Impact of prognostic nutritional index on postoperative outcome of acute empyema

Introduction

Acute empyema is a severe infection caused by pneumonia, thoracic surgery, or chest trauma and has a relatively poor prognosis (1,2). The primary treatment of acute empyema is antibiotic therapy and chest tube placement; however, surgery is often performed if the condition does not improve with nonoperative therapy (3,4). The renal, age, purulence, infection source, and dietary (albumin) factors (RAPID) scoring system is a prognostic factor for patients with acute empyema and is a useful tool for deciding whether to perform the surgery (5-7). However, in acute empyema, few reports are available on postoperative prognostic factors such as the RAPID score. Therefore, simpler and easier-to-use prognostic biomarkers after acute empyema surgery are needed.

The prognostic nutritional index (PNI) is a blood test-based score used to assess the nutritional and immune status of a patient and is considered a prognostic predictor in many respiratory diseases, including lung cancer, transplantation, and pneumothorax (8-10). It is easily calculated from only the serum albumin level and the total lymphocyte count. The relationship between nutrition and inflammation is clear (11); however, the relationship between the PNI and postoperative outcomes in acute empyema has not been reported. This study investigated the relationship between preoperative PNI and postoperative prognosis for acute empyema and the effect of improved postoperative nutritional status on postoperative prognosis for acute empyema. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1390/rc).

Methods

Patients

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of NHO Iwakuni Clinical Center (No. 0359; December 12, 2024). Informed consent for the present study was obtained in the form of opt-out on the web-site, as comprehensive consent to conduct research using clinical data was obtained when consent for surgical treatment was obtained. A retrospective cohort study was conducted on a cohort of patients who underwent surgery for pleural infection at NHO Iwakuni Clinical Center between November 2009 and March 2022, with an observation period through March 2023. Patients were included in the study if they underwent surgery for acute empyema, defined as pleural infection developing within 3 months from symptom onset. Acute empyema was diagnosed in patients who had a clinical presentation consistent with pleural infection and at least one of the following criteria: (I) pleural fluid that was macroscopically purulent; (II) pleural fluid that was positive on culture for bacterial infection; (III) pleural fluid with a pH ≤7.2 or low glucose level ≤55 mg/dL; (IV) computed tomography (CT) findings suggestive of pleural infection, including consolidation of the underlying lung with pleural effusion without other sources of infection (7,12). Patients who underwent surgery for chronic empyema symptomatic for more than 3 months, empyema with carcinomatous pleurisy, or chronic expanding hematoma were excluded from this study. In consideration of the potential influence of active malignancy or undergoing cancer treatment on both nutritional status and inflammatory responses, a supplemental analysis was also performed excluding those patients to minimize the potential for confounding effects. The preoperative and intraoperative characteristics and postoperative outcomes were compared between patients who survived and those who died within 1 year of surgery.

Surgical intervention

All patients underwent surgery under general anesthesia and one-lung ventilation. Our surgical approach for acute empyema is generally video-assisted thoracic surgery (VATS); however, we sometimes perform thoracotomy or open-window thoracostomy (OWT) because of difficulties in intraoperative manipulation, severe pleural adhesions, or infection control. After removing the septum of fibrin and fluid from the thoracic cavity, if the lung fails to expand adequately despite high positive end-expiratory pressure, the fibrin on the visceral pleura of the lung is decorticated. In cases of empyema without an air leak or with a minor air leak, the thoracic cavity is flushed with large amounts of saline or distilled water, and two or three chest tubes are placed. If the thoracic cavity is severely contaminated, saline is irrigated through chest tubes for several days after the procedure. In cases of empyema with massive air leakage, including bronchopleural fistulas, we usually perform an OWT and daily gauze changes in the thoracic cavity. Negative-pressure wound therapy (NPWT) is often performed after OWT. When the cavity is nearly sterile, it is closed using the muscles around the cavity or greater omentum. Patients who underwent surgery for acute empyema did not receive special nutritional support before or after the operation.

Data collection

The pH value of the pleural effusion is measured at the time of the first drainage of the pleural effusion. Serum albumin levels and total lymphocyte counts were measured within 3 days before and at 7 days after surgery. For patients who underwent NPWT after OWT, the perioperative PNI on postoperative day 7 was measured based on the date of the window surgery, not from the initiation of NPWT. The PNI was calculated using the following equation: PNI = [10 × serum albumin (g/dL)] + [0.005 × total lymphocyte count (/mm³)]. The RAPID score, calculated using blood urea nitrogen, age, pleural fluid purulence, infection source, and serum albumin level, was assessed in each patient (7). Each patient’s psoas muscle mass, which represents skeletal muscle mass, was evaluated by the psoas muscle index (PMI) using abdominal CT images (5.0 mm thick) on the day of admission. The cross-sectional areas of the right and left psoas muscles at the L3 level on CT images were defined as the psoas muscle mass areas (PMA). PMI was calculated according to the following equation: PMI = PMA/height² (cm²/m²) (13).

