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BMC Medical Imaging

, 19:7 | Cite as

The role of ultrasound in the diagnosis of the coexistence of primary hyperparathyroidism and non-medullary thyroid carcinoma

  • Jian Shen
  • Qiong Wu
  • Yan WangEmail author
Open Access
Research article
Part of the following topical collections:
  1. Head and neck imaging

Abstract

Background

The coexistence of primary hyperparathyroidism(PHPT) and papillary thyroid cancer(PTC) is a known entity; it is a rare and complicated setting for diagnostic imaging.

Methods

After reviewing clinical data of 112 patients who had been treated for PHPT in our facility between January 2015 and December 2017, we identified 7 non-medullary thyroid carcinoma (NMTC) (6.25%). All of them had taken an ultrasound scan and undergone operation. In addition, we have also reviewed relevant reports from other facilities addressing PHPT and NMTC (Mainly PTC).

Results

The 7 NMTCs were all pathologically confirmed PTC in our study, and they consisted of 6 parathyroid adenomas and 1 parathyroid carcinoma. 1 of the 7 patients had 2 malignant PTC nodules with neck lymph node metastasis, the rest 6 had single-focal PTC. Processing previous report data supported an association between PHPT and PTC, although the coexistence of PHPT and PTC is rare, but it does happen. Ultrasound, as an effective examination, would help screen the simultaneous lesions before operation, thus to avoid second surgery if not observed for both diseases at initial stage.

Conclusions

Ultrasound is a necessary choice for preoperative localization, because it has the ability to simultaneously examine the thyroid and parathyroid lesions.

Keywords

Primary hyperparathyroidism Papillary thyroid carcinoma Ultrasound Preoperative localization 

Abbreviations

NTMC

Non-medullary thyroid carcinoma

PHPT

Primary hyperparathyroidism

PTC

Papillary thyroid carcinoma

Background

The coexistence of primary hyperparathyroidism (PHPT) and non-medullary thyroid carcinoma (NMTC) was initially described by Ogburn and Black in 1956. According to their reports, 3 cases of synchronous PHPT and NMTC (including PTC and FTC) of the thyroid glands in patients operated for parathyroid adenoma was found [1]. NMTC with PHPT has been reported in 2–11% of patients undergone surgery for PHPT [2]. The majority of the cases were uni-focal occult PTC without cervical lymph nodes involvement in women. Besides, many of the cases were associated with a previous head and neck irradiation [3]. The coexistence of PHPT and PTC is rare; and PHPT was usually considered as the primary pathology and was diagnosed before the identification of the thyroid carcinoma that was usually diagnosed in a pathology specimen as an incidental finding after parathyroid surgery. Such phenomenon would further complicate the management process, especially resulting in the need of a second surgery [2]; therefore, a carefully preoperative imaging would be necessary. We present 7 cases of synchronous PHPT and PTC, trying to explore the significance of ultrasound in preoperative localization; furthermore, relevant reports from other research centers addressing PHPT and NMTC (Mainly PTC) were also reviewed.

Methods

We retrospectively studied 112 patients with PHPT admitted to our center between January 2015 and December 2017. Finally, 7 cases, pathologically confirmed as synchronous PHPT and PTC, were enrolled in. All the patients were healthy, and none of them had any risk factors related to thyroid cancer according to the American Thyroid Association (ATA) 2015 guidelines (i.e. prior thyroid cancer, family history, or exposure to external irradiation) [4]. And all of them had cervical ultrasound scan suggesting parathyroid lesion and were scheduled for an elective parathyroidectomy. The ultrasound scans were all operated by Professor Yan Wang, the corresponding author of this article. The number, size, location, border, blood supply and other relative detections were recorded. The ultrasonography was observed by using a linear probe of SIMENS 3000 and/or HITACH with a frequency of 8-12 MHz. Moreover, some patients were chosen to undergo 99mTc-MIBI or CT selectively. Surgery was achieved in patients who met the criteria for parathyroidectomy. As there were other thyroid lesions suspicious for PTC, the thyroid specimen was sent for an intraoperative frozen section pathologic examination, which confirmed PTC. Based on above information and consent approved, lobectomy or total thyroidectomy was performed in addition to the minimally invasive parathyroidectomy (MIP). The PUBMED and EMBASE electronic database was searched to identify relevant studies among recent years. With this purpose, we used the following terms: “primary hyperparathyroidism” and “non-medullary thyroid carcinoma” but limited to “human”. Moreover, relevant studies were also extensively searched by hand; language limitations were applied as English.

