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Three-Dimensional Sonography in the Evaluation of Primary Hyperparathyroidism Susan J. Frank, MD, Tova C. Koenigsberg, MD, Jennifer Lee, MD, Rebecca M. Sternschein, MD, Mordecai Koenigsberg, MD Three-dimensional sonography is useful in the preoperative evaluation of patients with primary hyperparathyroidism. In this pictorial essay, we review the characteristic spectrum of grayscale and Doppler appearances of parathyroid glands on 2-dimensional sonography and demonstrate the additional benefits of 3-dimensional scanning. Key Words—general ultrasound; parathyroid; sonography; 3-dimensional sonography
T Received April 24, 2013, from the Montefiore Medical Center/Albert Einstein College of Medicine, New York, New York USA (S.J.F., T.C.K., M.K.); and Albert Einstein College of Medicine, Bronx, New York USA (J.L., R.M.S.). Dr Lee is currently with the Albert Einstein Medical Center, Philadelphia, Pennsylvania USA; Dr Sternschein is currently with the New York University Medical Center, New York, New York USA. Revision requested May 14, 2013. Revised manuscript accepted for publication June 26, 2013. We gratefully acknowledge the contributions made by Steven K. Libutti, MD, and Young Lew, RDMS, RVT, RDCS. Our early experience with 3-dimensional parathyroid sonography was originally presented as an educational exhibit at the 97th Radiological Society of North America Scientific Assembly and Annual Meeting; November 27–December 2, 2011; Chicago, Illinois. Address correspondence to Susan J. Frank, MD, Montefiore Advanced Imaging Center, 3400 Bainbridge Ave, Bronx, NY 10467-2490 USA. E-mail: [email protected]
Abbreviations
PTH, parathyroid hormone; 3D, 3-dimensional; 2D, 2-dimensional doi:10.7863/ultra.33.3.511
hree-dimensional (3D) sonography, an extremely important development in ultrasound imaging,1,2 has proven useful in many clinical applications, especially in obstetrics, gynecology and musculoskeletal imaging, but it is not yet routinely performed in the evaluation of patients with hyperparathyroidism. Three-dimensional sonography enables postprocessing reconstruction of the images in all planes, including the coronal view, which is most similar to that of the surgical field.3 With volumerendered views, important information regarding the feeding arterial vessel, the regional vascularity, and the configuration of the vascularity of parathyroid nodules may be obtained. This information can be used to better evaluate an enlarged parathyroid, to facilitate the recognition of a parathyroid adenoma, and to display pathologic conditions in a more useful format for the surgeon.
Materials and Methods For this pictorial essay, we performed 3D sonography on 61 patients who were referred to our department for hyperparathyroidism or hypercalcemia. We received Institutional Review Board approval for this project and obtained informed consent from each patient. All images for this publication were obtained with a LOGIQ 9 3D ultrasound system (GE Healthcare, Milwaukee, WI), and an RSP616-D small-parts/pediatric linear transducer (frequency, 6–15 MHZ) was used for the 3D imaging. The 2-dimensional (2D) images were obtained with an ML6-15–D small-parts/pediatric linear transducer (frequency, 6–15 MHZ). Of the original 61 patients, 15 patients had primary hyperparathyroidism due to pathologically proven parathyroid adenomas or hyperplasia. They ranged in age from 31 to 83 years and were predominantly female (2 male and 13 female).
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Initially, a 2D grayscale and color Doppler sonographic evaluation was performed. This procedure was followed by a 3D scanning automatic sweep to obtain sagittal and transverse views. The sonographer acquired the 3D sweep with the transducer held in one position as the scan was acquired (Figure 1). Multiplanar reformatted images were then manipulated by a single radiologist, either directly on the ultrasound machine or at a workstation, to reconstruct the coronal view; all 3 orthogonal planes were displayed on the screen simultaneously. The position or orientation of one of the planes within the 3D imaging volume, usually the coronal reconstructed plane, was manually rotated into the correct orientation to optimize visualization of a specific structure (Figure 2). If necessary, additional planes were manipulated sequentially in a similar fashion to further enhance the image. In some cases, a surface- or volume-rendered image was also created. In each case, the reconstruction plane chosen was the one that best highlighted the anatomic relationships important to the surgeon, the regional vascularity, or the feeding vessel (Figure 3). Changing the orientations of the transverse and sagittal images changes both the coronal and surface-rendered images. Figure 4 demonstrates the usefulness of 3D multiplanar reformatted images in visualizing the feeding vessel.
