Original Article
Ultrasound scan-guided core sampling for diagnosis
versus freehand FNAC of the thyroid gland
P. Mehrotra1 J. G. H. Hubbard2 S. J. Johnson3 D. L. Richardson3 R. Bliss3 T. W. J. Lennard1
1University of Newcastle upon Tyne
2St. Thomas’s Hospital, London
3Royal Victoria Infirmary, Newcastle upon Tyne
Correspondence to: P. Mehrotra, 16 Shortridge Terrace, Jesmond, Newcastle upon Tyne, NE2 2JE Email: Pallavi.Mehrotra@ncl.ac.uk
Background and Aim: Freehand fine needle aspiration cytology (FNAC) is an obligatory investigation of the thyroid nodule. Between 5.0-43.1% of FNAC samples are reported as being initially unsatisfactory. In our unit, thyroid freehand FNAs are performed with a small needle (21 or 23G). Non-dominant nodules as part of multinodular goitres, difficult to palpate nodules or nodules with previously unsatisfactory freehand FNACs are sampled under ultrasound scan (USS) guidance with the larger 20G cutting core sampling technique. We aimed to compare the satisfactory sampling rate and safety of the two different methods. Patients and Methods: Cytology forms were reviewed for 262 freehand FNACs and USS-guided core samples, performed in our unit over a two-year interval (1 July 1999 to 30 June 2001). Results: Ultrasound-guided core samples for cytology were unsatisfactory (AC0-1) in 19/121 (15.6%) of the cases, compared with 66/141 (46.8%) of freehand FNACs (p value=<0.0001). Ten out of eleven patients (91%) had a satisfactory USS-guided core after an unsatisfactory freehand FNA; 7/15 patients (46.7%) had satisfactory repeat freehand FNACs following an initial unsatisfactory freehand FNAC (p value=0.0191). There were no complications as a result of either freehand FNAC or USS-guided core sampling. Conclusion: USS-guided cores provided more satisfactory samples for assessment than freehand FNACs. The USS-guided technique is safe despite the use of the larger cutting needle. The USS-guided core sampling was also a useful tool for repeat thyroid nodule sampling after an unsatisfactory freehand FNAC
Keywords: Fine Needle Aspiration (FNAC), cytology, ultrasound scan, thyroid gland Surgeon, 1 February 2005, 1-5
Solitary thyroid nodules of varying aetiology affect 3.2% of a non-iodine deficient population (0.8% males, 5.3% females) and are the most common condition presenting to the endocrine surgeon.1 Freehand FNAC in the clinic has become an obligatory part of the assessment of a thyroid nodule and serves to establish the diagnosis and initiate a treatment plan, where needed. There are, however, limitations with FNAC, particularly in the case of follicular lesions. In the latter, the technique is unable to differentiate between benign and malignant follicular neoplasms. Also, it is difficult to distinguish follicular neoplasms from hyperplastic nodules within a multinodular goitre. In addition, 5.0-43.1% of freehand FNACs are initially unsatisfactory necessitating repeat sampling.
2-8 Several authors have advocated the use of USS-guided biopsy for histology or USS-guided FNA for cytology to improve the diagnostic adequacy of thyroid nodule sampling (Table 1).3-5
| TABLE 1. REVIEW OF FREEHAND AND USS-GUIDED CYTOLOGY RESULTS | |||
|
Author
|
Freehand(FH)/ USS-guided |
Gauge of needle (G) | Percentage of unsatisfactory biopsies (%) |
| Rosen et al 1993 | USS | 22 or 25G | 32 |
|
Hatada et al 1998 |
FH | 22G | 30 |
| USS | 22G | 17 | |
|
Danese et al 1998 |
FH | 21 or 23G | 8.7 |
| USS | 21 or 23G | 3.5 | |
|
Carmeci et al 1998 |
FH | 22 or 25G | 16 |
| USS | 22 or 25G | 7 | |
|
McHenry et al 1999 |
FH | Not stated | 29 |
|
Leenhardt et al 1999 |
USS | 25G | 19 |
|
Baloch et al 2000 |
USS | 25G | 5 |
|
Tabaqchali et al 2000 |
FH | 23G | 43.1 |
|
Tangpricha et al 2001 |
FH | 21G | 12 |
| FH | 25G | 12 | |
| Court-Payen et al 2002 | USS | 21G | 16.4 |
| Ko et al 2003 |
FH | 23G | 5 |
In our institution, cytological examination of thyroid nodules is performed following either freehand FNA by clinicians using a 21 or 23 gauge needle or under USS guidance by a single radiologist using a 20 gauge core technique to provide a sample for cytology. The aim of this study was to audit the satisfactory sample rate of freehand FNA and USS-guided core for cytology and to examine the safety of the two techniques.