Statistical analysis

All statistical analyses were conducted using EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan) (14), a graphical user interface for R (R Foundation for Statistical Computing, Vienna, Austria). EZR is a modified version of R commander. It was developed to add statistical functions commonly used in biostatistics. The Mann-Whitney U test for continuous variables and Pearson’s Chi-squared test for categorical variables were used to analyze patient characteristics between patients without postoperative complications (non-complication group) and those with postoperative complications (complication group), and between patients who survived (survival group) and those who died within 1 year of surgery (death within 1-year group). The Spearman’s rank correlation coefficient was used for association analysis. Receiver operating characteristic (ROC) analyses using the Youden index were performed to set the cutoff value of the PNI for survival at 1-year after surgery. Based on the ROC analysis, the 1-year survival of patients with high and low PNI was analyzed using the Kaplan-Meier method, and the differences between the groups were evaluated using the log-rank test, followed by the Holm-Sidak test. Predict factors for 1-year survival after surgery were analyzed by multivariate analysis using a Cox proportional hazards model. Missing data were not replaced. Differences were considered statistically significant at P<0.05.

Results

Figure 1 shows a schematic diagram and Table 1 summarizes patients’ characteristics. Of 80 patients who underwent surgery for pleural infection, 75 patients underwent surgery for acute empyema, and 13 died within 1 year of surgery. Five patients, including patients who underwent surgery for chronic empyema symptomatic for more than 3 months (n=3), empyema with carcinomatous pleurisy (n=1), or chronic expanding hematoma (n=1), were excluded from this study. The mean postoperative follow-up period in this study was 891 (range, 11–3,816) days. Significant differences were observed between the survival group and the death within 1-year group in preoperative and intraoperative variables, including age (P=0.03), history of cancer (P=0.005), performance status (PS) (P=0.02), high risk in the RAPID score category (P=0.01), empyema with a fistula (P=0.03), and surgical approach (P=0.02). There were no significant differences between the two groups with regard to culture for bacterial infection (P=0.13), multidrug-resistant bacteria (P=0.37), and factors related to the compromised hosts, including steroid use (P>0.99), immunosuppressant use (P>0.99), chemotherapy (P=0.32), and the time since admission to operation (P=0.79). Unsurprisingly, the death within 1-year group had a significantly longer postoperative hospital stay (P=0.01) and a significantly higher proportion of postoperative complications (P<0.001) than the survival group. Table S1 shows the characteristics of 66 patients, excluding nine patients with active cancer or cancer currently undergoing treatment from the total 75 patients. Preoperative factors showed significant differences between the two groups in the RAPID score (P=0.043). Postoperative factors showed significant differences in postoperative hospital stay (P=0.047) and postoperative complications (P=0.002).

Figure 1 Flowchart of participants. Of 80 patients who underwent surgery for pleural infection, 75 patients, excluding five patients, including three patients with chronic empyema, one patient with carcinomatous pleurisy, and one patient with chronic expanding hematoma, were divided into a group that survived after surgery (survival group, n=62) and a group that died within 1 year after surgery (death within 1-year group, n=13).

In all patients, Stage 1 patients were all treated with VATS (P=0.58). In Stage 2, VATS was performed in 49 cases and open surgery in 5 cases (P=0.03). In Stage 3, VATS was performed in eight cases and open surgery in seven cases (P=0.002) (Table 2). Although differences were not statistically significant (Stage 1, P>0.99; Stage 2, P=0.14; Stage 3, P=0.058), a supplementary analysis showed similar trends (Table S2). OWT was performed in 6 of 75 patients and only 1 patient when excluding those undergoing cancer treatments. Among these patients, 4 died within 1 year. The median PNI in this group was 25.3 (range, 23.2–28.4), indicating a low nutritional status, and the median RAPID score was 5 (range, 4–5), reflecting severe disease. The median time from hospital admission to surgery was relatively long at 16 days (range, 2–35 days).