Sonographic Appearance of the Normal Parathyroid Gland There are 2 pairs of parathyroid glands. The upper pair is generally located deep to the medial midportion of the thyroid gland. The lower pair is usually located deep to and inferior to the lower pole (Figure 5). However, there is variability in the position of the glands, especially the inferior glands. Each gland is normally 0.5 × 0.3 × 0.1 cm and weighs 40 to 50 mg.4 We were not able to visualize mediastinal parathyroids, similar to the results when 2D sonography is used. Figure 2. Two-dimensional sonograms of a parathyroid gland in a 59year-old woman with hyperparathyroidism. A and B, Sagittal and transverse views are obtained from the automatic sweep. C, The coronal view is reconstructed automatically and then rotated manually into the correct anatomic orientation. A
B Figure 1. Three-dimensional sweep of the parathyroid glands. The sweep is performed electronically within the transducer as the probe is held in position.
C
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Figure 6 shows the 2D appearance of a normal parathyroid gland. It is identified as a relatively hypoechoic structure deep to the thyroid gland. A coronal reconstructed
image with color Doppler revealed no feeding vessel or peripheral vascularity.
Figure 3. Multiplanar 3D views of a parathyroid (blue arrows) with color Doppler in a 31-year-old woman with hyperparathyroidism. A and D, Coronal reconstructed image (A) and surface-rendered coronal view (D) show the peripheral vascularity (yellow arrows). B, Sagittal image. C, Transverse image. A
B
C
D
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Sonographic Appearance of Parathyroid Adenoma On 2D sonography, a parathyroid adenoma appears as a hypoechoic or heterogeneous nodule with well-defined margins that is larger than 0.9 cm in any dimension (Figure 7). Color Doppler evaluation shows regional increased blood flow, as well as characteristic peripheral vascularity. In an enlarged parathyroid, the feeding vessel initially supplies one pole of the long axis and then extends around the periphery of the enlarged gland (Figure 8).4–6 The color Doppler appearance is particularly useful in differentiating a parathyroid adenoma from a cervical lymph node, where the feeding vessel enters centrally, into the hilum (Figure 9A). However, the distinction may be more difficult with a pathologically enlarged lymph node when the normal lymphatic blood supply is damaged, and a hyperemic pathologic lymph node also may occasionally show peripheral vascularity similar to that of a parathyroid adenoma (Figure 9B). A 3D scan is particularly useful as a check for a surprising negative result on a sestamibi scan.7 The patient in Figure 10 had a negative sestimibi scan result; however, 3D reconstruction with color Doppler showed peripheral vascularity, and a hypercellular parathyroid was resected surgically.
In one of our cases, a lesion was identified superior to the upper pole of the thyroid on 2D scanning, an unusual location for a parathyroid gland (Figure 11, A and B). The 3D scan was instrumental in identifying the adenoma by clearly showing peripheral flow around the mass, typical of a parathyroid adenoma (Figure 11, C and D).
Figure 5. Anatomy of the parathyroid glands. The upper and lower pairs of glands (arrows) lie posterior to the thyroid lobes.
Figure 4. The coronal view is helpful in establishing the feeding vessel. Coronal color Doppler sonogram in a 49-year-old woman with hyperparathyroidism shows the feeding vessel (blue arrow) emanating from the carotid artery (yellow arrow).
Figure 6. Normal appearance of a parathyroid gland in a 69-year-old woman with symptoms of hyperparathyroidism. Sagittal grayscale image shows a normal parathyroid gland deep to the thyroid.
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Discussion Primary hyperparathyroidism is a common endocrine disease, estimated to occur in 3 of every 1000 people in the general population.8 Primary hyperparathyroidism is usually due to a single parathyroid adenoma and less likely due to hyperplasia.4 In the past, bilateral 4-gland exploration was the standard of care.9 With the opportunity to surgically
target only the affected gland, morbidity can be decreased by the use of newer, minimally invasive surgical techniques,3,10 although controversies have arisen as to the long-term effectiveness of this surgery.11,12 An intraoperative parathyroid hormone (PTH) assay permits the surgeon to resect the abnormal parathyroid gland and measure the PTH level immediately. This strategy is useful for predicting a postoperative euparathyroid state. The normal
Figure 7. Three-dimensional images in a 59-year-old woman with an elevated PTH level and hypercalcemia. These images show the benefits of 3D imaging in a patient with a parathyroid adenoma. A and B, Transverse and sagittal images of a smoothly marginated mass posterior to the right lobe of the thyroid. C, Coronal reconstructed image with color Doppler shows peripheral vascularity (arrow). D, Coronal reconstructed image with color Doppler shows the thyroidal artery branch (arrow) supplying the adenoma. The PTH level in the operating room dropped from 346 to 18 pg/mL after removal of this parathyroid, which proved to be an adenoma on pathologic examination. A
B
C
D
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range of PTH is 10 to 6 pg/mL; a 50% drop in the PTH level 10 minutes after excision predicts normalization of calcium levels.11 Accurate preoperative localization of the hyperfunctioning parathyroid gland is essential to the success of the targeted surgical approach.9 Additionally, studies have demonstrated certain preoperative and intraoperative clinical factors that may predict which patients are best served by a unilateral versus bilateral surgical approach.10,13,14 Currently, preoperative sonographic and sestimibi scans are often used to evaluate patients with suspected primary hyperparathyroidism. A recent article concluded that sonography may prove beneficial as the initial imaging modality, with sestimibi only necessary in select situations.15 Sonographic evaluation is advantageous, as it provides detailed anatomic information, involves no ionizing radiation, and is relatively inexpensive. Two-dimensional sonogFigure 8. Two-dimensional color Doppler appearance of a parathyroid adenoma in a 51-year-old woman with a normal PTH level but an abnormally elevated calcium level. Coronal image of the hypercellular parathyroid visualized in this patient with hyperparathyroidism shows peripheral vascularity (arrow).
