Abstract
This study aimed to determine whether lobectomy is appropriate for the long-term prognosis of 1–4-cm-sized differential thyroid cancer (DTC). This retrospective study included 2,178 patients with 1–4-cm DTC treated via thyroid lobectomy (LT) or total or near-total thyroidectomy (TT) and who were followed up for at least 3 years. The primary endpoint was a structural incomplete response, which was confirmed via imaging with or without a positive histological or cytological examination. Subgroup analysis was performed according to tumor size. LT was performed in 1,535 patients (70.48%), and TT was conducted in the remaining 643 (29.55%) patients. During an average follow-up period of 48.08 months, the recurrence rate was 7.2% in the LT group and 5.3% in the TT group, which was not significantly different (p = 0.108). There were no significant differences in disease-free survival between both groups (hazard ratio, 1.394; 95% confidence interval, 0.9761–1.990; p = 0.089). In the subgroup analysis, the recurrence rates in the LT group were higher than those in the TT group for both the 2–3-cm (13.6% vs. 2.6%, p < 0.01) and 3–4-cm categories (20.6% vs. 4.8%, p < 0.01). For 1–2-cm DTC, surgeons can choose LT or TT owing to their similar recurrence rate, whereas for 2–4-cm DTC, TT is preferred.
Keywords: Differentiated thyroid carcinoma, Recurrence, Lobectomy, Thyroidectomy
Subject terms: Surgical oncology, Thyroid diseases
Introduction
Thyroid cancer is the most common malignant tumor of the endocrine system in humans, and its incidence has increased worldwide in recent decades1. In China, the growth rate of thyroid cancer is 20% per year, ranking it 7th in terms of malignancy and 4thamong female malignant tumors2. Thyroid cancer originates from thyroid follicular or parafollicular epithelial cells, and the most common type is differentiated thyroid cancer (DTC), including papillary thyroid cancer (PTC) and follicular thyroid cancer (FTC), which account for more than 90%3,4.
Treatment for DTC includes procedures such as surgery, radioiodine therapy, and thyrotropin suppression5–7. Among these, surgery is the most important treatment for DTC and directly affects the subsequent treatment and follow-up methods8. The traditional surgical method is total or near-total thyroidectomy (TT). The American Thyroid Association 2015 edition guidelines (ATA2015) cite some trial results and suggest that patients with high-risk tumors should undergo TT, while patients with low-risk DTC ≤ 4 cm should undergo smaller-scale surgery, such as thyroid lobectomy (LT)9. For patients with a tumor size of 1–4 cm, the guidelines state that either TT or LT can be performed.
Since the trial results were released, LT has been widely used in the treatment of thyroid cancer, especially in patients with tumors measuring < 1 cm10,11. However, to date, the selection of surgical method for 1–4-cm DTC remains controversial. Some studies have suggested that the efficacy of 1–4-cm DTC in patients who underwent LT or TT was similar, while the incidence of surgical complications was lower and surgical damage was smaller in the former than in the latter12,13. Compared to LT, TT can improve the survival rate of patients and reduce the risk of recurrence8,14.
Currently, there is a lack of large-sample studies in China in this area; therefore, we conducted a retrospective study to evaluate the recurrence data of 1–4-cm thyroid cancer.
Methods
This retrospective cohort study included 2,178 patients with thyroid cancer who were admitted to the Second Affiliated Hospital of Soochow University Hospital between 2016 and 2020. This retrospective study was approved and the informed consent was waivered by the Ethics Committee of the the Second Affiliated Hospital of Soochow University Hospital (approval number: JD-LK2023067-I01) and was performed in accordance with appropriate guidelines. The The inclusion criteria were as follows: (1) patients pathologically diagnosed with differentiated thyroid cancer, (2) age > 18 years, (3) lesion diameter between 1 and 4 cm, and (4) patients undergoing surgery for the first time. The exclusion criteria were as follows: (1) patients who underwent contralateral surgery within one year after LT; (2) patients with distant metastasis detected by preoperative imaging examination; (3) patients with high-risk factors according to the ATA 2015 edition guidelines; and (4) follow-up time of < 3 years.
