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DOI:10.2214/AJR.06.0750
AJR 2007; 189:227-231
© American Roentgen Ray Society

Clinical Observations

Papillary Thyroid Carcinoma Manifested Solely as Microcalcifications on Sonography

Jin Young Kwak1, Eun-Kyung Kim1, Eun Ju Son1, Min Jung Kim1, Ki Keun Oh1, Ji Young Kim2 and Kwang Il Kim2

1 Department of Radiology and Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-Dong, Seodaemun-gu, Seoul 120-752, Korea.
2 Department of Pathology, Pochon CHA University College of Medicine, Gyeonggi-do, Korea.

Received June 5, 2006; accepted after revision February 12, 2007.

 
Address correspondence to E. K. Kim (ekkim{at}yumc.yonsei.ac.kr).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study is to assess the utility of sonographic detection and the role of sonography-guided fine-needle aspiration biopsy (FNAB) in thyroid carcinomas that appear only as microcalcifications without an associated mass.

CONCLUSION. This study covers 11 cases in which the only abnormal finding suggesting thyroid cancer was microcalcifications detected at sonography. All cases described were diagnosed as thyroid papillary carcinoma after surgery. Hence, it is shown that real-time high-resolution sonography is effective in the detection of thyroid carcinomas that appear as microcalcifications without an associated mass. The results of sonography-guided FNAB were satisfactory to diagnose these microcalcifications as thyroid carcinomas. Therefore, we believe that thyroid sonography combined with sonography-guided FNAB is a useful approach for diagnosing thyroid microcalcifications.

Keywords: cancer • fine-needle aspiration biopsy • thyroid gland • sonography


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Many studies have suggested that sonography can be considerably effective for predicting various thyroid malignancies such as microcalcifications, an absent halo sign, marked hypoechogenicity, extraglandular extensions, irregular or microlobulated margins, heterogeneous echotexture, and taller-than-wide shapes [1–3]. Among these sonography features, microcalcifications within the thyroid mass serve as a reliable diagnostic criterion [1, 4]. Our evaluation of the thyroid gland using high-frequency sonography revealed that some papillary thyroid carcinomas appeared only as microcalcifications without an associated mass. To our knowledge, there have been few reports of thyroid malignancy that appear solely as microcalcifications on sonography [5]. Therefore, we reviewed cases in which thyroid malignancy appeared only as microcalcifications on sonography.


Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Between January 2001 and December 2005, 2,158 patients in our hospital were diagnosed with thyroid carcinoma based on surgical pathology. During the same period, 22,842 neck sonography examinations were performed. Retrospectively, we reviewed either the sonography images (n = 1,850) or reports made after sonography (n =308) in all patients diagnosed with thyroid carcinoma. As a result, we identified 11 cases in which microcalcifications detected on sonography were the only abnormal finding suggesting the presence of thyroid carcinoma. All of the patients were female, with ages ranging from 15 to 68 years (mean age, 38 years). Among them, seven patients (age range, 15–68 years; mean age, 38.9 years) were diagnosed with usual papillary carcinoma. However, the remaining four patients (age range, 25–53 years; mean age, 37.5 years) were diagnosed with a diffuse sclerosing variant of papillary carcinoma.

Each patient underwent sonography-guided fine-needle aspiration biopsy (FNAB) and subsequent thyroidectomy. In this study, we defined sonography findings of microcalcifications as hyperechoic punctate foci that did not show posterior acoustic shadowing. We excluded both dense calcifications and precipitated colloid materials that exhibited comet-tail artifacts.

The sonography images were obtained using either a SONOLINE Antares (Siemens Medical Solutions) with a 5–13-MHz linear-array probe or an HDI 3000 or 5000 (Philips Medical Systems) with a linear 7–12-MHz probe. All sonography-guided FNABs were performed by either of two of the authors, who are radiologists experienced with the procedure, using a 23-gauge needle and a 20-mL disposable plastic syringe with an aspirator. Each target lesion was aspirated at least twice, and the region that appeared to be the densely populated area of microcalcifications was targeted.

