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| ORIGINAL ARTICLE |
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| Year : 2019 | Volume
: 26
| Issue : 2 | Page : 110-116 |
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Comparison of the diagnostic performance of ultrasonography with fine-needle aspiration cytology in thyroid nodules
Grace Oluyemisi Bayewu1, Ayotunde O Ogunseyinde1, Omolola Mojisola Atalabi1, Gabriel Olabiyi Ogun2, Adesoji Ebenezer Adetona2
1 Department of Radiology, University College Hospital, Ibadan, Oyo State, Nigeria
2 Department of Pathology, University College Hospital, Ibadan, Oyo State, Nigeria
| Date of Web Publication | 18-Jul-2019 |
Correspondence Address:
Dr. Grace Oluyemisi Bayewu
Department of Radiology, University College Hospital, Ibadan, Oyo State
Nigeria
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/wajr.wajr_30_18
Objective: The aim of the study was to correlate the sonographic (ultrasound [US]) and color flow Doppler findings with the results of US-guided fine-needle aspiration biopsy.
Materials and Methods: This is a cross-sectional study conducted in the ultrasound suite of our hospital, South Western, Nigeria. It is a cross-sectional study on 110 adult patients with clinically palpable thyroid nodule(s) in our hospital. Sonographic scans of 110 thyroid nodules in 110 patients were performed, and characteristics of thyroid nodules that were studied included microcalcifications, an irregular or microlobulated margins, marked hypoechogenicity/hypoechogenicity, a shape that was taller than it was wide, and color flow pattern in Color Doppler ultrasound. The presence and absence of characteristics of nodules were classified as having positive or negative findings, respectively.
Results: Among 110 solid thyroid nodules, 23 lesions were classified as positive considering the sonographic characteristics and 9 of them were proved to be malignant on histopathology. Of 87 lesions which were classified as negative, none was proved to be malignant. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value based on our sonographic classification method were 100%, 86%, 36%, and 100%, respectively.
Conclusion: This study showed that ultrasound can be sensitive and specific for thyroid nodules but the PPV is low.
Keywords: Diagnostic performance, fine-needle aspiration cytology, thyroid nodules, ultrasonography
How to cite this article:
Bayewu GO, Ogunseyinde AO, Atalabi OM, Ogun GO, Adetona AE. Comparison of the diagnostic performance of ultrasonography with fine-needle aspiration cytology in thyroid nodules. West Afr J Radiol 2019;26:110-6 |
How to cite this URL:
Bayewu GO, Ogunseyinde AO, Atalabi OM, Ogun GO, Adetona AE. Comparison of the diagnostic performance of ultrasonography with fine-needle aspiration cytology in thyroid nodules. West Afr J Radiol [serial online] 2019 [cited 2023 Sep 24];26:110-6. Available from: https://www.wajradiology.org/text.asp?2019/26/2/110/262934 |
| Introduction | |  |
Thyroid nodules occur with relatively high frequency in the general population with prevalence of 4%–7% by palpation alone and 13%–67% by sonographic evaluation.[1],[2] However, <7% of thyroid nodules are malignant.[3],[4] Imaging modality of choice for the investigation of thyroid nodules is high resolution ultrasound. Ultrasonography is the modality of choice for initial characterization of a thyroid nodule.[5] Ultrasound is helpful in distinguishing malignant from benign thyroid nodules. Although thyroid nodules may be detected at computed tomography and magnetic resonance imaging, these modalities are not useful for characterization of a nodule.[6] Positron emission tomography may occasionally help identify thyroid nodules, but it is considered by some authors to have limited utility in differentiating benign from malignant lesions.[1],[7],[8]
Fine-needle aspiration biopsy (FNAB) is considered to be the most effective and reliable procedure for the diagnosis of malignant thyroid nodules.[9]
As thyroid nodules are shown by US to be present in 30%–50% of the population and fewer than 5.0%–6.5% of these are malignant,[10] US-guided fine-needle aspiration (FNA) has become increasingly popular.[11]
Sonographic features of potentially malignant thyroid nodules include microcalcifications, marked hypoechogenecity, irregular or microlobulated margins, taller than wide shape, and intranodular central vascularity.[1] Although the individual ultrasonic features may be of limited value, when multiple features appear in combination, it is possible to make an accurate prediction and such nodules should be further assessed with FNA.[1],[12],[13]
Color Doppler ultrasound has become an established imaging technique for assessing thyroid nodules, and many international authors have shown its ability to identify lesions with more probability of malignancy with good sensitivity and specificity.[14],[15]
This study aimed at evaluating the various ultrasound criteria in thyroid nodules and comparing to FNA cytology (FNAC) diagnosis.