raphy, as well as 3D sonography, is operator dependent. In addition, variations in anatomy and body habitus may impair visualization of deep cervical structures. Differentiating adenomas from hyperplasia can be difficult, as all 4 glands must be visualized to confirm hyperplasia. The addition of Doppler evaluation to the sonographic examination has become crucial in clarifying vascular patterns that are helpful in the identification of parathyroid adenomas.4,6,9 Three-dimensional sonography has the advantage of providing the radiologist with a true 3D image of the parathyroid gland as well as its vasculature. It allows for postprocessing of the image data acquired during a single 3D sweep by the radiologist or sonographer, even after the patient has left the department, thereby reducing the examination time.1 In addition, multiplanar reconstructions of the images in 3 orthogonal views referenced to any base plane, as well as surface- and volume-rendered images of the vessels, can be obtained.16 Although older technologies for 3D imaging required a more cumbersome method of tracking the transducer in space while manually moving it across an organ, newer technologies allow the sweep to be performed electronically within the transducer itself.16 In fact, the sonographer acquires the 3D sweep automatically, with the transducer held in one position as the scan is acquired (Figure 1). The reformatted coronal view obtained from a 3D scan is most useful for establishing the type of vascularity surrounding the mass and facilitates visualization of the feeding vessel. The anatomy of this region is well delineated on the 3D scan: the superior parathyroid gland is supplied by a branch of the superior thyroidal artery, and the inferior parathyroid gland is supplied by a branch of the inferior or superior thyroidal artery.6 The coronal view is particularly helpful for surgical planning, as it most resembles the surgical field seen by the surgeon.3 In our series, 3D sonograms clarified peripheral vascularity and
Figure 9. Color Doppler appearance of normal and abnormal lymph nodes. A, The feeding vessel enters into the central hyperechoic hilum (arrow) of a normal lymph node in a 60-year-old woman. B, Hyperemic lymph node with peripheral perforating feeding vessels (arrow) in a 45-year-old woman with metastatic papillary cancer of the thyroid. A
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the parathyroid origin of extrathyroidal nodules. In 2 cases, it was also helpful in visualizing the supplying vessel. In 2 additional cases, the 2D examination was inconclusive without the 3D manipulation to optimize the images. Our surgeons maintain that 3D sonography enables more accurate visualization of parathyroid enlargement and it has been extremely helpful in surgical planning, especially in cases with negative sestimibi scan results. The surgeons also noted that 3D sonography allows for smaller incisions, shortens surgical time, and improves patient outcomes.
The 3D scan is particularly useful in conjunction with other modalities, such as the sestimibi scan, for investigating the parathyroid. When the sestimibi scan and 2D sonography are concordant in identification of an adenoma, 95% sensitivity has been reported for detecting an adenoma, as confirmed by surgery, in one series17 and 79% in another.11 However, even with a negative sestimibi scan result, sonography may reveal a typical appearance of a parathyroid adenoma.18 Three-dimensional reconstruction with power Doppler helps confirm the typical
Figure 10. This 49-year-old patient with elevated calcium and PTH levels had a negative sestimibi scan result. A–C, Three-dimensional color Doppler images in coronal (A), sagittal (B), and transverse (C) planes show a lesion suspicious for an enlarged parathyroid with peripheral vascularity (arrows). D, Surface-rendered reconstructed image shows the lesion after rotation to optimize visualization of the vascularity. At surgery, the PTH level dropped appropriately when the lesion was resected. Pathologic examination revealed a hypercellular parathyroid. A
B
C D
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increased vascularity commonly associated with an adenoma. In our series, 3 patients of the 15 patients with surgically documented enlarged parathyroid glands had negative sestimibi scan results. In another patient with a negative sestimibi scan result, a nodule was shown on 2D sonography, but 3D sonography was not able to adequately characterize the vascular characteristics, likely because of the nodule’s small size. One patient had a positive sestimibi scan result, but 2D sonography and 3D sonography were technically limited by a large thyroid nodule in this region. The added information that 3D sonography provides can be helpful in increasing the likelihood that a lesion represents an adenoma, as in our case with the unusual mass superior to the upper pole of the thyroid on 2D scanning.
