A nomogram for predicting the central lymph node metastasis in double primary carcinoma involving thyroid carcinoma
Highlight box
Key findings
• This study identified tumor size ≥0.95 cm, thyroglobulin (TG) ≥15.62 mg/L, lower tumor location and type B blood as significant predictors of central lymph node metastasis (CLNM) in double primary carcinoma (DPC) involving thyroid carcinoma. Based on these factors, we developed a nomogram with a strong predictive performance (C-index =0.892). Additionally, in the multifocal lung carcinoma subgroup, patients exhibited a higher tendency for multifocal thyroid carcinoma.
What is known and what is new?
• The influential factors of CLNM in DPC involving thyroid carcinoma remain unclear and further in-depth research is needed.
• This study is the first to explore the regulations of CLNM in DPC involving thyroid carcinoma, filling the gap in existing research.
What is the implication, and what should change now?
• The results suggested that the nomogram could serve as a potential diagnostic tool for predicting CLNM in DPC involving thyroid carcinoma. Future studies should further validate the model’s applicability in larger samples to promote its translational application. Additionally, clinicians should remain vigilant about the possibility of multifocal thyroid carcinoma in patients with multifocal lung carcinoma.
Introduction
According to recent statistics from the International Agency for Research on Cancer (IARC), thyroid carcinoma ranks as the seventh most common malignancy worldwide (1). Breast carcinoma survivors are at a much higher risk of developing thyroid carcinoma as a double primary carcinoma (DPC) (2). Although the incidence of DPC involving thyroid carcinoma is not negligible, this patient cohort has received limited research attention. Current case reports on DPC involving thyroid carcinoma have primarily focused on the lateral cervical lymph node metastases (3,4). In contrast, our study sought to investigate the clinicopathological features and the regulations of central lymph node metastasis (CLNM) in DPC involving thyroid carcinoma. Additionally, we aimed to develop and validate a nomogram specifically designed to predict the occurrence of CLNM in this distinct patient population, thereby filling a critical gap in current clinical research.
Preoperative systemic inflammatory markers, including neutrophil-to-lymphocyte ratio (NLR), platelet-to-lymphocyte ratio (PLR), systemic immune-inflammation index (SII) and Onodera’s prognostic nutritional index (OPNI), have been proven to be linked with lymph node metastasis, the distant metastases and prognosis of differentiated thyroid carcinoma (5-8). OPNI serves as a robust prognostic indicator that significantly correlates with clinical outcomes in cancer patients. Moreover, it is a valuable tool for comprehensively assessing both the nutritional status and immune function of patients (9,10). NLR >1.49529 has even been verified to be the prognostic indicator of pediatric thyroid carcinoma (11). At the same time, these indicators possess the advantages of convenience of acquisition and utilization (12). Consequently, systemic inflammatory markers have increasingly emerged as a pivotal focus in the research of thyroid carcinoma. ABO blood group, meanwhile, is known to be a prognostic factor in ovarian, endometrial, pancreatic, breast, and nasopharyngeal carcinomas. In addition, according to the study by Shi et al., there is a correlation between the ABO blood group and tumors in the head and neck region (13). These critical factors were systematically incorporated into our study.
We conducted retrospective research using data from the Second Affiliated Hospital of Jiaxing University. In our study, we retrospectively analyzed clinicopathological data of the 62 patients with DPC involving thyroid carcinoma. We present this article in accordance with the TRIPOD reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-206/rc).
Methods
Materials
The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of The Second Affiliated Hospital of Jiaxing University (No. 2025-060-01) and individual consent for this retrospective analysis was waived. DPC patients involving thyroid carcinoma diagnosed from January 1, 2021 to May 31, 2025 in The Second Affiliated Hospital of Jiaxing University were enrolled in this study. Inclusion criteria included: DPC patients involving thyroid carcinoma diagnosed by histopathology. Exclusion criteria included: (I) patients who were lost follow-up; (II) previous thyroid surgical history. The selection process is summarized in Figure 1. A total of 62 patients met the inclusion criteria (the DPC group).