Figure 2 and Figure S1 show a comparison of the PNI between the two groups, the relationship between the PNI and postoperative complications, and the relationship between the PNI and postoperative hospital stay. In all patients, the PNI was significantly higher in the survival and the non-complication groups than in the death within 1-year and the complication groups, respectively (survival group vs. death within 1-year group, P=0.01; non-complication group vs. complication group, P<0.001) (Figure 2A,2B). Moreover, PNI was significantly negatively associated with postoperative hospital stay (r=−0.51; P<0.001) (Figure 2C). In a supplemental analysis, PNI was similarly significantly higher in the survival group (P=0.04) (Figure S1A) and the non-complication group (P=0.007) (Figure S1B), and showed a significant negative correlation with postoperative hospital stay (r=−0.55; P<0.001) (Figure S1C). Regarding preoperative C-reactive protein (CRP) and postoperative CRP measured on day 7, in all patients, there was no significant difference between the survival group and the death within 1-year group in either preoperative CRP (P=0.11) or postoperative CRP (P=0.25) (Figure 3). In a supplementary analysis, as in all patients, there was no significant difference between the two groups in either preoperative CRP (P=0.08) or postoperative CRP (P=0.88) (Figure S2). Perioperative changes in PNI and CRP were significantly correlated (r=0.292, P=0.01).

Figure 2 Relationship between PNI and postoperative outcome in acute empyema. Preoperative PNI is shown as median values (black lines) and 5th and 95th percentiles (whiskers). (A) Patients who survived had a significantly higher PNI than those who died within 1 year of the surgery [29.80 (range, 20.63–59.30) vs. 23.30 (range, 19.89–32.05); P=0.01]. (B) Patients without postoperative complications had a significantly higher PNI than those with postoperative complications [30.09 (range, 25.76–59.30) vs. 25.16 (range, 19.89–33.85); P<0.001]. (C) Preoperative PNI was significantly negatively associated with postoperative hospital stay (r=−0.51; P<0.001). PNI, prognostic nutritional index.

Figure 3 Comparison of preoperative and postoperative day 7 CRP levels between the survival and death within 1-year groups. (A) Preoperative CRP was 20.6 (range, 0.6–49.4) mg/dL in the survival group and 14.6 (range, 5.0–28.9) mg/dL in the death within 1-year group (P=0.11). (B) Postoperative day 7 CRP was 5.63 (range, 1.03–21.19) mg/dL and 6.58 (range, 2.02–35.27) mg/dL, respectively (P=0.25). CRP, C-reactive protein.

A ROC analysis conducted to determine the cutoff value of the preoperative PNI for predicting postoperative 1-year survival for empyema yielded an area under the curve (AUC) of 0.73, with a sensitivity of 92% and a specificity of 52% associated with a cutoff value of 29.3 (Figure 4A). In comparison, the ROC analysis for the RAPID score showed a similar AUC of 0.73, with a sensitivity of 69% and a specificity of 71%, associated with a cutoff value of 5.0 (Figure 4B). In a supplementary analysis, preoperative PNI demonstrated an AUC of 0.73 with a sensitivity of 100% and specificity of 41% at a cutoff value of 32.1 (Figure S3A), whereas the RAPID score had an AUC of 0.72 with a sensitivity of 63% and specificity of 71% at a cutoff value of 5.0 (Figure S3B).

Figure 4 ROC curve analyses to determine the performance of a preoperative PNI and RAPID score in predicting 1-year postoperative survival. (A) In the ROC analysis of preoperative PNI, the AUC was 0.73 (sensitivity =92%; specificity =52%). (B) In the ROC analysis of RAPID score, the AUC was 0.73 (sensitivity =69%; specificity =71%). AUC, area under the curve; PNI, prognostic nutritional index; RAPID, renal, age, purulence, infection source, and dietary (albumin) factors; ROC, receiver operating characteristic.

According to the preoperative PNI cutoff value, we divided the patients into two groups based on a cutoff of 29.3 on the PNI [PNI >29.3 (preoperative PNI high group, n=34); PNI ≤29.3 (preoperative PNI low group, n=41)]. The preoperative PNI high group had significantly better 1-year survival compared to the preoperative PNI low group (P=0.02) (Figure 5). In a supplemental analysis, the preoperative PNI high group (PNI >32.1, n=24) had significantly better 1-year survival compared to the preoperative PNI low group (PNI ≤32.1, n=42) (P=0.03) (Figure S4). Patients in the low preoperative PNI group were further divided into two groups: those whose PNI at 7 days after the surgery improved from the preoperative PNI (PNI improved group) and those whose PNI at that time did not improve from the preoperative PNI (PNI not improved group). We compared 1-year survival after the surgery between the three groups. No significant difference was observed between the preoperative PNI high group and the PNI improved group (P=0.19). In contrast, the PNI not-improved group had significantly worse 1-year survival compared to the preoperative PNI high group (P=0.009) (Figure 6). In a supplementary analysis, the PNI not-improved group had significantly worse 1-year survival compared to the preoperative PNI high group (P=0.04) (Figure S5). Moreover, among patients with a preoperative PNI >29.3, 12 patients showed a postoperative decrease to <29.3. Of these, 2 patients (16.7%) died within 1 year. Due to the small sample size, statistical comparisons were not feasible. Unfortunately, multivariate analysis revealed that no variable reached statistical significance in predicting 1-year mortality (Table 3).