In this case, the 3D scan showed peripheral flow around the mass, typical of an enlarged parathyroid. However, one of the limitations of sonography (both 2D and 3D) is that neither can differentiate between an adenoma and hyperplasia solely on the basis of the size and appearance of a single gland, and the other glands must be assessed as well. In this situation, an intraoperative PTH assay can be beneficial by alerting the surgeon to the presence of multiglandular disease.19 There are several technical limitations that we have encountered in 3D imaging of the parathyroid glands. We need to change to a 3D probe after the 2D portion of the examination has been finished. The 3D probe used on our machine is larger and heavier than the 2D smallparts probe and more cumbersome, which occasionally makes it difficult to image the parathyroid glands, espe-
Figure 11. Sonograms from a 71-year-old woman with hypercalcemia and hyperparathyroidism reveal an atypical appearance of a parathyroid adenoma (arrows). A and B, Sagittal and transverse 2D images of a lesion superior to the upper pole of the thyroid, an unusual location for a parathyroid gland. C, Sagittal power Doppler image shows increased regional blood flow. D, Coronal power Doppler reconstruction shows a peripheral orientation of the blood flow, typical for an adenoma. At surgery, the intraoperative PTH level dropped from 511 to 45 pg/mL after resection of this lesion. A
C
D
B
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cially in a patient with a short neck or small, deep parathyroid glands. At times, we have used a 3D transvaginal probe (RIC5-9-D, with a frequency of 7–9 MHZ), which has a configuration more amenable to these anatomic situations but which necessitates sacrifice of the field of view and high-frequency imaging. Further evaluation with larger studies would be helpful to validate the usefulness of 3D imaging of the parathyroid glands, including the merits of 3D sonography relative to sestimibi imaging and relative to 2D imaging alone. In conclusion, 3D sonography helps in the localization and characterization of parathyroid glands in patients with primary hyperthyroidism by facilitating visualization of the characteristic peripheral vascularity and the feeding vessel. It visualizes the parathyroid gland in the coronal view, which most resembles the surgical field, and so assists in preoperative planning. The coronal images are particularly useful in the precise localization of parathyroid masses in patients undergoing minimally invasive focused parathyroidectomy for a solitary adenoma.3 It has been shown that the use of both grayscale and color Doppler sonography increases accuracy in identifying adenomas preoperatively.4,6,9 In our experience, 3D sonography also improves diagnostic accuracy in cases in which other imaging modalities are equivocal. Moreover, the use of 3D sonography allows for radiologist manipulation of data sets at a later time, thus potentially decreasing the examination time and facilitating more efficient use of departmental resources.
8.
References
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6.
7.
Benacerraf B. The future of ultrasound: viewing the dark side of the moon? Ultrasound Obstet Gynecol 2004; 23:211–215. Campbell S. 4D, or not 4D: that is the question. Ultrasound Obstet Gynecol 2002; 19:1–4. Miyabe R. Three-dimensional ultrasonography before minimally invasive focused parathyroidectomy: the importance of coronal images. Surg Today 2009; 39:98–103. Johnson NA, Tublin ME, Ogilvie JB. Parathyroid imaging: technique and role in the preoperative evaluation of primary hyperparathyroidism. AJR Am J Roentgenol 2007; 188:1706–1715. Wolf RJ, Cronan JJ, Monchik JM. Color Doppler sonography: an adjunct technique in assessment of parathyroid adenomas. J Ultrasound Med 1994; 13:303–308. Lane MJ, Desser TS, Weigel RJ, Jeffrey RB Jr. Use of color and power Doppler sonography to identify feeding vessels associated with parathyroid adenomas. AJR Am J Roentgenol 1998; 171: 819–823. Davis ML, Quayle FJ, Middleton WD, et al. Ultrasound facilitates minimally invasive parathyroidectomy in patients lacking definitive localization from preoperative sestimibi scan. Am J Surg 2007; 194:785–791.