A total of 262 thyroid cytology specimens were obtained in our unit over a two-year interval (1 July 1999 to 30 June 2001) and all were included in the study. This included both initial and repeat samples as well as freehand FNAs or USS-guided core samples sent along with cyst aspirations. The cytology request and result forms were examined in the Department of Cytology, Cellular Pathology. Note was taken of the clinical details, the individual performing the aspiration, the cytology results and the presence or absence of a cyst. The cytology results were expressed as free text and then summarised as an AC (Aspiration Cytology) grade as follows: AC0/1 - these are cytologically unsatisfactory specimens containing no follicular epithelial cells or less than six groups of epithelial cells (if, however, colloid and/or macrophages are present this may suggest a colloid nodule/cyst which would be useful in the appropriate clinical context); AC2 - these contain sufficient numbers of normal follicular epithelial cells (a non-neoplastic result); AC3 - an equivocal result, in practice usually reflecting a follicular lesion when thyroid lobectomy is required for a histological diagnosis; AC4 - suspicious of malignancy (type will be stated); AC5 - diagnostic of malignancy (type will be stated).
The freehand FNAs were all performed by an endocrine surgeon or an endocrinologist with either a 21 or 23 gauge needle and a 10ml disposable syringe for aspiration which was mounted on a dedicated syringe holder. A minimum of five passes were performed with the fine needle and local anaesthetic was not used. Non-dominant nodules as part of multinodular goitre, difficult to palpate nodules or nodules with previously unsatisfactory (AC0-1) freehand FNACs were sampled under USS guidance by a designated radiologist (DLR). The nodules were identified with a high frequency linear array transducer (7-10MHz, Toshiba and Siemens) and samples taken under local anaesthetic with a larger core cutting needle using the Biopty gun (20G, Bard). Following the procedure patients remained sitting for 15 minutes to observe for any complications.
The material obtained, either by freehand aspiration or USS-guided core, was then expressed onto glass microscope slides and spread (using another slide on top, under the weight of that slide and drawing the material across the slides). The slides were then rapidly air dried by waving in the air. The needle was washed out into a bottle of washout preservative fluid. Any fluid aspirated (e.g. from a cyst) was submitted in a plain container. No immediate assessment of cellularity was made at the time of aspiration. In the cytology department, the spread slides were stained with May-Grunwald-Giemsa (MGG); a megafunnel preparation was made from the washout fluid and stained with Papanicolau stain; six direct spreads were made from any fluid and then also stained with MGG. All cytology specimens were examined and reported by consultant cytopathologists.
Data were analysed using the Chi square test comparing the satisfactory sample result obtained by freehand FNAs to USSguided cores. A p value of less than 0.05 was considered to be statistically significant.
During the two-year study period a total of 262 thyroid cytology aspirates from 225 patients were obtained; 121 by USS-guided core and 141 by freehand FNA. These included both initial and repeat samples as well as freehand FNAs or USS-guided cores from colloid nodules or following cyst aspiration.
