Comparison of conventional cytology and SurePath in

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and SurePathâ (SP) (TriPath Imaging, Inc., Burlington, NC, USA) are increasing ..... tion biopsy of papillary thyroid carcinoma: logistic regression analysis.
Accepted: 17 February 2017 DOI: 10.1111/cyt.12430

ORIGINAL ARTICLE

Comparison of conventional cytology and SurePath in split thyroid fine needle aspiration materials D. Sahin1 | D. Yilmazbayhan2 | P. Firat2 | U. P. Hacisalihoglu2 | S. H. Kirimlioglu3 | E. Celenk4 | R. Arslan4 1 Department of Pathology, Acıbadem Health Group, Istanbul, Turkey 2 Department of Pathology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey 3

Acıbadem University, Istanbul, Turkey

4

Department of Radiology, Istanbul Faculty of Medicine, Istanbul, Turkey Correspondence Davut Sahin, Acıbadem Saglik Grubu, 34318, Istanbul, Turkey. Email: [email protected]

Objective: The aim of the present study was to compare the cytomorphological features and cytopathological diagnoses in thyroid aspiration materials prepared by SurePathâ (SP) and conventional cytology (CC). Materials and methods: Fine needle aspiration (FNA) materials from 180 thyroid nodules were divided into two groups to prepare three conventional smears and one SP slide. Twenty-nine cytomorphological features of thyroid lesions were compared in the CC and SP slides. The Kappa coefficiency was determined for each. The cytopathological diagnosis of CC and SP were compared. Results: The feature with the lowest Kappa coefficient was the haemorrhagic background, whereas nuclear molding had the highest Kappa coefficient. The rates of the atypical and suspicious cytopathological diagnostic categories were decreased, whereas the rates of benign and malignant categories were increased in SP. When the cytopathological diagnoses of CC and SP were compared with the histopathological diagnoses of the 31 thyroidectomy materials, the results were similar. Conclusion: The common problems seen in CC, such as an excessive number of slides, a haemorrhagic background and air drying artefact in the SP method were not encountered. Through these advantages, the rate of the indeterminate cytopathological diagnosis was low in SP. In addition to those advantages, the increased rates of non-diagnostic cases, the difficulty in evaluating the cytomorphologic features owing to tridimensional structures and the smaller size of the cells and the presence of tridimensional structures uninterpreted microscopically were the disadvantages of SP. The present results showed that SP could be used instead of CC in thyroid cytopathology. KEYWORDS

conventional cytology, fine needle aspiration, SurePath, thyroid

1 | INTRODUCTION

conventional cytology (CC) and liquid-based cytology (LBC), which are employed extensively.3–5 Problems associated with CC include

Palpable thyroid nodules occur in 4%–7% of the population,

the high incidence of non-diagnostic and indeterminate results, the

but nodules found incidentally on ultrasonography (USG) suggest a

encumbered workload for cytopathologists and the lack of reserved

prevalence of 19%–67%.1 The most common method to differentiate

material to use in cases with indeterminate diagnoses.3–6 These fac-

between neoplastic non-neoplastic and benign malignant thyroid

tors gave rise to the need to develop LBC as an alternative to CC.

nodules is fine needle aspiration (FNA) cytology.2–4 Two methods

Major reasons for non-diagnostic and indeterminate diagnosis with

are used for the preparation of thyroid aspiration materials:

CC are the hypocellularity of the aspirations, a haemorrhagic

Cytopathology. 2017;1–8.