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Adami S, Marcocci C, Gatti D, Epidemiology of primary hyperparathyroidism in Europe. J Bone Miner Res 2002; 17(suppl 2):N18–N23. Reeder SB, Desser TS, Weigel RJ, Jeffrey RB. Sonography in primary hyperparathyroidism: review with emphasis on scanning technique. J Ultrasound Med 2002; 21:539–552. Chen H, Sokoll LJ, Udelsman R. Outpatient minimally invasive parathyroidectomy: a combination of sestimibi-SPECT localization, cervical block anesthesia, and intraoperative parathyroid hormone assay. Surgery 1999; 126:1016–1022. Siperstein A, Berber E, Barbosa GF, et al. Predicting the success of limited exploration for primary hyperparathyroidism using ultrasound, sestimibi and intraoperative parathyroid hormone: analysis of 1158 cases. Ann Surg 2008; 248:420–428. Norman J, Lopez J, Politz D. Abandoning unilateral parathyroidectomy: why we reversed our position after 15,000 parathyroid operations. J Am Coll Surg 2012; 214:260–269. Augustine MM, Bravo PE, Zeiger MA. Surgical treatment of primary hyperparathyroidism. Endocr Pract 2011; 17(suppl 1):75–82. Lew JI, Solorzano CC. Surgical management of primary hyperparathyroidism: state of the art. Surg Clin North Am 2009; 89:1205–1225. Tublin ME, Pryma DA, Yim JH, et al. Localization of parathyroid adenomas by sonography and technetium Tc 99m sestamibi single-photon emission computed tomography before minimally invasive parathyroidectomy: are both studies really needed? J Ultrasound Med 2009; 28:183–190. Downey DB, Fenster A, Williams JC. Clinical utility of three-dimensional US. Radiographics 2000; 20:559–571. Arici C, Cheah WK, Ituarte PH, et al. Can localization studies be used to direct focused parathyroid operations? Surgery 2001; 129:720–729. Mihai R, Gleeson F, Buley ID, Roskell DE, Sadler GP. Negative imaging studies for primary hyperparathyroidism are unavoidable: correlation of sestamibi and high-resolution ultrasound scanning with histological analysis in 150 patients. World J Surg 2006; 30:697–704. Johnson NA, Carty SE, Tublin ME. Parathyroid imaging. Radiol Clin North Am 2011; 49:489–509.
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PICTORIAL ESSAY
Three-Dimensional Sonography in the Evaluation of Primary Hyperparathyroidism Susan J. Frank, MD, Tova C. Koenigsberg, MD, Jennifer Lee, MD, Rebecca M. Sternschein, MD, Mordecai Koenigsberg, MD Three-dimensional sonography is useful in the preoperative evaluation of patients with primary hyperparathyroidism. In this pictorial essay, we review the characteristic spectrum of grayscale and Doppler appearances of parathyroid glands on 2-dimensional sonography and demonstrate the additional benefits of 3-dimensional scanning. Key Words—general ultrasound; parathyroid; sonography; 3-dimensional sonography
T Received April 24, 2013, from the Montefiore Medical Center/Albert Einstein College of Medicine, New York, New York USA (S.J.F., T.C.K., M.K.); and Albert Einstein College of Medicine, Bronx, New York USA (J.L., R.M.S.). Dr Lee is currently with the Albert Einstein Medical Center, Philadelphia, Pennsylvania USA; Dr Sternschein is currently with the New York University Medical Center, New York, New York USA. Revision requested May 14, 2013. Revised manuscript accepted for publication June 26, 2013. We gratefully acknowledge the contributions made by Steven K. Libutti, MD, and Young Lew, RDMS, RVT, RDCS. Our early experience with 3-dimensional parathyroid sonography was originally presented as an educational exhibit at the 97th Radiological Society of North America Scientific Assembly and Annual Meeting; November 27–December 2, 2011; Chicago, Illinois. Address correspondence to Susan J. Frank, MD, Montefiore Advanced Imaging Center, 3400 Bainbridge Ave, Bronx, NY 10467-2490 USA. E-mail: [email protected]
Abbreviations
PTH, parathyroid hormone; 3D, 3-dimensional; 2D, 2-dimensional doi:10.7863/ultra.33.3.511
hree-dimensional (3D) sonography, an extremely important development in ultrasound imaging,1,2 has proven useful in many clinical applications, especially in obstetrics, gynecology and musculoskeletal imaging, but it is not yet routinely performed in the evaluation of patients with hyperparathyroidism. Three-dimensional sonography enables postprocessing reconstruction of the images in all planes, including the coronal view, which is most similar to that of the surgical field.3 With volumerendered views, important information regarding the feeding arterial vessel, the regional vascularity, and the configuration of the vascularity of parathyroid nodules may be obtained. This information can be used to better evaluate an enlarged parathyroid, to facilitate the recognition of a parathyroid adenoma, and to display pathologic conditions in a more useful format for the surgeon.