The aspirated material was smeared on four slides per lesion, then immediately fixed in 95% ethanol and stained by the Papanicolaou technique. Also, the syringe used for FNAB was rinsed in CytoLyt Solution (Cytyc Corporation) and additional cell-block or ThinPrep (Cytyc Corporation) preparations were created. We did not have a cytopathologist on site during FNAB to determine the adequacy of the obtained samples. Hence, the FNAB specimens of the patients included in this study were retrospectively reviewed by two experienced cytopathologists. We then compared the results of FNAB with the pathology obtained from surgical specimens during subsequent thyroidectomy.


Figure 1
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  		Fig. 1A —53-year-old woman with Graves' disease and diffuse sclerosing variant of papillary carcinoma. Transverse and longitudinal sonograms of right thyroid gland reveal scattered microcalcifications (arrows) and underlying heterogeneous hypoechogenicity.

 


Figure 2
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  		Fig. 1B —53-year-old woman with Graves' disease and diffuse sclerosing variant of papillary carcinoma. Transverse and longitudinal sonograms of right thyroid gland reveal scattered microcalcifications (arrows) and underlying heterogeneous hypoechogenicity.

 


Figure 3
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  		Fig. 1C —53-year-old woman with Graves' disease and diffuse sclerosing variant of papillary carcinoma. Scattered follicular cell clusters show enlarged vesicular nuclei with intranuclear inclusion (arrow). (ThinPrep [Cytyc Corporation], Papanicolaou stain, x400)

 


Figure 4
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  		Fig. 1D —53-year-old woman with Graves' disease and diffuse sclerosing variant of papillary carcinoma. Photomicrograph shows that few psammoma bodies are scattered in diffuse sclerosing variant of papillary carcinoma. (H and E, x200)

 
Sonograms of the 11 patients were analyzed retrospectively by two dedicated thyroid radiologists. The clinical history, the results of FNAB and surgery were also reviewed for each patient.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Five of 11 patients complained of a palpable neck mass. One patient was diagnosed clinically with Graves' disease. Among the remaining four patients, thyroid carcinomas were discovered incidentally on neck sonography. The original purpose of sonography for three cases was to rule out thyroid disease and that of one case was a health examination. All 11 patients denied having a family history of thyroid carcinoma or previous histories of radiation to the head and the neck.

Sonography showed microcalcifications of the thyroid gland on the right side in seven patients, on the left side in three patients, and on both sides in one patient. Focally distributed microcalcifications were present in less than one third of the area of the lobe in five patients and in greater than one third of the area of the lobe in six patients. The presence of metastatic lymph nodes was suspected in four patients: two at level IV, one at level II, and one at level VI. We considered a lymph node to be metastatic in origin if any of the following sonography findings were revealed: the absence of a structure identifiable as fatty hilum, increased echogenicity, cystic change, or internal microcalcifications. The underlying sonogram in nine patients showed heterogeneous hypoechogenicity. The remaining two patients showed normal echogenicity.


Figure 5
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  		Fig. 2A —47-year-old woman with thyroid papillary carcinoma and ipsilateral neck node metastasis. Lesion suspected to be thyroid carcinoma was incidentally discovered during sonography intended for evaluation of palpated cervical nodules, which were proven to be benign lymph nodes. Longitudinal sonogram of left thyroid gland reveals multiple microcalcifications (arrows) at low pole and underlying heterogeneous hypoechogenicity.

 


Figure 6
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  		Fig. 2B —47-year-old woman with thyroid papillary carcinoma and ipsilateral neck node metastasis. Lesion suspected to be thyroid carcinoma was incidentally discovered during sonography intended for evaluation of palpated cervical nodules, which were proven to be benign lymph nodes. Transverse sonogram reveals lymph node located at left level IV, measuring 0.7 cm in length, without identifiable structure, indicating fatty hilum (arrows).

