Value of Dual-Phase 99m Tc- Sestamibi Scintigraphy With Neck and Thoracic SPECT/CT in Secondary Hyperparathyroidism

Transcription

1 Nuclear Medicine and Molecular Imaging Original Research Yang et al. SPECT/CT of Hyperparathyroidism Nuclear Medicine and Molecular Imaging Original Research Jigang Yang 1 Ruirui Hao 2 Leilei Yuan 1 Chunlin Li 1 Jue Yan 3 Lishi Zhen 3 Yang J, Hao R, Yuan L, Li C, Yan J, Zhen L Keywords: delayed phase, early phase, secondary hyperparathyroidism, SPECT/CT, 99m Tc-sestamibi DOI: /AJR J. Yang and R. Hao contributed equally to this work and are the senior authors. C. Li and L. Zhen contributed equally to this work and after J. Yang can be considered corresponding authors. Received April 2, 2013; accepted after revision May 31, J. Yang was partially supported by the Natural Science Foundation of China ( ), Beijing Natural Science Foundation ( ), and Beijing Science and Technology New Star Plan (0051). 1 Department of Nuclear Medicine, Beijing Friendship Hospital of Capital Medical University, 95 Yong An Rd, XiCheng District, Beijing , PR China. Address correspondence to J. Yang (nmyangjigang@gmail.com). 2 Medical Healthcare Center, Beijing Friendship Hospital of Capital Medical University, Beijing, PR China. 3 Nuclear Medicine Department, China-Japan Friendship Hospital, Beijing, PR China. AJR 2014; 202: X/14/ American Roentgen Ray Society Value of Dual-Phase 99m Tc- Sestamibi Scintigraphy With Neck and Thoracic SPECT/CT in Secondary Hyperparathyroidism OBJECTIVE. Surgical intervention in the form of parathyroidectomy is generally considered only for severe secondary hyperparathyroidism (shpt). However, correct location of the parathyroid glands before parathyroidectomy is a challenge. The purpose of this study was to compare the diagnostic value of early and delayed phase 99m Tc-sestamibi SPECT/CT in the detection of parathyroid tissue to guide operative treatment of patients with shpt. SUBJECTS AND METHODS. Eighty patients with shpt who were undergoing hemodialysis were evaluated preoperatively with dual-phase 99m Tc-sestamibi SPECT/CT parathyroid scintigraphy to locate parathyroid tissue before parathyroidectomy. The scintigraphic results were classified as positive or negative. The accuracy of 99m Tc sestamibi early and delayed phase SPECT/CT scintigraphy was determined. RESULTS. Early phase 99m Tc-sestamibi SPECT/CT depicted 3.57 parathyroid glands (PTGs) and delayed phase 99m Tc-sestamibi SPECT/CT depicted 3.55 PTGs per study. The specificity of both early and delayed phase 99m Tc-sestamibi SPECT/CT in detecting PTGs was 100%. The 99m Tc-sestamibi SPECT/CT images of 7 of 80 patients showed positive findings in the delayed phase and negative findings in the early phase. The 99m Tc-sestamibi SPECT/CT images of 6 of 80 patients showed positive findings in the early phase and negative findings in the delayed phase. CONCLUSION. The results of our study indicate that both early and delayed phase 99m Tc-sestamibi SPECT/CT should be performed in the preoperative evaluation of hemodialysis patients with shpt due to chronic kidney disease. Performance of both early and delayed phase 99m Tc-sestamibi SPECT/CT did not increase the radiation dose compared with the use of only the early or the delayed phase. S econdary hyperparathyroidism (shpt) is a frequent and challenging issue in the treatment of patients with chronic kidney disease. Dysregulation of calcium and phosphorous homeostasis decreases renal phosphate excretion, increases serum phosphorous concentration, and reduces synthesis of calcitriol, the active form of vitamin D. All of these factors increase synthesis and secretion of parathyroid hormone (PTH) and parathyroid hyperplasia with diffuse polyclonal hyperplasia followed by monoclonal nodular hyperplasia [1, 2]. SHPT can cause substantial morbidity and mortality consequent to progressive osteodystrophy and vascular and soft-tissue calcification [3]. Current medical interventions have the potential to improve biochemical profiles and other surrogate markers. Surgical intervention in the form of parathyroidectomy is generally only considered in severe shpt [4]. In suitable candidates, parathyroidectomy dramatically ameliorates shpt symptoms and signs and increases survival rates and patient quality of life. However, the rate of persistent and recurrent disease after parathyroidectomy is high, ranging between 10% and 30% [5]. Most failures occur when the surgeon does not remove all hyperfunctioning parathyroid tissue [6]. Therefore, it is extremely important to correctly locate all parathyroid tissue preoperatively. SPECT/CT has a wide range of applications and affords the opportunity to shorten acquisition time, perform accurate attenuation correction, increase specificity, and improve localization of disease. SPECT/CT has been used in the diagnosis of thyroid carcinoma [7, 8], neuroblastoma [9], and bone lesions [10 12]. Dual phase 99m Tc-sestamibi planar parathyroid scintigraphy has been used in the diagnosis of primary hyperparathyroidism and 180 AJR:202, January 2014

