The influence of clinically suspected metastatic lymph node distribution on occult metastasis and recurrence in papillary thyroid carcinoma

Introduction

Papillary thyroid carcinoma (PTC) represents the most prevalent endocrine malignancy (1,2), with clinical N1 disease present in approximately 30% of cases (3). The 2015 American Thyroid Association (ATA) guidelines recommend therapeutic lateral neck dissection (typically encompassing levels II to IV) for patients with clinically confirmed lateral lymph node metastasis (LNM) (cN1b) regardless of the distribution of these lymph nodes (4). Recent advances in the understanding of thyroid cancer have led to a paradigm shift toward more conservative therapeutic strategies. The feasibility of reducing the extent of lymph node dissection has become a subject of active clinical debate (5).

Comparative studies have demonstrated that selective neck dissection (SND), which involves the resection of selective nodal levels, achieves comparable oncologic outcomes to comprehensive neck dissection and is now widely accepted. More recently, super-selective neck dissection (SSND) has been proposed as a further refinement, aiming to reduce surgical morbidity by limiting the extent of nodal resection while maintaining oncologic safety (6-8). SSND refers to the surgical excision of all fibroareolar tissue within no more than two contiguous cervical levels. Kim et al. reported no recurrence in 34 PTC patients with suspicious lateral neck nodes undergoing SSND during 31.6-month follow-up (9). Liang et al. demonstrated comparable short-term outcomes between SND and SSND in PTC patients, with no significant differences in overall complication rates (23.8% vs. 23.3%), regional recurrence (14.2% vs. 16.7%), or reoperation rates (16.7% vs. 17.4%) (10). The ongoing debate persists owing to the lack of high-level evidence to determine which surgical strategy maximizes patient benefit.

The primary aim of the present study was to evaluate the diagnostic performance of preoperative imaging in detecting lymph node metastases in the lateral neck compartments (levels II–V) among cN1b PTC patients. Secondary aims included: (I) characterizing the spatial distribution patterns of lymph node metastases; and (II) analyzing the influence of imaging-detected metastatic patterns on prognosis. Our findings may refine current surgical strategies by clarifying the optimal extent of therapeutic neck dissection, thereby providing an evidence-based rationale for selective versus comprehensive nodal excision. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-1-581/rc).

Methods

Data source and study cohort

This retrospective cohort study analyzed data from adult patients diagnosed with unilateral cN1b PTC between January 2000 and December 2017 at Cancer Hospital, Chinese Academy of Medical Sciences. Exclusion criteria included levels II–IV nodal metastasis or isolated level V nodal metastasis on imaging, pN0 and pN1a disease, neck dissection encompassing less than levels II–IV, anatomically unclassified lymph nodes, lymph node metastases originating from non-PTC malignancies, distant metastasis, incomplete critical data [e.g., extranodal extension (ENE) status, primary tumor size, or location], and lost to follow up (less than 12 months). Participants were stratified into three groups based on ultrasound/computed tomography (CT)-assessed lateral cervical LNM patterns: solitary, single-level multiple, and the multi-level groups. This study received approval from the Ethics Committee of the Cancer Hospital, Chinese Academy of Medical Sciences. Written informed consent was secured from all participants during preoperative procedures, explicitly authorizing the potential utilization of anonymized medical records for research purposes.

Demographic data (e.g., age, sex) were retrieved from clinical records. Preoperative ultrasound mapped suspicious nodes using malignancy criteria: microcalcifications, cystic changes, hyperechoic foci, peripheral vascularity, round shape, irregular margins, loss of fatty hilum, heterogeneous echotexture (5). For CT evaluation, suspicious metastatic lymph nodes were defined according to National Comprehensive Cancer Network (NCCN)-referenced imaging criteria (11,12). Radiologic ENE (rENE) was defined as interruption of the hyperechoic capsule with ill-defined borders. Lateral neck levels were classified via American Head and Neck Society (AHNS) guidelines (13). Once lateral neck metastasis was confirmed by fine-needle aspiration biopsy or intraoperative frozen pathology, therapeutic lateral neck dissection (at least levels II–IV) was conducted for metastatic disease, with inclusion of level V if metastases were clinically confirmed in this compartment. Decisions on the extent of surgery were at the discretion of the treating physician, with consideration for the patient’s preference. Primary tumor sizes, metastatic lymph node sizes, and the presence of Hashimoto’s thyroiditis were confirmed through postoperative histopathological evaluation. The ENE and gross extrathyroidal extension (gETE) were identified on surgical findings. Tumor staging was performed according to the eighth edition American Joint Committee on Cancer staging system.

