Fine needle aspiration is not a risk factor for cervical lymph node metastasis or prognostic factor in papillary thyroid microcarcinoma: A propensity score-matched analysis

doi:10.21203/rs.3.rs-1624222/v1

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Fine needle aspiration is not a risk factor for cervical lymph node metastasis or prognostic factor in papillary thyroid microcarcinoma: A propensity score-matched analysis

https://doi.org/10.21203/rs.3.rs-1624222/v1

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Background

Ultrasound-guided fine needle aspiration (UGFNA) has been widely used in clinical practice. Many patients may still worry about UGFNA-related metastasis. The aim of this article was to analyze the potential association between UGFNA and cervical lymph node metastasis (CLNM) of papillary thyroid microcarcinoma (PTMC) and whether UGFNA influences the long-term prognosis of PTMC.

Methods

A total of 367 adult patients with PTMC who underwent thyroidectomy in our hospital between January 2014 and December 2015 were enrolled in this retrospective cohort study. Univariate and multivariate analyses were conducted to explore the potential risk factors for CLNM. Propensity score (PS)-based 1:1 nearest neighbor matching was performed to select patients with homogeneous baseline characteristics. Then, the rate of CLNM was compared between matched samples with chi-square (χ2) tests. Survival analysis was performed with the Kaplan–Meier method in the PS-matched cohort. The recurrence-free survival (RFS) rate was compared between groups with the log-rank test.

Results

Multivariate analysis showed that male sex (OR = 3.997, 95% CI 2.148 ~ 7.439, P < 0.01) and larger tumor size (OR = 2.319, 95% CI 1.285 ~ 4.186, P < 0.01) were independent risk factors for CLNM. Younger age (< 55 years, OR = 1.809, 95% CI 0.937 ~ 3.492, P > 0.05), capsular invasion (OR = 1.218, 95% CI 0.415 ~ 3.572, P > 0.05), multifocality (OR = 1.949, 95% CI 0.905 ~ 4.196, P > 0.05) and Hashimoto's thyroiditis (HT) (OR = 0.824, 95% CI 0.401 ~ 1.696, P > 0.05) were not independent risk factors for CLNM. In the PS-matched cohort, the CLNM rate showed no significant difference between the UGFNA and non-UGFNA groups (29.5% vs. 23.7%, P > 0.05). With a median follow-up of 63.8 months (range 3.1–84.9 months), the 5-year cumulative RFS rate was 99.3% in the UGFNA group and 97.7% in the non-UGFNA group. After PS matching, the Kaplan–Meier curves showed no significant differences between groups (P > 0.05).

Conclusions

UGFNA is a very safe diagnostic tool that does not influence the CLNM rate or long-term prognosis of patients with PTMC. The fear of UGFNA-related metastasis should not deter UGFNA of the thyroid.

thyroid

papillary carcinoma

fine needle aspiration

cervical lymph node metastasis

risk factor

prognosis

Over the last several decades, the incidence of thyroid cancer (TC) has increased rapidly in both men and women globally.[1] Papillary thyroid carcinoma (PTC) is the most common and indolent type of TC, accounting for 80% of all TC cases.[1–3] Moreover, most of the newly diagnosed cancer cases are papillary thyroid microcarcinoma (PTMC) with a size of 1 cm or less[4, 5] due to the increasing use of medical imaging, such as ultrasound and computed tomography.[6, 7]

Early diagnosis is very important for PTC, as its 10-year survival rate can be as high as 90% in the early stage but decreases significantly in the later stage.[3] Ultrasound-guided fine needle aspiration (UGFNA) is the most common and cost-effective diagnostic method for TC, can help doctors distinguish malignant nodules from benign nodules before surgery and aids in treatment decision-making.[8, 9] Both the 2015 American Thyroid Association Management (ATA) Management Guidelines[9] and the 2017 ACR Thyroid Imaging, Reporting and Data System (TI-RADS)[10] do not recommend routine biopsy of thyroid nodules smaller than 1 cm, even if they are highly suspicious. However, this approach can be a serious psychological burden for some patients, especially those in China, because of the potential for malignant nodules. Therefore, patients often prefer to learn the nature of the nodules as soon as possible instead of undergoing long-term follow-up. Moreover, patients may also worry about UGFNA-associated tumor dissemination. To our knowledge, the prognostic influence of UGFNA in patients with PTMC has not been studied systematically before. In this study, we retrospectively analyzed the relationship between UGFNA and cervical lymph node metastasis (CLNM) and whether UGFNA influences the long-term prognosis of patients with PTMC.

