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European Radiology

, Volume 27, Issue 1, pp 431–436 | Cite as

Comparison of diagnostic yield of core-needle and fine-needle aspiration biopsies of thyroid lesions: Systematic review and meta-analysis

  • Kosma Wolinski
  • Adam Stangierski
  • Marek Ruchala
Open Access
Ultrasound

Abstract

Objectives

Thyroid nodular disease is one of the most commonly observed medical conditions. Cytological evaluation of the specimens obtained with fine-needle aspiration biopsy (FNAB) is the most accurate tool for selecting nodules which should be further surgically removed. A major limitation of this method is the high occurrence of non-diagnostic results. This indicates the need for improvement of the thyroid biopsy technique. The aim of this meta-analysis was to compare the diagnostic value of thyroid core-needle biopsies (CNBs) and FNABs.

Materials and methods

PubMed/MEDLINE, Cochrane Library, Scopus, Cinahl, Academic Search Complete, Web of Knowledge, PubMed Central, PubMed Central Canada and Clinical Key databases were searched. Risk ratios (RRs) of non-diagnostic results were meta-analysed using the random-effects model.

Results

Eleven studies were included in the quantitative analysis. CNB yielded significantly more diagnostic results – the pooled risk ratio (RR) of gaining a non-diagnostic result was 0.27 (p<0.0001). For lesions with one previous non-diagnostic FNAB, RR was 0.22 (p<0.0001).

Conclusions

CNB seems to be a valuable diagnostic technique yielding a higher proportion of diagnostic results than conventional FNAB. It is also significantly more effective in case of nodules with a prior non-diagnostic result of FNAB results than repeated FNABs.

Key Points

Core-needle biopsy yields a higher proportion of diagnostic results than fine-needle biopsy.

Core-needle biopsies may decrease the amount of unnecessary thyroidectomies.

Probability of gaining non-diagnostic result using core-needle biopsy is almost four times lower.

Keywords

Fine-needle aspiration biopsy Core-needle biopsy Thyroid· Thyroid lesions Biopsy 

Introduction

Thyroid nodular disease (TND) is one of the most commonly observed medical conditions, affecting a large number of individuals, especially women, subpopulations in iodine-deficient regions, elderly people and patients with some specific clinical conditions. The prevalence of TND is high, affecting 10–70 % of the general population and malignancies are observed in 3–10 % of patients [1, 2, 3, 4, 5]. Cytological evaluation of the specimens obtained with fine-needle aspiration biopsy (FNAB) is the most accurate tool for selecting nodules which should be further surgically removed (malignancies, indeterminate follicular lesions) [6]. One of the major limitations of this method is a high occurrence of non-diagnostic results, falling in group I of the Bethesda Classification [7]. According to numerous studies, around 10–20 % of FNABs yield non-diagnostic results [8, 9, 10]. Most endocrinological societies recommend consideration of total thyroidectomy in cases of repeated FNABs with non-diagnostic results [11]. This may increase the number of unnecessary thyroidectomies and also delay the final diagnosis of thyroid cancer. This indicates the need for improvement of the thyroid biopsy technique or even searching for new tools which may decrease the prevalence of non-diagnostic results. Biopsy with the use of a core needle (CNB) is believed to be reliable improvement on FNAB, bringing high diagnostic yield [12, 13]. The aim of the current meta-analysis was to compare the diagnostic value of thyroid CNBs and FNABs.

Materials and methods

Study selection

PubMed/MEDLINE, Cochrane Library, Scopus, Cinahl, Academic Search Complete, Web of Knowledge, PubMed Central, PubMed Central Canada and Clinical Key databases from January 2001 up to December 2014 were searched in order to find all relevant, full-text journal articles written in English. We used the search term: ((“core-needle”) or (core and needle)) and thyroid. Articles comparing the percentage of diagnostic results of thyroid FNAB and CNB, performed with sonographic guidance, were included in the meta-analysis. According to the Bethesda System for Reporting Thyroid Cytopathology [14], categories II–VI are interpreted as diagnostic results. Samples classified as Bethesda category III and IV are inconclusive results in the context of differentiation between benign and malignant lesions but assessed as adequate for cytological assessment. We excluded studies about very particular groups of lesions (e.g. hyalinasing trabecular tumours, follicular tumours) and studies where FNAB or CNB was performed without ultrasound guidance. Studies without control groups, comparing results of FNAB with FNAB and CNAB performed simultaneously (without distinct data about the FNAB and CNAB results) were systematically reviewed.

