The impact of gasless insufflation transaxillary endoscopic thyroidectomy on the parathyroid gland injury in patients with thyroid cancer: a retrospective analysis

Introduction

The occurrence rate of the thyroid cancer tends to ascend in recent years (1). And papillary thyroid cancer (PTC) is the most common pathological type (2). Currently, surgery remains the primary treatment for PTC (3,4). In the late 1990s, Miccoli et al. introduced the minimally invasive video-assisted thyroidectomy (MIVAT) technique, which has demonstrated favorable safety outcomes (5,6). Compared with conventional open thyroidectomy (COT), endoscopic thyroidectomy (ET) has the advantages of smaller incision, reduced postoperative scar length and pain. With the advancement of endoscopic technology, different surgical approaches have emerged, including axillary, anterior chest, breast, posterior ear, and oral approach (7-13). Studies have shown that laparoscopy has the function of magnifying the field of view, which is beneficial for identifying and protecting the parathyroid gland (PG) and recurrent laryngeal nerves (RLNs) (14). However, both COT and ET have a risk of postoperative complications.

The most common complications after thyroid surgery are RLN injury and hypoparathyroidism (HPT) (15-17). As thyroid surgical procedures are continually evolving, we now have a clearer understanding of RLN structure, and intraoperative nerve monitoring (IONM) can accurately identify the RLN and effectively avoid damage during the anatomical process (18). PTC most commonly metastasizes to the central lymph node (CLN), with a reported metastasis rate of up to 50–70% (19), and metastasis may occur even in small diameter tumors (20). However, patients CLN dissection (CLND) are at higher risk of the PG blood supply injury or misresection, leading to a more significant occurrence of postoperative HPT (21,22). HPT is mainly manifested by a decrease in parathyroid hormone (PTH) levels. A decrease in PTH levels in the blood can lead to a decrease in serum calcium content, resulting in symptoms such as convulsions and numbness in the hands and feet. In severe cases, it can lead to breathing difficulty or even suffocation, affecting the patient’s quality of life (23). Scholars have proposed that selective parathyroid autotransplantation (PA) during thyroid surgery is one of the effective measures to avoid blood supply damage or misresection of PG (24). Although there are many methods to prevent postoperative HPT, correctly identifying PG during surgery is the best way to protect its function. Therefore, how to protect the PG of patients during thyroid surgery and reduce postoperative complications is a difficult and hot topic in clinical research.

At present, there are few reports on the mechanism of PG injury in gasless insufflation transaxillary endoscopic thyroidectomy (GTET). This study is based on unilateral thyroidectomy combined with CLND (4), using nanocarbon tracers “negative development” to protect PG, and using PTH immunocolloidal test paper to qualitatively characterize PG (25). When performing PA, the sternocleidomastoid muscle or pectoralis major muscle is selected as the transplantation site, and the transplantation is performed using the particle embedding method (26). Based on the above, this study aimed to explore the impact of GTET on PG injury, in order to provide a basis for the selection of PTC surgery methods. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-24-234/rc).

Methods

Clinical date

This retrospective study included 405 patients with PTC who were treated in the department of general surgery at the First Affiliated Hospital of Xiamen University from December 2022 to December 2023.

According to the surgical approach, the patients were divided into a GTET group (139 cases) and COT group (266 cases). Inclusion criteria were as follows: (I) patients fulfilling the diagnostic criteria for thyroid cancer; (II) patients with single-nodule thyroid cancer diagnosed pathologically; (III) patients with no lateral neck lymph node metastasis and distant metastasis in preoperative examinations; (IV) patients with cT1 or cT2; (V) patients consented by signing an informed consent form. Exclusion criteria were as follows: (I) patients with history of neck or axillary surgery or radiation; (II) combined with other organ function damage; (III) patients with preoperative disorder of calcium metabolism and/or parathyroid function; (IV) patients having incomplete follow-up data; (V) patients being unable to cooperate due to mental illness.