Materials and Methods For this pictorial essay, we performed 3D sonography on 61 patients who were referred to our department for hyperparathyroidism or hypercalcemia. We received Institutional Review Board approval for this project and obtained informed consent from each patient. All images for this publication were obtained with a LOGIQ 9 3D ultrasound system (GE Healthcare, Milwaukee, WI), and an RSP616-D small-parts/pediatric linear transducer (frequency, 6–15 MHZ) was used for the 3D imaging. The 2-dimensional (2D) images were obtained with an ML6-15–D small-parts/pediatric linear transducer (frequency, 6–15 MHZ). Of the original 61 patients, 15 patients had primary hyperparathyroidism due to pathologically proven parathyroid adenomas or hyperplasia. They ranged in age from 31 to 83 years and were predominantly female (2 male and 13 female).
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Initially, a 2D grayscale and color Doppler sonographic evaluation was performed. This procedure was followed by a 3D scanning automatic sweep to obtain sagittal and transverse views. The sonographer acquired the 3D sweep with the transducer held in one position as the scan was acquired (Figure 1). Multiplanar reformatted images were then manipulated by a single radiologist, either directly on the ultrasound machine or at a workstation, to reconstruct the coronal view; all 3 orthogonal planes were displayed on the screen simultaneously. The position or orientation of one of the planes within the 3D imaging volume, usually the coronal reconstructed plane, was manually rotated into the correct orientation to optimize visualization of a specific structure (Figure 2). If necessary, additional planes were manipulated sequentially in a similar fashion to further enhance the image. In some cases, a surface- or volume-rendered image was also created. In each case, the reconstruction plane chosen was the one that best highlighted the anatomic relationships important to the surgeon, the regional vascularity, or the feeding vessel (Figure 3). Changing the orientations of the transverse and sagittal images changes both the coronal and surface-rendered images. Figure 4 demonstrates the usefulness of 3D multiplanar reformatted images in visualizing the feeding vessel.
Sonographic Appearance of the Normal Parathyroid Gland There are 2 pairs of parathyroid glands. The upper pair is generally located deep to the medial midportion of the thyroid gland. The lower pair is usually located deep to and inferior to the lower pole (Figure 5). However, there is variability in the position of the glands, especially the inferior glands. Each gland is normally 0.5 × 0.3 × 0.1 cm and weighs 40 to 50 mg.4 We were not able to visualize mediastinal parathyroids, similar to the results when 2D sonography is used. Figure 2. Two-dimensional sonograms of a parathyroid gland in a 59year-old woman with hyperparathyroidism. A and B, Sagittal and transverse views are obtained from the automatic sweep. C, The coronal view is reconstructed automatically and then rotated manually into the correct anatomic orientation. A
B Figure 1. Three-dimensional sweep of the parathyroid glands. The sweep is performed electronically within the transducer as the probe is held in position.
C
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Figure 6 shows the 2D appearance of a normal parathyroid gland. It is identified as a relatively hypoechoic structure deep to the thyroid gland. A coronal reconstructed
image with color Doppler revealed no feeding vessel or peripheral vascularity.
Figure 3. Multiplanar 3D views of a parathyroid (blue arrows) with color Doppler in a 31-year-old woman with hyperparathyroidism. A and D, Coronal reconstructed image (A) and surface-rendered coronal view (D) show the peripheral vascularity (yellow arrows). B, Sagittal image. C, Transverse image. A
B
C
D
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Sonographic Appearance of Parathyroid Adenoma On 2D sonography, a parathyroid adenoma appears as a hypoechoic or heterogeneous nodule with well-defined margins that is larger than 0.9 cm in any dimension (Figure 7). Color Doppler evaluation shows regional increased blood flow, as well as characteristic peripheral vascularity. In an enlarged parathyroid, the feeding vessel initially supplies one pole of the long axis and then extends around the periphery of the enlarged gland (Figure 8).4–6 The color Doppler appearance is particularly useful in differentiating a parathyroid adenoma from a cervical lymph node, where the feeding vessel enters centrally, into the hilum (Figure 9A). However, the distinction may be more difficult with a pathologically enlarged lymph node when the normal lymphatic blood supply is damaged, and a hyperemic pathologic lymph node also may occasionally show peripheral vascularity similar to that of a parathyroid adenoma (Figure 9B). A 3D scan is particularly useful as a check for a surprising negative result on a sestamibi scan.7 The patient in Figure 10 had a negative sestimibi scan result; however, 3D reconstruction with color Doppler showed peripheral vascularity, and a hypercellular parathyroid was resected surgically.
In one of our cases, a lesion was identified superior to the upper pole of the thyroid on 2D scanning, an unusual location for a parathyroid gland (Figure 11, A and B). The 3D scan was instrumental in identifying the adenoma by clearly showing peripheral flow around the mass, typical of a parathyroid adenoma (Figure 11, C and D).
Figure 5. Anatomy of the parathyroid glands. The upper and lower pairs of glands (arrows) lie posterior to the thyroid lobes.