Patients

In Chinese hospitals, UGFNA of thyroid nodules has been gradually carried out in clinical practice as a new preoperative diagnostic tool since 2015. Afterwards, an increasing number of patients have preferred preoperative UGFNA to learn about the nature of their thyroid nodules. Therefore, we selected patients who underwent thyroidectomy during January 2014 and December 2015 in our hospital as the subjects of our study. The application of UGFNA was based on the patients’ willingness and the results of the US evaluation. All patients were confirmed to have PTMC by postoperative pathology. Finally, a total of 367 adult patients were enrolled in this retrospective cohort study. Patients were divided into two groups according to whether they underwent preoperative UGFNA. There were 163 patients in the UGFNA group and 204 patients in the non-UGFNA group.

All procedures were implemented based on the principles of the Declaration of Helsinki: ethical principles for medical research involving human subjects.

Data Collection

The electronic medical records and surgical pathology reports of each patient were reviewed to collect demographic characteristics and clinicopathological data, including multifocality, capsular invasion, Hashimoto's thyroiditis (HT), tumor size, CLNM, operation method and cervical lymph node dissection. The size of the tumor was measured by postoperative pathology. For multifocal tumors, only the nodule with the largest diameter was selected for analysis. Cervical lymph node dissection was defined according to whether central lymph node dissection was performed. All operations were performed by the same surgical group in our hospital, and pathological analysis was then performed by the Department of Pathology. The follow-up data were collected by retrospectively reviewing the patients’ medical records and telephone interviews. The last follow-up was on January 10, 2021. Recurrence was recorded when there were suspicious cervical lymph nodes or thyroid nodules that were further confirmed to be malignant by UGFNA or pathology after a second surgery. Tumor recurrence was used as the end point of the analysis to assess the outcome. The recurrence-free survival (RFS) duration was calculated in months from the date of the first surgery to the date of recurrence or last follow-up.

Statistical analysis

Statistical analysis was performed with IBM SPSS Statistics Version 23. The data are expressed as medians for continuous variables and percentages for categorical variables. Comparisons between groups were performed with the Mann–Whitney U test for continuous variables and chi-square (χ2) test for categorical variables. In addition, univariate logistic and multivariate logistic regression were performed to explore the relationship between the clinical characteristics and CLNM in patients who underwent cervical lymph node dissection. The propensity score (PS) of each patient was calculated by logistic regression models by entering the following covariates: age group, sex, operative method, lymph node dissection, capsular invasion, tumor size and multifocality. Then, PS matching (1:1 nearest neighbor matching) was performed by using a caliper of 0.2 standard deviations to minimize the differences in covariates between the two groups. The survival curves were plotted using the Kaplan–Meier method. The RFS rate was compared between groups with the log-rank test in the PS-matching cohort. P values less than 0.05 were considered to be statistically significant. (*: P < 0.05, **: P < 0.01)

Comparisons of baseline characteristics between PTMC patients in the UGFNA group and the non-UGFNA group before PS matching

A total of 367 patients were enrolled in this study. Table 1 shows the clinical characteristics for all patients and by group. The median age of PTMC patients was 47 years, with a range of 22–76 years. The median age in the UGFNA group was significantly younger than that in the non-UGFNA group (P = 0.041). After dividing the patients into two groups by an age cutoff of 55 years, no significant difference in the distribution of age was found between the two groups (P = 0.588). Among all patients, 71.9% were female, and no significant difference in the proportion of females was found between the two categories (71.8% vs. 72.1%; P = 0.953). Additionally, none of the clinicopathological characteristics of patients with PTMC, including multifocality (P = 0.785), capsular invasion (P = 0.091), tumor size (P = 0.812) and HT (P = 0.678), showed significant differences between the two categories. The operative method was also not significantly different between the two groups (P = 0.168). Interestingly, the rate of cervical lymph node dissection in the UGFNA group was significantly higher than that in the non-UGFNA group (87.1% vs. 61.3%; P < 0.01).

