Meta-analysis of the diagnostic value of dual-energy computed tomography parameters for lymph node metastasis in papillary thyroid cancer

doi:10.21203/rs.3.rs-2100565/v1

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Meta-analysis of the diagnostic value of dual-energy computed tomography parameters for lymph node metastasis in papillary thyroid cancer

https://doi.org/10.21203/rs.3.rs-2100565/v1

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Objective: This study was to investigate the diagnostic value of quantitative parameters of dual-energy computed tomography (CT) for diagnosing lymph nodes (LNs) metastasis in papillary thyroid cancer (PTC).

Methods: PubMed, Cochrane, Embase, Web of Science, China Biology Medicine disc, WangFang, VIP, and China National Knowledge Infrastructure databases were searched up to April 20, 2022. Studies that evaluated the diagnostic value of dual-energy CT for detectingLNs metastasis in PTC patients were included. The standardized mean difference (SMD) and 95% confidence interval (CI) were used to assess the diagnostic value of quantitative parameters based on dual-energy CT for LNs metastasis in PTC. The publication bias and sensitivity analysis were performed.

Results: Twelve studies involving 1,522 PTC patients were included in this study. The iodine concentration (IC) in the venous phase (SMD: 0.33, 95% CI: 0.06 to 0.60, P=0.015), normalized iodine concentration (NIC) in venous phase (SMD: 0.15, 95% CI: 0.12 to 0.19, P<0.05), NIC in arterial phase (SMD: 0.22, 95% CI: 0.16 to 0.28, P<0.05), and the slope of the energy spectrum curve (λHU) in arterial phase (SMD: 0.99, 95% CI: 0.59 to 1.40, P<0.05) were associated with LNs metastasis in PTC.

Conclusion: The parameters based on the dual-energy CT showed diagnostic value in diagnosing LN metastasis in PTC patients which may serve as a promising tool for the diagnosis of LN metastasis in PTC.

dual-energy CT

lymph node metastasis

papillary thyroid cancer

quantitative parameter

meta-analysis

Thyroid cancer is the most common head and neck malignancy, and its incidence is increasing. Among the various subtypes, papillary thyroid carcinoma (PTC) accounts for 90% of thyroid cancer [1, 2]. Although PTC is inert cancer with relatively low recurrence and mortality rates, PTC is associated with frequent locoregional lymph node (LN) metastases, with approximately 30%-90% of PTC patients having LN metastases [3]. LN metastases are associated with local recurrence and cancer-related mortality in patients with PTC [4, 5]. Therefore, identification of LN is important for optimal staging, individualized treatment planning, and prognosis evaluation for patients with PTC.

Ultrasonography is a common imaging method for the evaluation of LN metastasis in PTC patients [6]. However, ultrasonography has suboptimal sensitivity and specificity in the detection of extrathyroidal extension and cannot reliably detect cervical LN metastases deep to the intact thyroid gland or in the infraclavicular, retropharyngeal, and parapharyngeal region [7, 8]. The good imaging quality and high spatial resolution of computed tomography (CT) can make up for the deficiency of ultrasonography. However, no matter ultrasonography or CT, the diagnosis of metastatic LNs in PTC patients is mainly based on qualitative image features in the clinical work process, which are limited in their subjectivity [7, 9]. Different from conventional CT scanning, dual-energy CT can not only obtain qualitative image features of LNs, but also generate iodine maps and energy spectrum curves by using X-rays of different energies to obtain more quantitative parameters [10]. Dual-energy CT has been widely used to detect LN and LN metastases in various cancers, including PTC [11, 12]. A previous study demonstrated that quantitative dual-energy CT parameters were very useful for small LNs that were difficult to be diagnosed only on conventional CT images [13]. A study by Gao et al. verified that quantitative dual-energy CT parameters such as normalized iodine concentration (NIC), have been helpful in the pre-operative diagnosis of metastatic LNs in patients with thyroid cancer [14]. However, Wu et al. found that the NIC had low sensitivity for diagnosing metastatic cervical LNs in PTC [12]. Given the controversial results, a meta-analysis is needed to further assess the diagnostic value of quantitative parameters of dual-energy CT for diagnosing LNs metastasis in PTC.