Surgical method
The surgical method was selected based on the preoperative assessment of the patient based on a clinician’s assessment, the condition of the disease, and the patient’s preferences. The surgical methods were divided into the LT and TT groups. The LT group underwent lobectomy with or without isthmectomy, whereas the TT group underwent total or TT. Prophylactic central compartment neck dissection was performed according to the surgeon’s experience, combined with the imaging characteristics of the thyroid nodules and intraoperative frozen pathology. Therapeutic central compartment neck dissection or modified radical neck dissection was performed if cervical lymph node metastasis was detected intraoperatively or preoperatively. For patients with lymph node metastasis during the primary surgery or multifocal disease found in pathology and who have only undergone LT surgery, considering various factors for optimizing treatment and avoiding unnecessary trauma, close follow-up was chosen instead of immediate re-operation. All patients received thyroid hormone suppression therapy postoperatively.
Postoperative follow-up endpoint
The primary endpoint of the study was structural incomplete response (SIR), which was confirmed via imaging examinations, such as ultrasound, computed tomography, and whole-body scan, with or without positive histological or cytological findings. The interval between the initial surgery and the discovery of SIR (disease-free survival; DFS) was compared. Other collected indicators included tumor size, intraoperative blood loss, operation time, hospital stay, and hospitalization costs. The cohort was divided into two groups according to the extent of surgery: patients who underwent LT and those who underwent TT. The demographic and pathological results and DFS of the two groups were compared. To calculate the recurrence rate and DFS stratified by tumor size, each group was divided into three subgroups according to the size of the tumor based on pathological results: 1–2, 2–3, and 3–4 cm.
Statistical analysis
Continuous variables were presented as means with standard deviations and analyzed using the Mann–Whitney U test and Student’s t-test. Descriptive statistics are expressed as n (%). Categorical variables are presented as numbers with percentages and were analyzed using Pearson’s test. DFS curves were plotted using the Kaplan–Meier method, and significance was determined using the log-rank test. Cox proportional hazard regression analysis was used to assess the risk of recurrence. Univariate and multivariate logistic regression models were used to identify the factors associated with the risk of recurrence. A p-value < 0.05 was considered statistically significant. Subgroup analysis was performed according to tumor size.
Results
Baseline characteristics
A total of 2,178 patients with a mean age of 41.68 ± 12.88 years were enrolled in this study. Of them, 1,636 (75.11%) were women, 1,535 (70.48%) underwent lobectomy, and 643 (29.55%) underwent TT. Regarding the pathological type, 2,099 patients (96.37%) had PTC, and 79 (3.63%) had FTC. Compared with the LT group, patients in the TT group have a higher prevalence of multifocality(28.9% vs. 14.9%, p < 0.01). The mean follow-up time was 48.08 ± 6.87 months.
The detailed clinical data of both groups are shown in Table 1. The tumors in the TT group were significantly larger than those in the LT group (2.16 ± 0.60 cm vs. 1.76 ± 0.66 cm, p < 0.01). The total hospitalization cost (15,118.62 ± 3,707.01 yuan vs. 17,289.51 ± 3,099.75 yuan; p < 0.01) and hospital stay (6.20 ± 1.46 days vs. 7.09 ± 1.86 days, p < 0.01) in the LT group were significantly lower than those in the TT group. Radioactive iodine(RAI) therapy exhibited significant difference between the two groups, since it was only conducted in the TT group. In postoperative complications, the LT group had a significantly lower incidence than the TT group(8.7% vs. 15.7%, p < 0.01). Hoarseness was the main complication in both group, while hypocalcemia was more frequent in the TT group.
Table 1.
Baseline characteristics of the study patients.
