Predictive factors for re-recurrence in papillary thyroid carcinoma following reoperation: a retrospective analysis

Introduction

Papillary thyroid carcinoma (PTC), the predominant histological type of thyroid malignancy, has exhibited a rising incidence globally. Despite a favorable long-term prognosis, with survival rates exceeding 95% at 10 years and 93% at 20 years (1), recurrence remains a significant clinical challenge. Up to 30% of patients with PTC who undergo initial treatment—including surgery, radioactive iodine (RAI) therapy, and thyroid-stimulating hormone suppression—experience recurrence (2,3). However, it is often unclear whether a recurrence represents a true recurrence after a period of disease-free status or persistent disease resulting from incomplete therapy.

According to American Thyroid Association guidelines, patients achieving “disease-free status” after total thyroidectomy are defined as having no clinical or imaging evidence of disease and demonstrating thyroglobulin (Tg) serum levels of unstimulated Tg <0.2 ng/mL and stimulated Tg <1 ng/mL (4). One study revealed that up to 77.2% of patients who underwent reoperation for PTC initially considered as recurrence actually represented persistent disease when both ultrasonographic findings were negative and Tg and Tg antibody levels were undetectable (5). Consequently, several studies have suggested that a disease-free period of at least 1 year following initial management is necessary to distinguish recurrence from persistent disease (6,7).

Additionally, repeated neck procedure are surgically demanding due to the increased risk of injury to the recurrent laryngeal nerve, external branch of superior laryngeal nerve, and parathyroid glands, which may be compromised by postoperative fibrotic tissue changes and disruption of normal anatomy. Clear classification between persistent and recurrent disease can play a critical role in providing valuable information to facilitate tailored treatment (8).

Few studies have investigated the risk factors for re-recurrence in patients with PTC who achieved disease-free status following initial treatment. Therefore, the aim of this study is to examine the risk factors for re-recurrence in PTC patients who underwent total thyroidectomy and central neck dissection, with or without lateral neck dissection, as the initial operation. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-189/rc).

Methods

Study population

Between February 2006 and October 2020, a total of 12,797 patients underwent either initial surgery or reoperation for PTC. Among them, we reviewed the medical records of patients who underwent reoperation due to recurrent PTC at Chonnam National University Hwasun Hospital. Patients were excluded if they were younger than 15 years old, had histologic types of thyroid malignancies other than PTC, undergone lobectomy or total thyroidectomy without lymph node (LN) dissection as their initial operation, had distant metastasis at the time of first recurrence, or presented with structural disease within 1 year after surgery. A total of 158 patients who had undergone reoperation following total thyroidectomy and central neck dissection, with or without lateral neck dissection, for PTC were enrolled. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the institutional review board of Chonnam National University Hwasun Hospital (No. CNUHH-2025-053). The need for informed consent from patients for this retrospective analysis was waived. All primary thyroid tumors, LNs, and loco-regional recurrences were confirmed by ultrasound-guided fine needle aspiration cytology. The patient’s clinicopathological and biochemical data were thoroughly reviewed.

Initial surgery and postoperative follow-up

All patients included in this study underwent total thyroidectomy and central neck dissection (prophylactic or therapeutic) as their initial operation. Lateral neck dissection (levels II, III, IV, and V) was performed in patients with metastatic lateral LN. All surgical specimens were evaluated by experienced pathologists. Patients presenting with LN metastases or gross extrathyroidal extension invading adjacent structures such as the recurrent laryngeal nerve, trachea, or esophagus were administered RAI therapy (30–180 mCi) 2–3 months postoperatively. However, RAI therapy was omitted in some cases due to patient refusal.

All patients attended regular follow-up visits every three to 6 months for the first 3 years and annually thereafter. At each visit, clinicians conducted physical examinations of the neck, ultrasound imaging, chest radiography, and measurements of serum-free thyroxine, thyrotropin, Tg, and anti-Tg antibody concentrations. Patients suspected of loco-regional recurrence during follow-up were further evaluated by ultrasound and fine needle aspiration cytology. When recurrence was confirmed pathologically, neck computed tomography (CT) with or without positron emission tomography (PET) was performed for further evaluation. In patients with elevated Tg or anti-Tg antibody levels but no visible structural lesions, a whole-body iodine scan with single photon emission CT (SPECT) was additionally performed. Follow-up duration was calculated from the date of the initial operation to either the date of recurrence or the last follow-up.