Data collection
The clinicopathological data that were collected included including patient ID, gender, age at diagnosis of thyroid carcinoma, past medical history, first primary carcinoma (FPC), second primary carcinoma (SPC), ABO blood group, pathology result [tumor size (the maximum diameter of tumor), tumor site/tumor longitudinal location of the largest tumor] according to standard preoperative sonography [the thyroid gland was trisected vertically (upper, middle, and lower of the thyroid gland)] (14), number of lesions, the CLNM status, extrathyroidal extension (tumor perimeter abutting >25% of the thyroid capsule or the loss of the capsule line) (15), whether combined with Hashimoto’s thyroiditis [according to thyroglobulin (TG) antibody and thyroperoxidase antibody status, hypothyroidism, pathological results, and preoperative ultrasound findings] or nodular goiter, and so on. The blood biochemical indexes were collected from patients within 1 week before the thyroid operation including preoperative serum TG, the absolute values of serum albumin level, the neutrophil (N), lymphocyte (L), and platelet (P) counts. NLR is the ratio of absolute values of N and L and PLR is the ratio of absolute values of P and L. SII = P × N/L. OPNI calculation formula is serum albumin level (g/L) + 5 × L (×109/L) (16).
Statistical analysis
The measurement data were expressed as mean ± standard deviation, the enumeration data were expressed as frequency or rate. Receiver operating characteristic (ROC) curves and Youden index (Youden index = sensitivity + specificity − 1) were used to determine the optimal cut-off values of TG (15.62 mg/L) and tumor size (tumor size =0.95 cm). Chi-squared test and t-test were adopted in the analysis of clinicopathological features.
Univariable and multivariable logistic regression analyses were performed to determine the factors associated with CLNM. A nomogram was constructed based on the results of logistic regression analyses. The model’s validity was assessed via k-fold cross-validation. Its predictive accuracy was evaluated using the C-index, calibration curve, and the Hosmer-Lemeshow test.
All statistical analyses were performed using SPSS (version 26.0) and R (version 4.5.0). When P<0.05, the difference was statistically significant.
Results
Clinicopathological characteristics of the DPC patients
In this study, as shown in Figures 2,3, lung cancer (43.55%), breast cancer (27.42%) were the two most common types of other primary carcinomas in DPC involving thyroid carcinoma. Fifty-eight (93.55%) patients were confirmed classic papillary thyroid carcinoma (PTC), and one of them had a combination of follicular carcinoma. One patient was diagnosed with a solid variant of PTC, while three others had the follicular variant PTCs.
As is shown in Table 1, among the 62 DPC patients in total, the majority of the patients were females aged 45 years and above. Meanwhile, the most common location of thyroid carcinoma was in the middle area and lower pole (67.74%). All cases had PTC and were in stage T1. Individuals with blood group A (32.26%) constituted the largest proportion among all DPC participants. Moreover, ten patients (16.13%) were diagnosed with multifocal thyroid carcinoma, while the remaining cases presented with a single-lesion thyroid carcinoma.
Table 1
| Characteristics | n | % |
|---|---|---|
| Tumor site | ||
| Upper | 20 | 32.26 |
| Middle | 28 | 45.16 |
| Lower | 14 | 22.58 |
| Tumor size (cm) | ||
| <0.95 | 47 | 75.81 |
| ≥0.95 | 15 | 24.19 |
| Age (years) | ||
| <45 | 9 | 14.52 |
| ≥45 | 53 | 85.48 |
| Blood group | ||
| A | 20 | 32.26 |
| B | 17 | 27.42 |
| O | 19 | 30.65 |
| AB | 6 | 9.68 |
| Sex | ||
| Female | 47 | 75.81 |
| Male | 15 | 24.19 |
| Extrathyroidal extension | ||
| Negative | 45 | 72.58 |
| Positive | 17 | 27.42 |
| Combined with Hashimoto’s thyroiditis | ||
| No | 37 | 59.68 |
| Yes | 25 | 40.32 |
| Combined with nodular goiter | ||
| No | 32 | 51.61 |
| Yes | 30 | 48.39 |
| Central lymph node metastasis | ||
| Negative | 46 | 74.19 |
| Positive | 16 | 25.81 |
| Number of thyroid lesions | ||
| One | 52 | 83.87 |
| Multiple | 10 | 16.13 |
| TG (mg/L) | ||
| <15.62 | 41 | 66.13 |
| ≥15.62 | 21 | 33.87 |
DPC, double primary carcinoma; TG, thyroglobulin.
