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Predictive value of ultrasonological characteristics of a thyroid nodule in the diagnosis of malignancy.

BACKGROUND

Thyroid diseases are arguably among the commonest endocrine disorders worldwide. Thyroid disorders can vary from innocent physiologic enlargements of the gland to life-threatening thyrotoxic crises, which require emergency medical interventions and thyroid cancers, which require skilful surgical management. The appropriate management and successful outcome depends on accurate diagnosis of the thyroid disease. Carcinoma of the thyroid gland is the most common endocrine malignancy in the world, and worldwide it constitutes about 1% of human neoplasms. [1] Thyroid carcinoma accounts for 1%-5% of all malignancies in females and less than 2% of all malignancies in males. [2] Papillary carcinoma is the most common thyroid neoplasm accounting for 70% - 80% of thyroid carcinoma. [3] The incidence of thyroid carcinoma and particularly papillary carcinoma has been on the rise around the globe. [2] Most patients with thyroid carcinoma, especially papillary carcinoma can expect an excellent prognosis with a 10-year survival rates above 95% for the most favourable stages. [3] Hence, early detection of thyroid carcinoma is very important.

Clinically, discrete swellings in the thyroid gland known as solitary nodules of the thyroid have a higher incidence of malignancy than a non-solitary nodule. [4] The incidence of malignancy in solitary thyroid nodule ranges from 5% to 15%. [3,5,6] A thyroid nodule is defined as any discrete lesion that is sonographically distinguishable from the adjacent thyroid parenchyma. [7] The evaluation of patients with clinically discrete swelling aims at identifying the presence or absence of a disorder of function or malignancy and aid in recognising those patients who require surgical intervention and to avoid inappropriate surgery in those with benign asymptomatic swellings. The practising clinician relies upon clinical information and judicious use of available diagnostic aids. Among the modern imaging modalities, high-resolution ultrasound is the first choice and most sensitive diagnostic modality for the detection of intrathyroidal lesions and it is necessary to perform ultrasonography for nodules found after palpation. [8] Because of its superficial location, the thyroid gland is ideally suited for high-frequency sonography (using 5-12 MHz linear array transducer), which facilitates the detection of even clinically non-palpable nodules of 2-3 mm size and allows a more accurate morphological characterisation of the lesion. [9] The prevalence of thyroid nodules detected by palpation is 3%-7% in most series and it increases with age in areas of iodine deficiency and with exposure to external radiation. But using high resolution ultrasound it has been shown that more than 50% of adults have thyroid nodules. [10] Sonological characters including nodule size, internal content, nodule shape, nodule margin, echogenicity, calcification, extracapsular invasion, vascularity and elastography are assessed to identify suspicious nodules. [11]

Documentation of nodule size during the initial scan is important to assess the interval growth of the nodule during followup. Rapid increase in size of the nodule is a predictor of malignancy. [12] Solid or predominantly solid nodules have a higher risk of malignancy than do mixed or predominantly cystic nodules. Cystic and almost completely cystic nodules have a very low likelihood of being malignant. Nodules with mixed composition have an average risk of malignancy. [7] The dimensions of the nodule are checked in the anteroposterior and transverse dimensions. A thyroid nodule which has a greater anteroposterior than transverse diameter (i.e. taller than wider) has been described as more likely to be malignant than benign. [13] The advent of high frequency ultrasound has allowed us to better characterise the margins of a thyroid nodule. Microlobulated or spiculated margins are suggestive of malignancy. [13] Thyroid nodules may be classified as hypoechoic, isoechoic or hyperechoic in comparison to adjacent thyroid parenchyma and strap muscles. [11] A hypoechoic nodule has increased risk of malignancy, but it is more so for a nodule with marked hypoechogenicity. Presence of microcalcifications and macrocalcifications are associated with malignancy. Pathologically, microcalcification is a psammoma body that is comprised of 10-100 [micro]m sized round, laminar, crystalline, calcific deposits which is very specific for thyroid carcinoma and especially for papillary thyroid carcinoma. Moon et al in their study on thyroid sonography reports a specificity of 86%-95% and a positive predictive value of 42% - 94% for the presence of microcalcifications and associated malignancy. [11] Yoon et al did not find any significant association between the presence of rim calcifications and malignancy in a thyroid nodule. [14] Tumour vascularity, extracapsular invasion and elastography are other important characters that needs to be assessed. Frates et al in a review of various studies focusing on the sonological features of thyroid nodules and their association with malignancy found out that hypoechogenic nature of a nodule has maximum sensitivity (26.4%-87.1%) and presence of microcalcifications has maximum specificity (85.8%-95%) in the identification of thyroid malignancy. [7] The identification of suspicious nodules by ultrasound helps in obtaining targeted FNACs (Fine needle aspiration cytology). Cai X J et al, in a study to assess the inadequate aspirate from FNAC found that the inadequacy rate was significantly lower for USG-guided FNAC (6.4%) than conventional FNAC (13%). [15] Solymosi et al, in a study comparing FNAC with and without USG guidance found that the positive predictive value of FNAC (45% v/s 16%), specificity (87% v/s 56%), sensitivity (92% v/s 57%) and diagnostic accuracy (87% v/s 66%) were all higher with USG-guided FNAC. [16]