| Materials and Methods | | |
This is a cross-sectional study that was approved by the Institutional Review Board on 110 consenting adults presenting with thyroid nodules.
Previously diagnosed malignant nodules and normal thyroids were excluded.
Clinical assessment of all patients in this study was carried out including history taking and local examination.
All studied participants had ultrasound examination using a high-resolution, 7.5–12 MHz, linear array transducer of Ultrasonix Sonix TOUCH ultrasound machine made in 2010 by Ultrasonic medical corporation in Canada for B-mode and color Doppler characteristics as well as FNAC.
For patients with multiple thyroid nodules, the nodule with the most suspicious sonographic features was evaluated and aspirated for cytology.
A careful evaluation of the following parameters was carried out on all lesions: echogenicity (Hyperechoic, isoechoic, hypoechoic or anechoic), echo structure (solid, spongiform, or cystic), margins (well defined or poorly defined) and presence or absence of hyperechoic spots (macrocalcifications or microcalcifications), shape (taller than wide or wider than tall), presence or absence of halo (thin or thick incomplete), and color flow pattern (peripheral, intranodal, and avascular).
Sonographic characteristics suggesting malignancy were defined as microcalcifications, an irregular or microlobulated margins, marked hypoechogenecity, a shape that was taller than it was wide, and intranodular vascularity in color Doppler study.
Nodules were prospectively classified as positive or negative based on previous studies.[16] If one or more features suggestive of malignancy were present, the nodule was classified as positive. If a nodule had no suspicious features, it was classified as negative (benign).
After US examination, an US-guided fine-needle aspiration was performed for all evaluated 110 nodules.
Ultrasound-guided FNAB was performed by the pathologist using a 23-gauge needle with a free hand technique. For a partially cystic nodule, the biopsy sampling was directed to the solid portion of the nodule. In patients with more than one nodule, FNA of the suspicious nodule was retained.
Aspirate was smeared on slides and stained by May–Grunwald–Giemsa stain. The cytological analysis was performed by a single pathologist. Cytological material was defined as adequate when six or more thyroid cell clusters were obtained. Adequate cytological material was classified as benign, malignant, or suspicious.
Based on previous study, cytologic results were classified as benign, suspicious, or malignant.[9]
Patients with a benign cytodiagnosis had no features suggestive of or diagnostic for malignancy. Patients with a suspicious cytodiagnosis had specimens showing hypercellularity and a pattern suggestive of follicular neoplasms or atypical features suggestive of, but not diagnostic for, malignancy. Patients with a malignant cytodiagnosis had cytologic findings that indicated the presence of malignant cells consistent with thyroid carcinoma.
Cytological variables consisted of malignant, benign, and suspicious cases.
Fisher's exact test was used to determine the association between categorical variables of interest and the dependent variable. Specificity, sensitivity, negative predictive value, and positive predictive value (PPV) of the ultrasound features were also determined. Level of statistical significance was set at <0.05.
| Results | | |
The study population of 110 cases obtained comprised 103 females and 7 males with a female to male ratio of 14.7:1. The ages ranged from 22 to 71 years with a mean of 44.05 ± 11.79 years [Table 1]. The majority of the patients 79 (71.8%) had tertiary education. Only 4 (3.6%) had no formal education.
The sonographic findings in malignant and benign nodules are summarized in [Table 2].