Thereby, this meta-analysis was conducted to evaluate the diagnostic value of dual-energy CT parameters for LN metastasis in PTC, which may guide the evaluation of LN metastasis in PTC.

This meta-analysis was performed and reported based on the Preferred Reporting Items for Systematic Reviews and Meta-analysis of Diagnostic Test Accuracy Studies (PRISMA-DTA) statement [13].

Retrieval strategy

From inception to April 20, 2022, relevant studies were searched via PubMed, Cochrane, Embase, Web of Science, China Biology Medicine disc, WangFang, VIP, and China National Knowledge Infrastructure databases. The search terms were: “Thyroid Cancer, Papillary” OR “Cancer, Papillary Thyroid” OR “Cancers, Papillary Thyroid” OR “Papillary Thyroid Cancer OR (“Papillary Thyroid Cancers OR “Thyroid Cancers, Papillary” OR “Thyroid Carcinoma, Papillary” OR “Carcinoma, Papillary Thyroid” OR “Carcinomas, Papillary Thyroid” OR “Papillary Thyroid Carcinomas” OR “Thyroid Carcinomas, Papillary” OR “Papillary Carcinoma Of Thyroid” OR “Papillary Thyroid Carcinoma” ) AND (“Lymphatic Metastasis” OR “Lymphatic Metastases” OR “Lymph Node Metastasis” OR “Lymph Nodes Metastasis” OR “Lymph Nodes Metastases” OR “Lymph Node Metastases” OR “Metastasis, Lymph Node” OR “Metastasis, Lymph Nodes” OR “Metastases, Lymph Node” OR “Metastases, Lymph Nodes”) AND (“dual source CT” OR “dual energy CT” OR “DECT” OR “DSCT” OR “X-Ray Computed Tomography” OR “Tomography, X-Ray Computerized” OR “Tomography, X Ray Computerized” OR “Computed X Ray Tomography” OR “X-Ray Computer Assisted Tomography” OR “X Ray Computer Assisted Tomography” OR “Tomography, X-Ray Computer Assisted” OR “Tomography, X Ray Computer Assisted” OR “Computerized Tomography, X Ray” OR “Computerized Tomography, X-Ray” OR “X-Ray Computerized Tomography” OR “CT X Ray” OR “CT X Rays” OR “X Ray, CT” OR “X Rays, CT” OR “Tomography, X Ray Computed” OR “X Ray Tomography, Computed” OR “X-Ray Tomography, Computed” OR “Computed X-Ray Tomography” OR “Tomographies, Computed X-Ray” OR “Tomography, Computed X-Ray” OR “Tomography, Xray Computed” OR “Computed Tomography, Xray” OR “Xray Computed Tomography” OR “CT Scan, X-Ray” OR “CT Scan, X Ray” OR “CT Scans, X-Ray” OR “Scan, X-Ray CT” OR “Scans, X-Ray CT” OR “X-Ray CT Scan” OR “X-Ray CT Scans” OR “Computed Tomography, X-Ray” OR “Computed Tomography, X Ray” OR “X Ray Computerized Tomography”).

Inclusion and exclusion criteria

Inclusion criteria follow PICOS (participants, interventions, comparisons, outcomes, and study design) principles; (1) participants: patients with PTC confirmed by pathology using a dual-energy CT machine for CT examination; (2) interventions and comparisons: the observation group was PTC patients with LN metastases, and the control group was PTC patients without LN metastases; (3) outcomes: iodine concentration (IC), NIC, and the slope of the energy spectrum curve (λHU) of LNs in the arterial and the venous phases were compared between metastatic and non-metastatic LNs; (4) study design: observational study; (5) articles published in English or Chinese; (6) if duplicate articles exist, only the one with the most complete information would be included.

The exclusion criteria were: (1) animal experiments, reviews, meta-analyses, conference abstracts, letters, guidelines, and errata; (2) studies with no control group.

Data extraction and quality assessment

Two authors (Wenhui WU and Jianming Li) independently reviewed the included studies and extracted the relevant information. Any discrepancies in this process were resolved through agreement by negotiation with a third researcher (An Zhang). Data extracted included the last name of the first author, publication year, the region where the study was conducted, the age and sex of the study participants, the sample size, the number of patients with LN metastasis, the number of LNs, diagnostic parameters, dual-energy CT model, and the quality of the literature.