Clinical variable assessment

The observation indexes included the following: (I) comparison of general information was conducted between the two groups. (II) Comparing the incidence of PG injury and hypocalcemia between two groups. We defined PG injury as a serum PTH levels of less than 15 mg/mL. Serum calcium levels compared here are all serum calcium levels corrected for the Payne formula, hypocalcemia as the corrected serum calcium level of less than 2.1 mmol/L. All patients had serum calcium level measured before surgery, 1-day, 3-day, and 1 month after surgery. (III) Compare the surgical related indicators of two groups of patients, including operation time of surgery, postoperative bleeding, and postoperative totally drainage, and observe the incidence of postoperative complications in both groups. The complications include hoarseness, difficulty swallowing, and wound infection, etc. (IV) Univariate and multivariate logistic regression analysis of related variables was performed to analyze the risk factors of PG injury. (V) Analysis of PTH levels after PA.

Operative techniques

The injection method of nanocarbon suspension

All surgeries were performed by the same surgeon at our center. In order to better identify PG, nanocarbon suspension (1 mL:50 mg, China National Medicine Standard H20073246, Chongqing Laimei Pharmaceutical Co., Ltd., Chongqing, China) were injected into each patient 1 day before surgery. Take the traditional way, the steps are as follows (27): we utilized a 1 mL syringe to extract the nanocarbon suspension (1 mL:50 mg, in accordance with China National Medicine Standard H20073246, provided by Chongqing Laimei Pharmaceutical Co., Ltd.). Subsequently, the needle of the 1 mL syringe was substituted with a 2 mL syringe needle to preclude inadequate needle length. Under the guidance of ultrasound, the needle was inserted into the middle of the upper one-third portion of the thyroid gland, being cautious to avoid inserting it into the tumor and large blood vessels in the neck. Prior to injection, the plunger was pulled back to avert accidental injection of the suspension into a blood vessel. Then, 0.1 mL was slowly administered while gradually withdrawing the syringe while maintaining negative pressure. After that, the identical method was repeated to inject 0.1 mL of nanocarbon suspension into the lower one-third of the thyroid. In total, 0.2 mL of nanocarbon suspension was infused into the unilateral thyroid. If the tumor was situated at the intended injection site, the injection location was adjusted upward or downward depending on the actual circumstances.

The method of GTET

The patients were put in the supine position under general anesthesia with intratracheal intubation, the head tilted back and turned to the opposite side, and the patient’s upper limb on the side of surgery was abducted 90° to fully expose the axilla, neck, and bilateral areolae, then routine disinfection and draping were performed. An incision of 4 to 5 cm was made at the natural crease between the anterior axillary line and the midaxillary line on the affected side, the electrotome was detached under direct vision. The tissues were separated subcutaneously until reaching the surface of the pectoralis major muscle. A 5-mm trocar was positioned near the incision, approximately 2 to 3 cm from the breast edge. Separation was performed along the surface of the pectoralis major muscle in the direction of the thyroid. A retractor was utilized to aid in the separation process (Figure 1A). After separation, an endoscopic lens was inserted into the target area (Figure 1B). Identified and opened up the clavicular and sternal heads of the sternocleidomastoid muscle to reach the space. The operator adjusted the position of the retractor under endoscope and gradually transected. With the assistance of the endoscope, the thyroid lobe on the affected side was exposed. The peripheral blood vessels were separated. The peripheral blood vessels were dissociated. RLN (Figure 2A), PGs (Figure 2B), superior laryngeal nerve (Figure 2C), and superior thyroid artery (Figure 2D) were routinely identified and preserved. The thyroid lobe and isthmus were resected completely. Unilateral central neck dissection was performed routinely. The incision was rinsed. At the same time, hemostasis was performed and a negative pressure drainage tube was inserted. Subsequently, the wound was sutured.

Figure 1 GTET external display of surgical device and traction. (A) The device used by GTET. (B) The intraoperative operation layout and traction method for surgeons performing GTET. GTET, gasless insufflation transaxillary endoscopic thyroidectomy.

