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Prognostic nutritional index predicts lateral lymph node metastasis and recurrence free survival in papillary thyroid carcinoma

BMC Cancer volume 24, Article number: 1039 (2024) Cite this article

Abstract

Background

Preoperative hematological parameters are predictors of pathological features and recurrence-free survival (RFS) in various malignancies. However, comprehensive studies of preoperative indicators associated with papillary thyroid carcinoma (PTC) are scarce. The present study investigated the association between preoperative indicators and RFS in patients with PTC. Accordingly, we explored the clinical impact of the prognostic nutritional index (PNI) on lymph node metastasis and RFS in patients with PTC.

Methods

A total of 619 PTC patients were retrospectively reviewed between Jan 2013 and Dec 2017. Laboratory values were measured and calculated. Receiver operating characteristic curves were generated to calculate the cutoff value. Univariate and multivariate analyses using the COX proportional hazard model were performed for RFS. The effects of PNI and age on RFS were investigated by the Kaplan-Meier method. Clinical characteristics and PNI were tested with the chi-square test. Univariate and multivariate logistic analyses were conducted to evaluate the predictive value of PNI for lymph node metastasis.

Results

In the multivariate Cox analysis, age, PNI and lymph node metastasis were independent prognostic indicators for RFS. The Kaplan-Meier method showed that the lower PNI group and age older than 55 years group displayed poor RFS. A low preoperative PNI was remarkably correlated with age, sex, extrathyroidal invasion, T stage, N stage and TNM stage. PNI was the only preoperative hematological indicator for lateral lymph node metastasis.

Conclusions

Among the preoperative hematological indicators, PNI may serve as a promising and effective predictor for RFS and lateral lymph node metastasis in PTC patients.

Peer Review reports

Introduction

Papillary thyroid cancer (PTC) is the most common endocrine malignancy, accounting for more than 80% of all thyroid cancers [1], with annual increases in the incidence rate. Although PTC has a long 10-year survival and good prognosis, the risk of recurrence is reportedly as high as 35% [2].

Predicting the tumor stage, recurrence and survival of patients with thyroid cancer will affect individualized patient treatment plans. Unlike patients with medullary thyroid cancer, in which calcitonin could serve as a biomarker, no effective biomarkers exist for patients with PTC. Therefore, patients with PTC continue to endure financial burdens and anxiety. In clinical practice, the tumor-node-metastasis (TNM) staging system is the most commonly used criterion to guide the selection of therapeutic schemes and predict prognosis. However, its biggest drawback is that accurate staging can only be determined by postoperative pathology. Therefore, some studies have begun to examine simple, fast and inexpensive preoperative methods to predict disease status and prognosis.

The tumor microenvironment, which is composed of immune cells and inflammatory mediators, is involved in the initiation, development and metastasis of tumors [3,4,5], including thyroid cancer [6]. Preoperative indictors based on immune cells can predict the TNM stages and prognosis of malignancies [7, 8]. For example, the neutrophil-to-lymphocyte ratio (NLR) can predict recurrence-free survival (RFS) and overall survival (OS) in various malignant tumors, such as gastric cancer [9], colon cancer [10], and breast cancer [11]. With regard to PTC, the predictive role of preoperative inflammatory indicators is still unclear. The NLR is significantly associated with the stage of PTC in patients [12]. In contrast, Weiheng Wen et al. reported that NLR was not associated with lymph node metastasis or TNM stage in elderly patients with PTC [1]. Therefore, a comprehensive study of preoperative indicators needs to be undertaken in the field of PTC.

Accordingly, the primary aim of this study was to evaluate the predictive role of commonly used preoperative inflammatory or nutritional indicators in patients with PTC.

Methods

Patients

The clinical and pathological data of 922 patients with PTC from January 2013 to December 2017 at Chongqing University Cancer Hospital were retrospectively analyzed. The inclusion criteria were as follows: patients older than 18 years old and postoperative pathological diagnosis of papillary thyroid carcinoma. Exclusion criteria were concurrent malignant tumors, the presence of blood system diseases, autoimmune diseases (except Hashimoto’s thyroiditis), liver and kidney dysfunction as indicated by elevated alanine aminotransferase or creatinine, the presence of other conditions affecting the number of immune cells, such as steroid therapy or concurrent infection (known to affect the immune cell count), and a follow-up duration of < 12 months. A total of 619 patients were included in the study (Fig. 1).