The evaluation of the quality of included studies was based on Newcastle-Ottawa Scale (NOS) [15]. The NOS comprises 9 items. In general, studies with a score of 5 or higher are considered high quality.

Statistical analysis

Statistical analyses were performed using Stata 15.0. The standardized mean difference (SMD) was used as the effect indicator, and the effect size was expressed by a 95% confidence interval (CI). Heterogeneity was tested using the Q test. I² ≥ 50% indicated the existence of significant heterogeneity, and the random-effect model was used as the pooling method; otherwise, the fixed-effects model was applied. Deeks’ funnel plot was used to assess publication bias. Sensitivity analysis was conducted to assess the stability of the results. P < 0.05 were regarded as having a statistically significant difference.

Literature search and basic chrematistics of the included studies

Initially, a total of 92 articles were retrieved from the database. After removal of the duplicates, 45 articles were left. After excluding meta-analyses, systematic reviews, animal experiments, and studies inconsistent with our topic and results, a total of 12 studies [11, 16–26] with 1,522 PTC patients were finally included in our study. The flow chart of data collection is described in Fig. 1. The detailed patient characteristics are shown in Table 1. T The quality of the included studies was high. The summary of the quality assessment using the NOS is illustrated in Table 1.

Diagnostic value of IC for LN metastasis in PTC

IC in the venous phase

For the evaluation of the diagnostic value of IC in the venous phase, data from 3 studies were analyzed. The fixed-effect model was selected for meta-analysis as the heterogeneity test showed I² = 0%. The results showed that the IC in the venous phase of the metastatic LN group was higher than that in the non-metastatic LN group (SMD: 0.33, 95% CI: 0.06 to 0.60, P = 0.015). The diagnostic value of IC in the venous phase for LNs metastasis in PTC is shown in Table 2 and Fig. 2.

Four articles evaluated the diagnostic value of IC in the venous phase of primary lesions of PTC for LN metastasis. The results of the random-effect model revealed that there was no statistically significant difference in IC in the venous phase of the primary lesion of PTC in the LN metastasis group compared with the non-LN metastasis group (I² = 93.1%, SMD: 0.44, 95% CI: -0.06 to 0.94, P = 0.085). The diagnostic value of IC in the venous phase of primary lesions of PTC for LN metastasis is described in Table 2.

IC in the arterial phase

Four included articles assessed the diagnostic value of IC in the arterial phase for LN metastasis in PTC. The heterogeneity test showed I² = 99.9%, so the random-effect model was applied. The IC in the arterial phase of metastatic LNs was not statistically higher than the arterial phase IC with non-metastatic LNs (SMD: 1.44, 95% CI: -0.86 to 3.74, P = 0.219). The diagnostic value of IC in the arterial phase for LN metastasis in PTC is depicted in Table 2.

The diagnostic value of IC of the primary lesion in the arterial phase for LN metastasis in PTC was explored in four articles. The result showed that there was no significant difference in IC in the arterial phase of the primary lesion between the LN metastasis group and the non-LN metastasis group (SMD: 0.23, 95% CI: -0.37 to 0.84, P = 0.451). The diagnostic value of IC of the primary lesion in the arterial phase for LN metastasis in PTC is shown in Table 2.

Diagnostic value of NIC for LN metastasis in PTC

NIC in the venous phase

Five articles investigated the diagnostic value of NIC in the venous phase for LN metastasis in PTC. The random-effect model analysis suggested that the NIC of metastatic LNs in the venous phase was higher than that of non-metastatic LNs (I² = 72.0%, SMD: 0.15, 95% CI: 0.12 to 0.19, P < 0.05). The diagnostic value of NIC in the venous phase for LN metastasis in PTC is shown in Table 2 and Fig. 3.

NIC in the venous phase of the primary lesion was examined in 4 studies. The result of the heterogeneity test indicated I² = 99.7%, so the random-effect model was used for meta-analysis. The result revealed that there was no statistically significant difference in NIC of the primary lesion in the venous phase between the LN metastasis group and the non-LN metastasis group (SMD: -0.12, 95% CI: -0.45 to 0.21, P = 0.468). The diagnostic value of NIC in the LN metastasis in the venous phase of the primary lesion is shown in Table 2.

