The investigation of factors influencing the prognostic nutritional index in patients with esophageal cancer—a cross-sectional study

Introduction

According to 2020 statistics from the World Health Organization/International Agency for Research on Cancer (WHO/IARC), China accounted for over half of the global new cases and deaths of esophageal cancer, with percentages reaching 53.70% and 55.35%, respectively (1,2). Consequently, China has become a high-incidence area for this type of cancer. In terms of incidence and mortality rates, esophageal cancer ranks sixth and fifth in China, respectively (3). The prevalence of malnutrition in patients with esophageal cancer ranges from 60% to 85%, making it the highest among all types of cancer-related malnutrition. The nutritional status of these patients significantly impacts their prognosis, including postoperative recovery, survival time, and overall quality of life etc. (4). Therefore, experts have emphasized the importance of nutritional risk screening and assessment for cancer patients.

The prognostic nutritional index (PNI) has been extensively utilized for assessing the nutritional status and prognostic outcomes of cancer patients, thereby possessing significant clinical applicability. The concept of PNI was initially proposed by Buzby (5), however, its calculation formula is intricate and many indicators are difficult to obtain in clinical practice. Subsequently, Onodera et al. introduced a simplified calculation method based on serum albumin (ALB) concentration and total lymphocyte count (LY) in peripheral blood (6), which is an indicator reflecting the nutritional and immune status of the human body. The results of various cancer studies have consistently demonstrated a significant correlation between low preoperative PNI levels and unfavorable postoperative outcomes in patients (7,8).

The PNI demonstrates high accuracy as an indicator of malnutrition in patients with esophageal cancer, exhibiting excellent diagnostic and predictive value for assessing nutritional risk in this patient population (9,10). However, the following key problems still exist in clinical applications: in addition to serum ALB and LY, other nutritional indicators [such as prealbumin (PA) and hemoglobin (Hb)] and inflammatory indicators, such as C-reactive protein (CRP), also affect the prognosis of patients (11-13). Furthermore, PNI combined with other indicators [neutrophil/lymphocyte ratio (NLR), systemic immune inflammation index (SII), etc.] can also well predict the prognosis of tumor patients (14-17), but the interaction between PNI and these indicators has not yet been clarified. Therefore, the main purpose of this study is to identify the key factors influencing PNI, providing a basis for improving PNI to optimize the prognosis of patients and for precise nutritional management of patients with esophageal cancer. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-120/rc).

Methods

Study participants

The clinical baseline data of patients with esophageal cancer who underwent surgery in Shanghai Chest Hospital from 2016 to 2020 were retrospectively collected (Figure 1). Inclusion criteria: (I) patients who were initially diagnosed with esophageal cancer and underwent surgery; (II) no history of other malignant tumors; (III) the functions of heart, lung, kidney, liver, and bone marrow were normal; (IV) physical status score 0–2; (V) Complete clinical baseline data. Exclusion criteria: (I) recurrent patients after radical chemoradiotherapy; (II) confirmed diagnosis of carcinoma of double origin; (III) those without baseline data; (IV) previous surgical history of other tumors. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Shanghai Chest Hospital (No. IS22032) and individual consent for this retrospective analysis was waived.

Figure 1 Step-by-step diagram depicting the methodology for participant selection.

Observation indicators

General information

Age, gender, height, weight, body mass index (BMI), therapeutic method, comorbidities, tumor characteristics such as pathological type, location, and lymph node metastasis. Emaciation is defined as a BMI <18.5 kg/m² while a normal range is considered to be between 18.5–23.9 kg/m² and overweight is defined as ≥24 kg/m².

Therapeutic method

Neoadjuvant therapy (NT), also known as preoperative therapy, refers to the initial treatment of cancer that involves reducing the tumor through chemotherapy, radiotherapy, and other methods prior to surgery (18). Currently, clinical practice primarily utilizes neoadjuvant radiotherapy (nRT), neoadjuvant chemotherapy (nCT), neoadjuvant chemoradiotherapy (nCRT), and neoadjuvant immunotherapy in combination with chemotherapy/chemoradiotherapy. This study categorized participants into those who underwent NT and those who did not.

Laboratory data

The preoperative biochemical and blood routine parameters of the recruited participants were collected, including: total bilirubin (TBIL), direct bilirubin (DBIL), total bile acid (TBA), total protein (TP), ALB, albumin/globulin ratio (A/G), PA, alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), γ-glutamyltransferase (GGT) (P<0.05), lactate dehydrogenase (LDH), creatine kinase (CK), blood urea nitrogen (BUN), creatinine (Cr), uric acid (UA), retinol binding protein (RBP), glycated albumin (GA), white blood cell count (WBC), absolute neutrophil count (ANC), LY, monocyte count (MONO), platelet count (PLT), Hb, CRP.