Figure 2 Important anatomical indicators during gasless insufflation transaxillary endoscopic thyroidectomy. (A) The white arrow points to lymph nodes stained with nanocarbon black. (B) The yellow arrow refers to the recurrent laryngeal nerve. (C) The green arrow points to the parathyroid glands. (D) The red arrow refers to the superior laryngeal nerve and the blue arrow refers to the superior thyroid artery.

The method of COT

After induction of general anesthesia, the patient was placed in the supine position. A 5- to 6-cm wound was made along the horizontal neck crease, which is located 2 cm above the sternoclavicular joint. The tissue was separated layer by layer, the thyroid gland was exposed. The thyroid lobe and isthmus were resected completely. Unilateral central neck dissection was performed routinely. The drainage tube was positioned, and the wound was stitched up.

The method of PA

During surgery, identifying each PG as much as possible and carefully preserving its blood supply to ensure that the PG was preserved in situ and had sufficient blood supply. When PG was cut off or unintentionally removed, the PTH immune gold technique was used to confirm parathyroid tissue. If confirmed, this PG would be chopped into 1 mm³ fragments and autografted. In the case of GTET, it was transplanted to the ipsilateral pectoralis major muscle, and in the case of COT, it was transplanted to the ipsilateral sternocleidomastoid muscle.

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of the First Affiliated Hospital of Xiamen University (No. XMYY-20022KYSB144) and individual consent for this retrospective analysis was waived.

Statistical analysis

Statistical analyses were performed using SPSS for Windows statistical software (ver. 27.0; SPSS Inc., Chicago, IL, USA). Measurement data are expressed as mean ± standard deviation (SD), and count data are expressed as percentages. The t-test was used for intergroup comparisons of measurement data, and the χ² test was used for intergroup comparisons of count data. Univariate analysis and logistic regression were used to identify factors associated with PG injury. The odds ratio (OR) and 95% confidence interval (CI) for each independent variable were calculated. P≤0.05 was regarded as a statistically significant difference.

Results

General information

A retrospective analysis was conducted on 405 patients diagnosed with PTC, including 139 cases (34.3%) treated with GTET and 266 case (65.7%) treated with of COT. There were no statistically significant differences in age, gender, body mass index (BMI), tumor location, tumor diameter, Hashimoto’s thyroiditis (HT), preoperative calcium level, and PTH level between the two groups of patients (P>0.05). General information was comparable in both groups (Table 1).

Incidence of PG injury

A total of 51 patients experienced PG injury, 7 patients (5.0%) in the GTET group and 44 patients (16.5%) in the COT group, with a statistically significant difference (P<0.001). Among them, the incidence of GTET group injured one PG was 50.4%, two were 2.9%, and COT group were 59.8% and 7.9%, respectively. The comparison of PG injuries showed statistical differences (P=0.006) (Table 2). Patients with parathyroid injury were temporary, and their PTH secretion returned to normal 1 month after surgery.

Postoperative serum calcium and PTH level

The comparison of serum calcium and PTH levels at 1- and 3-day after surgery between GTET group and COT group revealed no statistically significant difference in serum calcium levels between the two groups (P=0.46 and P=0.13). However, a statistically significant difference was observed in PTH levels at 1- and 3-day after surgery between the two groups (P<0.001 and P=0.01) (Table 3).

Analysis of related factors of PG injury

Univariate analysis revealed that age, gender, BMI, tumor location and maximum tumor diameter were not statistically significant, while surgical method (P<0.001) and HT (P=0.042) showed statistical significance (Table 4). Variables with a P<0.05 in the univariate analysis were included in the multivariable analysis, which indicated that GTET (OR, 0.251; 95% CI, 0.110–0.576; P=0.001) was a protective factor for PG injury, whereas HT (OR, 2.722; 95% CI, 1.114–6.654; P=0.02) was a risk factor for PG injury (Table 5).