Postoperative treatments included conventional thyrotropin suppression at appropriate levels and radioactive iodine (RAI) ablation. Physical examinations, thyroid function tests, neck ultrasound, and CT or chest radiography were performed regularly every 6 months within the first 5 years and every 12 months thereafter. Local recurrence was defined as disease recurrence within the thyroid bed or residual thyroid tissue, while regional recurrence referred to disease within the central or lateral cervical lymph nodes. Both local and regional recurrences were classified as structural recurrence, which was detected via ultrasonographic or CT imaging, followed by pathological confirmation. Distant metastases were diagnosed based on CT or emission computed tomography (ECT) imaging criteria. Overall recurrence includes both structural recurrence and distant metastasis. Survival data were extracted from institutional medical records combined with systematic follow-up calls.

Statistical analysis

Categorical variables were expressed as frequencies analyzed by Pearson’s Chi-squared test. Heatmap visualization was used to present spatial distribution patterns of cervical LNM. The diagnostic performance of preoperative imaging was evaluated by calculating sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) for each level, with 95% confidence intervals (CIs) calculated using the Wilson score method. Survival was estimated by the Kaplan-Meier method. Cox proportional-hazards regression analyses were conducted to assess associations between clinicopathological characteristics and recurrence-free survival (RFS). The results were expressed as relative ratios [hazard ratios (HRs)] accompanied by their corresponding 95% CIs. Statistical analyses were conducted using SPSS (Version 27.0), with a two-tailed P value <0.05 considered significant.

Results

Clinicopathological characteristics of enrolled patients

A total of 1,574 cN1b PTC patients were initially identified. After rigorous exclusion criteria were applied, 729 patients comprised the final cohort (Figure 1). The cohort demonstrated a female predominance (68.2%), with most patients aged ≤55 years (87.5%). Imaging evaluation revealed a low overall incidence of rENE (5.1%), with most metastatic lymph nodes measuring 1–3 cm in diameter (62.6%). Surgical interventions included total thyroidectomy (TT) in 63.6% of cases. Primary tumors were predominantly 1–2 cm (46.0%), with frequent multifocality (50.3%) and coexisting Hashimoto thyroiditis (22.5%). Patients were stratified into three groups according to lymph node distribution: the solitary metastasis group (n=159), the single-level multiple metastases group (n=276), and the multi-level metastases group (n=294). The solitary metastasis group exhibited the highest rate of no central LNM (21.4%), which was notably higher than that in the single-level multiple metastasis group (7.6%) and the multi-level metastases group (9.9%) (P<0.001). Other baseline characteristics showed no significant difference among the three groups (P>0.05) (Table 1).

Figure 1 Flowchart of patient inclusion and exclusion. LN, lymph node.

Spatial distribution patterns of cervical LNM

Heatmap illustrates the correspondence between imaging-suspected metastatic lymph node levels (rows) and pathologically confirmed metastatic levels (columns), with numeric values representing the count of the matched cases (Figure 2). Intergroup analysis revealed significantly higher level IV metastatic involvement in single-level multiple metastases cases (81.9%) than in solitary metastasis cases (55.3%), with reduced involvement in level II (12.6% vs. 4.0%) and level III (32.1% vs. 14.1%). The imaging-indicated levels exhibited a significantly higher number of pathologically confirmed metastases compared to other anatomical areas. Furthermore, the metastatic burden demonstrated a spatially decreasing gradient pattern, with higher metastatic density observed in adjacent anatomical regions surrounding the imaging-identified zones. Notably, a more evident decreasing trend in regional metastasis was observed in the solitary metastasis group compared with the single-level multiple metastases group, and across all three groups, level V consistently showed the lowest incidence of metastatic involvement.

Figure 2 Spatial distribution patterns of cervical lymph node metastases. Heatmaps display the correspondence between preoperative imaging-suspected metastatic lymph node levels (rows) and postoperative pathologically confirmed metastatic levels (columns) in the solitary metastasis group (A), single-level multiple metastases group (B), and multi-level metastases group (C). Numeric values represent the count of cases with pathologically confirmed metastasis at each level, with darker shades indicating higher counts. For example, (A) among 88 patients with imaging-suspected level IV metastasis, 42 had occult level II metastases.