wileyonlinelibrary.com/journal/cyt

© 2017 John Wiley & Sons Ltd

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background, the thickness of the smear, inadequate fixation and

along with the other slide that was fixed with alcohol. The air-

crush artefacts. To increase the quality of the smears and establish

dried slide was stained with MGG. After the CC slides had been

standardisation in thyroid cytology, the use of FDA-approved LBC

prepared, residual material that remained in the needle and syr-

techniques, ThinPrepâ (TP) (Cytyc Corp., Marlborough, MA, USA)

inge was rinsed in the 25-cc SP CytorichTM red preservative fluid

and SurePathâ (SP) (TriPath Imaging, Inc., Burlington, NC, USA) are

in the falcon tube. The material that was placed in the SP Cytor-

increasing steadily.5,7 It has been demonstrated that the high-quality

ich solution was first homogenised via vortex, and then half of

smears and cell blocks increase the diagnostic sensitivity while

this material was extracted from the falcon tubes and placed in

decreasing the cytopathologist’s workload. LBC allows for the prepa-

special cytocentrifuge tubes to prepare SP preparate. The material

ration of new preparates before the final diagnosis in doubt cases

remaining in the falcon tubes was stored as reserve material. The

and reserves material for immunohistochemistry (IHC) or molecular

SP slides were stained with modified PAP stain in the slide pro-

pathological tests, which are the additional advantages of LBC over

cessor apparatus (Prep Stainâ Slide Processor). The SP slides were

CC.5,7,8 As a result of these advantages, LBC should be preferred

examined by a cytopathologist for specimen adequacy. From the

over CC.8,9

SP slides, 49 cases were deemed inadequate for a cytopathologi-

Most of the studies that compared CC and LBC were CC-TP

cal diagnosis, and three cases with staining artefacts were

comparisons.5,7–11 Very few studies have compared CC with SP.12–14

excluded from the study. The adequacy criteria for SP was the

One of the aims of this study was to compare the 29 cytomorpho-

same as in CC; five to six groups containing at least 10 cells were

logical features used in the diagnosis of thyroid lesions in CC and SP

deemed adequate.

preparates that have been prepared from the split materials and to

An SPSS data table were compiled comparing the Kappa coeffi-

determine the Kappa coefficient. Another aim is to answer the ques-

cient between CC and SP preparates based on 29 cytomorphological

tion of whether SP can be presented as an alternative method to

features and the CC and SP diagnoses. The SP preparates of each

CC.

case were evaluated by one senior and one junior cytopathologist (DYB, DS). Each of the 29 cytomorphological features of Kappa coefficiency that were examined was entered into the SPSS table as

2 | MATERIALS AND METHODS

absent or indistinct (0), present (1), or very prominent (2). SP cytopathological diagnoses were also noted in the table. Two inde-

This prospective study, entailing subjects who underwent FNA, was

pendent cytopathologists, one of them senior and the other junior

conducted at Istanbul University Medical Faculty’s Radiology Depart-

(PF, PH) who did not know the SP data and diagnoses, examined the

ment. Informed consent obtained from 254 patients. USG-guided

CC preparates, and entered their own scores and diagnoses into the

aspirations were performed by radiologists using 22-gauge needles

table. Five categories (other than nondiagnostic) from the Bethesda

and 10-cc syringes. Bethesda System adequacy criteria were applied.

system were entered into the diagnosis column. These diagnostic

Twenty-two cases that did not have an adequate number of cells at

categories were: 1 - Benign, 2 - Atypical, 3 - Suspicious for follicular

on-site evaluation slides, 49 cases that had an adequate number of

neoplasm (SFN), 4 - Suspicious for a malignancy (SM) and 5 - Malig-

cells for CC but not SP and three cases that had staining artefacts at

nant. After entering the data and diagnoses into the data table, the

SP slides were excluded from the study. FNA of 180 from 168

29 cytomorphological characteristics were cross-tabulated in a simi-

patients during the July–December 2013 period and the subsequent

lar Table 1. The results from the 29 cross tables were then collected

31 resections from the period between 2014 and 2015 at the same

into a common table (Table 2). Two separate tables were designed

facility were included in the study. The study was conducted with

to compare the assigned CC and SP diagnoses and the histopatho-

the FNA specimens of 180 thyroid nodules from 168 patients pos-

logical diagnoses between the CC and SP (Tables 3 and 4).

sessing an adequate number of cells for evaluation and the thyroidectomy materials of 31 patients. For the CC and SP preparates, samples composed of at least 10 cells containing five to six follicle

T A B L E 1 The cross tabulation of cellularity SP

epithelial cell groups were accepted as adequate. Re-aspiration was performed for the cases with an inadequate number of cells. No

Cellularity

more than three aspirations were performed.