The incidence of postoperative complications between two groups

The incidence of vocal dysfunction (P=0.04), pitch drops (P=0.01) and choking on drinking water (P=0.01) were significantly lower in the GTET group compared to the COT group. There were no significant differences in the incidence of wound infection (P=0.18) and postoperative bleeding (P=0.69) between the two groups. The surgery time (P<0.001) and postoperative drainage (P<0.001) in the GTET group were significantly higher than that in the COT group (Table 6).

Postoperative PTH level after PA

There was a statistically significant difference in the number of PA and the PTH level at 1-day after surgery (P<0.001), whereas no statistically significant difference was observed in the PTH level at 3-day after surgery (P=0.24) (Table 7).

Discussion

The transaxillary approach has emerged as a prominent focus of research since the past decade. Compared to other surgical methods, it offers a short learning curve, high safety and feasibility, and is easily adopted by major hospitals. Additionally, it effectively reduces the risk of characteristic postoperative complications and has gained popularity among surgeons. However, regardless of the surgical approach, postoperative parathyroid dysfunction is inevitable. While most studies have indicated no significant disparity in parathyroidism occurrence between ET and COT, some research suggests a lower prevalence of permanent HPT following ET compared to COT (13,28,29). In this study, there was no statistically significant difference in postoperative serum calcium levels between the two groups of patients, it may be related to our postoperative preventive calcium supplementation for patients. However, postoperative temporary HPT was higher in GTET group than in COT group. Multivariate logistic regression analysis showed that GTET is a protective factor for postoperative HPT, indicating that GTET has a better protective effect on postoperative HPT than COT and can reduce the incidence of postoperative HPT. The possible reason for this may be due to the magnifying effect of endoscopic thyroid surgery, which can clearly show the lesion and surrounding tissue structure. During the surgical process, endoscopic thyroid surgery is more precise than COT, and the possibility of vascular, parathyroid, and surrounding tissue injury during surgery is reduced, which can better identify and protect the PG.

In addition, there are reports suggesting that patients with PTC combined with HT are more prone to postoperative HPT than those without HT (30), which is similar to the results of this study. The reason may be reactive lymph node enlargement caused by HT, which is easily mistaken for metastatic lymph nodes, resulting in a larger number of lymph nodes being cleaned and more severe damage to the surgical area, The incidence of PG damage increases accordingly (31). Additionally, the thyroid tissue in HT is fragile and fibrotic, with more abundant blood vessels, which increases the operation time and difficulty of GTET (32), thereby increasing the direct damage to PG and the disruption of PG blood supply. Nanocarbon suspension is a new type of lymphatic tracer. Studies have shown that the application of nanocarbon tracers in thyroid surgery can improve the detection rate of lymph nodes and reduce the injury of PG (33,34). However, due to the formation of thyroid fibrosis in HT patients, the diffusion of nanocarbon tracers is affected, resulting in poor lymph node staining and difficulty in identifying PG.

A retrospective cohort study (35) showed that tumor diameter is closely related to postoperative HPT. Especially when the tumor diameter is greater than 1.1 cm, the protective effect of nanocarbon tracers is limited, leading to an increased incidence of PG injury. However, this study showed no correlation between tumor diameter and postoperative HPT (P=0.63). Interestingly, studies have reported that women are one of the risk factors for postoperative HPT in thyroid surgery (36), it may be related to the anatomical and morphological differences in PG between men and women, or the effects of sex steroids on PTH secretion. However, the exact mechanism behind gender differences is still unclear. In this study, it was found that there was no correlation between gender and the occurrence of postoperative HPT in thyroid surgery, which is consistent with the findings of Salem (22).

In terms of complications, the incidence of vocal dysfunction, hoarseness and choking on drinking water after GTET group is lower than that of COT group, but the GTET group operation time was longer and the postoperative totally drainage was more than COT group, which is related to the construction of a cavity on the surface of the pectoralis major muscle and the complexity of the surgery. Overall, GTET can achieve the therapeutic effect of COT while reducing the incidence of postoperative complications.