Thus, it is clear that ultrasound increases the detection of thyroid nodules and helps in identification of suspicious nodules, thus improving the diagnostic capability of guided FNAC.

MATERIALS AND METHODS

The study was conducted in patients with solitary thyroid nodules attending the outpatient and inpatient department of general surgery on T.D.M.C.H. Vandanam over a period of one year from January 2013 to January 2014.

Study Design- Descriptive study.

Inclusion Criteria

Patients with solitary nodule of thyroid on clinical examination who underwent pre-operative ultrasound evaluation and proceeded to thyroidectomy.

Study Procedure

High frequency ultrasonography was done using ultrasound system with high frequency (5-12 MHz) probe in a group of 50 patients who presented with clinically diagnosed solitary nodule of thyroid. Various features of the nodule like shape, margin, echogenicity and calcification were assessed. Patients who proceeded to thyroidectomy were included in the study. The association between above mentioned sonological characters and malignancy were statistically analysed in 12 patients who had histopathologically proven malignancy. Informed consent was taken prior to the procedure.

Statistical Analysis

Qualitative variables were summarised using percentages and proportions. Quantitative variables were summarised using mean with standard deviation. Sensitivity and specificity, each of the above mentioned sonological characters were found out by comparing it with histopathologic examination report. Data was entered in MS Excel data sheet and analysed using SPSS software.

RESULTS

Among the 50 patients, there were 10 cases of papillary carcinoma and 2 cases of follicular carcinoma (Table I and Figure I). Ultrasonological characteristics of the nodule-like hypoechogenicity, taller than wide dimensions, presence of spiculated margins, macrocalcifications and microcalcifications were assessed. Statistical analysis was done to find out correlation between these characters and malignancy in 12 histopathologically proven cases of malignancy. The presence of hypoechogenicity, microcalcifications and being taller than wide were highly suggestive of a malignant thyroid nodule with a sensitivity of 83%, 75% and 75% respectively (Tables II, III, IV, V, X, XI and Figures II, III, IV). Maximum negative predictive values are observed for the criteria of a nodule being taller than wide (91.4%) and lacking microcalcification (90.6%) as shown in Tables IV, V, X, XI and Figures III and VI. Hence, a nodule not being taller than wide and lacking microcalcification has more than 90% chance of not being malignant. Spiculated margins are highly specific for malignant nodules, and there is 90% accuracy in detection of a malignant nodule using this criterion (Tables VI, VII and Figure IV).

Correlation of Hypoechogenicity of Thyroid Nodule with Malignancy

Correlation of Taller than Wide Dimension of Thyroid Nodule with Malignancy

Correlation of Spiculated Margins in the Thyroid Nodule with Malignancy

Correlation of Macrocalcifications in the Thyroid Nodule with Malignancy

Correlation of Microcalcifications in Thyroid Nodule with Malignancy

DISCUSSION

Based on the data obtained from the study, the efficacy of ultrasound characteristics of solitary thyroid nodules in predicting the risk of malignancy in a nodule was assessed. It was found that

1. Presence of spiculated margins in a nodule is highly suggestive of malignancy (100% specificity and 90% accuracy).

2. Absence of microcalcifications (Negative predictive value-90.6%) and a nodule which is not taller than wide (Negative predictive value-91.4%) in dimension has a great chance of not being malignant.

3. Ultrasonological characteristics of thyroid nodule can be used to identify malignant nodules, but cannot be used as diagnostic markers as maximum sensitivity in diagnosing a malignant thyroid nodule with these characters is 83% according to this study (Table XII).

CONCLUSION

In this prospective analysis of the sonological findings of thyroid nodule in correlation with tissue diagnosis, the most predictive of malignant tissue diagnosis were presence of hypoechogenicity, microcalcifications and nodules being taller than wide. The results of our study were encouraging, in that we were able to identify the most appreciable US features for differentiating benign from malignant solid nodules.