 
All patients underwent sonography-guided FNAB of thyroid microcalcifications. Three patients also underwent sonography-guided FNAB of suspicious lymph nodes. Ten patients showed papillary carcinoma of thyroid microcalcifications on FNAB. One patient's FNAB was found to be negative for malignancy in the thyroid microcalcification; however, a neck lymph node was found to be metastatic. All cases were confirmed with the initial diagnosis of thyroid papillary carcinoma via pathology obtained from subsequent thyroidectomy. Four of the patients were diagnosed with a diffuse sclerosing variant of papillary carcinoma (Figs. 1A, 1B, 1C, and 1D). Four patients with suspicious neck lymph nodes on sonography were diagnosed with metastatic thyroid papillary carcinoma (Figs. 2A and 2B). An additional two patients with no suspicious neck lymph nodes on sonography were also diagnosed on pathology with metastatic lymph nodes. Five of nine patients showed heterogeneous hypoechogenicity on sonography and underlying lymphocytic thyroiditis on pathology (Figs. 3A, 3B, 3C, and 3D). However, three of nine patients who showed heterogeneous hypoechogenicity on sonography were diagnosed with the diffuse sclerosing variant of papillary carcinoma.


Figure 7
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  		Fig. 3A —44-year-old woman with thyroid papillary carcinoma incidentally found on thyroid sonography during health examination. Transverse and longitudinal sonograms of right thyroid gland reveal clustered linear microcalcifications (arrows) and underlying heterogeneous hypoechogenicity.

 

Figure 8
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  		Fig. 3B —44-year-old woman with thyroid papillary carcinoma incidentally found on thyroid sonography during health examination. Transverse and longitudinal sonograms of right thyroid gland reveal clustered linear microcalcifications (arrows) and underlying heterogeneous hypoechogenicity.

 

Figure 9
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  		Fig. 3C —44-year-old woman with thyroid papillary carcinoma incidentally found on thyroid sonography during health examination. Sheet of papillary carcinoma shows slightly irregular nuclei with vesicular chromatin and occasional nuclear grooves (arrow). (ThinPrep [Cytyc Corporation], Papanicolaou stain, x1,000)

 

Figure 10
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  		Fig. 3D —44-year-old woman with thyroid papillary carcinoma incidentally found on thyroid sonography during health examination. Photomicrograph shows a few psammoma bodies scattered in papillary carcinoma. (H and E, x200)

 

Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Thyroid calcifications within a mass are an important sonographic finding, and a malignant nodule may show both coarse calcifications and microcalcifications [6]. Calcifications within a solitary mass can be considered an indicator of malignancy [7]. Recently, a panel discussion held by the Society of Radiologists in Ultrasound concluded that microcalcifications within a nodule on thyroid sonography raised the likelihood of malignancy [8]. Although coarse dystrophic calcifications are considered to be of no diagnostic value, some articles have suggested that this type of calcification seems to have an association with carcinoma [6, 9].

Histopathologically, thyroid calcifications are divided into psammoma bodies and dystrophic calcifications. Psammoma bodies are laminated, basophilic, spherical concretions and are a characteristic finding of papillary carcinoma [10]. Most microcalcifications on sonography represent psammoma bodies, suggesting malignancy [6].

Although many reports address thyroid calcifications within a mass, there are few published studies regarding thyroid carcinoma as microcalcifications on sonography without an associated mass [5]. Our review, which covers a period of approximately 5 years, revealed 11 thyroid carcinomas appearing only as thyroid microcalcifications on sonography.

Interestingly, nine of 11 patients in our study showed underlying heterogeneous hypoechogenicity on sonography. This finding could make the detection of microcalcification relatively easier compared with a normal hyperechoic thyroid gland. The high prevalence of hypoechogenicity in our patients may suggest an inflammatory process as a potential contributor in this disease category.

Among the nine patients showing underlying diffuse heterogeneous hypoechogenicity on sonography, six patients revealed underlying diffuse lymphocytic thyroiditis or diffuse hyperplasia on pathology. The remaining three, who had diffuse heterogeneous hypoechogenicity on sonography but no diffuse thyroid disease on pathology, were diagnosed with a diffuse sclerosing variant of papillary carcinoma. This diffuse sclerosing variant of papillary carcinoma is represented histologically by diffuse involvement of both thyroid lobes with dense fibrosis, extensive squamous metaplasia with morphologically benign nuclei, patchy lymphoid infiltration with germinal centers, psammoma bodies, and an area of conventional papillary carcinoma [11]. Scattered microcalcifications and heterogeneous hypoechogenicity seen on sonography in the diffuse sclerosing variant of papillary carcinoma seem to reflect lesions such as psammoma bodies, extensive fibrosis, and lymphocytic infiltration. Corresponding lesions were identified during histopathologic review of the obtained specimens.