A study has found a negative correlation between intraoperative PG recognition and unintentional PG resection (37). Unexpected parathyroidectomy always increases the risk of temporary and permanent postoperative HPT (38,39). Different scholars have different research results on PA. Ahmed et al. believes that PA is the preferred method to ensure good PG function (40). Qiu et al. believes that PA is a preventive factor for permanent HPT (41). But some scholars believe that performing PA during surgery increases the risk of permanent HPT after surgery (42). In this study, we further found that the incidence of PTH decreased on the first day after surgery in 17.9%, 21.4%, and 52% in patients with parathyroid preservation in situ, one PA, and two PA, respectively (P<0.001). Therefore, we believe that maximal preservation of the PG in situ is essential for maintaining its function, however, selective PA remains an effective method for salvaging function when glands are mistakenly removed or compromised blood supply is experienced during surgery.

There are still certain limitations to this study, such as limited sample size, retrospective analysis, etc., which may introduce bias into the results. In addition, drawing definitive conclusions from a single surgeon’s study is not feasible. Therefore, future research should focus on larger sample sizes and involve multicenter or prospective studies to validate these findings and explore additional factors related to PG injury.

Conclusions

GTET reduces the incidence of PG injury and nerve injury. On the contrary, the operation time and postoperative totally drainage increase compared to COT, and when PTC is combined with HT, it increases the risk of PG injury.

Acknowledgments

We thank all the members for their generous participation.

Funding: This study was funded by the 2024 Xiamen Medical and Industrial Integration Guidance Project (No. 3502Z20244ZD2011), and the 2022 Xiamen Medical and Health Guidance Project (No. 3502Z20224ZD1002).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-24-234/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-234/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-234/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-234/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 (as revised in 2013). The study was approved by the Ethics Committee of the First Affiliated Hospital of Xiamen University (No. XMYY-20022KYSB144) 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/.