In the USS-guided group, 19/121 (15.6%) cytology samples were cytologically unsatisfactory (AC0-1) as opposed to 66/141 (46.8%) freehand FNAs; this analysis included cysts and colloid nodules (Figure 1, Table 2). This is a statistically significant difference (Chi square=28.748, p value=<0.0001). Seventy of these cytology samples were obtained from solitary nodules and 51 from multinodular goitres.
Figure 1: Freehand FNAs and USS-guided cytology results.
|
TABLE 2. FREEHAND FNA AND USS-GUIDED CYTOLOGY OUTCOMES |
||
| Cytology Report | USS-Guided Core (%) |
Freehand FNA (%) |
|
Unsatisfactory (AC0-1)
|
19 (15.6) | 66 (46.8) |
| Satisfactory (AC2-5) | 102 (84.4) | 75 (58.2) |
| Total FNAs | 121 | 141 |
If all cysts and colloid nodules are excluded from analysis of adequacy, 8/65 (12.31%) USS-guided cores were cytologically unsatisfactory (AC0-1), compared with 38/73 (52.05%) of freehand FNAs (Figure 2, Table 3). This is a statistically significant difference (Chi square=24.444, p value=<0.0001). Thirty-four of the patients with initial unsatisfactory freehand or USS-guided samples had repeat FNAs. In this group, 26 patients had the initial sample taken by freehand FNA. Of these, 11 patients had had the subsequent sample taken by USS-guided core, 10 (91%) of which were satisfactory. Fifteen patients had the initial unsatisfactory freehand FNA followed by a repeat freehand FNA, of which only seven (46.7%) were satisfactory (Table 4). This is a statistically significant difference
(Chi square=5.488, p value =0.0191).
Figure 2: Freehand FNA and USS-guided cytology outcomes (excluding cysts and colloid nodules).
| TABLE 3. FREEHAND FNA AND USS-GUIDED CYTOLOGY OUTCOMES (EXCLUDING CYSTS AND COLLOID NODULES) | ||
| Cytology Report | USS-Guided Core (%) |
Freehand FNA (%) |
| Unsatisfactory (AC0-1) | 8 (12.31) | 38 (52.05) |
|
Satisfactory (AC2-5) |
57 (87.69) | 35 (47.95) |
| Total FNAs | 65 | 73 |
Four surgical consultants, four medical consultants, five surgical middle grades and five medical middle grades performed the freehand FNAs during the study period. The inadequacy rate for freehand FNAs was lower for surgical consultants and middle grades (34.3% and 35.1% respectively) than for medical consultants and middle grades (65.0% and 58.3% respectively). There were no clinical complications as a result of the USS-guided core sampling for cytology; there were also no complications as a result of the freehand FNAs.
Freehand FNAC for the diagnosis of thyroid nodules is regarded as a rapid, safe and inexpensive investigation. However, several authors have outlined the high proportion of cytologically unsatisfactory samples obtained which ranged from 5.0 to 43.1%.2-8 This enhances patient worry and doctor frustration, especially if combined with worrying features on USS examination and/or clinical assessment that necessitate repeat sampling. Included in these samples will be colloid nodules/cysts which will typically produce few if any epithelial cells.
|
TABLE 4. REPEAT SAMPLING FOLLOWING INITIAL UNSATISFACTORY FREEHAND FNAs |
|||
| Repeat Procedure | Number of Samples |
Satisfactory Sample (%) |
Unsatisfactory Sample (%) |
| Freehand FNA | 15 | 7 (46.7) | 8 (53.3) |
|
USS core biopsies |
11 | 10 (91.0) | 1 (9.0) |
Recent work has shown that USS-guided samples for cytological or histological examination of the thyroid gland can increase the sensitivity and specificity for diagnosis of neoplasia and decrease the unsatisfactory rate, compared with freehand FNAs.3-5 As a result, the use of USS as an aid to obtain thyroid specimens for histology or cytology has expanded in recent years. Its main advantages are that it allows a greater definition of the character of the thyroid nodule, compared with manual palpation alone, and can identify non-palpable nodules as small as 0.3cm.