2 SPECT/CT of Hyperparathyroidism shpt [13]. Previous studies have shown that SPECT can improve accuracy compared with planar imaging in parathyroid adenoma [14]. The goal of this study was to compare the diagnostic value of early and delayed phase 99m Tc-sestamibi SPECT/CT in the detection of parathyroid tissue to guide operative treatment of patients with shpt. To our knowledge, no study has directly compared early with delayed phase 99m Tc-sestamibi SPECT/ CT in the detection of parathyroid tissue in shpt patients. Subjects and Methods Patients The study population consisted of 80 patients (51 women, 29 men; average age, 66.1 ± 8.2 [SD] years) with chronic kidney disease treated by hemodialysis consecutively registered between January 2006 and December 2012 who also underwent evaluation with both early and delayed phase 99m Tc-sestamibi SPECT/CT scintigraphy before parathyroidectomy for shpt at a major academic medical institution. Preoperatively, all patients underwent dual-phase 99m Tc-sestamibi SPECT/CT scintigraphy. According to the National Kidney Foundation Kidney Disease Outcomes Quality Initiative 2003 guideline [4], patients with a parathyroid hormone concentration greater than 600 pg/ ml, calcium concentration greater than 10.4 mg/ dl, serum phosphate concentration greater than 6.6 mg/dl, calcium-phosphate product greater than 55, or worsening symptoms resistant to medical therapy should be considered for surgical treatment. Dual-Phase 99m Tc-Sestamibi Scintigraphy With SPECT/CT Patients were given an IV injection of 740 MBq (range, MBq) of 99m Tc-sestamibi. Image acquisition was performed with a 4-MDCT scanner (Symbia T2, Siemens Healthcare) and a dual-head gamma camera equipped with 5/8-inch NaI crystals. Early phase SPECT/CT images of the neck were obtained 15 minutes and delayed phase SPECT images 120 minutes after injection. Anterior neck images were acquired for 10 minutes in a matrix with a 20% window centered on the 140- kev photopeak with a pinhole collimator. The SPECT volume session included the neck and thorax with an axial FOV of cm. A matrix was used, and second projections were acquired over 360. The SPECT data were reconstructed with a 3D iterative algorithm. Images were smoothed with a 3D spatial gaussian filter. Immediately after early phase SPECT acquisition, a CT topogram was acquired and followed by a helical CT acquisition performed in a volume session similar to that of the SPECT acquisition. CT acquisition parameters were as follows: tube current, 60 ma; collimation, mm; pitch, 2. For CT data reconstruction, a 3-mm section thickness with 2-mm increment and a B70 kernel filter were used. No contrast medium was injected during the procedure. In the delayed phase, only SPECT data were acquired for SPECT/CT because CT acquisition data in the early phase can be used for delayed phase SPECT/CT. Early and delayed phase SPECT/CT data were analyzed at a workstation (e.soft, Siemens Healthcare) that provided transaxial, sagittal, and coronal slices of SPECT, CT, and fused SPECT/CT data. CT data were displayed in the neck or mediastinum window settings. Interpretation of 99m Tc-sestamibi scintigraphy was performed in consensus by two experienced nuclear medicine physicians. The image findings were scored as positive or negative. A scintigraphic finding was recognized as positive if there was a definite focus of increased or separate 99m Tcsestamibi uptake relative to the uptake in the thyroid tissue of the neck or mediastinum on either early or delayed SPECT/CT images. The precise location of each focus was reported. When a corresponding nodular mass was found on an integrated CT scan, its axial diameter was measured. A scintigraphic finding was negative when focal uptake in the neck or mediastinum was absent in both early and delayed phase SPECT/CT