CC

0

First, three CC slides were prepared from the aspiration materials from each nodule. Two of them were fixated in 95% ethyl

1

alcohol solution, and one of the slides was air-dried at room tem€ nwald-Giemsa (MGG) stain. One slide perature for the May-Gru

2

that was fixated in 95% ethyl alcohol and stained for 1 min with haematoxylin and several seconds with eosin was then subjected to on-site evaluation via a light microscope performed by a cytopathologist. The slide that was examined during onsite evaluation was destained, then restained with Papanicolaou (PAP) stain

Total

0

1

2

Total

N

2

1

0

3

%

1.1

0.6

0.0

1.7

N

1

62

7

70

%

0.6

34.4

3.9

38.9

N

0

61

46

107

%

0.0%

33.9

25.6

59.4

N

3

124

53

180

%

1.7

68.9

29.4

100.0

Kappa correlation: 0.302.

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T A B L E 2 Comparison of conventional cytology and SurePath for the Kappa coefficient for 29 cytomorphological features Cytomorphological features Value n (%)

Conventional cytology 0 n (%)

Cellularity

1 n (%)

3 (1.7)

Hemorrhage

SurePath 2 n (%)

0 n (%)

70 (38.9)

107 (59.4)

3 (1.7)

1 n (%)

2 n (%)

Kappa value

124 (68.9)

53 (29.4)

0.302

57 (31.7)

78 (43.3)

45 (25.0)

170 (94.4)

9 (5.0)

1 (0.6)

0.025

Fixation artifact

5 (2.8)

101 (56.1)

74 (41.1)

9 (5.0)

73 (40.6)

98 (54.4)

0.401

Watery colloid

134 (74.4)

31 (17.2)

15 (8.3)

145 (80.6)

30 (16.7)

5 (2.8)

0.519

66 (36.7)

84 (46.7)

30 (16.7)

59 (32.8)

93 (51.7)

28 (15.6)

0.674

Dens colloid Dens cytoplasm

158 (87.8)

9 (5.0)

13 (7.2)

159 (88.3)

15 (8.3)

6 (3.3)

0.592

Honey comb

123 (58.3)

33 (18.3)

24 (13.3)

113 (62.8)

45 (25.0)

22 (12.2)

0.420

Macrofollicle

80 (44.4)

65 (36.1)

35 (19.4)

100 (55.6)

60 (33.3)

20 (11.1)

0.418

Microfollicle

121 (67.2)

47 (26.1)

12 (6.7)

131 (72.8)

40 (22.2)

9 (5.0)

0.580

Papillae

151 (83.9)

14 (7.8)

15 (8.3)

155 (86.1)

16 (8.9)

9 (5.0)

0.646

Caps

168 (93.3)

8 (4.4)

4 (2.2)

165 (91.7)

11 (6.1)

4 (2.2)

0.607

3D structures

169 (93.9)

7 (3.9)

4 (2.2)

111 (61.7)

57 (31.7)

12 (6.7)

0.045

_Isolated cells

36 (20.0)

85 (47.2)

59 (32.8)

63 (35.0)

100 (55.6)

17 (9.4)

0.372

151 (83.9)

25 (13.9)

4 (2.2)

141 (78.3)

35 (19.4)

4 (2.2)

0.683

Pleomorphism

56 (31.1)

89 (49.4)

35 (19.4)

72 (40.0)

85 (47.2)

23 (12.8)

0.613

Nucleomegaly

95 (52.8)

51 (28.3)

33 (18.3)

111 (61.7)

50 (27.8)

19 (10.6)

0.601

NCI

132 (73.3)

29 (16.1)

19 (10.6)