Table 1

Comparison of clinicopathological characteristics between PTMC patients in the UGFNA group and non-UGFNA group.
Characteristics	Total (N = 367) N (%)	UGFNA ^a (+) (N = 163) N (%)	UGFNA (-) (N = 204) N (%)	P value
Age (years)				0.588
< 55	249 (67.8)	113 (69.3)	136 (66.7)
≧ 55	118 (32.2)	50 (30.7)	68 (33.3)
Female sex	264 (71.9)	117 (71.8)	147 (72.1)	0.953
Multifocality	52 (14.2)	24 (14.7)	28 (13.7)	0.785
Capsular invasion	19 (5.2)	12 (7.4)	7 (3.4)	0.091
Tumor size (cm)				0.812
≦ 0.5	243 (66.2)	109 (66.9)	134 (65.7)
> 0.5	124 (33.8)	54 (33.1)	70 (34.3)
HT ^b	73 (19.9)	34 (20.9)	49 (19.1)	0.678
Operative method				0.168
LT ^c	245 (66.8)	115 (70.6)	130 (63.7)
TT ^d	122 (33.2)	48 (29.4)	74 (36.3)
Cervical lymph node dissection	267 (72.8)	142 (87.1)	125 (61.3)	0.000**
^a UGFNA = Ultrasound-guided fine needle aspiration; ^b HT = Hashimoto's thyroiditis; ^c LT = Lobectomy; ^d TT = Total thyroidectomy. **: P < 0.01

Ugfna Showed No Significant Influence On Clnm In The Ps-matched Cohort

Before PS matching, the rate of CLNM in the UGFNA group was significantly higher than that in the non-UGFNA group. To balance the heterogeneity of baseline characteristics between the UGFNA group and the non-UGFNA group, PS matching (1:1 nearest neighbor matching) was performed with a caliper of 0.2 standard deviations. After PS matching, there were 139 matched PTMC patients in each group. No baseline characteristics, including cervical lymph node dissection, showed significant differences between the two groups after PS matching. (Table 2) In the PS-matched cohort, the rate of CLNM was 29.5% in the UGFNA group and 23.7% in the non-UGFNA group, which was not a significant difference (OR = 1.344, 95% CI 0.788 ~ 2.293, P = 0.278).

Table 2

**Comparison of clinicopathological characteristics between PTMC patients in the UGFNA group and non-UGFNA group after PS matching.**
Characteristics	Total (N = 278) N (%)	UGFNA ^a (+) (N = 139) N (%)	UGFNA (-) (N = 139) N (%)
Age (years)				0.250
< 55	187 (67.3)	89 (64.0)	98 (70.5)
≧ 55	91 (32.7)	50 (36.0)	41 (29.5)
Female sex	195 (70.1)	95 (68.3)	100 (71.9)	0.512
Multifocality	46 (16.5)	24 (17.3)	22 (15.8)	0.747
Capsular invasion	16 (5.8)	9 (6.5)	7 (5.0)	0.607
Tumor size (cm)				0.381
≦ 0.5	179 (64.4)	86 (61.9)	93 (66.9)
> 0.5	99 (35.6)	53 (38.1)	46 (33.1)
HT ^b	56 (20.1)	28 (20.1)	28 (20.1)	1.000
Operative method				0.798
LT ^c	188 (67.6)	93 (66.9)	95 (68.3)
TT ^d	90 (32.4)	46 (33.1)	44 (31.7)
Cervical lymph node dissection	238 (85.6)	119 (85.6)	119 (85.6)	1.000
^a UGFNA = Ultrasound-guided fine needle aspiration; ^b HT = Hashimoto's thyroiditis; ^c LT = Lobectomy; ^d TT = Total thyroidectomy.