|
Total (n = 2,178) n (%) |
LT (n = 1,535) n (%) |
TT (n = 643) n (%) |
p-value | |
|---|---|---|---|---|
| Mean age (years) | 41.68 ± 12.88 | 41.73 ± 12.89 | 41.55 ± 12.88 | 0.770 |
| Sex | ||||
| Male (%) | 542 (24.9) | 390 (25.4) | 152 (23.6) | 0.353 |
| Female (%) | 1636 (75.1) | 1145 (74.6) | 491 (76.4) | |
| Tumor pathology | ||||
| PTC (%) | 2099 (96.4) | 1476 (96.2) | 623 (96.9) | 0.067 |
| FTC (%) | 79 (3.6) | 59 (3.8) | 20 (3.1) | |
| Primary tumor size: cm | ||||
| Mean | 1.86 ± 0.64 | 1.74 ± 0.62 | 2.16 ± 0.60 | < 0.01 |
| 1–2 (%) | 1663 (76.4) | 1236 (80.5) | 427 (66.4) | < 0.01 |
| 2–3 (%) | 389 (17.9) | 236 (15.4) | 153 (23.8) | |
| 3–4 (%) | 126 (5.8) | 63 (4.1) | 63 (9.8) | |
| Multifocal Disease | 414(19.0) | 228(14.9) | 186(28.9) | < 0.01 |
| Mean lymph node count | 2.74 ± 1.63 | 2.74 ± 1.64 | 2.73 ± 1.61 | 0.928 |
| Mean follow-up period: months | 48.08 ± 6.87 | 48.00 ± 6.90 | 48.26 ± 6.81 | 0.408 |
| Mean intraoperative hemorrhage: mL | 5.93 ± 2.58 | 5.95 ± 2.56 | 5.89 ± 2.64 | 0.601 |
| Mean total hospitalization costs: Yuan | 15,759.52 ± 3673.92 | 15,118.62 ± 3707.01 | 17,289.51 ± 3099.75 | < 0.01 |
| Mean days of hospitalization: Days | 6.47 ± 1.64 | 6.20 ± 1.46 | 7.09 ± 1.86 | < 0.01 |
| Recurrence patients | 144 (6.6) | 110 (7.2) | 34 (5.3) | 0.108 |
| RAI administration | 108(5.0) | 0 | 108(16.8) | < 0.01 |
| Complications | 235(10.8) | 134(8.7) | 101(15.7) | < 0.01 |
| Hoarseness | 146(6.7) | 89(5.8) | 51(7.9) | |
| Hypocalcemia | 58(2.7) | 26(1.8) | 37(5.8) | |
| Others | 31(1.4) | 18(1.2) | 13(2.0) | |
FTC: follicular thyroid cancer; LT: thyroid lobectomy; PTC: papillary thyroid cancer; TT: total or near-total thyroidectomy; RAI: radioactive iodine.
Primary outcomes
According to the follow-up results, there was no significant difference in the recurrence rate between both groups (7.2% vs. 5.3%, p = 0.108). Among those who had recurrence, there were no significant differences between both groups in terms of sex, age, tumor type, tumor size, or lymph node number (Table 2). The recurrence time of the LT group was significantly earlier than that of the TT group (28.54 ± 7.87 months vs. 35.49 ± 6.65 months, p = 0.001). The main recurrence site was the cervical lymph nodes (69.4%), followed by contralateral metastasis (only in the LT group, 22.2%) and lung metastasis (7.6%).
Table 2.
Characteristics of patients with recurrence.
|
Total (n = 144) n (%) |
LT (n = 110) n (%) |
TT (n = 34) n (%) |
p-value | |
|---|---|---|---|---|
| Mean age (years) | 41.67 ± 11.95 | 41.98 ± 12.11 | 40.65 ± 11.52 | 0.571 |
| Sex | ||||
| Male (%) | 29 (20.1) | 22 (20.0) | 7 (20.6) | 0.940 |
| Female (%) | 115 (79.9) | 88 (80.0) | 27 (79.4) | |
| Tumor pathology | ||||
| PTC(%) | 137 (95.1) | 106 (96.4) | 31 (91.2) | 0.440 |
| FTC(%) | 7 (4.9) | 4 (3.6) | 3 (8.8) | |
| Primary tumor size: cm | ||||
| Mean | 2.07 ± 0.71 | 2.06 ± 0.74 | 2.07 ± 0.59 | 0.961 |
| 1–2 (%) | 92 (63.9) | 65 (59.1) | 27 (79.4) | 0.064 |
| 2–3 (%) | 36 (25.0) | 32 (29.1) | 4 (11.8) | |
| 3–4 (%) | 16 (11.1) | 13 (11.8) | 3 (8.8) | |
| Mean lymph node count | 2.71 ± 1.685 | 2.67 ± 1.69 | 2.82 ± 1.53 | 0.643 |
| Mean recurrence period: months | 30.18 ± 8.14 | 28.54 ± 7.87 | 35.49 ± 6.65 | 0.001 |
| Recurrence site | ||||
| Contralateral (%) | 32 (22.2) | 32 (29.1) | 0 | |
| Cervical lymph nodes (%) | 100 (69.4) | 71 (64.5) | 29 (85.3) | |
| Lung (%) | 11 (7.6) | 7 (6.4) | 4 (11.8) | |
| Bone (%) | 1(0.7) | 0 | 1 (2.9) | |
| RAI administration | 11(7.6) | 0 | 11(32.4) | < 0.01 |
FTC: follicular thyroid cancer; LT: thyroid lobectomy; PTC: papillary thyroid cancer; TT: total or near-total thyroidectomy; RAI: radioactive iodine.