Most of the nodules 103 (93.6%) were wider than tall, isoechoic 59 (53.6%), mostly spongiform [Figure 1] 83 (75.5%), mostly well-defined 101 (91.8%) with thin surrounding halo 93 (92.1%). Calcification was present in 18 (16.4%) patients, of which 5 (27.8%) were macrocalcifications while 13 (72.2%) were microcalcifications [Figure 2]. Color flow was present in 84 (76.4%) nodules, of which 76 (69.1%) were peripheral while intranodal [Figure 3] were 8 (7.3%). | Figure 1: Transverse USS of the thyroid gland showing a huge fairly oval-shaped isoechoic nodule with mixed solid and cystic components (spongiform) which was confirmed to be benign with fine-needle aspiration cytology
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 | Figure 2: Transverse USS of the thyroid gland showing a huge isoechoic nodule with both microcalcifications and macrocalcification which was confirmed to be malignant with fine-needle aspiration cytology
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 | Figure 3: Transverse USS of the thyroid gland with color Doppler interrogation showing a lobulated, poorly defined, isoechoic nodule with intranodal flow and incomplete thick halo which was confirmed to be malignant with fine-needle aspiration cytology
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Among 110 thyroid nodules, 23 nodules were classified as positive considering the sonographic characteristics while 87 nodules were classified as negative as shown in [Table 3].
At cytological evaluation, 101 lesions were benign (91.8%) and 9 were malignant (8.2%) as shown in [Table 4].
The correlation of ultrasound categories with cytologic findings and the correlation of sonographic features with cytologic findings are shown in [Table 5] and [Table 6], respectively.
Among 110 thyroid nodules, 23 lesions were classified as positive considering the sonographic characteristics and 9 of them were proved to be malignant on FNAC. Of 87 lesions which were classified as negative, none was malignant after FNAC.
Of the 9 confirmed by FNAC to be malignant, 6 had nodal involvement on ultrasound.
In these 110 nodules, our sonographic classification method resulted in a sensitivity of 100% (9/9), specificity of 86% (87/101), PPV of 39% (9/23), and negative predictive value of 100% (87/87). The sensitivity of each sign was ranging from 62% to 86%, but the specificity was from 97% to 100%. These are illustrated in [Table 7].
| Discussion | | |
There are many USS criteria for differentiating benign from malignant thyroid nodules. Such differentiation is important for selecting patients for further FNAC in cases in which malignancy is suspected and to avoid unnecessary biopsy for those with benign criteria. It has been found in literature that no single criteria can predict malignancy, and combination of the known criteria of malignancy gives higher sensitivity and specificity than depending on single ultrasound feature.[8]
The female to male ratio of 14.7:1 in this study concurs with 10:1, 11.1, and 14.1 recorded for Port-Harcourt, Kano, and Enugu from Southern, North East, and South Eastern parts of Nigeria, respectively.[17],[18],[19] It however differs slightly with the reports from Lagos and Ife, both from Western Nigeria, which recorded ratio of 7:1 and 6:1, respectively,[20],[21] as well as reports from the United States of America, Saudi Arabia, and Pakistan, which recorded female to male ratios of 7:1, 6.2:1, and 4.5:1, respectively.[22],[23],[24]
Ijomone et al.[17] gave reasons that the difference was probably due to geographical and socioeconomic variation in these areas; however, this reason is not in agreement with this work as this index study is also from Western part of Nigeria where it was claimed to have a relatively low female to male ratio.
The mean age of patients in this study was 44 years with a range of 22–71 years. The age group 36–45 had the highest prevalence of thyroid nodules 36 (32.7%). This is similar to the findings in other studies from Southern Nigeria where the majority of cases were found in the age group 30–39 from Lagos and 31–40 from Port-Harcourt.[20],[25] Tsegaye and Ergete [26] found out that 85% of thyroid diseases were found in the age group 20–59. This shows that thyroid diseases are not common in extremes of age.