Risk Factors For Cervical Lymph Node Metastasis

The rate of cervical lymph node dissection was significantly different between the two groups. Only patients who underwent cervical lymph node dissection were selected for the analysis of risk factors for CLNM in PTMC. In univariate logistic regression analysis, we found that CLNM in patients with PTMC was associated with male sex (OR = 3.504, 95% CI 1.984 ~ 6.188, P < 0.01) and larger tumor size (OR = 2.105, 95% CI 1.229 ~ 3.605, P < 0.01). Furthermore, after adjusting for confounding variables by performing multivariate logistic regression analysis, male sex (OR = 3.997, 95% CI 2.148 ~ 7.439, P < 0.01) and larger tumor size (OR = 2.319, 95% CI 1.285 ~ 4.186, P < 0.01) remained independent risk factors for CLNM. Younger age (OR = 1.809, 95% CI 0.937 ~ 3.492, P > 0.05), capsular invasion (OR = 1.218, 95% CI 0.415 ~ 3.572, P > 0.05), multifocality (OR = 1.949, 95% CI 0.905 ~ 4.196, P > 0.05) and Hashimoto's thyroiditis (HT) (OR = 0.824, 95% CI 0.401 ~ 1.696, P > 0.05) were not independent risk factors for CLNM. UGFNA was not an independent risk factor for CLNM, which was consistent with the previous result in the PS-matched cohort. (Table 3)

Table 3

**Risk factors for cervical lymph node metastasis in patients who underwent cervical lymph node dissection.**
Variables	Unadjusted		Adjusted
Variables	OR ^a (95% CI ^b)	P value	OR (95% CI)	P value
Age < 55, years	1.749 (0.943 ~ 3.243)	0.074	1.809 (0.937 ~ 3.492)	0.077
Male sex	3.504 (1.984 ~ 6.188)	0.000**	3.997 (2.148 ~ 7.439)	0.000**
Multifocality	1.662 (0.829 ~ 3.329)	0.149	1.949 (0.905 ~ 4.196)	0.088
Capsular invasion	1.929 (0.732 ~ 5.082)	0.178	1.218 (0.415 ~ 3.572)	0.720
Tumor size > 0.5 cm	2.105 (1.229 ~ 3.605)	0.006**	2.319 (1.285 ~ 4.186)	0.005**
UGFNA ^c	1.232 (0.729 ~ 2.084)	0.436	1.199 (0.681 ~ 2.109)	0.530
HT ^d	0.692 (0.360 ~ 1.328)	0.266	0.824 (0.401 ~ 1.696)	0.600
^a OR = odds ratio; ^b CI = confidence interval; ^c UGFNA = Ultrasound-guided fine needle aspiration; ^d HT = Hashimoto's thyroiditis. **: P < 0.01

Follow-up And Prognosis

The median follow-up time was 63.8 months (range 3.1–84.9 months). A total of 13.4% of the patients were initially lost to follow-up. Six patients, 2 patients in the UGFNA group and 4 patients in the non-UGFNA group, showed disease recurrence at the follow-up visit. The 5-year cumulative RFS rate was 99.3% in the UGFNA group and 97.7% in the non-UGFNA group. In the PS-matched cohort, Kaplan–Meier curves showed no significant difference between the two groups (P = 0.927) (Fig. 1). Therefore, UGFNA did not influence the patients’ long-term prognosis.

UGFNA is generally considered a simple, reliable and safe diagnostic tool. The most common complications following UGFNA are local pain or discomfort and small to moderate hematoma, which are usually self-limited.[11, 12] Some serious complications, such as massive hematomas and tumor dissemination, are very rare but may influence the patients’ long-term prognosis.[13] Theoretically, UGFNA may result in tumor dissemination, ad these cells can then be released into the surrounding tissues or circulation. An increasing number of patients worry about UGFNA-related metastasis. The most commonly reported UGFNA-related metastasis cases in patients with PTMC are due to needle tract implantation (NTI).[14–16] The relationship between UGFNA and CLNM in patients with PTMC has not been reported before. Our study demonstrated that UGFNA did not influence CLNM or the long-term prognosis of patients with PTMC, providing guidance for patients and doctors in the application of UGFNA.