128 (71.1)

39 (21.7)

13 (7.2)

0.541

INSI

133 (73.9)

34 (18.9)

13 (7.2)

146 (81.1)

26 (14.4)

8 (4.4)

0.655

Monotonous atypia

Overlapping

125 (69.4)

33 (18.3)

22 (12.2)

140 (77.8)

25 (13.9)

15 (8.3)

0.646

Molding

145 (80.6)

22 (12.2)

13 (7.2)

153 (85.0)

17 (9.4)

10 (5.6)

0.778

Lymphocytes

149 (82.8)

14 (7.8)

17 (9.4)

138 (76.7)

18 (10.0)

24 (13.3)

0.549

Oncocytes

160 (88.9)

12 (6.7)

8 (4.4)

150 (83.3)

18 (10.0)

12 (6.7)

0.555

Macrophages

113 (62.8)

52 (28.9)

15 (8.3)

77 (42.8)

62 (34.4)

41 (22.8)

0.375

Swirl pattern

166 (92.2)

8 (4.4)

6 (3.3)

177 (98.3)

1 (0.6)

2 (1.1)

0.280

Giant cells

164 (91.1)

11 (6.1)

5 (2.8)

167 (92.8)

7 (3.9)

6 (3.3)

0.413

Nuclear details

23 (12.8)

90 (50.0)

67 (37.2)

22 (12.2)

80 (44.4)

78 (43.3)

0.288

137 (76.1)

30 (16.7)

13 (7.2)

150 (83.3)

23 (12.8)

7 (3.9)

0.528

Nuclear grooves

132 (73.3)

35 (19.4)

13 (7.2)

142 (78.9)

30 (16.7)

8 (4.4)

0.698

Uninterpreted

173 (96.1)

6 (3.3)

1 (0.6)

147 (81.7)

28 (15.6)

5 (2.8)

0.046

Powdrey chromatin

Caps: dome-like papillary fragments. 3D Structures: three-dimensional tissue fragments. NCI: nuclear conture irregularity. INCI: intranuclear cytoplasmic pseudoinclusion. Uninterpreted: the structures whose cytological details cannot be interpreted.

T A B L E 3 The comparison of the cytopathological diagnosis with conventional cytology (CC) and SurePath (SP) SP diagnosis

CC diagnosis

Total

Atipical

Atipical

Benign

SFN

SM

Malignant

Total

13

8

0

2

0

23

Benign

1

119

0

0

0

120

SFN

0

2

2

4

0

8

SM

2

0

1

7

2

12

Malignant

0

0

0

0

17

17

16

129

3

13

19

180

SFN, suspicious for follicular neoplasm; SM, suspicious malignancy.

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T A B L E 4 Comparison of cytopathological diagnoses of conventional cytology and SurePath with histopathological diagnosis of 31 thyroidectomy materials N

CC diagnosis

SP diagnosis

Histopatholgical diagnosis

12

Malignant

Malignant

Malignant

1

Suspicious for malignancy

Malignant

Malignant

6

Suspicious for malignancy

Suspicious for malignancy

Malignant

3

Suspicious for follicular neoplasia

Suspicious for malignancy

Malignant

2

Suspicious for malignancy

Atypical

Malignant

1

Suspicious for follicular neoplasia

Benign

Benign

1

Suspicious for follicular neoplasia

Suspicious for follicular neoplasia

Malignant

3

Malignant

Suspicious for malignancy

Malignant

1

Atypical cells

Suspicious for malignancy

Malignant

1

Suspicious for follicular neoplasia

Suspicious for malignancy

Benign

3 | RESULTS

number of non-diagnostic cases in LBC in the literature is higher than that of CC.13–15 The present results did not correlate with the

This study was conducted prospectively, with 180 entailing subjects

results of the study by Jung et al., which compared CC and SP in

that underwent FNA and 31 of them entailing subjects that had sub-

split material.12 Jung et al. prepared two CC and two SP slides, and

sequent resection between January 2014 and December 2015. Ade-

subsequently stated that SP slides were more cellular than CC slides.