studies. Agreement between the two physicians was achieved in all cases [15]. Surgical Procedures Subtotal or total parathyroidectomy with implant was performed on young patients or candidates for kidney transplantation. Total parathyroidectomy was performed on elderly patients without autotransplants. All patients underwent bilateral transcervical thyroidectomy. The surgeon referred to the 99m Tc-sestamibi scintigraphic results during preoperative planning. Subtotal parathyroidectomy included ablation of three glands and one half of the fourth gland. The half of the gland with the closest to normal appearance (or determined to be in an anatomic position that facilitated reintervention in the case of recurrence) was left in situ and marked with a nonresorbable thread or metallic clip to facilitate future detection. The choice of the gland with the lowest chance of recurrence was based on size criteria, vascularization, appearance at gross surgical examination, and when possible, lack of 99m Tc-sestamibi uptake. The excised glands were sent for frozen sections, and on the basis of the histologic finding, parathyroid hyperplasia was classified as either diffuse or nodular. Statistical Analysis Statistical software (SPSS 15.0 for Microsoft Windows XP, SPSS) was used for data analysis. Comparisons of the average longitudinal diameter of PTGs and weight of PTGs were performed with the Student t test. Comparisons between early and delayed phase 99m Tc-sestamibi SPECT/CT scintigraphy in the detection of shpt were performed with the McNemar test. A nonparametric method was used for comparing paired dichotomous data. A value of p < 0.05 was considered statistically significant. Results Surgical Results Assuming four PTGs per patient, there should have been a total of 316 PTGs in 80 patients (two patients had undergone previous hemithyroidectomy). In our series, 278 PTGs were identified and surgically resected in the 80 patients. Fifty-two of 80 patients had four PTGs, 10 patients had PTGs located in mediastinum, six patients had five PTGs (three intrathyroid, two in supernumerary retroesophageal ectopic glands), six patients had three PTGs, six patients had two PTGs (two patients had undergone previous hemithyroidectomy). At pathologic examination, 58 PTGs (20.8%) exhibited diffuse hyperplasia and 220 PTGs (79.2%) exhibited nodular hyperplasia. Early and Delayed Phase 99m Tc-Sestamibi SPECT/CT Scintigraphic Results Evaluation of the early phase 99m Tc-sestamibi SPECT/CT images showed that 61 patients had positive results for shpt: A total of 218 PTGs were detected in these patients. At TABLE 1: Comparison of Average Number, Longitudinal Diameter, and Weight of Parathyroid Glands Detected at Early and Delayed Phase SPECT/CT Comparison Average No. Average Diameter (mm) Average Weight (mg) Early phase ± ± 96 Delayed phase ± ± 99 t p > 0.05 > 0.05 > 0.05 AJR:202, January

3 Yang et al. the same time, delayed phase images showed 62 patients had positive results for shpt: a total of 220 PTGs in these patients. On average 3.57 PTGs were detected in each early phase 99m Tc-sestamibi SPECT/CT study compared with 3.55 PTGs detected in each delayed phase study, indicating that early and delayed phase SPECT/CT can depict similar numbers of PTGs (t = 1.721, p > 0.05). The average longitudinal diameter of PTGs detected on early phase images was 9.3 ± 0.9 mm and on delayed phase images was 9.5 ± 0.6 mm, indicating that the diameters of PTGs detected with early and delayed phase SPECT/CT were similar (t = 1.162, p > 0.01). The average weight of PTGs at pathologic examination that had positive early phase 99m Tc-sestamibi SPECT/CT results was 1054 ± 96 mg (range, mg), whereas the average weight of PTGs with positive results on delayed phase images was 1031 ± 99 mg (range, mg), indicating that the weights of PTGs detected with early and delayed phase SPECT/CT were similar (t = 0.974, p > 0.05) (Table 1). The specificity of both early and delayed phase 99m Tc-sestamibi SPECT/CT in detecting PTGs was 100%. The sensitivity of dualphase 99m Tc-sestamibi SPECT/CT in detecting PTGs was 85% (68/80). There were no false-positive findings in either early or delayed phase imaging. The images of 7 of the 80 patients showed positive findings in the delayed phase and negative findings in the early phase (Fig. 1). The 99m Tc-sestamibi SPECT/ CT images of 6 of 80 patients showed positive findings in the early phase and negative findings in