Screening for influential factors of CLNM
According to the CLNM status, we divided the 62 DPC patients into two groups [the CLNM (+) group (n=16) and the CLNM (−) group (n=46)]. As shown in Table 2, there was no statistical difference in sex, age, pathological features (extrathyroidal extension, whether combined with nodular goiter) and preoperative systemic inflammatory markers (NLR, PLR, OPNI, SII) between the two groups. P values of tumor site (P=0.03), tumor size (P=0.001), whether combined with Hashimoto’s thyroiditis (P=0.008) and TG (P=0.01) were statistically significant.
Table 2
| Characteristics | CLNM (−) | CLNM (+) | χ2/t | P value |
|---|---|---|---|---|
| Tumor site | 6.899 | 0.03 | ||
| Upper | 18 (39.1) | 2 (12.5) | ||
| Middle | 21 (45.7) | 7 (43.7) | ||
| Lower | 7 (15.2) | 7 (43.7) | ||
| Tumor size (cm) | 12.083 | 0.001 | ||
| <0.95 | 40 (87.0) | 7 (43.7) | ||
| ≥0.95 | 6 (13.0) | 9 (56.3) | ||
| Sex | 0.585 | 0.51 | ||
| Female | 36 (78.3) | 11 (68.8) | ||
| Male | 10 (21.7) | 5 (31.2) | ||
| Age (years) | 0.312 | 0.68 | ||
| <45 | 6 (13.0) | 3 (18.8) | ||
| ≥45 | 40 (87.0) | 13 (81.2) | ||
| Blood group | 6.601 | 0.09 | ||
| A | 16 (34.8) | 4 (25.0) | ||
| B | 10 (21.7) | 7 (43.7) | ||
| O | 17 (37.0) | 2 (12.5) | ||
| AB | 3 (6.5) | 3 (18.8) | ||
| Extrathyroidal extension | 1.101 | 0.34 | ||
| Negative | 35 (76.1) | 10 (62.5) | ||
| Positive | 11 (23.9) | 6 (37.5) | ||
| Combined with Hashimoto’s thyroiditis | 6.937 | 0.008 | ||
| No | 23 (50.0) | 14 (87.5) | ||
| Yes | 23 (50.0) | 2 (12.5) | ||
| Combined with nodular goiter | 0.186 | 0.78 | ||
| No | 23 (50.0) | 9 (56.3) | ||
| Yes | 23 (50.0) | 7 (43.7) | ||
| Number of thyroid lesions | 1.255 | 0.27 | ||
| One | 40 (87.0) | 12 (75.0) | ||
| Multiple | 6 (13.0) | 4 (25.0) | ||
| TG (mg/L) | 7.891 | 0.01 | ||
| <15.62 | 35 (76.1) | 6 (37.5) | ||
| ≥15.62 | 11 (23.9) | 10 (62.5) | ||
| NLR | 2.67±1.44 | 2.71±0.95 | −0.111 | 0.55 |
| PLR | 143.37±49.56 | 139.27±37.87 | 0.302 | 0.76 |
| OPNI | 53.80±5.64 | 51.68±5.52 | 1.302 | 0.20 |
| SII | 577.53±301.60 | 535.34±215.16 | 0.515 | 0.61 |
Data are presented as n (%) or mean ± standard deviation. CLNM, central lymph node metastasis; NLR, neutrophil-to-lymphocyte ratio; OPNI, Onodera prognostic nutritional index; PLR, platelet-to-lymphocyte ratio; SII, systemic immune-inflammation index; TG, thyroglobulin.