The aim of our study was to specifically assess the satisfactory and unsatisfactory rates of USS-guided core sampling for cytology and freehand FNAC. Our results indicate that USS-guided core sampling for cytology provides fewer unsatisfactory samples (15.6%) than freehand FNAs (46.8%). These results compare favourably with other studies which report an USS-guided unsatisfactory rates ranging from 16.4% to 32%.3,9-11 However, the USS-guided unsatisfactory rate is reported to be even lower in a few centres.4,5,12
Cysts and colloid nodules usually contain few if any epithelial cells, and fluid specimens are often not assigned a cytology grade. The data on FNA adequacy were analysed, including cytology samples that were reported to be either cysts or colloid nodules on the cytology request form. The data were subsequently analysed following exclusion of these lesions. The unsatisfactory rate of USS-guided core sampling for cytology decreased from 15.6% to 12.31%. However, the freehand FNA unsatisfactory rate increased from 46.8% to 52.05%. This analysis suggests that if a cystic lesion or a solitary colloid nodule are suspected freehand FNAC should be the initial investigation of choice. However, if the nodule which needs to be sampled is part of a multinodular goitre, then it may be preferable to initially perform an USS-guided core sample for cytology.
Fine needle aspiration assessment is still important in cystic lesions as rarely some malignancies can have a cystic component.6 For the clinician, a nodule with a reassuring USS and clinical features along with an AC0/1 cytology grade consistent with a colloid nodule is reassuring. Therefore, not all “inadequate” (AC0/1) FNAs are repeated.
The USS-guided technique provided a greater satisfactory rate (91%) compared with freehand FNAC (46.7%), when used to provide a repeat sample following an unsatisfactory freehand FNA. This supports the role of USS-guided cores to supply repeat cytology samples following unsatisfactory freehand FNAC.
There are a number of possible explanations for the greater reliability rate of USS-core sampling compared with freehand FNAs. Firstly, the USS-guided cores are all performed by a designated radiologist with many years experience in interventional radiology whereas the freehand FNAs are performed by endocrinologists and endocrine surgeons with a variable range of experience. Notably, in our study, the consultant endocrine surgeons and middle grades had a greater adequacy rate for freehand FNAs than the consultant endocrinologists and medical middle grades. This provides further argument for a move towards a designated FNA service with limits on the numbers of aspirators in order to improve FNA quality. Secondly, the USS-guided core is performed using a larger needle (20G) compared with freehand FNAs (21 or 23G needles) and provides more cellular specimens. This may partly account for the greater reliability rates of USSguided cores. Thirdly, thyroid nodules can be localised far more accurately under direct vision using USS which may be another factor contributing to the improved rates in the USScore group. It is important to recognise that the two techniques are, in part, used in different patient groups and this in itself may affect results.
USS-guided core sampling for cytology was not associated with any clinical complications. The use of the larger needle is widely thought to produce more concomittant contamination by blood, therefore preventing adequate cytological examination. In our study, the core technique was associated with a greater reliability rate in comparison with freehand FNA without any additional complications. A larger study is currently underway to assess and compare the diagnostic accuracy of the two procedures.
A direct cost comparison is difficult to quantify between the two techniques. The cytologist times would be similar for both groups per FNA. However, the extra costs of radiologist time along with the extra core Biopty gun and needles would be offset against the extra freehand FNAs that are performed in outpatient clinics due to high rates of unsatsifactory cytology and extra clinic appointments and time delays required to make a diagnosis.
In experienced hands, USS-guided core sampling for cytological examination leads to a greater proportion of satisfactory samples than freehand FNA. The USS-guided technique is safe despite the use of the larger, cutting core needle. It is also a useful tool for repeat thyroid sampling following an unsatisfactory freehand FNA or as part of the assessment of multinodular goitre.
Copyright 14 December 2004
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