The incidence of malignant nodules was 8.2% in this study which is significantly lower than benign nodules; this is in agreement with findings by Abdulkareem et al.[20] and Anidi et al.[18] who got an incidence of 7% and 8.3%, respectively, although findings by Papini et al.,[27] Hegedüs et al.,[28] and Kunreuther et al.[29] however showed higher percentage of malignancy (9.2%–13.0%) which is slightly higher than the findings in this index study.
Calcifications occurring in thyroid nodules include microcalcifications, coarse calcifications, and peripheral calcifications. Thyroid microcalcifications are psammoma bodies which in ultrasound appear as punctuate hyperechoic foci; usually without acoustic shadowing.[1] The presence of microcalcification is one of the most specific features of thyroid malignancy.[30] In this study, its specificity is 100%, which is in agreement with other studies where it is stated as 85.8%–95%[8],[31] and its PPV is 100% which is also in agreement with other studies where it has been 4.8%–94.2%.[13] The presence of poorly defined margin was considered a feature for a malignant nodule. In our study, it was about 78% sensitive and 98% specific. The reported sensitivity of poorly defined margins ranges widely (53%–89%).[31] Results of current study were similar with the one reported by Papini et al.[27] The difference in the range may be due to their larger patient sample size.
Since poorly defined margins may also be demonstrated in 15%–59% of benign nodules,[8],[32] Hoang et al.[1] state that unless frank invasion beyond capsule is demonstrated, the ultrasound appearance of margins of thyroid nodule alone is an unreliable basis for determining malignancy or benignity.
Hypoechogenicity in solid thyroid nodules was considered a finding suggestive of malignancies such as carcinomas and lymphomas. However, 55% of benign nodules are also solid and hypoechoic.[1],[27] In this study, no attempt was made to differentiate markedly hypoechoic lesions from other hypoechoic lesions, and both were considered a finding indicative of malignancy. The specificity for detection of a malignancy in hypoechoic solid nodule is 87%, but sensitivity is 67% and is described in other studies as well.[1],[8],[27]
A nodule shape taller than wide is regarded as a potentially useful ultrasound feature suggestive of malignancy [1] signifying that the lesion is aggressive and is growing against the soft tissue planes. This feature has been described by Kim et al.[3] and has high specificity for malignancy (93%), which is in agreement with this study (97%) which also has high sensitivity value (86%). Color Doppler US has become an established imaging technique for assessing thyroid nodules, and many authors have shown its ability to identify lesions with more probability of malignancy with good sensitivity and specificity and have been proven to be statistically significant criteria when deciding for FNA.[14],[15] In this study, predominantly central color flow pattern in solid nodules is predictive of malignancy with 67% sensitivity and 98% specificity with 75% PPV and 97% negative predictive value. De Nicola et al.[14] and Cerbone et al.[33] state that most thyroid carcinomas have exuberant central vascularization which is described as having chaotic and irregular pattern.
In this study, of the 101 nodules that showed halo sign, 93 had thin halo while 8 showed thick incomplete halo. Ninety-six percentage of the nodules with thin halo were proven to be benign while 75% (60) of nodules with thick incomplete halo were malignant. This was in agreement in previous studies of Papini et al.[27] in Italy, Kim et al.[3] in Korea, and Frates et al.[34] in USA where thin halo sign was found to be highly predictive of benignity. Papini et al.[27] found no benign nodule with thick incomplete halo.
This study confirms that gray scale ultrasound features are helpful in differentiating the malignant from benign lesions, but we found that there is no single gray scale ultrasound criterion that could distinguish benign from malignant thyroid nodules with 100% reliability. However, the presence of microcalcifications within a nodule is associated with thyroid cancer among the rest of the ultrasonic features which buttress the point of view of Cappelli et al.[35] and Lyshchik et al.[36] that intrinsic microcalcification is the strongest criterion predicting malignancy.