Reoperation and subsequent management

Structural disease was defined as recurrence or re-recurrence. All prior imaging studies were thoroughly reviewed to differentiate true recurrence from persistent disease. The extent of reoperation was determined based on the initial surgical procedure and the anatomical location of the recurrent lesion. If recurrence occurred in the previously dissected surgical field, en bloc compartment-oriented lateral neck dissection was performed. Selective neck dissection was carried out in cases involving previously dissected compartments, guided by preoperative ultrasound and indigo-carmine solution marking of the recurred lesion. Intraoperative neuro-monitoring was used when recurrence was located near the recurrent laryngeal nerve on ultrasound. Pathologic examination and postoperative management were conducted using the same protocols as in the initial surgery. RAI therapy (100–180 mCi) was administered 2–3 months after reoperation, with the dose determined according to the disease status; however, it was omitted in patients who showed no abnormal uptake on the iodine scan. No patients received systemic therapy such as radiotherapy or tyrosine kinase inhibitors during the study period.

Statistical analysis

The primary endpoint of this study was re-recurrence. Follow-up duration was calculated from the date of either the initial operation or the first reoperation to the date of structural recurrence or re-recurrence, or to the last follow-up. Continuous variables were expressed as means with standard deviations or medians with ranges, while categorical variables were presented as counts with percentages. The area under the curve and optimal cutoff value for LN ratio (LNR) and the number of metastatic LN were determined using receiver operating characteristics curve analysis. The Cox proportional hazards model was used to assess associations between clinicopathological variables. Re-recurrence-free survival curves were generated and analyzed using the Kaplan-Meier method, and differences in re-recurrence-free survival were evaluated using the log-rank test. All statistical analyses were performed using SPSS Statistics for Windows, version 29.0 (IBM Corp., Armonk, NY, USA). A two-sided P value <0.05 was considered statistically significant.

Results

Patients’ demographics at initial management

Table 1 shows the demographics of the patients at the time of initial treatment in this study. The mean age (standard deviation) was 43.9±12.9 years, and 42 (26.6%) patients were male. A total of 94 (59.5%) patients had a main tumor size larger than 1 cm. The most common T stage was T1a (36.7%), followed by T1b (28.5%) and T4a (13.9%). Forty-two (26.6%) patients had gross extrathyroidal extension. N stage findings were as follows: N0, 24 (15.2%); N1a, 77 (48.7%); and N1b, 57 (36.1%). Lymphovascular invasion was observed in 5 (3.2%) patients. LN dissection during the initial operation included only central neck dissection in 101 (63.9%) patients, central neck dissection with ipsilateral modified radical neck dissection in 46 (29.1%), and bilateral modified radical neck dissection in 11 (7.0%). The median time between initial surgery and first recurrence was 31.1 months (range, 13.6–148.4 months).

Patients’ characteristics after recurrence

Among the 158 patients who underwent reoperation for recurrence, 46 (29.1%) experienced recurrence in the central compartment, 93 (58.9%) in the lateral compartment, and 19 (12.0%) in both central and lateral compartments. The mean number (± standard deviation) of harvested and metastatic LNs was 14.4±14.6 and 3.0±2.8, respectively. Following the first reoperation, 137 (86.7%) patients received RAI ablation. Based on post-reoperative unstimulated maximal Tg levels, 83 (52.5%) patients had Tg <1 ng/mL, 54 (34.2%) had Tg between 1 and 5 ng/mL, and 21 (13.3%) had Tg ≥5 ng/mL. The median time between the first recurrence and either second recurrence or last follow-up was 101.3 months (range, 12.1–223.7 months) (Table 2). The distribution of recurrent lesions at the first and second recurrence according to initial surgery is presented in Figure 1.

Figure 1 Distribution pattern of recurrent lesions according to initial operation. CND, central neck dissection; MRND, modified radical neck dissection; TT, total thyroidectomy.