Two researchers (K.W. and A.S.) searched all included databases independently and prepared a list of included studies. In case of discrepancies between lists, authors read questionable articles together.

Quality assessment of the studies

All included studies were assessed using the Newcastle-Ottawa Scale [15]. Studies with a result of seven stars or more were included.

Statistical analysis

All calculations were performed using Statistica v.10 with the medical package from Statsoft. Risk ratios (RRs) of non-diagnostic result were meta-analysed using the random-effects model. Publication bias was assessed using Kendall’s tau.

Results

The search results and steps of selection are shown in the flowchart (Fig. 1). Eleven studies were included to the meta-analysis – the basic data are shown in Table 1 [6, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25]. CNB yielded significantly a higher amount of diagnostic results. The forest plot is shown on Fig. 2. The pooled RR of non-diagnostic results was 0.27 with a 95 % confidence interval (CI) 0.16–0.46 (p<0.0001). There is no evidence for publication bias (Kendall’s tau = −0.24, two-tailed p-value = 0.31). There was evidence of significant heterogeneity (Q =85.3, df=10, i2=88.3 %, p<0.0001).
Fig. 1

Flowchart showing the steps included in the literature search and selection

Table 1

Studies comparing the diagnostic efficacy of core-needle biopsy (CNB) and fine-needle aspiration biopsy (FNAB) in lesions with a previous non-diagnostic FNAB result

Author

Year

Country

Design

Needles

FNAB – diagn.

FNAB – ndg.

CNB – diagn.

CNB – ndg.

Chen et al. [16]

2014

USA

Retrospective; no specific selection criteria – FNAB and CNB interchangeably dependent on the preference of the radiologist

FN: 25–27 G; CN: 20 G, semi-automatic biopsy device

70

26

359

6

Choi et al. [17]

2014

South Korea

Retrospective; lesions with previous ndg.

FNA: 21–23 G; CN: 18 G; automatic biopsy gun used

108

72

178

2

Lee et al. [18]

2014

South Korea

Retrospective; lesions with previous ndg.

FN: no data; CN: 18 G; automatic biopsy gun used

260

129

122

3

Stangierski et al. [19]

2013

Poland

Prospective; lesions with previous ndg.

FN: 25 G; CN: 22 G

30

29

17

13

Na et al. [20]

2012

South Korea

Prospective; FNAB and CNB simultaneously; lesions with previous ndg.

FN: 25, 23 and 21 G; CN: 18 G; automatic biopsy gun used

46

18

63

1

Samir et al. [21]

2012

USA

Retrospective; FNAB and CNB simultaneously; lesions with previous ndg.

CB: 20 G; FN: 25 G;

42 (36)*

48 (33)*

69 (51)*

21 (18)*

Sung et al. [22]

2012

South Korea

Retrospective; FNAB and CNB simultaneously

CN: 18 G; FN: 21, 23 and 25 G; automatic biopsy gun used

521

34

547

8

Park et al. [23]

2011

South Korea

Retrospective; lesions with previous ndg. FNAB

CN: 18 G, FN: no data; automatic biopsy gun used

73

69

53

1

Renshaw et al. [6]

2007

USA

Retrospective; CNB and FNAB simultaneously – lesions with previous ndg. FNAB and also as first choice

FN: 25, 23 and 21 G; CN: 18, 20, 21 G

265

112

310

67

Strauss et al. [24]

2007

USA

CNB and FNAB – lesions with previous ndg. FNAB

CN: 20 G; FN: 22, 25 G

22

59

43

38

Karstrup et al. [25]

2001

Denmark

Palpable lesions only; FNAB and CNB simultaneously;

CN: 18 G, automatic biopsy gun used; FN: 21 G

75

2

68

9

*Results for lesions with only one prior non-diagnostic biopsy were included

FN – fine needle, CN core needle, diagn. diagnostic results, ndg. non-diagnostic results

Table 2

Studies assessing the usefulness of core-needle biopsy (CNB) not included in the meta-analysis

Author

Year

Country

Design

Needles

FNAB – diagn.