Figure 4. The coronal view is helpful in establishing the feeding vessel. Coronal color Doppler sonogram in a 49-year-old woman with hyperparathyroidism shows the feeding vessel (blue arrow) emanating from the carotid artery (yellow arrow).
Figure 6. Normal appearance of a parathyroid gland in a 69-year-old woman with symptoms of hyperparathyroidism. Sagittal grayscale image shows a normal parathyroid gland deep to the thyroid.
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Discussion Primary hyperparathyroidism is a common endocrine disease, estimated to occur in 3 of every 1000 people in the general population.8 Primary hyperparathyroidism is usually due to a single parathyroid adenoma and less likely due to hyperplasia.4 In the past, bilateral 4-gland exploration was the standard of care.9 With the opportunity to surgically
target only the affected gland, morbidity can be decreased by the use of newer, minimally invasive surgical techniques,3,10 although controversies have arisen as to the long-term effectiveness of this surgery.11,12 An intraoperative parathyroid hormone (PTH) assay permits the surgeon to resect the abnormal parathyroid gland and measure the PTH level immediately. This strategy is useful for predicting a postoperative euparathyroid state. The normal
Figure 7. Three-dimensional images in a 59-year-old woman with an elevated PTH level and hypercalcemia. These images show the benefits of 3D imaging in a patient with a parathyroid adenoma. A and B, Transverse and sagittal images of a smoothly marginated mass posterior to the right lobe of the thyroid. C, Coronal reconstructed image with color Doppler shows peripheral vascularity (arrow). D, Coronal reconstructed image with color Doppler shows the thyroidal artery branch (arrow) supplying the adenoma. The PTH level in the operating room dropped from 346 to 18 pg/mL after removal of this parathyroid, which proved to be an adenoma on pathologic examination. A
B
C
D
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range of PTH is 10 to 6 pg/mL; a 50% drop in the PTH level 10 minutes after excision predicts normalization of calcium levels.11 Accurate preoperative localization of the hyperfunctioning parathyroid gland is essential to the success of the targeted surgical approach.9 Additionally, studies have demonstrated certain preoperative and intraoperative clinical factors that may predict which patients are best served by a unilateral versus bilateral surgical approach.10,13,14 Currently, preoperative sonographic and sestimibi scans are often used to evaluate patients with suspected primary hyperparathyroidism. A recent article concluded that sonography may prove beneficial as the initial imaging modality, with sestimibi only necessary in select situations.15 Sonographic evaluation is advantageous, as it provides detailed anatomic information, involves no ionizing radiation, and is relatively inexpensive. Two-dimensional sonogFigure 8. Two-dimensional color Doppler appearance of a parathyroid adenoma in a 51-year-old woman with a normal PTH level but an abnormally elevated calcium level. Coronal image of the hypercellular parathyroid visualized in this patient with hyperparathyroidism shows peripheral vascularity (arrow).
raphy, as well as 3D sonography, is operator dependent. In addition, variations in anatomy and body habitus may impair visualization of deep cervical structures. Differentiating adenomas from hyperplasia can be difficult, as all 4 glands must be visualized to confirm hyperplasia. The addition of Doppler evaluation to the sonographic examination has become crucial in clarifying vascular patterns that are helpful in the identification of parathyroid adenomas.4,6,9 Three-dimensional sonography has the advantage of providing the radiologist with a true 3D image of the parathyroid gland as well as its vasculature. It allows for postprocessing of the image data acquired during a single 3D sweep by the radiologist or sonographer, even after the patient has left the department, thereby reducing the examination time.1 In addition, multiplanar reconstructions of the images in 3 orthogonal views referenced to any base plane, as well as surface- and volume-rendered images of the vessels, can be obtained.16 Although older technologies for 3D imaging required a more cumbersome method of tracking the transducer in space while manually moving it across an organ, newer technologies allow the sweep to be performed electronically within the transducer itself.16 In fact, the sonographer acquires the 3D sweep automatically, with the transducer held in one position as the scan is acquired (Figure 1). The reformatted coronal view obtained from a 3D scan is most useful for establishing the type of vascularity surrounding the mass and facilitates visualization of the feeding vessel. The anatomy of this region is well delineated on the 3D scan: the superior parathyroid gland is supplied by a branch of the superior thyroidal artery, and the inferior parathyroid gland is supplied by a branch of the inferior or superior thyroidal artery.6 The coronal view is particularly helpful for surgical planning, as it most resembles the surgical field seen by the surgeon.3 In our series, 3D sonograms clarified peripheral vascularity and
Figure 9. Color Doppler appearance of normal and abnormal lymph nodes. A, The feeding vessel enters into the central hyperechoic hilum (arrow) of a normal lymph node in a 60-year-old woman. B, Hyperemic lymph node with peripheral perforating feeding vessels (arrow) in a 45-year-old woman with metastatic papillary cancer of the thyroid. A
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the parathyroid origin of extrathyroidal nodules. In 2 cases, it was also helpful in visualizing the supplying vessel. In 2 additional cases, the 2D examination was inconclusive without the 3D manipulation to optimize the images. Our surgeons maintain that 3D sonography enables more accurate visualization of parathyroid enlargement and it has been extremely helpful in surgical planning, especially in cases with negative sestimibi scan results. The surgeons also noted that 3D sonography allows for smaller incisions, shortens surgical time, and improves patient outcomes.