NIC in the arterial phase

A total of 6 studies assessed the diagnostic value of NIC in the arterial phase for LN metastasis in PTC. The result demonstrated that the NIC of LN metastasis in the arterial phase was higher than that of non-metastatic LNs (I² = 90.9%, SMD: 0.22, 95% CI: 0.16 to 0.28, P < 0.05). The diagnostic value of NIC in the arterial phase for LN metastasis in PTC is depicted in Table 2 and Fig. 4.

The NIC of the primary lesion in the arterial phase was evaluated in 4 studies. Results of the random-effect model showed that the LN metastasis group did not have a statistically higher NIC in the arterial phase of the primary lesion than in the non- LN metastasis group (I² = 93.5%, SMD: 0.01, 95% CI: -0.03 to 0.05, P = 0.614) (Table 2).

Diagnostic value of λHU for LN metastasis in PTC

λHU in the venous phase

Five articles were used to evaluate the diagnostic value of λHU in LN metastasis in the venous phase. The heterogeneity test showed I² = 97.5%, so the random-effect model analysis was used. The result showed that there was no significant difference in the λHU between metastatic and non-metastatic LNs in the venous phase (SMD: 0.55, 95% CI: -0.05 to 1.16, P = 0.074). The diagnostic value of λHU in LN metastasis in the venous phase is summarized in Table 2.

λHU in the arterial phase

The diagnostic value of λHU for LN metastasis in PTC in the arterial phase was evaluated in 6 studies. The result of random-effect analysis indicated that the λHU in the arterial phase of metastatic LNs was higher than that of non-metastatic LNs in PTC (SMD: 0.99, 95% CI: 0.59 to 1.40, P < 0.05). The diagnostic value of λHU for LN metastasis in PTC in the arterial phase is shown in Table 2 and Fig. 5.

Sensitivity analysis and publication bias

Sensitivity analyses showed that no single study would influence the overall findings, indicating the reliability and robustness of the results. The results of heterogeneity revealed no evidence of publication bias in this meta-analysis.

In recent years, dual-energy CT has shown good application prospects in detecting LN metastasis in PTC [11]. However, there is still no meta-analysis to assess the diagnostic value of dual-energy CT parameters for LN metastasis in PTC. Herein, we conducted this meta-analysis, based on the included studies to evaluate whether parameters based on dual-energy CT are associated with LN metastasis in PTC. The results illustrated that the use of dual-energy CT parameters including IC, NIC, and λHU was related to the LN metastasis.

IC and NIC can reflect the difference in iodine contents of LNs, and indirectly, their blood supply [27]. In our study, IC metastatic LNs were significantly higher than those without LNs. A study assessing the preoperative of cervical LN metastases in patients with PTC found that metastatic LNs showed significantly higher values for IC [26]. However, Tawfik et al. suggested that the iodine content of metastatic LNs of squamous cell carcinoma was lower than that of non-metastatic LNs, which was different from the results of the present study. We hypothesized that it might be related to the different types of LNs [28]. The measured IC was divided by the intra-arterial IC, known as the NIC, which was designed to reduce differences between patients, scan time, and IC. In this meta-analysis, the NIC of metastatic LNs was higher than that of non-metastatic LNs in both arterial and venous phases. Consistent with our findings, Liu et al. found that NIC during both arterial and venous phases was significantly higher in metastatic than in benign LNs [29]. A study by Wu et al. reported that the NIC of metastatic LNs was significantly higher than those of benign LNs [12]. IC of LNs can accurately show the uptake of iodine contrast agent, and the increase in the number of small vascular beds in metastatic LNs and the altered pattern of tumor-associated vessels may contribute to the increase of IC and NIC values [30, 31].

