesity group had a higher incidence of major morbidity and chyle leak, but there was no statistically significant difference compared with the normal group.

There are several limitations in this study. Firstly, the present study is retrospective in nature despite the patient data being recorded in a prospectively maintained database. Secondly, this study exclusively included patients from China and the prevalence of obesity (BMI ≥30 kg/m²) in the cohort was low. Therefore, it is necessary to obtain international multi-center data to validate the influence of low-BMI and high-BMI on postoperative complications. Thirdly, the evaluation of initial weight presents a challenge for pancreatic cancer patients with a history of weight loss, which is a commonly encountered limitation.

Conclusions

This large-scale multicenter study indicated that the BMI can serve as an independent predictor of postoperative mortality, morbidity, and CR-POPF following PD. These findings suggest the importance of developing individualized surveillance and treatment strategies for patients undergoing PD, taking into account their BMI.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-158/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-158/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-158/prf

Funding: This study was supported by the Naval Medical University Research Physician Training Project (V1.0: 20170206).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-158/coif). The authors have no 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 conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received ethical approval from the Institutional Ethics Committee of Lishui Municipal Central Hospital [No. 2025 (I)-227-01]. Additionally, the Ethics Committees of Shanghai Changzheng Hospital, Changshu First People Hospital, People’s Hospital of Haimen City, and Lu’an People’s Hospital of Anhui Province approved the study and granted an ethical exemption for this research. Informed consent was taken from all the patients.

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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