| Conclusion | | |
USS is highly sensitive than specific for diagnosis of thyroid masses in this study. However, its PPV is very low.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Hoang JK, Lee WK, Lee M, Johnson D, Farrell S. US features of thyroid malignancy: Pearls and pitfalls. Radiographics 2007;27:847-60.  |
| 2. | Bertagna F, Treglia G, Piccardo A, Giubbini R. Diagnostic and clinical significance of F-18-FDG-PET/CT thyroid incidentalomas. J Clin Endocrinol Metab 2012;97:3866-75. |
| 3. | Kim JM, Ryu JS, Kim TY, Kim WB, Kwon GY, Gong G, et al. 18F-fluorodeoxyglucose positron emission tomography does not predict malignancy in thyroid nodules cytologically diagnosed as follicular neoplasm. J Clin Endocrinol Metab 2007;92:1630-4. |
| 4. | Chen YK, Ding HJ, Chen KT, Chen YL, Liao AC, Shen YY, et al. Prevalence and risk of cancer of focal thyroid incidentaloma identified by 18F-fluorodeoxyglucose positron emission tomography for cancer screening in healthy subjects. Anticancer Res 2005;25:1421-6. |
| 5. | Tan GH, Gharib H. Thyroid incidentalomas: Management approaches to nonpalpable nodules discovered incidentally on thyroid imaging. Ann Intern Med 1997;126:226-31. |
| 6. | Ishigaki S, Shimamoto K, Satake H, Sawaki A, Itoh S, Ikeda M, et al. Multi-slice CT of thyroid nodules: Comparison with ultrasonography. Radiat Med 2004;22:346-53. |
| 7. | Brander AE, Viikinkoski VP, Nickels JI, Kivisaari LM. Importance of thyroid abnormalities detected at US screening: A 5-year follow-up. Radiology 2000;215:801-6. |
| 8. | Frates MC, Benson CB, Charboneau JW, Cibas ES, Clark OH, Coleman BG, et al. Management of thyroid nodules detected at US: Society of radiologists in ultrasound consensus conference statement. Radiology 2005;237:794-800. |
| 9. | Gharib H, Goellner JR. Fine-needle aspiration biopsy of the thyroid: An appraisal. Ann Intern Med 1993;118:282-9. |
| 10. | Ross DS. Nonpalpable thyroid nodules – Managing an epidemic. J Clin Endocrinol Metab 2002;87:1938-40. |
| 11. | Harnsberger H. Diagnostic Imaging: Head and Neck. Salt Lake City, UT: Amirsys; 2004. p. 24-40. |
| 12. | Hamming JF, Goslings BM, van Steenis GJ, van Ravenswaay Claasen H, Hermans J, van de Velde CJ, et al. The value of fine-needle aspiration biopsy in patients with nodular thyroid disease divided into groups of suspicion of malignant neoplasms on clinical grounds. Arch Intern Med 1990;150:113-6. |
| 13. | Amal AS, Khaled A, Faten W. Fine needle aspiration of thyroid nodules has high sensitivity and specificity. Rawal Med J 2008;33:221-4. |
| 14. | De Nicola H, Szejnfeld J, Logullo AF, Wolosker AM, Souza LR, Chiferi V Jr., et al. Flow pattern and vascular resistive index as predictors of malignancy risk in thyroid follicular neoplasms. J Ultrasound Med 2005;24:897-904. |
| 15. | Choi YJ, Yun JS, Kim DH. Clinical and ultrasound features of cytology diagnosed follicular neoplasm. Endocr J 2009;56:383-9. |
| 16. | Yunus M, Ahmed Z. Significance of ultrasound features in predicting malignant solid thyroid nodules: Need for fine-needle aspiration. J Pak Med Assoc 2010;60:848-53. |
| 17. | Ijomone EA, Duduyemi BM, Udoye E, Nwosu SO. Histopathological review of thyroid diseases in Southern Nigeria-A ten year retrospective study. J Med Med Sci 2014;5:127-32. |
| 18. | Anidi AI, Ejeckam GC, Ojukwu J, Ezekwesili RA. Histological pattern of thyroid diseases in Enugu, Nigeria. East Afr Med J 1983;60:546-50. |