quate material was obtained by performing FNA once in 76.92% of

However, in the SP technique, after the vortex procedure, the cyto-

the cases, twice in 15.38% of the cases and three times in 7.69% of

logical material is divided into two parts, one of which is placed in

the cases, respectively. No more than three aspirations were per-

the cytorich solution and reserved, whereas the other part is used

formed. The average age of the patients was 49.17 years (min 15,

for the preparation of the slides. After the second centrifugation,

max 83). The time for determination of the nodules varied between

50% of the material placed in the slide processor apparatus is again

15 days and 30 years, and 78.3% of the patients did not have any

divided into two. Part of this is placed on the slides, and the rest is

clinical symptoms. The most frequent symptom was dysphagia

used in cell-block preparation. Using this technique, a maximum of

(10.6%). The average diameter of the nodules was 18.74 mm (5–

25% of the aspiration material can be found on one SP slide and

70 mm); 45% of the nodules were located in the left lobe; whereas

50% of the material on two. Because of this technical procedure, SP

43.3 were located in the right lobe; 6.1% were bilateral; and 4.4%

slides cannot be more cellular than the CC slides.

were located in the isthmus. Upon USG, 83.3% of the nodules were shown to be solid, 10% solid with a cystic component, and 6.1% cystic. USG also revealed the nodules to be 71.1% hypoechoic, 5.6%

4.2 | Benign

hyperechoic, and 23.4% isoechoic. Microcalcifications were present

In the present study, 120 (66.66%) of the cases at CC and 129

in 33.2% of the nodules. While 30.04% of the cases were being sub_ for the first time, the others had one or more aspirajected to I_IA

(71.66%) at SP were diagnosed as benign (Table 3). These results

tions performed previously. Of the samples that had prior _I_IA, 28.9%

colloid-rich background is an important feature for the diagnosis of

were reported as benign, 6.1% as insufficient, 5.6% as suspicious,

the benign nodules in thyroid aspiration materials.3 We could not

2.8% as atypical and 0.6% as malignant. The FNA results of the

find data for the comparison of colloid between SP and CC in the lit-

other subjects were unknown beforehand. The number of subjects

erature. According to the present results, SP is superior to CC in

with a history of thyroidectomy was 13.84%.

demonstrating colloid. Watery colloid is seen less frequently in SP

correlate well with the prevalent literature.16,17 The presence of a

than in CC. This may be because the liquid colloid is diluted in cytor-

4 | DISCUSSION

ich solution (Table 2). As another cytological feature of benign thyroid nodules, large-cell layers with a honeycomb appearance were

4.1 | Satisfactory and cellularity

more frequent in the CC method. The Kappa coefficiency for large

In the present study, the cellularity of CC slides was higher than that

ment. It was determined that the Kappa coefficients of lymphocytes

of SP slides. A low Kappa coefficient (fair agreement category)

and oncocytes were in the moderate-agreement category. The litera-

between CC and SP in terms of cellularity (Tables 1 and 2) was

ture states that Hashimoto thyroiditis can be more easily demon-

determined. Forty-nine of the cases (21.12%) that had adequate cells

strated in SP. In this study, the diagnosis of Hashimato thyroiditis

for CC interpretation did not have adequate cells for SP. These cases

was given to 18 (10%) cases in CC and 27 (15%) cases in SP. The

were excluded from the study. In correlation with our results, the

present results are in correlation with the literature.12 More

cell layers with a honeycomb appearance was of moderate agree-

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lymphocytes and oncocytes in SP than in CC were determined. Differentiating lymphocytes from naked nuclei in CC is not easy.12,14

5

4.4 | Suspicious for follicular neoplasm

The nuclei and cytoplasm of lymphocytes are more easily visible in

In our study, the diagnosis of ‘suspicious for follicular neoplasm’