References

1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2021;71:209-49. [Crossref] [PubMed]
2. Ghossein R, Barletta JA, Bullock M, et al. Data set for reporting carcinoma of the thyroid: recommendations from the International Collaboration on Cancer Reporting. Hum Pathol 2021;110:62-72. [Crossref] [PubMed]
3. Hegedüs L. Clinical practice. The thyroid nodule. N Engl J Med 2004;351:1764-71. [Crossref] [PubMed]
4. Bible KC, Kebebew E, Brierley J, et al. 2021 American Thyroid Association Guidelines for Management of Patients with Anaplastic Thyroid Cancer. Thyroid 2021;31:337-86. [Crossref] [PubMed]
5. Alesina PF, Wahabie W, Meier B, et al. Long-term cosmetic results of video-assisted thyroidectomy: a comparison with conventional surgery. Langenbecks Arch Surg 2021;406:1625-33. [Crossref] [PubMed]
6. Anuwong A, Ketwong K, Jitpratoom P, et al. Safety and Outcomes of the Transoral Endoscopic Thyroidectomy Vestibular Approach. JAMA Surg 2018;153:21-7. [Crossref] [PubMed]
7. Zhang Y, Dong Z, Li J, et al. Comparison of endoscopic and conventional open thyroidectomy for Graves' disease: A meta-analysis. Int J Surg 2017;40:52-59. [Crossref] [PubMed]
8. Xu S, Yang Z, Guo Q, et al. Surgical Steps of Gasless Transaxillary Endoscopic Thyroidectomy: From A to Z. J Oncol 2022;2022:2037400. [Crossref] [PubMed]
9. Yang Y, Sun D, Yang J, et al. Endoscopic Thyroidectomy in Anterior Chest Approach Versus Open Thyroidectomy for Patients with Papillary Thyroid Carcinomas, a Retrospective Study. J Laparoendosc Adv Surg Tech A 2020;30:488-94. [Crossref] [PubMed]
10. Yan HC, Xiang C, Wang Y, et al. Scarless endoscopic thyroidectomy (SET) lateral neck dissection for papillary thyroid carcinoma through breast approach: 10 years of experience. Surg Endosc 2021;35:3540-6. [Crossref] [PubMed]
11. Dong F, Yang A, Ouyang D. Retroauricular Single-Site Endoscopic Thyroidectomy-A Balanced Endoscopic Approach for Thyroid Excision. JAMA Surg 2023;158:548-9. [Crossref] [PubMed]
12. Jongekkasit I, Jitpratoom P, Sasanakietkul T, et al. Transoral Endoscopic Thyroidectomy for Thyroid Cancer. Endocrinol Metab Clin North Am 2019;48:165-80. [Crossref] [PubMed]
13. Dabsha A, Khairallah S, Elkharbotly IAMH, et al. Learning curve and volume outcome relationship of endoscopic trans-oral versus trans-axillary thyroidectomy; A systematic review and meta-analysis. Int J Surg 2022;104:106739. [Crossref] [PubMed]
14. Rossi L, Materazzi G, Bakkar S, et al. Recent Trends in Surgical Approach to Thyroid Cancer. Front Endocrinol (Lausanne) 2021;12:699805. [Crossref] [PubMed]
15. Abdel-Halim CN, Rejnmark L, Nielsen VE. Post-operative parathyroid hormone can be used as a predictor of normocalcaemia after total thyroidectomy. Dan Med J 2015;62:A5157.
16. Alhefdhi A, Mazeh H, Chen H. Role of postoperative vitamin D and/or calcium routine supplementation in preventing hypocalcemia after thyroidectomy: a systematic review and meta-analysis. Oncologist 2013;18:533-42. [Crossref] [PubMed]
17. Ambe PC, Brömling S, Knoefel WT, et al. Prolonged duration of surgery is not a risk factor for postoperative complications in patients undergoing total thyroidectomy: a single center experience in 305 patients. Patient Saf Surg 2014;8:45. [Crossref] [PubMed]
18. Mizuno K, Takeuchi M, Kanazawa Y, et al. Recurrent laryngeal nerve paralysis after thyroid cancer surgery and intraoperative nerve monitoring. Laryngoscope 2019;129:1954-60. [Crossref] [PubMed]
19. Yu W, Cao X, Xu G, et al. Potential role for carbon nanoparticles to guide central neck dissection in patients with papillary thyroid cancer. Surgery 2016;160:755-61. [Crossref] [PubMed]
20. Su AP, Wang B, Gong YP, et al. Carbon nanoparticles facilitate lymph nodes dissection and parathyroid glands identification in reoperation of papillary thyroid cancer. Medicine (Baltimore) 2017;96:e8380. [Crossref] [PubMed]
21. Sun R, Sheng J, Zhou Y, et al. Relationship between the extent of central node dissection and parathyroid function preservation in thyroid cancer surgery. Gland Surg 2021;10:1093-103. [Crossref] [PubMed]