FNAB – ndg.

CNB – diagn.

CNB – ndg.

Yeon et al. [26]

2013

South Korea

Retrospective; lesions with previous ndg. FNAB; no control group

CN: 18 G; FN: no data; automatic biopsy gun used

No data

No data

135

2

Khoo TK [31]

2008

USA

CNB and FNAB simultaneously compared with lesions that underwent FNAB only

No data

296

15

303*

37*

Zhang et al. [32]

2007

USA

Retrospective; CNB and FNAB simultaneously, in most cases after two ndg. FNABs

CN: 20, 22 G; FN: 25, 23 G

409

39

217*

8*

Mehrotra et al. [33]

2005

UK

Retrospective; US-guided CNB and freehand FNAB compared

CN: 20 G, automatic biopsy gun used; FN: 21 or 23 G

75

66

102

19

Harvey et al. [34]

2004

UK

Retrospective; CNB in random patients; FNAB partially without sonographic guidance

CN: 18 G; FN: 21–25 G;

159

107

69

10

Screaton et al. [35]

2002

UK

Retrospective; no control group; CNB – lesions with previous ndg. FNAB and also as first choice

CN: 16–18 G

No data

No data

199

10

*Summary data for simultaneous CNB and FNAB – without distinction of FNAB and CNB component

FN – fine needle, CN core needle, FNAB fine-needle aspiration biopsy, diagn. diagnostic results, ndg. non-diagnostic results

(Table 2)
Fig. 2

Forest plot showing individual and pooled risk ratios (RRs) of gaining non-diagnostic results with core-needle biopsy in comparison to fine-needle aspiration biopsy; with 95 % confidence intervals and p-values given in columns 2–4

We have also performed some analyses in subgroups.

Seven studies focused on lesions with one previous non-diagnostic result of FNAB [17, 18, 19, 20, 21, 23, 24]. The forest plot is shown on Fig. 3. The pooledRR of gaining a non-diagnostic result was 0.22 (95 % CI 0.10–0.45, p=0.0001). There is no evidence for publication bias (Kendall’s tau = −0.33, two-tailed p-value = 0.29). There was evidence of significant heterogeneity (Q =47.5, df=6, i2=87.37 %, p<0.0001).
Fig. 3

Cumulative forest plot for studies comparing risk ratios (RRs) of gaining non-diagnostic results with core-needle biopsy in comparison to fine-needle aspiration biopsy; with 95 % confidence intervals and p-values given in columns 2–4

Four studies from South Korea were performed with very similar methodology [17, 18, 20, 23]. Lesions with one previous non-diagnostic FNAB were included, in all studies the ACECUT system by TSK, Japan was used. For these studies the pooled RR was 0.05 (95 % CI 0.02–0.10, p<0.0001). ). There is no evidence for publication bias (Kendall’s tau = 0.0, two-tailed p-value = 1.0). There was no evidence of significant heterogeneity (Q =1.2, df=3, i2=0.0 %, p=0.76).

Discussion

CNB yielded a significantly higher percentage of diagnostic results than FNAB in lesions with previous non-diagnostic results with FNAB. RR was 0.27, which means that the probability of gaining a non-diagnostic result was almost four times lower. However, the number of studies comparing the diagnostic efficacy of FNAB was rather low. We found 11 case-control studies on the topic. In addition, these studies differed with regard to the diameters of needles and design of the study (CNB as the first-line procedure or as a procedure performed after one or more non-diagnostic FNABs, prospective/retrospective character, simultaneous CNB and FNAB, or CNB and FNAB performed in distinct groups of subjects). Among these studies, nine had shown significantly higher diagnostic effectiveness of CNB, in one the difference was not significant [19], and in one FNAB had a significantly higher percentage of diagnostic results with borderline significance [25].

We also performed subgroup analyses. We found seven studies comparing FNAB and CNB in lesions with previous non-diagnostic results with FNAB; however, those studies were diverse in terms of methodology. Among those seven studies, four showed that CNB yielded incomparably higher diagnostic effectiveness – RR of non-diagnostic result <0.1 [17, 18, 20, 23]. According to two studies, CNB was significantly more effective; however, the result was less impressive than that of the four studies mentioned above [21, 24]. Another study did not reveal any advantage of CNB over repeated FNAB [19].