SP because of the clear background and good fixation. Moreover,

was given to eight (4.44%) cases in CC and three (1.66%) cases in

the fact that naked nuclei appear less in SP affords another advan-

SP (Table 3). One reason for the difference may be the misinterpre-

tage (Table 2). Although oncocytes are small, they are seen more fre-

tation of lymphocytic thyroiditis and hyperplastic benign nodules as

quently in SP than in CC. The oncocyte cytoplasms are dense, and

neoplastic lesions in CC. Because of better fixation, the differentia-

the nuclei are more hyperchromatic. One reason that the lesser diag-

tion between the reactive and neoplastic follicular epithelial cells

nosis of atypical and SFN was given at SP could be a more accurate

can be made easily in SP. The other reason can be more common

diagnosis of Hashimoto thyroiditis at SP. The Kappa coefficient was

detection of the microfollicles at CC than SP. The Kappa coefficient

found to be low in relation to demonstrating the macrophages.

for micro and macro-follicles were moderate agreement category.

There were more cases with macrophages in SP (Table 2). This was

These features were determined to be more frequent in CC

postulated to be because of the clearer demarcation of the cyto-

(Table 2).

plasm on a clean background and the maintenance of its integrity.

4.5 | Suspicious for malignancy 4.3 | Atypical (Atypia of undetermined significance or follicular lesion of undetermined significance)

The number of cases in the ‘suspicious for malignancy’ category is

In the present study, the number of cases diagnosed as atypical

because some cases that were interpreted as atypical or SFN in CC

were 23 (12.77%) at CC and 16 (8.88%) at SP. The results

were interpreted as SM in SP (Tables 3 and 4).

higher in SP (7.22%) than in CC (6.66%). This difference might be

obtained for CC and SP correlate with the previous literature (Table 3).12,13 In the literature, it has been demonstrated that, because of the fast and efficient fixation of LBC methods, drying

4.6 | Malignant

artefacts are prevented and the image quality is increased, caus-

Our results show that the numbers of cases diagnosed to be malig-

ing a decrease in the incidence of atypical and suspicious diag-

nant were 17 (9.44%) and 19 (10.55%) cases in CC and SP, respec-

noses (Figure 1A,B).12–15 The number of cases in the present

tively. This result correlates with the literature.15,16,18,19 Powdery

study with good fixation and ascribed the degree score of 2 were

chromatin is one of the nuclear features of papillary thyroid carci-

higher in SP (n=98) than in CC (n=74) (Table 2). Although pleo-

noma. The Kappa coefficient for powdery chromatin was the moder-

morphism and nucleomegaly were more frequently observed in

ate-agreement category. This feature was found more frequently

CC compared with SP, the Kappa coefficients were high for these

with CC than with SP (Table 2). The explanation of the higher pow-

features. The haemorrhagical background is a common problem in

dery chromatin detection in CC can be a misinterpretation because

CC, which makes it difficult to reach make a definite diagnosis.