Recurrence analysis
There was no statistically significant difference in DFS between the two groups (hazard ratio [HR], 1.394; 95% confidence interval [CI], 0.9761–1.990; p = 0.089) (Fig. 1). The 3-year DFS of the LT group was lower than that of the TT group (p = 0.025), while the 5-year DFS was similar in both groups (p = 0.108). Univariate and multivariate analyses of DFS showed that the surgical method was not related to disease recurrence in the univariate analysis (HR, 0.718; 95% CI, 0.488–1.054; p = 0.091); however, the opposite result was observed in the multivariate analysis (HR, 0.617; 95% CI, 0.417–0.913; p = 0.016). Moreover, both univariate and multivariate analyses showed that tumor size was an important factor affecting disease recurrence (Table 3).
Fig. 1.
Disease-free survival (DFS) curve according to the groups. LT, thyroid lobectomy; TT: total or near-total thyroidectomy.
Table 3.
Impact of different factors on recurrent disease.
CI, confidence interval; FTC, follicular thyroid cancer; HR, hazard ratio; LT, thyroid lobectomy.
Subgroup analysis
The patients were stratified according to tumor size. The results showed no difference in disease recurrence rates between the two groups in the 1–2-cm category (5.3% vs. 6.3%, p = 0.407). However, in the LT group, the recurrence rates were higher than those in the TT group for both the 2–3-cm (13.6% vs. 2.6%, p < 0.01) and 3–4-cm categories (20.6% vs. 4.8%, p < 0.01). Similarly, there was no significant difference in DFS between both groups for 1–2-cm tumors (HR, 1.16; 95% CI, 0.741–1.823; p = 0.512); however, DFS was significantly lower in the LT than in the TT group for 2–3-cm tumors (HR, 0.181; 95% CI: 0.064–0.512; p = 0.001) and 3–4-cm tumors (HR, 0.193; 95% CI: 0.054–0.683; p = 0.011).
Discussion
For DTC without preoperative lymph node metastasis or evidence of extrathyroidal invasion, the current ATA guidelines recommend both LT and TT as acceptable initial surgical options9. Survival and overall survival are not affected by the mode of thyroidectomy15,16. However, this conservative choice of surgery results in a considerable proportion of patients having to undergo completion lobectomy after the initial surgical pathology results classify them as being at high risk of relapse postoperatively. Therefore, the optimal surgical option for 1–4-cm DTC has been a topic of debate.
Disease recurrence is not related to the type of thyroid cancer surgery12,13. However, in a previous study involving 16,057 patients, those who underwent LT had a higher recurrence rate than did those who underwent TT (9.4% vs. 5.7%; p = 0.001), the DFS of LT was lower than that of TT (p= 0.007), and on multivariate analysis, the extent of thyroidectomy was an independent risk factor for DFS14. Compared with other studies, our study mainly included patients admitted after 2016. At this stage, owing to the release of the ATA2015, surgeons gradually became accustomed to performing LT surgery. In our study, the LT group had significantly more patients than did the TT group, which was not the case in previous studies and is also consistent with the current situation. This study aimed to compare the long-term recurrence of 1–4-cm DTC, which was not statistically significant; however, the 2–4-cm subgroup analysis showed an HR value of 1.93. The National Cancer Database analysis also found that TT can improve the overall survival rate of patients with ≥ 2 cm compared with LT17.