PNI

PNI was calculated by peripheral blood lymphocytes and serum albumin before surgery. PNI = 5 × peripheral blood lymphocyte count (10⁹/L) + serum albumin (g/L). PNI was grouped according to the standard formulated by Onodera (6), take 45 as the critical value, PNI ≥45 was considered as good nutrition group, and <45 was considered as poor nutrition group.

Statistical analysis

All data were analyzed by SPSS25.0 software. The quantitative data with normal distribution or approximately normal distribution were expressed as mean ± standard deviation, the quantitative data with skewed distribution were expressed as median (interquartile range), and the count data were expressed as the number of cases (percentage).

According to gender, the differences in age, BMI, PNI, treatment methods, comorbidities, tumor characteristics, laboratory data, and other indicators between different genders were analyzed. According to PNI, the subjects were divided into low PNI group and high PNI group, and the correlation between PNI and BMI, treatment methods, comorbidities, tumor characteristics, nutrition and immunity and other laboratory tests was analyzed. Independent sample t-test, Mann-Whitney U test and chi-square test were used for statistical analysis. Pearson or Spearman correlation analysis was used for correlation analysis. For further analysis, binary logistic regression analysis was performed with PNI as the dependent variable to evaluate the influence of different variables on PNI. A two-tailed P value <0.05 was considered statistically significant.

Results

Baseline information

From January 2016 to December 2020, a total of 1,894 patients diagnosed with esophageal cancer and meeting the inclusion criteria were enrolled. The age range of these patients was between 38 and 87 years, with an average age of (63.77±7.86) years. Among them, there were 1,599 males (84.4%) and 295 females (15.6%).

Overall, 327 (17.3%) patients received NT and 359 (19.0%) patients had preoperative complications. Squamous cell carcinoma (SCC), adenocarcinoma (AC), and other types accounted for 95.7%, 2.5%, and 1.8% of cases, respectively. The distribution of the tumour’s location in the cervical + upper thoracic segments was 13.3%, the proportion of the mid-thoracic segments was 52.3%, the proportion of the lower thoracic segments was 32.0%, the proportion of the oesophagogastric junction was 2.4%. The proportion with lymph node metastasis was 51.2%. In gender subgroups, males exhibited higher than females in height, weight, and incidence of lymph node metastasis, while age was higher in females (P<0.05) (Table 1). The biochemical and blood routine indexes, these indicators (including DBIL, A/G, PA, CK, Cr, RBP, WBC, ANC, Hb, CRP, etc.) exhibited higher levels in males compared to females. Conversely, TP, ALB, ALP, LDH, UA, and GA showed higher levels in females than males (P<0.05).

The average value of PNI was 49.21±4.77, and in the gender subgroups, PNI was higher in females than in the male group (P<0.05).

Characteristics of the clinical data of PNI groups

In Table 2, the average age of the low PNI group was higher than that of the high PNI group, which was (65.32±8.45) and (63.46±7.70) years old, respectively. Moreover, the percentage of Geriatric individuals aged ≥65 years in the low PNI group (55%) was significantly higher than that in the high PNI group (46.6%) (P<0.05). The body weight and BMI of the high PNI group were significantly higher than those of the low PNI group, and the incidence of overweight was higher in the high PNI group, and the incidence of emaciation was higher in the low PNI group. The rate of NT treatment was higher in the low PNI group (P<0.05).

The high PNI group exhibited higher levels of TP, ALB, A/G, PA, CK, Cr, UA, and RBP in the biochemical indexes compared to the low PNI group; whereas GA was lower in the high PNI group than in the low PNI group. Additionally, WBC, ANC, LY, PLT, Hb, and CRP showed significantly higher values in the high PNI group than in the low PNI group among blood routine indexes (P<0.05).

Correlation analysis with PNI

Table 3 showed that PNI was positively correlated with weight, BMI, TBIL, DBIL, TP, ALB, A/G, PA, ALT, AST, CK, UA, RBP, WBC, ANC, LY, MONO, PLT, and Hb (P<0.05). PNI was negatively correlated with Age, NT, BUN, GA, and CRP (P<0.05).