Dual-energy CT scanning can simultaneously obtain material data under high and low-energy X-rays, obtain the attenuation data of material under different energies, and form the energy spectrum curve of substances [32]. The λHU value measured on the energy spectrum curve describes the dynamic change of CT values, and each tissue type has its characteristic λHU [33]. The results of this study illustrated that the λHU of metastatic LNs in the arterial phase of PTC were higher than those of non-metastatic LNs. Wu et al. also found that λHU of metastatic LNs was significantly higher than those of benign LNs [12]. A study by Liu et al. demonstrated that the λHU had significantly high accuracy in identifying metastatic cervical LNs in PTC patients [29]. A study evaluating dual-energy CT for the detection of metastatic LNs in patients with hepatocellular carcinoma has found that dual-energy CT quantitative parameter analysis can be used in the diagnosis of LN metastasis in PTC [27]. The maximum short-axis diameter in the portal phase combined with quantitative parameters (IC, NIC, or λHU) of dual-energy CT has more advantages in the evaluation of regional LNs. In the future, the diagnostic value of CT image features combined with quantitative dual-energy CT parameters for LN metastasis of PTC needs more studies to explore. In addition, no significant difference in the λHU between metastatic and non-metastatic LNs in the venous phase in this study. We speculate that the possible reason is the difference in blood supply between the venous and arterial phases [34].

Dual-energy CT provides an objective, quantitative, and non-invasive evaluation method for the diagnosis and differential diagnosis of diseases. In addition to conventional image features, dual-energy CT can obtain quantitative parameters based on iodine maps and energy spectrum curves. Our study found that quantitative parameters based on dual-energy CT had clinical value in the diagnosis of LN metastasis in PTC, which provides ideas for the clinical judgment of LN metastasis in PTC. Using these quantitative parameters to evaluate LN metastasis in PTC patients can help radiologists avoid subjective bias related to experience. Our study may encourage more studies to explore the diagnostic accuracy of quantitative parameters based on dual-energy CT.

However, this meta-analysis has some limitations. First, our results may be influenced by the small number of included studies and the limited sample size. Second, this study did not conduct a stratified analysis of the models of dual-energy CT, which may have influenced the accuracy of the results. Third, due to this meta-analysis containing a limited number of studies, we did not conduct a subgroup analysis for the location of LN metastasis. More studies are needed to explore the relationship and diagnostic value of quantitative parameters based on dual-energy CT for LN metastasis in PTC.

The current meta-analysis indicated that the IC, NIC, and λHU were associated with LN metastases in patients with PTC. The parameters obtained on dual-energy CT may have important clinical value for the evaluation of LN metastases in patients with PTC.

i) Ethics approval and consent to participate

Not applicable.

ii) Consent for publication

Not applicable.

iii) Availability of Data and Material (ADM)

The datasets used or analysed during the this study are available from the corresponding author on reasonable request.

iv) Competing interests

The authors declare that they have no competing interests.

v) Funding

There was no funding source for this study. All authors

had full access to all the data in the study ,and the corresponding author had final responsibility for the decision to submit for publication.

vi) Authors' contributions

Wenhui Wu, Jianming Li and An Zhang contributed to the literature search and study concept and design. Wenhui WU and Jianming Li contributed to the data acquisition. Wenhui Wu,Jianming Li and Xuewen Fang contributed to the data analysis.Wenhui Wu, Jianming Li ,An Zhang and Xuewen Fang contributed to the data interpretation. Wenhui Wu ,Xuewen Fang and Jianming Li drafted the manuscript. All authors contributed to critical revision to the manuscript.Wenhui Wu prepared figures 1-5,Jianming Li and An Zhang prepared Table 1 and Table 2. All authors reviewed the manuscript.

vii) Acknowledgment

Not applicable.

Statements of Data

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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Table 1 Basic characteristics of included studies