Fig. 1
figure 1

Study flowchart of patient enrollment

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The Ethics Committee of the Chongqing University Cancer Hospital authorized and approved the study and exempted the requirement of a written informed consent form. The study was conducted in accordance with the Declaration of Helsinki.

The final follow-up point was September 2022. The end point of the study was RFS. Demographic characteristics were obtained from the database of the Chongqing University Cancer Hospital, including age, sex, smoking or alcohol consumption history, height, weight, and postoperative pathological characteristics. Hematological results were derived from the peripheral venous blood of patients within two weeks before the operation.

Definitions

Pathologic staging was defined according to the 8th edition of the International Union against Cancer and the American Joint Committee on Cancer (UICC/AJCC). The RFS was calculated from the operative date to the date of recurrence or the last follow-up. Multifocality was defined as two or more lesions within the thyroid gland. Bilaterality was characterized as tumors located in both lobes of the thyroid gland. Extrathyroidal invasion encompasses both microscopic extrathyroidal extension (micro-ETE) and macroscopic extrathyroidal extension (macro-ETE). Disease recurrence was defined as any structural abnormality evaluated by cytological or pathological results as well as CT- or PET/CT-diagnosed metastatic lesions with increased Tg or TgAb levels. This is in accordance with traditional clinical recurrence defined as the novel appearance of structural or biochemical disease in patients previously classified in clinical remission.

Calculation of indicators

Patient information, cancer characteristics and complete blood cell counts, as well as other experimental data were extracted from the electronic medical records. The BMI value was obtained with the formula BMI = weight (kg) / height2 (m). The NLR and platelet-to-lymphocyte ratio (PLR) were calculated by dividing neutrophil or platelet counts by lymphocyte counts, respectively. The lymphocyte-to-monocyte ratio (LMR) was defined as the lymphocyte count divided by the monocyte count. The systemic inflammation index (SII) was calculated using the following formula: platelet count × neutrophil count/lymphocyte count. The systemic inflammation response index (SIRI) was calculated using the following formula: neutrophil count × monocyte count/lymphocyte count. The fibrinogen/albumin ratio (FAR) was calculated as fibrinogen (g/L) divided by albumin (g/L). The prognostic nutritional index (PNI) was calculated using the following formula: albumin (g/L) + 5 × lymphocyte count.

Statistical analysis

Continuous variable data are displayed as medians and interquartile ranges (IQRs), and categorical variables are displayed as percentages. The chi-square test was used for categorical variables. The predictive ability of the parameters was obtained from the receiver operating characteristic (ROC) curve, and the corresponding cutoff value was calculated based on the area under the curve (AUC) and 95% confidence interval (CI). According to the cutoff value, preoperative indicators were converted to binary variables for the next logistic regression and Cox proportional hazards regression analysis. The logistic regression model was used to calculate the predictive ability of lymph node metastasis. A Cox proportional hazards regression model was used to calculate survival prediction ability. Kaplan-Meier analysis and the log-rank test were used to compare survival between the two groups. Variables with P less than 0.05 in univariate analysis were included in multivariate analysis to identify independent prognostic factors. All P values are two-tailed, and P values less than 0.05 are considered statistically significant. Statistical calculations were performed using SPSS software (v25; IBM Corp, Armonk, NY, USA) or MedCalc software (v16.4.3; MedCalc, Mariakerke, Belgium).