of a haemorrhagic background and the pale nuclear appearance

The present results pertaining to the negative effects of a haem-

caused by a dry artefact. In terms of papillary structures and cap-like

orrhagic background are in correlation with the prevalent litera-

papillary fragments, the results of CC and SP were close, and the

ture.12–15 This study confirmed that the SP method is superior to

Kappa coefficient was a good agreement category (Table 2). Papillary

CC in terms of obtaining a non-haemorrhagical and clean back-

structures are three-dimensional in SP. Because of that difference, a

ground. Among 29 cytomorphological features that we compared,

longer time is spent determining the cytomorphological features and

we determined that the feature with the lowest Kappa coefficient

the multiple and longer duration of microfocussing. At some of the

(the poor-agreement category) was the haemorrhagical background

tridimensional papillary structures, nuclear details of the cells cannot

(Table 2). Because of the haemorrhagical background in CC prepa-

be visualised (Figure 1C,D). It was determined that isolated cells are

rations, some cells with enlarged nuclei, cyst epithelium, macro-

seen more frequently in CC than in SP and that the Kappa coeffi-

phages and endothelial cells might not be recognised and

cient was low. Isolated cells appear on the CC slides because the

misinterpreted as atypical follicle epithelial cells (Figure 1A,B). As

cells become separated from the mechanical effect created by

described in the literature, differentiation between the follicle

spreading the material on the slide. In the present study, isolated

epithelial cells and the other cells was difficult, and this may be

epithelial cells did not appear on SP slides of benign thyroid lesions,

the reason for

increased atypical and suspicious diagnoses

but this feature was seen in papillary and medullary carcinomas. This

(Table 3).15,18,19 In SP, the number of cases with benign and

is because malignant cells lose their cohesion properties. It is stated

malignant diagnoses is high because in CC, the morphology of

that nuclear membrane irregularity is seen more frequently in LBC

the cells are disrupted because of the haemorrhagical background,

than CC (Table 2). The results of this study are correlated with the

The advantages of the

literature.12,18 In SP, some of the nuclei of some papillary carcinoma

SP method are erythrolysis and good fixation; the artefacts caus-

cells revealed nuclear membrane irregularities, which can be

artefacts of air drying and spreading.

11,12

ing atypical appearance are reduced. These advantages are effi-

described as ‘the broken-stone appearance’. The nuclei with the bro-

cient in decreasing the atypical diagnosis in SP.

ken-stone

appearance

and

a

half-missing

appearance

were

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(B)

(C)

(D)

(E)

(F)

F I G U R E 1 Benign cyst lining cells. (a) Conventional cytology. PAP 9 400. (b) Cyst lining cells with fine chromatin and prominent nucleoli. SurePath. PAP 9 400. Papillary carcinoma. (c) Papillary structures. Conventional cytology. PAP 9 200. (d) Because there are disadvantages to this technique, the cytologic details cannot be identified at the three-dimensional papillary structures. SurePath. PAP 9 200. Papillary carcinoma. (e). Intranuclear cytoplasmic pseudoinclusions. MGG 9 1000. (f) Intranuclear cytoplasmic pseudoinclusions, nuclear grooves, nuclear membrane irregularity, and pleomorphism in a threedimensional cell layer. At the threedimensional cell layers, cytologic details are hardly fixed. The size of the cells in SP are smaller than that of CC at the same highpower fields. SurePath. PAP 9 1000.

demonstrated at different levels with microfocussing. The Kappa

demonstrated than CC (Figure 1A,B). It can be said that, in the

coefficient were in the good agreement category for intranuclear

demonstration of nuclear details, the SP method is harder but also

cytoplasmic pseudo-inclusions and nuclear grooves. In SP, along with

more reliable than the CC method.

the shrinking nuclei, the inclusions also show concomitant shrinkage.

Three-dimensional structures were not seen in CC, whereas they

Because of this shrinkage, it is more difficult to see nuclear inclu-

were seen in 38.4% of the SP cases (Figure 1C,D). Similar results

sions and grooves with SP than it is with CC (Figure 1E,F). The fact

have been stated in the literature.12 The reason for the increased

that overlapping, molding and nuclear grooving demonstrate a high

frequency of the three-dimensional tissue structures in the SP

Kappa coefficient shows that these three characteristics are reliable

method is that, in this technique, aspiration material is not spreading.