In this study, before PS matching, the rate of CLNM in the UGFNA group was 28.8%, which was significantly higher than that in the non-UGFNA group (17.2%). Notably, the lymph node dissection rate was significantly higher in patients undergoing preoperative US-FNA than in those who did not undergo preoperative UGFNA (87.1% vs. 61.3%; P < 0.01). It is possible that less CLNM was found in the non-UGFNA group because fewer lymph node dissections were performed. Therefore, PS matching was performed to minimize the effect of confounding factors. After PS matching, we concluded that the rates of CLNM and recurrence between the UGFNA group and the non-UGFNA group were not significantly different. In previous studies, the reported rate of metastasis following UGFNA was extremely low. Ito et al. demonstrated that the incidence of NTI was 0.14% in PTC patients who underwent UGFNA.[17] Hayashi et al. reported that the cumulative incidence rates of NTI in thyroid cancer were 0.15% and 0.37% at 5 and 10 years, respectively, after UGFNA.[18] One hypothesis for the low UGFNA-related metastasis rate is that the disseminated tumor cells were destroyed by the host immune response or other mechanisms before giving rise to clinically apparent metastases.[12] Therefore, when patients have thyroid nodules measuring less than 1 cm, the fear of FNA-related metastasis should not deter UGFNA of the thyroid.

Moreover, we found that male sex and larger tumor size were independent risk factors for lymph node metastasis, as has been reported before.[19–21] As the eighth AJCC/TNM cancer staging system raised the age cutoff for staging from 45 to 55 years, our study selected 55 years as the age cutoff, which was different from previous studies.[22] Younger age, capsular invasion and multifocality were not independent risk factors for CLNM, although their significance has been demonstrated in several previous studies.[19–21] HT was also not related to CLNM in our study, and researchers have not reached an agreement on whether HT is a risk factor for CLNM.[23]

There are still some limitations in our study. First, the sample size was not large enough, with only 367 patients included. As patients with PTMC had a relatively low recurrence rate, more patients and longer follow-up durations are needed. Second, this was a single-center analysis, and there might be some selection bias. A multicenter study is needed to further confirm our results. Third, although PS matching was performed to balance the heterogeneity of baseline characteristics, there were still some variables that were not included in this study. Therefore, their potential confounding effects on the results could not be adjusted and were unavoidable.

In conclusion, this study indicated that UGFNA did not influence CLNM or the long-term prognosis of patients with PTMC and was considered a relatively safe preoperative diagnostic tool. The fear of UGFNA-related metastasis should not deter UGFNA of the thyroid.

Acknowledgments

We would like to thank Zhoukan Chen for assisting with data collection.

Authors’ contributions

MD and ZFZ were responsible for the study design, data collection and analysis, and manuscript writing. DX and TYL assisted with the data analysis and manuscript writing. JF, RLX and DJS gave instructions for the study design, data analysis and manuscript writing. All authors issued final approval for the version to be submitted.

Funding

This work was supported by the Project of Shanghai Municipal Health Commission. (Grant No. 20214Y0223) and Medical-Engineering Cross Foundation of Shanghai Jiao Tong University (Grant No. YG2019ZDA17).

Availability of data and materials

The datasets used and analyzed in the current study are available from the corresponding author on reasonable request.

Ethics approval and consent to participate

The Ethics Committee of Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, approved this study. This was a retrospective cohort study, and the data of the patients were anonymous. Therefore, there was no need for informed consent.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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No competing interests reported.

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Fine needle aspiration is not a risk factor for cervical lymph node metastasis or prognostic factor in papillary thyroid microcarcinoma: A propensity score-matched analysis

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Introduction

Materials And Methods

Patients

Data Collection

Statistical analysis

Results

Ugfna Showed No Significant Influence On Clnm In The Ps-matched Cohort

Risk Factors For Cervical Lymph Node Metastasis

Follow-up And Prognosis

Discussion

Declarations

References

Additional Declarations

Status:

Version 1