22. Salem FA, Bergenfelz A, Nordenström E, et al. Central lymph node dissection and permanent hypoparathyroidism after total thyroidectomy for papillary thyroid cancer: population-based study. Br J Surg 2021;108:684-90. [Crossref] [PubMed]
23. Bilezikian JP. Hypoparathyroidism. J Clin Endocrinol Metab 2020;105:1722-36. [Crossref] [PubMed]
24. Zhang D, Gao L, He G, et al. Predictors of graft function after parathyroid autotransplantation during thyroid surgery. Head Neck 2018;40:2476-81. [Crossref] [PubMed]
25. Wang B, Zhu Y, Zhou S, et al. The effect of carbon nanoparticles vs. immune colloidal gold technique test strips on parathyroid protection in total thyroidectomy: A randomized clinical trial study. Head Neck 2024;46:1727-36. [Crossref] [PubMed]
26. Moffett JM, Suliburk J. Parathyroid autotransplantation. Endocr Pract 2011;17:83-9. [Crossref] [PubMed]
27. Zhan HL, Huang HQ, Zheng MM, et al. Comparison of the Safety and Thoroughness of Preoperative Versus Intraoperative Injection of Nanocarbon Tracers in Thyroid Cancer Surgery. Indian J Surg 2022. doi: 10.1007/s12262-022-03388-2. [Crossref]
28. Sun H, Wang X, Zheng G, et al. Comparison Between Transoral Endoscopic Thyroidectomy Vestibular Approach (TOETVA) and Conventional Open Thyroidectomy for Patients Undergoing Total Thyroidectomy and Central Neck Dissection: A Propensity Score-Matching Analysis. Front Oncol 2022;12:856021. [Crossref] [PubMed]
29. Akritidou E, Douridas G, Spartalis E, et al. Complications of Trans-oral Endoscopic Thyroidectomy Vestibular Approach: A Systematic Review. In Vivo 2022;36:1-12. [Crossref] [PubMed]
30. McManus C, Luo J, Sippel R, et al. Is thyroidectomy in patients with Hashimoto thyroiditis more risky? J Surg Res 2012;178:529-32. [Crossref] [PubMed]
31. Donangelo I, Walts AE, Bresee C, et al. Lymphocytic thyroiditis is associated with increased number of benign cervical nodes and fewer central neck compartment metastatic lymph nodes in patients with differentiated thyroid cancer. Endocr Pract 2016;22:1192-8. [Crossref] [PubMed]
32. Saadi R, Brandt A, Kim Y, et al. Degree of technical difficulty of thyroidectomy for autoimmune thyroid disease. Head Neck 2020;42:262-8. [Crossref] [PubMed]
33. Rao S, Wang Z, Pan C, et al. Preliminary Study on the Clinical Significance and Methods of Using Carbon Nanoparticles in Endoscopic Papillary Thyroid Cancer Surgery. Contrast Media Mol Imaging 2021;2021:6652315. [Crossref] [PubMed]
34. Spartalis E, Giannakodimos A, Athanasiadis DI, et al. The Potential Role of Carbon Nanoparticles in Lymph Node Tracing, Recurrent Laryngeal Nerve Identification and Parathyroid Preservation During Thyroid Surgery: A Systematic Review. Curr Pharm Des 2021;27:2505-11. [Crossref] [PubMed]
35. Chen PP, Zhang X, Li JG, et al. Predictors of impaired effectiveness of carbon nanoparticle-based central lymph node tracing in patients who underwent surgery for papillary thyroid cancer: A retrospective cohort study. Medicine (Baltimore) 2022;101:e31257. [Crossref] [PubMed]
36. Sands NB, Payne RJ, Côté V, et al. Female gender as a risk factor for transient post-thyroidectomy hypocalcemia. Otolaryngol Head Neck Surg 2011;145:561-4. [Crossref] [PubMed]
37. Sorgato N, Pennelli G, Boschin IM, et al. Can we avoid inadvertent parathyroidectomy during thyroid surgery? In Vivo 2009;23:433-9.
38. Cho JN, Park WS, Min SY. Predictors and risk factors of hypoparathyroidism after total thyroidectomy. Int J Surg 2016;34:47-52. [Crossref] [PubMed]
39. Lo CY, Lam KY. Postoperative hypocalcemia in patients who did or did not undergo parathyroid autotransplantation during thyroidectomy: a comparative study. Surgery 1998;124:1081-6; discussion 1086-7.
40. Ahmed N, Aurangzeb M, Muslim M, et al. Routine parathyroid autotransplantation during total thyroidectomy: a procedure with predictable outcome. J Pak Med Assoc 2013;63:190-3.
41. Qiu Y, Xing Z, Qian Y, et al. Selective Parathyroid Autotransplantation During Total Thyroidectomy for Papillary Thyroid Carcinoma: A Cohort Study. Front Surg 2021;8:683041. [Crossref] [PubMed]
42. Sitges-Serra A. Etiology and Diagnosis of Permanent Hypoparathyroidism after Total Thyroidectomy. J Clin Med 2021;10:543. [Crossref] [PubMed]