indicators of neoplastic proliferation (Table 2). The swirl pattern can

Another cytomorphological feature that was found to have the low-

be demonstrated in 14%–17% of the cases with papillary carci-

est Kappa coefficient (fair-agreement category) after a haemorrhagi-

noma.18 The Kappa coefficient was low for swirl patterns that were

cal background and tridimensional figures was determined to be

demonstrated more commonly in CC than SP. The Kappa coefficient

tissue fragments, whose cytomorphological details cannot be clearly

was found to be low for chromatin structure and nucleoli-like

identified. This feature was seen in 18.4% of SP (Table 2). When

nuclear details. These characteristics were demonstrated more com-

preparing SP samples, the material taken from the centrifuge and

monly with SP. In SP, there is shrinkage of the cell and nucleus, and

applied to the slides contains tridimensional tissue fragments and cell

one must perform more careful and detailed evaluations to demon-

layers. As some of these structures are very thick and stain deeply,

strate chromatin structure, inclusions, nuclear grooves and nuclear

adequate evaluation is not possible because the cytological details

membranes. Although the nuclei are smaller in SP, morphological

are not visualised with microfocussing. Another problem caused by

details, such as nucleoli and chromatin structure, can be better

tridimensional tissue fragments is that they cause covering of

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ET AL.

T A B L E 5 Comparison of conventional cytology and SurePath in thyroid cytology Parameters

Conventional cytology

7

concomitant risk for SFN category to be 15%-30%.2–4 The present results coincide with the literature.

SurePath

5 | CONCLUSIONS

Background

Hemorrhagic

Clear

Fixation quality

_Inadequate

High

Cell type intepretation

Difficult

Easy

The problems of thyroid cytology in CC were determined, such as a

Rate of indeterminate diagnosis

High

Low

haemorrhagic

Cellularity

High

Low

SP. Those properties of SP that are superior to CC afford fewer

Nondiagnostic rate

Low

High

diagnoses of undetermined, and more diagnoses of benign and

Uninterpreted tissue fragments

No

Yes

malignant. However, the hypocellularity of the preparates, as well as

Three dimensional cell layers

No

Yes

Artifacts

Crush and air drying

Staining and covering

cussing. Although this study was conducted with only a few cases,

Number of slides

Much

Less

method to CC, which could be used in thyroid cytopathology.

€nwald-Giemsa May-Gru stainable

Yes

No

Reserved material and additional tests

No

Yes

Cost effectivty

Yes

background,

air-drying

and

crush

artefacts,

an

increased workload owing to high numbers of slides were solved in

the high number of non-diagnostic cases and structures that cannot be interpreted, are problems in SP. An disadvantage of SP, tri-dimentional structures and smaller cells need more attention and microfothe present results (Table 5) showed that SP was an alternative

REFERENCES

High cost

artefacts that may preclude microscopic evaluation (Table 5). Twenty-six (14%) SP slides covered by an automatic apparatus containing covering artefacts that precluded examination were uncovered and recovered manually. According to previous literature, some of the cytomorphological features found in LBC preparates but not in CC are tridimensional structures which cannot be interpreted microscopically, hobnail pattern of cells, naked capillaries, eosinophilic nucleoli and perinuclear halo, which are seen in papillary carcinoma.12,15,18–20. Other features are cell shrinkage, a ball shape of the follicles caused by the invisible follicular lumens, the dense basophilic debris on the background in the haemorrhagic aspirations in which inadequate Cytorich solution is used and a tridimensional appearance of the nuclei in papillary carcinomas, which makes some nuclear parts invisible (broken-stone appearance). When the cytopathological diagnoses of CC and SP with the histopathologic diagnoses of 31 thyroidectomy cases were compared, incompatibility for only three cases that affect the therapeutic approach was determined (Table 4). Of the two cases with histopathological diagnoses of malignancy, one had the diagnosis of atypical in CC, and the other had the same diagnosis in SP. For a case in which the SP and histological diagnoses were benign (in lymphocytic thyroiditis), it was noted that CC assigned a diagnosis of ‘suspicious for follicular neoplasia’. According to these results, both methods were inefficient in determining one of 30 thyroid carcinoma. Using the CC method, one benign lesion had the overdiagnosis of ‘suspicious for follicular neoplasia’. In the current literature, the rates of cases assigned with atypical diagnoses have a 5%-15% chance of being found to be malignant upon resection and the

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How to cite this article: Sahin D, Yilmazbayhan D, Firat P, et al. Comparison of conventional cytology and SurePath in split thyroid fine needle aspiration materials. Cytopathology. 2017;00:1-8. https://doi.org/10.1111/cyt.12430