Diagnostic performance of preoperative imaging in metastatic lymph nodes

The metastatic rates and overall diagnostic performance of preoperative imaging for levels II–IV are presented in Table 2. Among cases with imaging-suspected solitary level III metastasis, the NPVs for level II and IV involvement was 49.0% and 47.1%, respectively. For multiple level III metastases, the NPVs were 41.0% (level II) and 30.8% (level IV). In cases with imaging-suspected solitary level IV metastasis, pathological analysis demonstrated an NPV of 52.3% for level II and 33.0% for level III. Similarly, in multiple level IV metastases, the NPVs were 55.8% (level II) and 28.8% (level III). In patients with combined imaging-suspected level III–IV metastases, the NPV for level II involvement was 51.7% (Table 3). These findings suggest that preoperative imaging may underestimate the risk of metastasis in adjacent nodal levels.

Association between imaging-suspected metastatic lymph node level and prognosis

The median duration of follow-up for the entire study population was 52 months (range, 4–181 months), with no statistically significant difference observed among the comparison groups (P=0.21). Kaplan-Meier analysis showed no statistically significant differences in unadjusted 5-year RFS between patients with solitary, single-level multiple, and multi-level metastases groups, both for 5-year overall RFS rate (solitary: 91.4% vs. single-level multiple: 90.5% vs. multi-level: 89.5%, log-rank P=0.71; Figure 3A) and regional RFS (solitary: 93.0% vs. single-level multiple: 91.4% vs. multi-level: 90.0%, log-rank P=0.67; Figure 3B). After adjusting for sex, age, size of metastatic lymph node, rENE, extent of surgery, ENE, primary tumor size, Hashimoto’s thyroiditis, multifocality, central LNM, and bilateral tumor involvement, preoperative imaging-suspected lymph node distribution showed no independent association with either overall recurrence (single-level multiple metastases group: HR =1.32, 95% CI: 0.68–2.57, P=0.42; multi-level group: HR =1.30, 95% CI: 0.66–2.55, P=0.44) or regional recurrence (single-level multiple metastases group: HR =1.27, 95% CI: 0.61–2.62, P=0.52; multi-level group: HR =1.33, 95% CI: 0.65–2.74, P=0.44) (Figure 3C,3D).

Figure 3 RFS analysis in the study cohort. (A) Unadjusted overall RFS. (B) Unadjusted regional RFS. (C) Overall RFS after adjusting for other prognostic factors. (D) Regional RFS after adjusting for other prognostic factors. RFS, recurrence-free survival.

Discussion

This cohort study retrospectively analyzed 729 cN1b PTC cases treated with lateral neck dissection. Our findings showed that levels III and IV were the main areas where metastases occurred, while level V exhibited the lowest metastatic involvement rates. The metastatic burden displayed a distinct spatial gradient pattern, with higher metastatic density observed in anatomical regions surrounding the imaging-identified zones. Although this pattern of metastatic spread supports biological plausibility for super-selective surgical strategies, the results revealed that compared to preoperative imaging assessments, postoperative pathological analysis of levels II, III, and IV demonstrated significantly high rates of residual occult metastases. Further survival analysis indicated that neither single-level nor multi-level involvement detected by imaging had a significant impact on 5-year RFS or regional RFS (P>0.05).

Given the characteristics of PTC, including its high incidence, relatively indolent biological behavior, and tendency toward cervical lymph node dissemination (2,14,15), the ATA guidelines recommend therapeutic lateral neck dissection for patients with biopsy-proven metastatic involvement, although the precise extent of dissection is not clearly defined (4,5). Previous investigations consistently indicate that levels III and IV are the most common metastatic sites (16,17), which aligns with our findings. A meta-analysis of 18 studies reported metastatic rates of 71% for level III and 66% for level IV among PTC patients presenting with clinically evident disease (14). Consequently, routine dissection of levels III and IV is generally regarded as indispensable in the management of cN1b patients. Consistent with our data, level V exhibits the lowest incidence of metastatic frequency across the lateral compartments (18). Moreover, resection of level V has not been shown to confer survival or recurrence benefits but is frequently accompanied by increased shoulder-related morbidity (19,20). These studies suggested that level V dissection should be reserved for cases with confirmed or radiologically suspected metastasis based on preoperative evaluation (16).