the delayed phase (Fig. 2). Therefore, the accuracy rates of early and delayed phase 99m Tc-sestamibi SPECT/CT are similar (chi-square, 1.167; p > 0.05) (Table 2). Discussion A large number of patients with end-stage renal disease experience a severe form of shpt that necessitates surgical treatment [16]. In light of recent advances in medical therapy for shpt, elucidation of the specific role of parathyroidectomy is pertinent [16]. Moreover, for the substantial number of dialysis patients with an uncontrollable form of shpt who cannot afford or otherwise obtain new therapeutics, parathyroidectomy remains the best treatment option [16]. However, surgical results among shpt patients with uremia are less satisfactory than those among patients with primary hyperparathyroidism, the rates of persistent and recurrent disease Fig year-old woman with history of chronic kidney disease treated with hemodialysis who has workup findings of increased serum calcium (10.8 mg/dl) and parathyroid hormone (679 pg/ml) concentrations. Early phase coronal (top left) and transaxial (center left) SPECT and CT (bottom left) images from 99m Tc-sestamibi scan show no abnormal radioactive accumulation in neck or mediastinum. Delayed phase coronal (top right) and transaxial (center right) SPECT and CT (bottom right) images from 99m Tc-sestamibi scan show one area of intense tracer uptake in lower part of right thyroid (arrow). Surgical pathologic result was diffuse parathyroid hyperplasia. Fig year-old man with history of chronic kidney disease treated with hemodialysis who has workup findings of increased serum calcium (11.7 mg/dl) and parathyroid hormone (768 pg/ml) concentrations. Early phase coronal (top left) and transaxial (center left) SPECT and CT (bottom left) images from 99m Tc-sestamibi scan show one area of intense tracer uptake in lower part of left thyroid (arrow). Delayed phase coronal (top right) and transaxial (center right) SPECT and CT (bottom right) images from 99m Tc-sestamibi scan shows no abnormal radioactivity accumulation in neck or mediastinum. Surgical pathologic result was diffuse parathyroid hyperplasia. 182 AJR:202, January 2014

4 SPECT/CT of Hyperparathyroidism TABLE 2: Comparison of Early and Delayed Phase 99m Tc-Sestamibi SPECT/CT Delayed Phase Positive Early Phase Negative Positive Negative Total Note Values are numbers of findings; chi-square, 1.167; p = > 0.05 (McNemar test). Total being higher. The main cause of surgical failure is incomplete intraoperative identification of all PTGs [17]. CT, MRI, arteriography, and high-resolution ultrasound have all been used in the diagnosis of shpt [18]. However, the performance of these anatomic techniques is not satisfactory in preoperative identification of shpt [18]. Parathyroid scintigraphy is almost universally regarded as the best preoperative localizing method for patients with primary hyperparathyroidism or shpt [5]. Technetium 99m sestamibi has been used in parathyroid scintigraphy. This tracer can accumulate early in the parathyroid and thyroid glands and usually washes out of normal thyroid tissue more rapidly than it does out of abnormal parathyroid tissue. This is the principle of the dual-phase method, which was first reported in 1992 [19]. In that study, a dual-phase 99m Tcsestamibi protocol was used in the diagnosis of shpt. Hybrid SPECT/CT has since emerged. The SPECT/CT camera can provide more information, including functional and anatomic images, which have been widely used in many diagnostic nuclear medicine scans [9, 20]. Previous studies have evaluated many parathyroid scintigraphic methods, including 99m Tcsestamibi SPECT of the parathyroids [14, 21]. However, in these studies only a single set of SPECT images, either early or delayed phase, is acquired. Some investigators [22, 23] have described the application of SPECT/CT to parathyroid scintigraphy. However, the optimal scintigraphic protocol of 99m Tc-sestamibi parathyroid scanning was not clear for primary hyperparathyroidism or shpt because few studies have directly compared different scintigraphic protocols. Although some studies directly compared the different methods, no consistent conclusion was made. Therefore, different scintigraphic protocols have been used in parathyroid scans. Ciappuccini et al. [13] reported the use of dual-phase 99m Tcsestamibi SPECT/CT parathyroid scanning in the diagnosis of primary hyperparathyroidism. However, the use of dual-phase 