These discrepancies suggest that further studies are strongly recommended. One of the possible reasons could be different diameters of fine and core needles used in particular studies. Stangierski et al. [19] used 25 G fine and 22 G core needles, Samir et al. [21] used 25 and 20 G, respectively; in the study performed by Na et al. [20] 18 G needles were used for CNB and different types of needles for FNAB (21–25 G, proportion unknown), Lee et al. [18] used 18 G core needles, data about fine needles were not given. Similarly, Yeon et al. [26] reported very a high percentage of diagnostic results with CNB with 18 G needles in lesions after one non-diagnostic FNAB (over 98 %); however, this study was not included in the meta-analysis due to the lack of a control group.

Another possible reason for this heterogeneity could result from many variables, rather difficult to meta-analyse, such as experience of the radiologist/endocrinologist performing the biopsy, number of passes, equipment used, etc. Four studies performed using similar equipment (automatic biopsy guns from the same manufacturer) in patients with one previous non-diagnostic FNAB showed very homogenous results [17, 18, 20, 23]. This fact can suggest that equipment used and group of patients selected are the most important factors influencing the findings; homogeneity in these two areas resulted in very homogenous results. Pooled results of these studies were very impressive – the risk of gaining a non-diagnostic result was 20 times lower than in the case of FNAB. According to this data, automatic biopsy guns can be helpful in patients with non-diagnostic results with FNAB. However, the invasiveness of the procedure should also be taken into account.

Another aspect worth considering is a pain sensation among patients undergoing both kinds of procedures. The number of studies on this topic is limited. Reports performed by Stangierski et al. [19] and Nasrollah et al. [27] indicate CNB is slightly more painful than FNAB; however, it is tolerable for most patients. But it is worth keeping in mind that the difference in the diameter of core and fine needles in both studies was quite small – 21G versus 23G. In a study performed by Capri et al. [28], fine needles and large needles were used. The authors report no difference in pain sensation accompanying the two procedures; however, a small amount of anaesthesia was injected subcutaneously before the biopsy. According to the accessible data, it seems that the use of core needles is not accompanied by patient intolerance and a severe pain sensation.

The current study constitutes a large meta-analysis which aims to systematize this important topic. An interesting study on this issue was published by Trimboli et al. in 2014 [29]. These authors found and briefly described many previously published studies. However, it was systematic review so there was no quantitative synthesis of the results. There was also one conceptually similar meta-analysis published by Li et al. [30]. However, the authors of that study included a smaller number of studies, five, whereas 11 studies were included in the current study. Partially this difference can be explained by the fact that quite a few studies have been published recently and were not available for Li et al. [16, 17, 18, 19]. A greater number of included studies allowed for additional analyses in subgroups (e.g. comparison of FNAB and CNB in lesions with one previous non-diagnostic FNAB). Finally, the meta-analysis published by Li et al. brought some confounding results: a visible, but nonsignificant difference in the diagnostic values of FNAB and CNB. Our study including more studies provides more definite, clinically important conclusions.

In conclusion, the CNB seems to be a valuable diagnostic technique yielding a higher proportion of diagnostic results than conventional FNAB. It is also significantly more effective in cases of nodules with prior non-diagnostic results with FNAB than repeated FNABs. However, further studies on the topic are required.

Notes

Acknowledgments

The scientific guarantor of this publication is Prof. Marek Ruchala, Head of the Department of Endocrinology, Metabolism and Internal Medicine, Poznan University of Medical Sciences. The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. This study was supported by the Poznan University of Medical Sciences, Faculty of Medicine II (grant nr 502-14-02221354-41127). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

One of the authors has significant statistical expertise. Institutional Review Board approval was not required because the study is a meta-analysis. Written informed consent was waived by the Institutional Review Board. Some study subjects or cohorts have not been previously reported.

Methodology: meta-analysis, performed at one institution.

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Copyright information

© The Author(s) 2016

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Kosma Wolinski
    • 1
  • Adam Stangierski
    • 1
  • Marek Ruchala
    • 1
  1. 1.Department of Endocrinology, Metabolism and Internal MedicinePoznan University of Medical SciencesPoznanPoland

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