As shown in Tables 3,4, the univariable and multivariable logistic regression analyses indicated that tumor size ≥0.95 cm (P=0.02), TG ≥15.62 mg/L (P=0.02), lower tumor location in the thyroid (P=0.02) and type B blood (P=0.04) were risk factors of CLNM in DPC involving thyroid carcinoma.
Table 3
| Characteristics | OR (95% CI) | P |
|---|---|---|
| Tumor site | 0.048 | |
| Upper | Reference | |
| Middle | 1.618 (0.203–3.000) | |
| Lower | 5.739 (0.017–9.000) | |
| Tumor size (cm) | 0.001 | |
| <0.95 | Reference | |
| ≥0.95 | 8.571 (2.316–31.716) | |
| Sex | 0.45 | |
| Female | Reference | |
| Male | 1.636 (0.460–5.816) | |
| Age (years) | 0.58 | |
| <45 | Reference | |
| ≥45 | 0.650 (0.142–2.974) | |
| Blood group | 0.10 | |
| A/O/AB | Reference | |
| B | 2.800 (0.834–9.399) | |
| Extrathyroidal extension | 0.30 | |
| Negative | Reference | |
| Positive | 1.909 (0.565–6.453) | |
| Combined with Hashimoto’s thyroiditis | 0.02 | |
| No | Reference | |
| Yes | 0.143 (0.029–0.701) | |
| Combined with nodular goiter | 0.67 | |
| No | Reference | |
| Yes | 0.778 (0.248–2.443) | |
| No. of thyroid lesions | 0.27 | |
| One | Reference | |
| Multiple | 2.222 (0.537–9.195) | |
| TG (mg/L) | 0.007 | |
| <15.62 | Reference | |
| ≥15.62 | 5.303 (1.559–17.925) | |
| NLR | 1.025 (0.669–1.570) | 0.91 |
| PLR | 0.998 (0.986–1.011) | 0.76 |
| OPNI | 0.923 (0.819–1.042) | 0.20 |
| SII | 0.999 (0.997–1.002) | 0.61 |
CI, confidence interval; NLR, neutrophil-to-lymphocyte ratio; OR, odds ratio; OPNI, onodera prognostic nutritional index; PLR, platelet-to-lymphocyte ratio; SII, systemic immune-inflammation index; TG, thyroglobulin.
Table 4
| Characteristics | β | SE | Wald | P value | OR | 95% CI |
|---|---|---|---|---|---|---|
| Tumor size | 2.422 | 1.002 | 5.844 | 0.02 | 11.263 | 1.581–80.220 |
| Tumor site | 1.490 | 0.630 | 5.592 | 0.02 | 4.436 | 1.291–15.246 |
| Blood group | 1.854 | 0.894 | 4.299 | 0.04 | 6.386 | 1.107–36.846 |
| TG | 2.026 | 0.867 | 5.456 | 0.02 | 7.586 | 1.385–41.535 |
| Combined with Hashimoto’s thyroiditis | −0.027 | 1.046 | 0.001 | 0.98 | 0.973 | 0.125–7.561 |
CI, confidence interval; OR, odds ratio; SE, standard error; TG, thyroglobulin.
Construction and validation of the nomogram
According to the regression results, we took tumor site, tumor size, blood group and TG into the construction of a nomogram (Figure 4) for predicting CLNM of DPC involving thyroid carcinoma. The C-index for the nomogram was 0.892 [95% confidence interval (CI): 0.878–0.906]. The sensitivity and specificity of the model were 75.0% and 91.3%. The high accuracy of the model was validated through internal verification using the k-fold cross-validation method (k=5, C-index =0.893).