Figure 5 Comparison of high preoperative PNI and low preoperative PNI in postoperative prognosis. Using the cutoff value 29.3 of the preoperative PNI, 1-year survival after surgery for acute empyema was significantly better in patients with high preoperative PNI than in those with low preoperative PNI (P=0.02). PNI, prognostic nutritional index.

Figure 6 Comparison between patients with high preoperative PNI and those with low preoperative PNI who improved it at 7 days after surgery and those with low preoperative PNI who did not improve it at 7 days after surgery. Although patients with improvement of postoperative PNI had as good 1-year survival as those with high preoperative PNI (P=0.19), patients without improvement of postoperative PNI had significantly worse 1-year survival than them (P=0.009). PNI, prognostic nutritional index.

Discussion

In this study, preoperative low PNI resulted in developed postoperative complications, prolonged postoperative hospital stay, and poor 1-year postoperative survival. However, if patients with a low preoperative PNI could improve their PNI during the first 7 days after surgery, their 1-year survival would be similar to that of patients with a high preoperative PNI. In a supplementary analysis that excluded patients with active cancer or undergoing cancer treatment—potential confounding factors—low PNI levels remained significantly associated with poor postoperative outcomes, including 1-year mortality. Similarly, patients with bronchopleural fistula, a potential confounder, were excluded in the supplementary analysis, as most of them were undergoing cancer treatment. Nevertheless, low PNI levels remained significantly associated with poor postoperative outcomes, including 1-year mortality. Therefore, in acute empyema, PNI could be a predictor of postoperative outcome and an indicator of treatment after surgery. To our knowledge, this is the first study to investigate the relationship between PNI and postoperative outcomes in patients with acute empyema.

Unsurprisingly, the death within 1-year group included significantly more patients with older age, a history of cancer, and poor PS than the survival group. Patients with these characteristics usually exhibit frailty, which is associated with poor outcomes in many fields (15). The PNI is also associated with frailty and general health (8). Generally, immune function, inflammation, and wound healing are adversely affected by malnutrition (16,17). The PNI is predictive of mortality in patients with lung inflammation (18). In a previous study, a lower PNI was associated with a prolonged duration from surgery to chest tube removal (19). In the present study, due to the limited sample size, it was not possible to identify independent predictors of 1-year mortality in multivariate analysis. Nevertheless, a lower PNI was consistently associated with the development of postoperative complications, a longer hospital stay, and poor 1-year survival. Therefore, PNI may be a useful predictor in patients with acute empyema.

The RAPID score, which is based on renal function, age, fluid purulence, infection source, and serum albumin level, is a useful scoring system for the risk of mortality in patients with acute empyema (6,7). Moreover, the RAPID score may be useful in determining the timing of surgical intervention for acute empyema and has been reported to predict early postoperative mortality after severe empyema surgery (5,20,21). The death within 1-year group also included more patients in the high-risk category of the RAPID score than the survival group in the present study. The RAPID scoring system can be a significant prognostic factor in patients undergoing surgery for acute empyema; however, calculating the RAPID score requires pleural fluid test results and is more complicated than calculating the PNI score. In addition, if antimicrobial therapy for acute empyema is initiated without a pleural fluid test performed by the primary care physician, the results of the pleural fluid test may be incorrect. The PNI can be calculated easily and quickly using only two parameters: serum albumin level and total lymphocyte count. In ROC analysis, both preoperative PNI and RAPID score have comparable overall discriminative ability, although preoperative PNI tends to have higher sensitivity and RAPID score higher specificity, suggesting that the two scores may provide complementary information for risk stratification in patients with acute empyema. Moreover, in severe acute empyema, performing OWT before a further decline in preoperative PNI or an increase in RAPID score may be preferable. While our study demonstrates that preoperative PNI may be a useful prognostic marker, further studies are warranted to validate these findings in larger, multi-center cohorts and in diverse patient populations, ensuring the generalizability of these results.