Results

Pathological characteristics

The demographic characteristics of the 619 patients with papillary thyroid cancer are shown in Table 1. At the time of diagnosis, the median age of the patients was 46 years old (IQR, 37–53 years). This study included 485 (78.4%) female patients and 134 (21.6%) male patients. A total of 68 (11%) and 29 (4.7%) patients had a history of smoking or alcohol consumption, respectively. The median follow-up time was 48 months (IQR, 18.5–65 months). Regarding pathological features, a tumor with a size smaller than 1 cm, which was characterized as papillary thyroid microcarcinoma, was found in 278 (44.9%) cases. Hashimoto’s thyroiditis was pathologically proven in 92 (14.9%) patients. Multifocality was observed in 188 (30.3%) cases, and tumors located in both lobes of the thyroid were found in 126 (20.4%) cases. Extrathyroidal invasion and capsule invasion were observed in 114 and 37 patients (18.4% and 6.0%), respectively. According to TNM-8, 544 (87.9%), 65 (10.5%), 7 (1.2%) and 3 (0.5%) patients were characterized with stages I, II, III and IV, respectively. During the study period, 43 patients were diagnosed with relapse, accounting for 6.94% of the cohort. Among 43 patients with recurrence, 36 patients had local recurrence. Seven patients showed recurrence in the lung. The mean duration of recurrence was 26 months (range: 1–92 months).

Table 1 Clinicopathological characteristics in PTC patients
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Cutoff values for the indicators

To determine the optimal cutoff value, ROC curve analysis was performed for RFS (Table 2; Fig. 2). Tumor size showed the highest AUC value (0.67) for RFS, with a cutoff value of 2.3 cm (51.16% for sensitivity, 80.34% for specificity, P < 0.001). In terms of preoperative indicators, lymphocytes (56.1% for sensitivity, 66.86% for specificity, P = 0.02) and PNI (85% for sensitivity, 40.36% for specificity, P = 0.01) showed the highest AUC values for RFS (Table 2; Fig. 2). The other preoperative indicators showed no significant difference (Table 2; Fig. 2). These indicators were divided into two groups for further analysis according to cutoff values, except for tumor size.

Fig. 2
figure 2

Comparison of indicators predicting recurrence-free survival. The doughnut chart shows the values for the area under the receiver operating characteristic curve (AUCs) for recurrence free survival. BMI body mass index, WBC white blood cells, NLR neutrophil-to-lymphocyte ratio, PLR platelet-to-lymphocyte ratio, LMR lymphocyte-to-monocyte ratio, PNI prognostic nutritional index, FAR fibrinogen-to-albumin ratio, SII systemic inflammation index, SIRI systemic inflammation response index

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Table 2 Cutoff values of indicators for recurrence-free survival
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Univariate and multivariate analyses of preoperative indicators for RFS

The results of the Cox regression analysis of the prognostic indicators for RFS are summarized in Table 3. Univariate Cox proportional hazard regression models revealed that sex (HR, 2.13; 95% CI, 1.12–4.03; P = 0.02), age (HR, 2.74; 95% CI, 1.46–5.13; P = 0.002), lymphocyte counts (HR, 2.15; 95% CI, 1.16–3.99; P = 0.02), albumin levels (HR, 2.82; 95% CI, 1.25–6.37; P = 0.01), PLR (HR, 2.29; 95% CI, 1.01–5.16; P < 0.05), PNI (HR, 3.54; 95% CI, 1.49–8.44; P = 0.004), FAR (HR, 1.95; 95% CI, 1.05–3.64; P = 0.04), SIRI (HR, 2.17; 95% CI, 1.06–4.44; P = 0.03) index, tumor size (HR, 2.38; 95% CI, 1.20–4.73; P = 0.01) and lymph node metastatic (HR, 2.79; 95% CI, 1.13–6.93; P = 0.03 for central lymph node metastasis (CLNM) and HR, 6.38; 95% CI, 2.72–14.95; P < 0.001 for lateral lymph node metastasis (LLNM)) status were significantly associated with RFS (Table 3). However, multivariate analysis associations emerging from the univariate analysis (P < 0.05) showed that age, PNI index and lymph node metastatic status were prognostic factors for RFS (Table 3). These results suggested that patients older than 55 years (HR 2.84, 95% CI, 1.49–5.41, P = 0.002), a lower PNI index (HR 2.78, 95% CI, 1.16–6.69, P = 0.02) and a wider range of lymph node metastasis (HR 2.72, 95% CI, 1.08–6.85 for CLNM and 5.44, 95% CI, 2.29–12.90 for LLNM, P < 0.05) independently predicted poor RFS outcomes.