Each risk factor could be scored. When PTC was located in the upper portion, it was 0 point, 31 points in the middle portion and 100 points in the lower portion; 0 point when tumor size <0.95 cm and 84 point when tumor size ≥0.95 cm; 0 point when TG <15.62 mg/L and 74 points when TG ≥15.62 mg/L; 64 points for B blood type and 0 point for A/O/AB blood type. The total points could be obtained by summing the points of risk factors (Table 5).
Table 5
| Risk factor | Classification | Points |
|---|---|---|
| Tumor site | Upper | 0 |
| Middle | 31 | |
| Lower | 100 | |
| Tumor size (cm) | <0.95 | 0 |
| ≥0.95 | 84 | |
| Blood group | A/O/AB | 0 |
| B | 64 | |
| Thyroglobulin (mg/L) | <15.62 | 0 |
| ≥15.62 | 74 |
As is shown in Figure 5, we used a calibration curve to estimate the diagnostic performance and the predictions showed a very good discriminative ability. The results of the Hosmer-Lemeshow test showed the goodness of fit (χ2=11.348, P=0.18).
Discussion
In this study, lung cancer and breast cancer were the two most prevalent types of other primary carcinomas. Elevated risk of breast carcinoma was observed among females who had a history of thyroid carcinoma (17-20). Yet there has been very little research on DPC of thyroid carcinoma and lung carcinoma. Interestingly, we found that five out of twenty-seven patients with DPC of thyroid carcinoma and lung carcinoma had multifocal lung carcinoma patients and they all had multifocality in thyroid carcinoma. It indicated that we needed to be more cautious about multifocal lung carcinoma patients who had multiple thyroid nodules to avoid a second thyroid operation owing to the fact that a second surgery might cause hypoparathyroidism and vocal fold paralysis due to altered anatomy (21).
Our study suggested that the DPC patients involving thyroid carcinoma mainly affected patients 45 years or older. This was primarily because lung carcinoma was the most prevalent malignancy, excluding thyroid carcinoma, in our study cohort. Additionally, the average age of diagnosis of lung carcinoma was 70 years old (22).
Young age, extrathyroidal extension, and tumor site were proven to be independent risk factors of CLNM in PTC patients, while combining with Hashimoto’s thyroiditis was a protective factor according to several studies (23-30). However, in our research, neither age nor extrathyroidal extension was significantly associated with CLNM in DPC with thyroid carcinoma. We found that tumor site, tumor size, blood group and TG were influential factors of CLNM in DPC involving thyroid carcinoma. As a result, we took these factors into the development of the nomogram for predicting the CLNM for DPC involving thyroid carcinoma and the nomogram we constructed showed good discrimination and good performance.
Nevertheless, due to the limited sample size of our study, the number of cases was insufficient, which undermined the article’s credibility. Furthermore, our study, being a single-center retrospective study, led to potential selection bias. Therefore, additional cases are essential to bolster the reliability of our findings. If our results can be replicated in a larger cohort, it will significantly facilitate decision-making regarding the appropriate extent of thyroid surgery for these patients.
Conclusions
In conclusion, tumor size ≥0.95 cm and TG ≥15.62 mg/L were risk factors of CLNM in the DPC patients involving thyroid carcinoma. Meanwhile, lower tumor location in the thyroid and type B blood were risk factors of CLNM. Tumor site, tumor size, blood group and TG were taken into the construction of a nomogram. The nomogram model is a reliable tool for accurate prognostic prediction in CLNM of the DPC patients involving thyroid carcinoma.
Additionally, our study showed that multifocal lung carcinoma patients always tended to have a higher rate of multifocality in thyroid carcinoma. As a result, multifocal lung carcinoma patients with multiple thyroid nodules should therefore be managed more aggressively.
Acknowledgments
None.
Footnote
Reporting Checklist: The authors have completed the TRIPOD reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-206/rc
Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-206/dss
Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-206/prf
Funding: None.
Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-206/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 The Second Affiliated Hospital of Jiaxing University (No. 2025-060-01) 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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