Multivariate analysis of influencing factors of PNI

To investigate the effect of each indicator on PNI in patients with esophageal cancer, binary logistic regression analysis was performed on the variables in Table 4. The multivariate logistic regression equation was constructed by including age, BMI, NT, TBIL, DBIL, TP, A/G, PA, CK, Cr, UA, RBP, GA, WBC, ANC, PLT, Hb, and CRP, which showed that age [odds ratio (OR) =0.574, 95% confidence interval (CI): 0.399–0.824, P=0.003] and NT (OR =0.186, 95% CI: 0.118–0.295, P<0.001) were risk factors for high PNI group. TP (OR =17.194, 95% CI: 10.555–28.009, P<0.001), A/G (OR =5.128, 95% CI: 3.159–8.324, P<0.001), PA (OR =3.195, 95% CI: 1.942–5.256, P<0.001), WBC (OR =3.627, 95% CI: 1.729–7.608, P=0.001), PLT (OR =1.905, 95% CI: 1.047–3.465, P=0.035) and Hb (OR =2.499, 95% CI: 1.653–3.778, P<0.001) were protective factors in the high PNI group.

Discussion

The present study revealed that the prevalence of malnutrition in patients with esophageal cancer was 16.6% when a PNI <45 was employed as the criterion for assessing malnutrition. Additionally, the low PNI group exhibited a higher proportion of Geriatric individuals, as well as a higher proportion of patients with low BMI and NT treatment. The levels of TBIL, DBIL, TP, ALB, A/G, PA, CK, Cr, UA, RBP, WBC, ANC, LY, PLT, Hb, and CRP in the high PNI group were significantly elevated compared to those in the low PNI group; however, GA exhibited a lower value. The multivariate regression analysis showed that age and NT were independent risk factors for the development of malnutrition. While TP, A/G, PA, WBC, PLT and Hb were protective factors for malnutrition.

In a retrospective study of 4,146 esophageal squamous cell carcinoma (ESCC) patients in China, the results showed that the detection rate of PNI <45 was 32.8%. Even after excluding 334 esophageal cancer patients who received non-surgical treatment (chemotherapy, radiotherapy or conservative treatment), the detection rate of PNI <45 was 29.9%, which was higher than the results of this study (19). Another retrospective study involving 236 patients with resectable esophageal cancer who underwent NT before surgery demonstrated a detection rate of 28.39% for the low PNI group (20), which was still higher than that observed in the present study (16.6%). The higher proportion of their screened subjects receiving adjuvant therapy may account for this disparity. Multivariate logistic regression analysis revealed that NT was identified as a risk factor for malnutrition (PNI <45), which aligns with the findings of previous studies. Multivariate logistic regression analysis in this study showed that NT was a risk factor for malnutrition (PNI <45), which was consistent with the reduction of PNI after adjuvant therapy in previous studies (21).

The term NT refers to the initial treatment of cancer that involves chemotherapy, radiotherapy, or other methods to shrink the tumor before surgery. This approach has been shown to effectively reduce the size of primary tumor lesions, eliminate micrometastases, lower tumor staging, increase surgical resection rates, extend patient survival time, and significantly enhance postoperative quality of life for individuals with cancer (22,23). However, some studies have found that nutritional indicators, such as BMI, ALB, and Hb, are significantly reduced in esophageal cancer patients after chemotherapy or radiotherapy (24,25), which can lead to the occurrence of malnutrition. Nakatani et al. observed a decrease in PNI following nRT, nCT, or nCRT (26,27). Similarly, Rietveld et al. reported an increase in the prevalence of malnutrition among esophageal cancer patients undergoing nCRT, rising from 8% prior to treatment to 17% post-treatment (28). Therefore, the nutritional status of patients receiving NT should be closely monitored to prevent the occurrence of malnutrition. The possible mechanism is that NT can cause symptoms such as nausea, vomiting, loss of appetite, and esophagitis. These symptoms can lead to reduced food intake and an inflammatory state, thereby deteriorating the nutritional status (28,29). In addition, studies have found that during NT, patients with esophageal cancer experience loss of skeletal muscle mass and an increased incidence of sarcopenia, resulting in a poor prognosis (30-32). This might also be one of the mechanisms by which NT leads to malnutrition, but large-sample prospective studies are still needed for verification.

In addition, age is also a risk factor for the development of malnutrition in patients with esophageal cancer. The proportion of older adults with esophageal cancer has increased dramatically in recent decades due to increased life expectancy (33). Dysphagia is prevalent among Geriatric patients with esophageal cancer, and when combined with comorbidities, polypharmacy, and age-related physiological changes such as muscle loss and geriatric issues including cognitive, mobility, and mood changes, it further exacerbates the issue of malnutrition (29). A previous study has shown that the nutritional risk of most patients with malignant tumors gradually worsens with the increase of age (4). Cao et al. also found that the older the age of patients with esophageal cancer, the higher the nutritional risk (34), which is consistent with the results of this study. Meanwhile, the results of this study showed that the malnutrition group with low PNI was higher in older patients over 65 years of age, which is in line with the results of Mohri et al. (35). However, in a retrospective study of 4,146 ESCC patients in China, researchers found that the proportion of patients over 61 years old in the malnutrition group (PNI <45 group) was 62.2%, which was higher than the results of this study, which may be related to the different cut-off values of age groups (19). In contrast, a retrospective study of patients with ESCC who underwent neoadjuvant immunochemotherapy and radical surgery did not find a difference in age between PNI groups (36). In a further study by Hirahara et al., age (>70 years old) was found to be an independent predictor of poor prognosis of esophageal cancer (37).