Table 3 Cox proportional hazards model for recurrence-free survival in PTC patients
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To investigate the predictive role of preoperative indicators in PTC, we performed multivariate analysis without tumor size and lymph node metastasis. Multivariate analysis showed that male sex (HR, 1.98, 95% CI, 1.00-3.92, P < 0.05), older age (HR, 2.55, 95% CI, 1.33–4.89, P = 0.005) and lower PNI index (HR, 3.29, 95% CI, 1.37–7.91, P = 0.008) were independent prognostic factors for RFS (Table 4).

Table 4 Multivariable prognosis analysis in PTC patients
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RFS in terms of PNI

PNI index could be a predictor of tumor relapse in patients with PTC. We investigated the role of the PNI index in RFS. Kaplan-Meier survival curve analysis (Fig. 3A) showed that the RFS of the low PNI group was significantly shorter than that of the high PNI group (P = 0.007). Moreover, a correlation was observed between patients older than 55 years and inferior RFS (P ≤ 0.001, Fig. 3B).

Fig. 3
figure 3

Kaplan-Meier curves of recurrence-free survival in PTC patients according to PNI (A) and age (B) PTC papillary thyroid carcinoma, PNI prognostic nutritional index

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Relationship between PNI and pathological characteristics

It is well known that pathological characteristics are closely associated with prognosis. In our previous study, we found that PNI serves as a prognostic indicator in PTC patients. Therefore, we speculate that PNI could be a predictor of pathological characteristics, and the relationship between them was evaluated. According to the cutoff value of PNI, the patients were classified into two groups (high PNI group, PNI > 55.79, n = 217 (35.06%); low PNI group, PNI ≤ 55.79, n = 402 (64.94%)). In the correlation analyses, older age (P = 0.004), female sex (P = 0.03), more aggressive extrathyroidal invasion (P = 0.03), and higher T stage (P = 0.01), N stage (P = 0.04) and TNM stage (P = 0.001) were significantly associated with a low PNI (Table 5). However, no significant relationships were observed between the two groups regarding Hashimoto’s thyroiditis, multifocality, bilaterality, or capsule invasion.

Table 5 Clinicopathological features according to PNI in PTC patients
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Predictive role of preoperative indicators in LNM

Table 6 shows the logistic regression analysis for LNM in patients with PTC. The same cutoff values used in the RFS analysis were used for further LNM analysis. In the univariate and multivariate analyses, sex and tumor size were significantly associated with LNM. Male sex (HR, 2.07, 95% CI, 1.38–3.09, P < 0.005) and larger tumor size (HR, 4.46, 95% CI, 3.18–6.26, P < 0.001) were independent factors of a high prevalence of LNM. Preoperative indicators did not show any significant differences.

Table 6 Logistic regression model for lymph node metastasis in PTC patients
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In the univariate analysis, sex, PNI index, SIRI index and tumor size were significantly associated with LLNM. Male sex (HR, 2.08, 95% CI, 1.36–3.17, P = 0.001), PNI (HR, 1.53; 95% CI, 1.01–2.32; P = 0.04), SIRI (HR, 1.83; 95% CI, 1.12–2.99; P = 0.02) and larger tumor size (HR, 6.9, 95% CI, 4.19–11.35, P < 0.001) were indicators of a high prevalence of LLNM. However, the SIRI was no longer a predictor of LLNM in the multivariate analysis. Multivariate analysis showed that male sex (HR, 2.01, 95% CI, 1.25–3.23, P = 0.004), lower PNI index (HR, 1.72, 95% CI, 1.09–2.69, P = 0.02) and larger tumor size (HR, 6.67, 95% CI, 3.99–11.15, P = 0.001) were independent predictors for LLNM (Table 7).