Author	Year	Country	Study design	Number of patients	Patients	Number of patients with LN metastasis	Number of LNs (metastasis: non-metastatic)	Age (years)	Sex (male: female)	Dual-energy CT model	Quantitative parameters	Quality
Jin	2017	China	Retrospective study	50	PTC	NA	51:22	29.63±11.21	15:35	Somatom Definition, Siemens Healthcare, Forchheim, Germany	λHU	7
Zheng	2017	China	Retrospective study	43	PTC	NA	55:64	43.4±14.3	11:32	Siemens Definition dual source CT Scanner	IC, NIC, λHU	6
Jin	2018	China	Retrospective study	50	PTC	NA	51:22	29.63±11.21	15:35	Syngo MMWP, version 2008A; Siemens Medical Solutions	NIC	7
Huang	2019	China	Retrospective study	95	PTMC	59	NA	43±11	24:71	Somatonm Definition Flash, Siemens Healthcare, Forchheim, Germany	IC, NIC	7
Guo	2019	China	Retrospective study	30	PTC	NA	49:25	37.0±1.5	11:19	Siemens Somatom Definition Flash dual-source spiral CT	IC, NIC, λHU	7
Min	2020	China	Retrospective study	340	PTC	178	NA	52.09±7.88(case); 47.52±10.31(control)	33:91(case); 67:149(control)	Somatonm Definition F1ash, Siemens Medical Solutions, Forchheim, Germany	IC, NIC, λHU	6
Zou	2021	China	Retrospective study	417	PTC	139	NA	47±11	106:311	Siemens Somatom Definition Flash second generation dual-source 64-slice CT scanner	IC, NIC	7
Xu	2021	China	Retrospective study	103	PTC	NA	107:138	45±7	48:55	Siemens Force third generation dual-source CT	NIC, λHU
Meng	2021	China	Retrospective study	165	PTC	79	NA	44.91±13.26(case); 50.42±14.11(control)	32:47(case); 19:67(control)	Somatom definition Force CT	IC, NIC	7
Chou	2021	China	Retrospective study	75	PTC	NA	70:89	53.54±4.02	23:52	Somatom definition Flash	NIC, λHU	7
Zou	2021	China	Retrospective study	52	PTC	NA	139:220	44.3±11.4	11:42	Somatom Definition Flash, Siemens Healthcare, Forchheim, Germany	IC, NIC, λHU	7
Yoon	2021	Korea	Retrospective study	102	PTC	49	NA	46±15	32:70	iU22, Philips Healthcare, Andover, MA, USA; Aplio i700, Canon Medical Systems Corporation, Tustin, CA, USA	IC, NIC, λHU	6

Notes: LN, lymph node; CT, computed tomography; PTMC, papillary thyroid microcarcinoma; PTC, papillary thyroid cancer; IC, iodine concentration; NIC, normalized iodine concentration; λHU: slope of the energy spectrum curve

Table 2 The diagnostic value of quantitative parameters of dual-energy CT for LNs metastasis in PTC

Quantitative parameters	Outcomes	SMD (95%CI)	P	I²(%)
IC in the venous phase	LN metastasis	0.33 (0.06 to 0.60)	0.015	0.00
IC in the venous phase	LN metastasis of the primary lesions	0.44 (-0.06 to 0.94)	0.085	93.10
IC in the arterial phase	LN metastasis	1.44 (-0.86 to 3.74)	0.219	99.90
IC in the arterial phase	LN metastasis of the primary lesions	0.23 (-0.37 to 0.84)	0.451	94.80
NIC in the venous phase	LN metastasis	0.15 (0.12 to 0.19)	0.006	72.00
NIC in the venous phase	LN metastasis of the primary lesions	-0.12 (-0.45 to 0.21)	0.468	99.70
NIC in the arterial phase	LN metastasis	0.22 (0.16 to 0.28)	<0.05	90.90
NIC in the arterial phase	LN metastasis of the primary lesions	0.01 (-0.03 to 0.05)	0.614	93.50
λHU in the venous phase	LN metastasis	0.55 (-0.05 to 1.16)	0.074	97.50
λHU in the arterial phase	LN metastasis	0.99 (0.59 to 1.40)	<0.05	97.80

Notes: LN, lymph node; CT, computed tomography; PTC, papillary thyroid cancer; SMD, standardized mean difference; CI, confidence interval; IC, iodine concentration; NIC, normalized iodine concentration; λHU: slope of the energy spectrum curve.

No competing interests reported.

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Meta-analysis of the diagnostic value of dual-energy computed tomography parameters for lymph node metastasis in papillary thyroid cancer

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Abstract

Figures

Introduction

Methods

Retrieval strategy

Inclusion and exclusion criteria

Data extraction and quality assessment

Statistical analysis

Results

Diagnostic value of IC for LN metastasis in PTC

IC in the venous phase

IC in the arterial phase

Diagnostic value of NIC for LN metastasis in PTC

NIC in the venous phase

NIC in the arterial phase

Diagnostic value of λHU for LN metastasis in PTC

λHU in the venous phase

λHU in the arterial phase

Sensitivity analysis and publication bias

Discussion

Conclusions

Declarations

References

Tables

Additional Declarations

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