Univariate and multivariate analyses according to re-recurrence

In univariate analysis, T4a stage at initial operation (P=0.006), LNR >0.7 (P=0.049), and post-reoperative unstimulated maximal Tg ≥1 ng/mL (P=0.02) were statistically significance predictive factors for re-recurrence. Other factors, including sex, age, tumor size, extrathyroidal extension, multiplicity, bilaterality, lymphovascular invasion, recurrent lesion, and the number of metastatic LNs at reoperation, were not statistically significant (Table 3 and Figure 2). Multivariate Cox regression analysis showed that T4a stage [vs. T1–T3b; hazard ratio (HR), 2.782; 95% confidence interval (CI): 1.201–6.447; P=0.02] and unstimulated maximal Tg ≥1 ng/mL after the first reoperation (vs. <1 ng/mL; HR, 2.427; 95% CI: 1.054–5.588; P=0.04) were strong predictors of re-recurrence (Table 4).

Figure 2 Kaplan-Meier curves in disease-free survival after re-operation according to T stage at initial operation (A), LNR at initial operation (B) and unstimulated maximal thyroglobulin (on Tg) level after re-operation (C). LNR, lymph node ratio; Tg, thyroglobulin.

Complications associated with each operation

Among the 158 patients, transient hypoparathyroidism was observed in 14 (8.9%) patients after the initial operation and in 2 (1.3%) patients after reoperation; however, except for one patient who developed permanent hypoparathyroidism after the initial operation, no additional cases occurred following reoperation. Transient recurrent laryngeal nerve injury occurred in 13 (8.2%) patients only after the initial operation, while no additional cases were observed following reoperation beyond the 7 patients who had permanent RLN injury. Patients who had experienced hemotome (four patients after initial operation and one patient after reoperation) or chyle leakage (one patient after initial operation) recovered after conservative management. One patient with a surgical site infection was successfully cured with antibiotic management (Table 5).

Discussion

This study was designed to identify predictive factors for re-recurrence in patients with PTC who underwent total thyroidectomy and central neck dissection, with or without lateral neck dissection as their initial surgery. Among the 158 patients who experienced loco-regional recurrence, re-recurrence occurred despite comprehensive surgical treatment and RAI therapy. Our analysis indicated that T4a stage, LNR >0.7, and unstimulated maximal Tg ≥1 ng/mL were associated with re-recurrence based on univariate analyses. In multivariate analysis, T4a stage and unstimulated maximal Tg ≥1 ng/mL were strongly associated with elevated risk of re-recurrence.

Persistent or recurrent disease in PTC is frequently found in cervical LNs or the thyroid bed (9,10). Differentiating true recurrence from persistent disease is crucial for accurately identifying risk factors for re-recurrence. Sapuppo et al. demonstrated that 85.7% of patients with persistent disease were not cured by their last visit due to incomplete initial treatment, whereas patients with recurrent disease had better outcomes (7). Compartment-oriented central neck dissection is essential to minimize the need for secondary surgical intervention (11). A considerable number of patients were found to have subclinical LN metastases following initial surgery in clinically node-negative PTC (12). In the present study, patients who underwent total thyroidectomy without LN dissection were excluded due to the potential presence of subclinical LN metastases, which could hinder accurate assessment of nodal status. Additionally, patients who underwent lobectomy alone were excluded to avoid the confounding effect of occult thyroid cancer (13). Therefore, this study specifically included patients who underwent prophylactic or therapeutic central neck dissection, allowing for accurate evaluation of LN status after the initial surgery and subsequent reoperation.

Given that minimal extrathyroidal extension does not affect disease-related survival, it is excluded from T3 classification in the American Joint Committee on Cancer (AJCC) 8^th edition. Moreover, recurrence has not been reported in cases where anterior extrathyroidal extension was confined to perithyroidal fat tissue or strap muscles (14). Primary tumor invasion into adjacent structures beyond the strap muscles at initial surgery is a significant prognostic factor for recurrence and contributes to re-recurrence despite optimal reoperation (15). In our analysis, T4a stage at initial surgery emerged as a significant predictor of re-recurrence, whereas the presence of gross extrathyroidal extension did not reach statistical significance. Therefore, our results support the rationale behind the AJCC 8^th edition’s refined T staging system as a more meaningful criterion than gross extrathyroidal extension alone in T classification.