REFERENCES

[1] Gandolfi PP, Frisina A, Raffa M, et al. The incidence of thyroid carcinoma in multinodular goiter: a retrospective analysis. Acta Biomedica 2004;75(2):114-7.

[2] Kilfroy BA, Zheng T, Halford TR, et al. International patterns and trends in thyroid cancer incidence, 1973-2002. Cancer Causes Control 2009;20(5):525-31.

[3] Smith PW, Salomone LJ, Hanks JB. Thyroid. In: Townsend CM, Beauchamp RD, Evers BM. eds. Sabiston textbook of surgery: the biological basis of modern surgical practice. 19th edn. Elsevier 2012:886-923.

[4] Frates MC, Benson CB, Doubilet PM, et al. Prevalence and distribution of carcinoma in patients with solitary and multiple thyroid nodules on sonography. The Journal of Clinical Endocrinology & Metabolism 2006;91(9):3411-7.

[5] Krukowski ZH. The thyroid and parathyroid glands. In: Williams NS, Bulstrode CJK, O'Connell PR. eds. Bailey and Love's short practice of surgery. 26th edn. CRC Press, Taylor and Francis Group 2013:741-77.

[6] Khan SA, Gafur MA, Khan MK, et al. Pattern of malignancy in clinically solitary thyroid nodule. Mymensingh Medical Journal 2012;21(1): 1-7.

[7] Frates MC, Benson CB, Charboneau JW, et al. Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound Consensus Conference Statement. Radiology 2005;237(3):794-800.

[8] Cooper DS, Doherty GM, Haugen BR, et al. Revised American Thyroid Association Management Guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19(11):1167-214.

[9] Chaudhary V, Bano S. Imaging of the thyroid: recent advances. Indian Journal of Endocrinology and Metabolism 2012;16(3):371-6.

[10] Perros P. Thyroid nodules. In: Mazzaferri EL, Harmer C, Mallick UK, et al. eds. Practical management of thyroid cancer: a multidisciplinary approach. London: Springer 2006:75-81.

[11] Moon WJ, Baek JH, Jung SL, et al. Ultrasonography and the ultrasound-based management of thyroid nodules: consensus statement and recommendations. Korean Journal of Radiology 2011;12(1):1-14.

[12] Alexander EK, Hurwitz S, Heering JP, et al. Natural history of benign solid and cystic thyroid nodules. Ann Intern Med 2003;138(4):315-8.

[13] Kim EK, Park CS, Chung WY, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. American Journal of Roentgenology 2002;178(3):687-91.

[14] Yoon DY, Lee JW, Chang KS, et al. Peripheral calcification in thyroid nodules ultrasonographic features and prediction of malignancy. Journal of Ultrasound in Medicine 2007;26(10):1349-55.

[15] Cai XJ, Valiyaparambath N, Nixon P, et al. Ultrasound guided fine needle aspiration cytology in the diagnosis and management of thyroid nodules. Cytopathology 2006;17(5):251-6.

[16] Solymosi T, Toth GL, Bodo M. Diagnostic accuracy of fine needle aspiration cytology of the thyroid: impact of ultrasonography and ultrasonographically guided aspiration. Acta Cytologica 2001;45(5):669-74.

Sajikumar N. Raghavan (1), Ramkumar Venugopala Panicker (2)

(1) Additional Professor, Department of General Surgery, Government T. D. Medical College, Alappuzha.

(2) Senior Resident, Department of General Surgery, Government T. D. Medical College, Alappuzha.

Financial or Other, Competing Interest: None.

Submission 02-03-2017, Peer Review 15-03-2017, Acceptance 17-03-2017, Published 22-03-2017.

Corresponding Author:

Dr. Sajikumar N. Raghavan, Additional Professor, Department of General Surgery, T. D. Medical College, Alappuzha-688005, Kerala.

E-mail: drsajikumarnr@gmail.com

DOI: 10.14260/jemds/2017/430

Caption: Figure I. Histopathology Reporting of the Study Population
Table I. Histopathology Reporting of the Study Population

Histopathology Report   Count   Percentage
Papillary Carcinoma      10         20
Follicular Carcinoma      2         4
Colloid Nodule           38         76

Table II. Correlation of Hypoechogenicity
of Thyroid Nodule with Malignancy

                      Class

Hypoechoic   Malignant   Benign   Total

Yes             10         28      38
No               2         10      12
Total           12         38      50

Table III. Prediction of Hypoechogenicity of
Thyroid Nodule being associated with Malignancy

Sensitivity                         83.30%
Specificity                         26.30%
False Negative                      16.70%
False Positive                      73.70%
Predictive Value of Positive Test   26.30%
Predictive Value of Negative Test   83.30%
Accuracy                            40.00%