Table 7 Logistic regression model for lateral lymph node metastasis in patients with PTC
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To investigate the role of preoperative indicators in predicting LLNM, we performed multivariate analysis without tumor size. Multivariate analysis showed that male sex (HR, 2.27, 95% CI, 1.45–3.55, P = 0.001) and lower PNI index (HR, 1.68, 95% CI, 1.10–2.58, P = 0.02) were independent predictors for LLNM (Table 8).

Table 8 Multivariate analysis for lateral lymph node metastasis
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Discussion

Pretreatment hematological indicators could serve as significant predictors of OS or RFS in solid tumors [7, 13]. To determine the role of preoperative inflammatory indices in predicting the prognosis of patients with PTC, a retrospective study was conducted. To the best of our knowledge, this is the first study to report the different roles of the inflammation-related index in PTC. We revealed that a lower PNI was significantly associated with the pathological characteristics of PTC and could serve as an independent prognostic biomarker for RFS in patients with PTC.

The systemic inflammatory response, which can promote tumor cell proliferation, survival, and angiogenesis and inhibit the antitumor immune response, plays an important role in the initiation and development of cancer [14, 15]. However, the relationship between inflammatory markers and the biological behavior of PTC remains controversial. In female patients with PTC, NLR has no significant correlation with clinicopathological features, whereas high PLR is associated with lateral lymph node metastasis [16]. Similarly, Brian et al. also reported that NLR has no significant correlation with RFS and occult LNM in 191 patients with PTC [17]. However, Wen Zhang et al. showed that patients with PTC with an increased NLR are more likely to exhibit extrathyroidal invasion, LNM, and multiple tumors [18]. Kwan Ho Lee reported that a low NLR was correlated with prolonged disease-free survival in patients with PTC who were older than 45 years; however, this association was not observed in patients younger than 45 years [19]. Low LMR is positively correlated with poor prognosis in patients with PTC [20, 21]. Similar results have also been reported in undifferentiated thyroid cancer [22]. Furthermore, patients with PTC with hyperfibrinogenemia are also more likely to have advanced TNM staging and tumor recurrence [23]. Another study that enrolled 116 cases analyzed the prognostic role of PNI, NLR, LMR, and PLR in low-risk differentiated TC and reported that only PLR was a predictor of recurrence in such patient [24]. In accordance with prior research, our study, along with the majority of related investigations, supports the hypothesis that pretreatment hematological indicators can predict clinicopathological features and prognosis in patients with TC. In our study, several indicators commonly used to predict cancer prognosis were comprehensively compared, and most of these indicators were not associated with RFS in PTC patients. However, we found that PNI was closely associated with clinicopathological features and RFS in patients with PTC. Although Wenjie Chen et al. reported that PNI was correlated with recurrence in patients with PTC, they did not demonstrate a relationship between PNI and the pathological characteristics of patients with PTC or the Kaplan-Meier survival curve in terms of PNI due to the short follow-up time, with a mean follow-up time of 12 months [25]. In this study, the relationship between PNI and pathological features as well as recurrence in patients with PTC was comprehensively analyzed. We first reported that PNI was significantly associated with T and N classification, and tumor stage in patients with PTC, and the patients in the low PNI group had a significantly worse RFS than those in the high PNI group.

The exact mechanisms driving the relationship between PNI and the biological behaviors of cancer are not clearly understood. The PNI is capable of reflecting host immune and trophic status based on its calculation of lymphocytes and serum albumin. Lymphocytes, especially tumor infiltrating lymphocytes, play an important role in the tumor microenvironment and cancer progression [7]. Therapies targeting lymphocytes, such as anti-PD-1/PD-L1, demonstrate remarkable antitumor effects against solid tumors. This advancement is contingent upon presence and activation of all kinds of lymphocytes, including CD4 + T cells, CD8 + T cells, and B cells [26]. erum albumin levels reflect nutritional and inflammatory status and are associated with cancer survival in several types of cancers [27, 28]. The COUNT score calculated via measurement of albumin, cholesterol, and lymphocytes predicts prognosis in patients with TC treated with tyrosine kinase inhibitors [29].