Previous large-scale analyses have identified the interval from admission to surgery as an important prognostic factor for mortality in patients undergoing surgery for empyema (22). This effect may be partly attributable to worsening nutritional status during a prolonged waiting period before surgery. In contrast, our study did not demonstrate such an association between the survival and death within 1-year groups, either in all patients or in the subgroup excluding patients with active cancer. We speculate that this discrepancy may be due to the relatively early surgical decision-making at NHO Iwakuni Clinical Center, which results in a generally short waiting time before surgery across all patients. Because the interval to surgery was uniformly brief in the present study, it may not have provided sufficient variability to exert a measurable impact on postoperative outcomes.

In surgical cases of acute empyema, the PNI may be a useful marker as a prognostic factor and an indicator of the effectiveness of surgical intervention combined with perioperative nutritional support and infection control measures. Malnutrition negatively affects immune function, inflammation, and wound healing (16,17). In the present study, a significant correlation was observed between perioperative changes in PNI and CRP levels, suggesting that improvements in PNI may partly reflect resolution of systemic inflammation. Moreover, acute empyema with a pro-inflammatory response associated with hypercatabolism can cause significant nutritional and immunomodulatory deficits (23,24). Therefore, nutritional support and reduction of inflammation are necessary to treat acute empyema. The primary goals of surgery for acute empyema are complete evacuation of potentially infected pleural fluid or material and full re-expansion of the lung (3), which may lead to infection control and improve the patient’s nutritional status. A previous study suggests that improvement of PNI may induce a shorter duration from surgery to chest tube removal and a shorter length of postoperative hospital stay (19). In the present study, even if patients with acute empyema had a decreased preoperative PNI, improvement in postoperative PNI resulted in a 1-year survival rate comparable to that of patients without a decreased preoperative PNI. Moreover, among patients with a preoperative PNI >29.3, 12 patients experienced a postoperative decline below the cutoff value, and 2 of them (16.7%) died within 1 year. Although the small sample size precluded statistical analysis, this finding suggests that postoperative deterioration of nutritional and immune status may also negatively influence outcomes. Therefore, physicians should pay attention to the perioperative nutritional status and infection control and strive to improve them, particularly in patients with decreased preoperative PNI. Unfortunately, methods for improving perioperative nutrition and immune status have not yet been established. Although our study did not test specific nutritional regimens, recent systematic reviews and clinical guidelines support the role of perioperative nutritional optimization, including high-protein diets, immune-modulating nutrients such as arginine and omega-3 fatty acids, and timely enteral nutrition, in reducing postoperative complications and infections in high-risk surgical patients (25-27). Evidence from other surgical populations, including patients undergoing surgery for cavitary nontuberculous mycobacteria disease, suggests that such nutritional optimization is associated with improved outcomes (28-30). Combined measures of infection control and targeted nutritional support may improve PNI and clinical outcomes (26). However, research specifically in patients with acute empyema is lacking, and further studies are warranted to validate the present findings.

This study had some limitations. First, this was a single-institution, retrospective study with a limited number of patients, which also restricted the statistical power of multivariate analyses and made it difficult to identify independent prognostic factors. Second, several indicators of nutritional status have been reported previously; however, no other indicators other than PNI were examined in this study. Third, at NHO Iwakuni Clinical Center, the indication for surgery was primarily determined by whether lung re-expansion could be achieved after chest drain placement and whether infection could be controlled without surgery, regardless of the stage of empyema. Therefore, the relationship between empyema stage and surgical procedure was evaluated only in an additional analysis. In this analysis, open surgery was more frequently performed in advanced stages, which was consistent with the clinical difficulty of VATS in the treatment of empyema. Fourth, the indications and surgical approaches were not standardized because the situations and physicians varied from case to case. Fifth, all the participants were Japanese; however, the physical and nutritional characteristics differ according to the country. However, given the paucity of reports on the association between PNI and postoperative outcomes in acute empyema, our findings suggest that PNI may be a prognostic factor and an indicator of surgical efficacy in acute empyema. The association between PNI and postoperative outcomes in patients with acute empyema warrants further investigation, including larger, multicenter studies.

Conclusions

The PNI and RAPID score in patients with acute empyema may be a predictor of postoperative outcomes. Perioperative nutritional assessment of patients with acute empyema using the PNI may help to assess the efficacy of treatment better and predict postoperative outcomes. The results of this study suggest the need for further research, especially large-scale clinical studies, to clarify the relationship between PNI and acute empyema.

Acknowledgments

We would like to thank Editage (www.editage.com) for English language editing.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1390/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1390/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1390/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1390/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. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of NHO Iwakuni Clinical Center (No. 0359) and individual consent for this retrospective analysis was obtained in the form of opt-out on the web-site.

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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