99m Tc-sestamibi SPECT/CT of the parathyroids in the diagnosis of shpt has not been reported previously, to our knowledge. In our study, we directly compared early and delayed phase 99m Tc-sestamibi SPECT/ CT. All patients underwent the early and delayed phases of imaging. On average 3.57 PTGs were detected in each early phase and 3.55 PTGs were detected in each delayed phase study, indicating that early and delayed phase SPECT/CT can depict similar numbers of PTGs. PTG diameters and weights were similar on early and delayed phase SPECT/ CT images. All of these data showed that the ability to detect parathyroid tissue in shpt patients is the same with early and delayed phase 99m Tc-sestamibi SPECT/CT. However, the findings that 7 of 80 patients had positive results in the delayed phase and negative results in the early phase and that 6 of 80 patients had positive results in the early phase and negative results in the delayed phase suggests that either early or delayed phase 99m Tc-sestamibi SPECT/CT can depict new lesions to the same degree as imaging in the other phase. Early and delayed phase 99m Tc-sestamibi SPECT/CT together can depict more lesions than with either phase alone. Schachter et al. [24] reported that delayed phase 99m Tc-sestamibi may be nondiagnostic when similar washout rates between thyroid and parathyroid tissue are found. They reported that only 60% of adenomas exhibited retention of activity on delayed phase images. They concluded that early phase SPECT is useful for localizing parathyroid adenomas and is superior to dual-phase delayed imaging. Delayed phase SPECT is not recommended because it may cause false-negative results due to rapid washout [24]. Perez-Monte et al. [15] also reported that early phase 99m Tc-sestamibi SPECT is most accurate in the detection and localization of parathyroid adenomas. Carty et al. [25] reported that early phase scanning in dualphase 99m Tc-sestamibi SPECT was more sensitive than the delayed phase in the detection of PTGs (sensitivity, 92% and 74%). However, Civelek et al. [21] reported that delayed phase SPECT is a promising protocol in the preoperative detection and localization of parathyroid adenomas in both unexplored and reexplored patients. Although all patients underwent both early and delayed phase scanning in our study, CT data were acquired only once. The CT data can be used in not only the early phase but also in the delayed phase of 99m Tc-sestamibi SPECT/CT. This method does not entail more radiation dose than early or delayed phase scanning alone. There were no false-positive results in our study, and the specificity of early and of delayed phase 99m Tc-sestamibi SPECT/CT was 100%. Although previous studies showed some false-positive findings on static planar 99m Tc-sestamibi scintigrams related to hyperplastic lymph nodes, lymphomatous lesions, thyroid adenomas, and Hashimoto thyroiditis, none were observed in our study population [26, 27]. The most likely explanation for our lack of false-positive findings is the high initial positive predictive value in our patient population because the parathyroid hormone concentrations were all greater than 600 pg/ ml, and all patients were undergoing hemodialysis for chronic kidney disease. Another advantage of SPECT/CT is the accurate and anatomic depiction of PTG location, size, and adjacent tissues and structures, which facilitates operative planning. Hybrid SPECT/CT systems that combine conventional CT with SPECT have become available for clinical application. SPECT/ CT has been found to be more specific and sensitive in the detection and interpretation of small PTGs. This is due to the combination of precise anatomic detail available with high-spatial-resolution CT and the metabolic and functional information acquired through SPECT [28, 29]. Conclusion Our study results indicate that both early and delayed 99m Tc-sestamibi SPECT/CT should be performed in the preoperative evaluation of hemodialysis patients with shpt due to chronic kidney disease. The combination of early and delayed 99m Tc-sestamibi SPECT/CT did not increase the radiation dose compared with early or delayed imaging alone. References 1. Slatopolsky E, Brown A, Dusso A. Pathogenesis of secondary hyperparathyroidism. Kidney Int Suppl 1999; 73:S14 S19 2. Cunningham J, Locatelli F, Rodriguez M. Secondary hyperparathyroidism: pathogenesis, dis- AJR:202, January

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