The diffuse sclerosing variant of papillary carcinoma appears to have a tendency toward younger age distribution and a higher incidence of cervical lymph node metastases compared with papillary thyroid carcinoma [12]. However, there was no difference in age distribution between papillary carcinoma and the diffuse sclerosing variant of papillary carcinoma in this study. Metastatic lymph nodes were confirmed in six of 11 patients and, interestingly, three of four patients diagnosed with the diffuse sclerosing variant of papillary carcinoma showed multiple neck lymph node metastases. This result suggests that the diffuse sclerosing variant of papillary carcinoma might have a higher incidence of cervical nodal metastases [12].

We performed sonography-guided FNAB in all cases because of its simplicity, safety, and high sensitivity. Ten patients had malignant cytologic results from the thyroid microcalcifications. The remaining patient had a malignant cytologic result for a lymph node suspected to be metastatic in nature based on sonography findings. Thus, we conclude that sonography-guided FNAB can be satisfactory for diagnosis of thyroid carcinomas without a mass that manifest as microcalcifications on sonography.

The limitation of this study is the small sample size. A prospective study covering a larger population will be necessary to estimate the rate of malignancy and the role of FNAB for both benign and malignant lesions presenting solely as microcalcifications on sonography.

In conclusion, real-time high-resolution sonography allows good visualization of thyroid carcinomas appearing only as microcalcifications without an associated mass. In this study, underlying hypoechogenicity helped in the detection of echogenic microcalcifications of the thyroid gland. Furthermore, to evaluate thyroid microcalcifications, sonography-guided FNAB can be a useful diagnostic tool to correlate with sonography findings.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Kim EK, Park CS, Chung WY, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR 2002;178 : 687-691[Abstract/Free Full Text]
  2. Alexander EK, Marqusee E, Orcutt J, et al. Thyroid nodule shape and prediction of malignancy. Thyroid 2004;14 : 953-958[CrossRef][Medline]
  3. Koike E, Noguchi S, Yamashita H, et al. Ultrasonographic characteristics of thyroid nodules: prediction of malignancy. Arch Surg 2001; 136:334 -337[Abstract/Free Full Text]
  4. Holtz S, Powers WE. Calcification in papillary carcinoma of the thyroid. Am J Roentgenol Radium Ther Nucl Med1958; 80:997 -1000[Medline]
  5. Robinson PC, Rifkin MD, Price A. Papillary carcinoma of the thyroid gland in a young child. Ultrasound Q2004; 20:101 -103[CrossRef][Medline]
  6. Takashima S, Fukuda H, Nomura N, Kishimoto H, Kim T, Kobayashi T. Thyroid nodules: re-evaluation with ultrasound. J Clin Ultrasound 1995; 23:179 -184[Medline]
  7. Khoo ML, Asa SL, Witterick IJ, Freeman JL. Thyroid calcification and its association with thyroid carcinoma. Head Neck2002; 24:651 -655[CrossRef][Medline]
  8. 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 : 794-800[Abstract/Free Full Text]
  9. Taki S, Terahata S, Yamashita R, et al. Thyroid calcifications: sonographic patterns and incidence of cancer. Clin Imaging 2004; 28:368 -371[CrossRef][Medline]
  10. Merino MJ, Middleton LP. Pathology of the thyroid. In: Pilch BZ, ed. Head and neck surgical pathology. Philadelphia, PA: Lippincott Williams & Wilkins, 2001:358 -363
  11. Baloch ZW, Livolsi VA. Pathology of thyroid and parathyroid diseases. In: Mills SE, ed. Sternberg's diagnostic surgical pathology, 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins, 2004: 557-619
  12. Lam AK, Lo CY. Diffuse sclerosing variant of papillary carcinoma of the thyroid: a 35-year comparative study at a single institution. Ann Surg Oncol 2006;13 : 176-181[Abstract/Free Full Text]

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