The recurrence time of patients undergoing LT was significantly shorter than that of those undergoing TT; the reason might be that there were some patients with contralateral recurrence in the LT group. TT can effectively remove the primary lesion, reducing reoperation, recurrence, and metastasis rates. This was also the main reason why the 3-year DFS in the LT group was lower than that in the TT group (p = 0.025).
In this study, tumor size was an independent risk factor for DFS. In the multifactorial analysis, 2–3- and 3–4-cm tumors were approximately 1.845 times (95% CI: 1.250–2.722; p < 0.001) and 2.667 times (1.555–4.572) more likely to demonstrate recurrence than 1–2-cm tumors, respectively. Therefore, accurate preoperative measurement of the tumor is crucial for the surgical effect in patients with 1–4-cm DTC and should be used to determine the extent of thyroidectomy. Moreover, the baseline tumor sizes in both groups were not balanced, which may be related to the clinical judgment of the surgeon; when the tumor is large, the surgeon tends to choose conservative TT.
Patients with DTC have an extremely high survival rate postoperatively, and improving their quality of life is particularly important. Thyroid lobectomy has been associated with a lower incidence of surgical complications, such as hypocalcemia and hoarseness in our study, which is also an important reason for the promotion of LT-type surgery18,19. Unfortunately, we did not collect data on postoperative quality of life. However, when comparing hospitalization costs and times, the LT group was significantly better than the TT group. Lang et al. found that, compared to TT, LT is a lower-cost and more beneficial choice, which is consistent with the results of our study20.
The study had a few limitations. The first and main limitation of this retrospective study is the selection bias; all study participants were from a large hospital, but the same operator did not perform their surgeries, and the experience and technical differences could not be verified and excluded, which may have had some impact on the results of the study. Second, our study center did not have an independent nuclear medicine department, which resulted in a lack of postoperative iodine treatment data. Third, although high-risk patients were excluded because of the high cost, they did not undergo BRAFor other gene testing, which may have led to the inclusion of some high-risk patients. Finally, because the patients selected for this study were all treated after 2016, the follow-up time was not sufficiently long. Although recurrence of differentiated thyroid cancer usually occurs within 2 years postoperatively, a small number of patients experience recurrence after a longer period, even 5 years21. Ideally, an evaluation period of more than 5 years is required. Considering that patients with DTC have a relatively long survival period, the current follow-up duration is insufficient to evaluate the differences in survival time. We will continuously conduct follow-up and tracking in the hope of obtaining subsequent results.
Conclusions
In conclusion, for 1–2-cm DTC, surgeons can choose LT or TT because of their similar recurrence rates, while for 2–4-cm DTC, TT should be preferred.
Acknowledgements
We are grateful to colleagues who gave of their opinion and thank Yan Di for his thoughtful comments on the draft. Additionally, we would like to thank Editage (www.editage.cn) for English language editing. Finally, we thank my anonymous reviewers for helpful input on the manuscript.
Abbreviations
- ATA
American Thyroid Association
- CI
Confidence Interval
- DFS
Disease-free survival
- DTC
Differentiated thyroid cancer
- FTC
Follicular thyroid cancer
- HR
Hazard ratio
- LT
Thyroid lobectomy
- PTC
Papillary thyroid cancer
- SIR
Structural incomplete response
- TT
Total or near-total thyroidectomy
- RAI
Radioactive iodine
Author contributions
JX and QY acquisited data and wrote the draft of manuscript. JX and ZW analysised the data. ZW gave the primary thought. YL and WD played key leading roles in optimizing the research design, guiding data analysis, and coordinating result discussions, ensuring scientific and rigorous research progress and the paper’s quality. All authors read and approved the final manuscript.
Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
This study was approved by the Ethics Committee of the Second Affiliated Hospital of Soochow University Hospital (approval number: JD-LK2023067-I01). This retrospective cohort study included 2,178 patients with thyroid cancer who were admitted to the Second Affiliated Hospital of Soochow University Hospital between 2016 and 2020. Informed consent was waived owing to the retrorespective nature of the study.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Jun Xu and Qixian Yao are the co‐first authors.
Contributor Information
Wenhuan Dou, Email: 1024929909@qq.com.
Yujing Liu, Email: dybodiablo@163.com.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.