The 3D scan is particularly useful in conjunction with other modalities, such as the sestimibi scan, for investigating the parathyroid. When the sestimibi scan and 2D sonography are concordant in identification of an adenoma, 95% sensitivity has been reported for detecting an adenoma, as confirmed by surgery, in one series17 and 79% in another.11 However, even with a negative sestimibi scan result, sonography may reveal a typical appearance of a parathyroid adenoma.18 Three-dimensional reconstruction with power Doppler helps confirm the typical
Figure 10. This 49-year-old patient with elevated calcium and PTH levels had a negative sestimibi scan result. A–C, Three-dimensional color Doppler images in coronal (A), sagittal (B), and transverse (C) planes show a lesion suspicious for an enlarged parathyroid with peripheral vascularity (arrows). D, Surface-rendered reconstructed image shows the lesion after rotation to optimize visualization of the vascularity. At surgery, the PTH level dropped appropriately when the lesion was resected. Pathologic examination revealed a hypercellular parathyroid. A
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increased vascularity commonly associated with an adenoma. In our series, 3 patients of the 15 patients with surgically documented enlarged parathyroid glands had negative sestimibi scan results. In another patient with a negative sestimibi scan result, a nodule was shown on 2D sonography, but 3D sonography was not able to adequately characterize the vascular characteristics, likely because of the nodule’s small size. One patient had a positive sestimibi scan result, but 2D sonography and 3D sonography were technically limited by a large thyroid nodule in this region. The added information that 3D sonography provides can be helpful in increasing the likelihood that a lesion represents an adenoma, as in our case with the unusual mass superior to the upper pole of the thyroid on 2D scanning.
In this case, the 3D scan showed peripheral flow around the mass, typical of an enlarged parathyroid. However, one of the limitations of sonography (both 2D and 3D) is that neither can differentiate between an adenoma and hyperplasia solely on the basis of the size and appearance of a single gland, and the other glands must be assessed as well. In this situation, an intraoperative PTH assay can be beneficial by alerting the surgeon to the presence of multiglandular disease.19 There are several technical limitations that we have encountered in 3D imaging of the parathyroid glands. We need to change to a 3D probe after the 2D portion of the examination has been finished. The 3D probe used on our machine is larger and heavier than the 2D smallparts probe and more cumbersome, which occasionally makes it difficult to image the parathyroid glands, espe-
Figure 11. Sonograms from a 71-year-old woman with hypercalcemia and hyperparathyroidism reveal an atypical appearance of a parathyroid adenoma (arrows). A and B, Sagittal and transverse 2D images of a lesion superior to the upper pole of the thyroid, an unusual location for a parathyroid gland. C, Sagittal power Doppler image shows increased regional blood flow. D, Coronal power Doppler reconstruction shows a peripheral orientation of the blood flow, typical for an adenoma. At surgery, the intraoperative PTH level dropped from 511 to 45 pg/mL after resection of this lesion. A
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cially in a patient with a short neck or small, deep parathyroid glands. At times, we have used a 3D transvaginal probe (RIC5-9-D, with a frequency of 7–9 MHZ), which has a configuration more amenable to these anatomic situations but which necessitates sacrifice of the field of view and high-frequency imaging. Further evaluation with larger studies would be helpful to validate the usefulness of 3D imaging of the parathyroid glands, including the merits of 3D sonography relative to sestimibi imaging and relative to 2D imaging alone. In conclusion, 3D sonography helps in the localization and characterization of parathyroid glands in patients with primary hyperthyroidism by facilitating visualization of the characteristic peripheral vascularity and the feeding vessel. It visualizes the parathyroid gland in the coronal view, which most resembles the surgical field, and so assists in preoperative planning. The coronal images are particularly useful in the precise localization of parathyroid masses in patients undergoing minimally invasive focused parathyroidectomy for a solitary adenoma.3 It has been shown that the use of both grayscale and color Doppler sonography increases accuracy in identifying adenomas preoperatively.4,6,9 In our experience, 3D sonography also improves diagnostic accuracy in cases in which other imaging modalities are equivocal. Moreover, the use of 3D sonography allows for radiologist manipulation of data sets at a later time, thus potentially decreasing the examination time and facilitating more efficient use of departmental resources.
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