Table IV. Correlation of Taller than wide
Dimension of Nodule with Malignancy

Taller than Wide             Class

                   Malignant   Benign   Total
Yes                9           6        15
No                 3           32       35
Total              12          38       50

Table V. Prediction of Taller than wide Dimension of
Thyroid Nodule being associated with Malignancy

Sensitivity                         75.00%
Specificity                         84.20%
False Negative                      25.00%
False Positive                      15.80%
Predictive Value of Positive Test   60.00%
Predictive Value of Negative Test   91.40%
Accuracy                            82.00%

Table VI. Correlation of Spiculated Margins
of the Thyroid Nodule with Malignancy

Spiculated Margins              Class

                     Malignant   Benign    Total

Yes                      7          0        7
No                       5         38       43
Total                   12         38       50

Table VII. Prediction of Spiculated Margin of Thyroid
Nodule being associated with Malignancy

Sensitivity                         58.30%
Specificity                         100.00%
False Negative                      41.70%
False Positive                       0.00%
Predictive Value of Positive Test   100.00%
Predictive Value of Negative Test   88.40%
Accuracy                            90.00%

Table VIII. Correlation of Macrocalcifications
in the Thyroid Nodule with Malignancy

Macrocalcifications              Class

                      Malignant   Benign   Total

Yes                       3         7       10
No                        9         31      40
Total                    12         38      50

Table IX. Prediction of Macrocalcification in
Thyroid Nodule being associated with Malignancy

Sensitivity                         25.00%
Specificity                         81.60%
False Negative                      75.00%
False Positive                      18.40%
Predictive Value of Positive Test   30.00%
Predictive Value of Negative Test   77.50%
Accuracy                            68.00%

Table X. Correlation of Microcalcifications
in Thyroid Nodule with Malignancy

Microcalcifications              Class

                      Malignant   Benign   Total
Yes                       9         9       18
No                        3         29      32
Total                    12         38      50

Table XI. Prediction of Microcalcification in Thyroid
Nodule being associated with Malignancy

Sensitivity                         75.00%
Specificity                         76.30%
False Negative                      25.00%
False Positive                      23.70%
Predictive Value of Positive Test   50.00%
Predictive Value of Negative Test   90.60%
Accuracy                            76.00%

Table XII. Comparison of the Diagnostic Indices of
Ultrasonological Parameters in Detecting Malignancy *

              Hypoechoic    Taller     Spiculated      Macro-
                           Than Wide    Margins     Calcification

Sensitivity      83.3         75          58.3           25
Specificity      26.3        84.2         100            81
PPV              26.3         60          100            30
NPV              83.3        91.4         88.4          77.5
Accuracy          40          82           90            68

                 Micro-
              Calcification

Sensitivity        75
Specificity       76.3
PPV                50
NPV               90.6
Accuracy           76

* All values in percentage.

Figure II. Prediction of Hypoechogenicity of Thyroid
Nodule being associated with Malignancy

Senstitivity           83.3
Specificity            26.3
Positive
  predictive power     26.3
Negative
  Predictive power     83.3
Accuracy               40.0

Note: Table made from bar graph.

Figure III. Prediction of Taller than Wide Dimension
of Thyroid Nodule being associated with Malignancy

Senstitivity           75.0
Specificity            84.2
Positive
  predictive power     60.0
Negative
  Predictive power     91.4
Accuracy               82.0

Note: Table made from bar graph.

Figure IV. Prediction of Spiculated Margin
of Nodule being associated with Malignancy

Senstitivity           58.3
Specificity            100.0
Positive
  predictive power     100.0
Negative
  Predictive power     88.4
Accuracy               90.0

Note: Table made from bar graph.

Figure V. Prediction of Macrocalcification in Thyroid
Nodule being associated with Malignancy

Senstitivity           25.0
Specificity            81.6
Positive
  predictive power     30.0
Negative
  Predictive power     77.5
Accuracy               68.0

Note: Table made from bar graph.

Figure VI. Prediction of Microcalcification in Thyroid
Nodule being associated with Malignancy

Senstitivity           75.0
Specificity            76.3
Positive
  predictive power     50.0
Negative
  Predictive power     90.6
Accuracy               76.0

Note: Table made from bar graph.
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Article Details
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Title Annotation:Original Research Article
Author:Raghavan, Sajikumar N.; Panicker, Ramkumar Venugopala
Publication:Journal of Evolution of Medical and Dental Sciences
Article Type:Report
Geographic Code:9INDI
Date:Mar 23, 2017
Words:2709
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