The therapeutic management strategy for level II is still under debate. Some surgeons propose omitting prophylactic level II dissection based on imaging evaluation under specific clinical conditions (e.g., preoperative ultrasound shows no suspicious level III nodes) (21). However, ultrasonography demonstrates limited sensitivity (<60%) in detecting metastatic lymph nodes across levels II–IV during preoperative evaluation (22,23). Level II also represents a frequent site of metastasis in PTC, particularly for tumors located in the upper lobe or larger than 1 cm (24). Several studies have indicated comparable metastatic rates between levels II and III/IV during lateral neck dissection, with reported level II metastasis rates ranging from 53.4% to 56.9% across different series (14). Some argue that SSND may be considered when preoperative imaging identifies either solitary level III–IV nodal metastasis with a non-upper lobe primary tumor or isolated level IV involvement without radiologic macroscopic extension. This approach is supported by evidence showing that SSND and SND yield comparable short-term outcomes in terms of complications, recurrence, and reoperation rates. Notably, current proposals for superselective dissection remain primarily based on single-center, small-sample retrospective analyses, with conclusions yet to be validated by higher-level evidence (23,25). Our evaluation of the diagnostic performance of preoperative imaging for metastatic lymph nodes further revealed that the NPV for level II metastases were low (41–56%) across all subgroups lacking imaging evidence of involvement. Even in cases where ultrasound detected metastases confined to level IV, the NPV for level II reached merely 52%, indicating a substantial 48% probability of occult metastases. While SSND of levels III–IV improves cosmetic outcomes and reduces costs, it may increase long-term morbidity due to elevated risks of persistent or recurrent disease in level II (6,26). When regional recurrence occurs, salvage surgery for recurrent nodal disease is associated with an elevated risk of postoperative complications and increased healthcare expenses (21). Despite ongoing efforts to enhance preoperative diagnostic accuracy for cervical LNM in PTC, including the development of artificial intelligence-assisted models (27), there are still no reliable biomarkers capable of predicting occult metastasis in level II. Collectively, overly conservative modification of lateral neck dissection in cN1b patients may compromise therapeutic efficacy. Our findings, demonstrating occult level II metastases in 41–56% of patients, provide further evidence for this concern. Although RFS did not differ significantly among groups, all patients underwent comprehensive dissection, which may have mitigated the oncologic consequences of occult disease. Therefore, the selection of SSND in cN1b patients warrants careful consideration.

Nevertheless, there are several limitations in this study. First, as a retrospective single-institution study, the generalizability of our findings is inherently limited, underscoring the necessity for standardized multicenter prospective controlled trials for validation. Second, given the long inclusion period [2000–2017], advances in ultrasound and CT technology as well as evolving radiologic criteria for LNM may have influenced detection sensitivity, potentially affecting occult metastasis rates and imaging-based subgroup classification. Third, the 2015 ATA guidelines suggested that TT and neck dissection should be performed for cN1b PTC patients. However, the main principle of surgery in Cancer Hospital, Chinese Academy of Medical Sciences during the study period was to completely remove the tumor. A considerable number of patients in our study were treated with lobectomy and neck dissection. According to previous studies, lobectomy exhibited a similar prognosis to TT (28-30). Fourth, the feasibility of SSND is discussed based on the occult metastasis, which does not mean clinical recurrence in PTC.

Conclusions

Our results indicate that limited neck dissection confined to levels III–IV may be associated with a substantially increased risk of residual occult nodal disease, even in patients with clinically solitary metastasis. Large-scale prospective studies are warranted to evaluate the long-term prognostic significance of selective dissections involving levels II and V and to optimize surgical decision-making.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-1-581/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-1-581/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-1-581/prf

Funding: The study was funded by the National Natural Science Foundation of China (No. 82372893) and the CAMS Innovation Fund for Medical Sciences (No. 2024-I2M-C&T-B-060) for data collection and analysis.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-1-581/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 approved by the Ethics Committee of the Cancer Hospital, Chinese Academy of Medical Sciences. Written informed consent was secured from all participants during preoperative procedures, explicitly authorizing the potential utilization of anonymized medical records for research purposes.

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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