| 19. | Edino ST, Mohammed AZ, Ochicha O, Malami SA, Yakubu AA. Thyroid cancers in nodular goiters in Kano, Nigeria. Niger J Clin Pract 2010;13:298-300. [ PUBMED] [Full text] |
| 20. | Abdulkareem FB, Banjo AA, Elesha SO. Histological review of thyroid lesions: A 13-year retrospective study (1989-2001). Niger Postgrad Med J 2005;12:210-4. |
| 21. | Nggada HA, Ojo OS, Adelusola KO. A histopathological analysis of thyroid diseases in ile-ife, Nigeria. A review of 274 cases. Niger Postgrad Med J 2008;15:47-51. |
| 22. | Chung EB, Rogers N, White JE. Thyroid diseases in black patients. J Natl Med Assoc 1977;69:573-7. |
| 23. | Abu-Eshy SA, Al-Shehri MY, Khan AR, Khan GM, Al-Humaidi MA, Malatani TS. Causes of goiter in the Asir region: A histopathological analysis of 361 cases. Ann Saudi Med 1995;15:74-6. |
| 24. | Hussain N, Anwar M, Nadia N, Ali Z. Pattern of surgically treated thyroid diseases in Karachi. Biomedica 2005;21:18-20. |
| 25. | Seleye-Fubara D, Numbere N, Etebu EN. Pathology of common diseases of the thyroid gland in Port-Harcourt. Port Harcourt Med J 2009;3:312-7. |
| 26. | Tsegaye B, Ergete W. Histopathologic pattern of thyroid disease. East Afr Med J 2003;80:525-8. |
| 27. | Papini E, Guglielmi R, Bianchini A, Crescenzi A, Taccogna S, Nardi F, et al. Risk of malignancy in nonpalpable thyroid nodules: Predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 2002;87:1941-6. |
| 28. | Hegedüs L, Bonnema SJ, Bennedbaek FN. Management of simple nodular goiter: Current status and future perspectives. Endocr Rev 2003;24:102-32. |
| 29. | Kunreuther E, Orcutt J, Benson CB, Doubilet PM, Cibas ES, Moore FD, et al. Prevalence and distribution of carcinoma in the uninodular and multinodular goiter. Presented at the 76 th Annual Meeting of the American Thyroid Association. Vancouver, British Columbia, Canada; 29 September, 3 October, 2004. |
| 30. | Solbiati L, Arsizio B, Ballarati E, Cioffi V, Poerio N, Croce F, et al. Micro-calcifications: A clue in the diagnosis of thyroid malignancies. Radiology 1990;117:140. |
| 31. | Koike E, Noguchi S, Yamashita H, Murakami T, Ohshima A, Kawamoto H, et al. Ultrasonic characteristics of thyroid nodules: Prediction of malignancy. Arch Surg 2001;136:334-7. |
| 32. | Wienke JR, Chong WK, Fielding JR, Zou KH, Mittelstaedt CA. Sonographic features of benign thyroid nodules: Interobserver reliability and overlap with malignancy. J Ultrasound Med 2003;22:1027-31. |
| 33. | Cerbone G, Spiezia S, Colao A, Di Sarno A, Assanti AP, Lucci R, et al. Power Doppler improves the diagnostic accuracy of color Doppler ultrasonography in cold thyroid nodules: Follow-up results. Horm Res 1999;52:19-24. |
| 34. | Frates MC, Benson CB, Doubilet PM, Cibas ES, Marqusee E. Can color Doppler sonography aid in the prediction of malignancy of thyroid nodules? J Ultrasound Med 2003;22:127-31. |
| 35. | Cappelli C, Castellano M, Pirola I, Cumetti D, Agosti B, Gandossi E, et al. The predictive value of ultrasound findings in the management of thyroid nodules. QJM 2007;100:29-35. |
| 36. | Lyshchik A, Higashi T, Asato R, Tanaka S, Ito J, Mai JJ, et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005;237:202-11. |
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]
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