RAI therapy showed limited therapeutic efficacy in patients with persistent or recurrent disease, even among those with RAI-avid lesions (16-18). While surgery remains the cornerstone of treatment, a multidisciplinary approach is crucial due to the increased risk of complications following multiple reoperations (19-21). A study evaluating long-term outcomes after surgical resection for recurrent or persistent metastatic LN in PTC demonstrated that patients with an excellent response, regardless of the number of reoperations, did not develop either structural or biochemical evidence of recurrence (9). Therefore, considering the potential risks and benefits associated with multiple surgical interventions, a careful and individualized assessment of surgical extent should be conducted prior to the initial operation and subsequent reoperations.

Ultrasonography is the primary imaging modality for detecting thyroid nodules and LNs preoperatively, as well as for assessment during postoperative surveillance. However, interpretation of ultrasonography can vary between operators, potentially impacting clinical decision-making. Guidelines suggest an appropriate size threshold for recurrent lesions as >8 mm for central LNs and >10 mm for lateral LNs (4). Conversely, some authors have proposed larger size criteria for recurrent central LNs, taking into account surgical morbidity and therapeutic outcomes (22). The biochemical complete response rates following reoperation ranged from 20% to 66% (23). Overall survival rates for patients with biochemical evidence of disease and persistent disease were 100% and 85%, respectively (24). Aligned with our study objectives, we thoroughly reviewed the initial and subsequent postoperative ultrasonographic and CT images of patients undergoing reoperation, identifying abnormalities in several cases. Consequently, our institution proceeded cautiously with reoperation, even when recurrent lesions were smaller than guideline recommendations, emphasizing the importance of surgical expertise and careful clinical judgement. All operations for enrolled patients in this study were performed at our institution.

Previous studies identified various predictive factors for re-recurrence. A study of 232 patients who received their first reoperation for persistent or recurrent PTC found that age at reoperation ≥55 years, recurrent tumor size >4 cm, and the number of recurrent LNs ≥10 were associated with worse recurrence-free survival (25). Based on these findings, the authors proposed a revised risk stratification model incorporating these prognostic factors to better predict re-recurrence. The study identified post-reoperative unstimulated Tg >10.1 ng/mL and metastatic LNs with extranodal extension as independent predictors of re-recurrence in PTC (26). They also demonstrated that surgical intervention should be considered with discretion for patients with RAI-avid lesions, because squamous differentiated component in recurrent cervical LN specimens were detected in some patients who had been exposed to repeated empirical RAI therapy. Lee et al. demonstrated that a post-reoperative stimulated Tg level <1 ng/mL was the only predictive factor for re-recurrence in patients with recurrent or persistent PTC (27). Additionally, Lamartina et al. identified age ≥45 years, aggressive histologic subtype, and LNR ≥0.6 at the initial surgery were risk factors for biochemical or structural incomplete responses after the first reoperation (28). Park et al. demonstrated that LNR ≥0.15 was an independent predictor of decreased re-recurrence-free survival in recurrent thyroid carcinoma (29). Notably, these previous studies included heterogeneous populations, such as patients who underwent thyroid lobectomy or those who did not undergo central neck dissection at the initial operation. Furthermore, some studies incorporated patients with true recurrence or persistent disease. In contrast, the present study involved a rigorous review to identify risk factors related to re-recurrence following total thyroidectomy and LN dissection in patients who initially achieved a disease-free status.

The present study has several limitations. First, this retrospective study was conducted at a single institution with a small sample size. Second, although the management of patients remained consistent, the outcomes of initial operations and reoperations for enrolled patients could have been influenced by different surgeons. Third, most patients in this study had classical PTC. Therefore, we did not analyze PTC subtypes or aggressive variants. Fourth, oncogenic mutations, such as BRAF^v600E and the telomerase reverse transcriptase promoter, were not evaluated due to incomplete data collection. Further studies with a sufficient number of cases are needed to validate our results.

Conclusions

Reoperations in the neck due to PTC can be challenging. The present study found that T4a stage and unstimulated maximal Tg >1 ng/mL were associated with a high rate of re-recurrence in patients with PTC who underwent total thyroidectomy and central neck dissection with or without lateral neck dissection as the initial operation. Short-term follow-up with appropriate imaging modalities is necessary for patients with T4a stage disease and those with elevated Tg levels after the first reoperation for PTC.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-189/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-189/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-189/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-189/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 Chonnam National University Hwasun Hospital (No. CNUHH-2025-053). The need for informed consent from patients 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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