Early LNM is one of the characteristics of PTC and is a risk factor for local recurrence and distant metastasis of PTC. The number of LNMs and molecular biomarkers such as BRAF, RAS or TERT could be predictors of recurrence. Approximately 27–80% of patients with PTC will develop LNM, and jumping LNM can even be as high as 37% [30]. In our study, 53.5% (331/619) of patients with PTC had LNM. Furthermore, 42.3% (140/331) of these patients exhibiting LNM developed LLNM. Therefore, predicting LLNM as early as possible is crucial. However, these data are postoperative or incur additional costs. We showed that, in preoperative indicators, male sex and lower PNI were unfavorable factors for LLNM in multivariate analysis. Men are more prone to LLNM in patients with PTC, but this does not affect RFS. Only PNI could predict LLNM and prognosis in PTC patients.

This study has several limitations. First, this study was retrospective. Second, all data were collected from a single-center, with some inherent limitations such as selection bias. The main conclusions still need to be further verified by multicenter research. Moreover, the participation of different surgeons in the management of patients may lead to the adoption of different surgical practices. Prospective studies are needed to verify the relationship between inflammatory indicators and RFS.

Conclusion

Despite the aforementioned limitations, this study provides novel insights into the relationship between preoperative inflammatory markers and PTC. To the best of our knowledge, this is the first comprehensive study examining the relationship between inflammatory indicators and PTC, and the sample size was larger than that of similar studies. We first reported that low PNI predicted LLNM and disease recurrence in patients with PTC.

Data availability

The datasets obtained and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

Not applicable.

Funding

This work was supported by the Cancer Research Youth Science Foundation of Chinese Anti-Cancer Association (CAYC18A49), Chongqing Science and Technology Commission Research Institute Performance Incentive Program of China (cstc2017jxjl30022), Natural Science Foundation of Chongqing (msxmX0498) and Beijing Xisike Clinical Oncology Research Foundation (Y-Young2021-0071).

Author information

Author notes

  1. Junbin Zhang and Jinglin Gong contributed equally to this work.

Authors and Affiliations

  1. Department of Thyroid Oncology, Chongqing Key Laboratory of Translational Research for Cancer Metastasis and Individualized Treatment, Chongqing University Cancer Hospital, Chongqing, 400030, P.R. China

    Junbin Zhang, Hong Liu, Ming Cai & Chengyao Zhang

  2. Head and Neck Cancer Center, Chongqing Key Laboratory of Translational Research for Cancer Metastasis and Individualized Treatment, Chongqing University Cancer Hospital, Chongqing, 400030, P.R. China

    Jinglin Gong

  3. Department of Pathology, Chongqing Key Laboratory of Translational Research for Cancer Metastasis and Individualized Treatment, Chongqing University Cancer Hospital, Chongqing, 400030, P.R. China

    Wenwen Zhou

Authors
  1. Junbin Zhang
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  2. Jinglin Gong
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  3. Hong Liu
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  4. Wenwen Zhou
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  5. Ming Cai
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  6. Chengyao Zhang
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Contributions

ZCY and CM conceived the idea, reviewed, and edited the manuscript. ZJB and GJL wrote the manuscript. ZJB, GJL, LH and ZWW carried out research selection, data extraction, and statistical analysis. ZJB and GJL prepared tables and figures.All authors reviewed the manuscript.

Corresponding authors

Correspondence to Ming Cai or Chengyao Zhang.

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Ethic approval and consent to participate

This study was performed in accordance with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Chongqing University Cancer Hospital. The Ethics Committee of Chongqing University Cancer Hospital waived the need to obtain informed consent, given the non-interventional retrospective design.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

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Zhang, J., Gong, J., Liu, H. et al. Prognostic nutritional index predicts lateral lymph node metastasis and recurrence free survival in papillary thyroid carcinoma. BMC Cancer 24, 1039 (2024). https://doi.org/10.1186/s12885-024-12801-w

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  • DOI: https://doi.org/10.1186/s12885-024-12801-w

Keywords

BMC Cancer

ISSN: 1471-2407

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