The advanced age of patients with EC, in conjunction with the impact of the tumor itself and comorbidities, results in significantly diminished physiological function compared to healthy individuals within the same age group. Impaired immune response and compromised nutrient absorption further decrease tolerance towards radiotherapy and chemotherapy, consequently diminishing overall quality of life. The aforementioned statement implies that factors beyond nutrition (such as age, treatment modality, etc.) may also exert an influence on the variables determining the PNI and have an immeasurable impact on the occurrence of complications or mortality.

In the present study, we also found that TP, A/G, PA, WBC, PLT, and Hb were significantly higher in the high PNI group than in the low PNI group, and multivariate logistic analysis also showed that the above indicators remained favorable for the development of malnutrition, even after controlling for confounding factors. TP consists of albumin and globulin, with the former being synthesized by hepatocytes in the liver and the latter being produced by immune organs in the body. In cases where liver or immune function is impaired, there may be a reduction in albumin synthesis, potentially resulting in an inversion of the A/G ratio. Patients undergoing adjuvant therapy may suffer from varying degrees of liver injury and impaired immune function due to treatment methods, resulting in a significant decrease in the level of immune cells (38). Impaired immune function and elevated levels of inflammation will increase nutrient consumption, thereby exacerbating malnutrition. Similar results were observed in the present study, with higher rates of adjuvant therapy and lower levels of immune cells in the low PNI group.

It is noteworthy that the protein index PA is considered more sensitive due to its shorter half-life compared to albumin. A study has found that PA is associated with nutritional status and prognosis of esophageal cancer. Zhao et al. showed that PNI was positively correlated with PA in ESCC patients receiving radical radiotherapy (39). This is consistent with the results of the present study. In a retrospective study of 1,374 resected ESCC patients, serum PA level was found to be an independent prognostic indicator, and low preoperative serum PA level was associated with poor overall survival in resected ESCC patients who did not receive neoadjuvant or adjuvant therapy. More interestingly, they also found that preoperative serum PA level was superior to serum ALB level in predicting long-term survival of ESCC patients (12). Plasma PA levels were also found to be significantly associated with long-term postoperative survival in another study of Geriatric patients with esophageal cancer undergoing nCT (40). In addition, Zhao et al. demonstrated a positive correlation between PNI and Hb (39), while also establishing a relationship between Hb levels and changes with the disease progression of patients suffering from esophageal cancer (38). These findings align consistently with the results obtained in this study.

There are some limitations in this study. First of all, although the sample size of this study was adequate, it was a single-center retrospective study. The retrospective design introduced potential recall bias. Future studies should adopt prospective designs with standardized data collection to minimize confounding variables. Secondly, lifestyle factors such as smoking and alcohol consumption, as well as tumor stage, were not included in the study. Furthermore, the role of body composition was not considered. But this part of the content is already being collected. Finally, there was no further study on the impact of these factors on the long-term prognosis and survival of patients, and no subgroup analysis was conducted. Again, this study has some implications. Firstly, this study represents the first comprehensive exploration of the influencing factors of PNI in patients diagnosed with esophageal cancer. Secondly, it is recommended to utilize different cut-off values for PNI when assessing nutritional status and predicting prognosis in esophageal cancer patients of varying ages and those undergoing adjuvant therapy. However, prospective studies with large samples are still needed in the future to provide clinical evidence for further exploration of more accurate nutritional assessment indicators.

Conclusions

In conclusion, in patients with esophageal cancer, ≥65 years old and NT would reduce PNI. Additionally, TP, A/G, PA, WBC, PLT, Hb, and other indicators would also have a favorable impact on PNI. Therefore, when using PNI to evaluate malnutrition or prognosis, it should be analyzed comprehensively in conjunction with other indicators of the patient. It also suggests that we should pay close attention to the nutritional status during treatment for Geriatric patients and patients receiving NT, so as to take nutritional intervention measures in time.

Acknowledgments

The authors would like to thank all the participants and researchers, and in particular the departmental colleagues for their support and the clinical teachers for their co-operation.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-120/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-120/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-120/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-2025-120/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 Ethics Committee of Shanghai Chest Hospital (No. IS22032) and individual consent for this retrospective analysis was waived.

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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