Results

Patients

A total of 112 patients who underwent parathyroidectomy for PHPT were selected. All the patients had taken a cervical ultrasound scan. Mean age of 7 patients with synchronous PHPT and PTC was 50 years (34–57 y) and 6/7 (85.7%) were female. None of these patients had a history of radiation exposure. 1 of the 7 patients underwent lobectomy, with the pathological diagnosis of thyroid adenoma. Preoperatively, the serum calcium of these patients was 2.51~3.63 mmol/L (Normal 2.09~2.6 mmol/L), serum phosphate was 0.75~1.34 mmol/L (Normal 0.8~1.6 mmol/L), and serum parathyroid hormone was 57.99~ 425 pg/mL (Normal 15~ 65 pg/mL).

In most case reports describing the coexistence of these two lesions, PHPT was usually diagnosed before the identification of the thyroid carcinoma which was usually diagnosed in pathology specimen as an incidental finding after the surgery [2, 5, 6]. However, in our study, most of the cases were admitted by annual thyroid nodule examination, and the parathyroid lesion was prompted by following ultrasound (Table 1).
Table 1

Patient characteristics and disease etiology

Characteristic

Patient

1

2

3

4

5

6

7

Gender

F

F

F

F

M

F

F

Age, years

56

34

57

54

52

50

49

Reason

Thyroid nodule follow-up.

Bone pain (mainly right upper limb) for half a year.

Thyroid nodule follow-up.

Thyroid nodule follow-up.

Thyroid and parathyroid nodule during annual examination

Thyroid nodule follow-up.

Thyroid nodule follow-up.

History

No history of radiation exposure

·Lobectomy history (Left lobe-thyroid adenoma).·Brown tumor.·No history of radiation exposure

No history of radiation exposure

No history of radiation exposure

No history of radiation exposure

No history of radiation exposure

No history of radiation exposure

Preoperative biochemistry

 Calcium, mg/dL

2.65

3.63

2.66

3.01

2.75

2.51

2.98

 Phosphate, mg/dL

1.15

0.98

1.34

0.87

0.95

0.75

 Parathyroid hormone, pg/mL

189.9

769.2

57.99

164.3

114.9

86.87

425

Ultrasound features

 Number

1

2

1

1

1

1

1

 Echo

Hypoechoic/Homogeneous/Calcification

Hypoechoic/Homogeneous

Hypoechoic/Heterogeneous

Hypoechoic/Heterogeneous

Hypoechoic/Heterogeneous

Hypoechoic/Homogeneous

Hypoechoic/Homogeneous

Hypoechoic/Homogeneous/Calcification

 Size

10 mm × 6 mm

12 mm× 8 mm

22 mm × 15 mm × 32 mm

21 mm × 10 mm× 5 mm

16 mm× 9 mm

23 mm × 9 mm

12 mm × 7 mm

7.5 mm × 7.2 mm

 Location

Posterior to the right thyroid lobe, lower pole

Inferior pole of the right thyroid lobe, adjacent to the trachea

Zone of left thyroid lobe

Near the upper pole, posterior to the right thyroid lobe

Inferior pole of the left thyroid lobe

Posterior to the middle right thyroid lobe, adjacent to the trachea

Near the superior pole of the right thyroid lobe

Inferior pole of the left thyroid lobe

 Form

regular

regular

irregular

regular

regular

regular

regular

irregular

 Border

clear

unclear

unclear

clear

clear

clear

clear

clear

 Blood

II

III

III

III

III

III

III

III

 Elastography

1

2

2

3

 Other

Hypoechoic thyroid nodule measuring 8.6 mm × 9.1 mm to the upper pole of left lobe with irregular form, unclear border, calcification, a little blood. Elastography grade: 4.

Several hypoechoic thyroid nodules and cysts in the right lobe.

Hypoechoic thyroid nodule measuring 5.9 mm× 6.8 mm in the middle of right lobe next to the anterior membrane, taller-than-wide, irregular form, unclear border. No blood detected.

Hypoechoic thyroid nodule measuring 14 mm× 6 mm in the left lobe with irregular form, unclear border, micro-calcification, a little blood.

Several small (Diameter 3 mm to 10 mm) hypoechoic thyroid nodules highly suspicious malignant according to the ATA 2015 guideline.

Hypoechoic thyroid nodule measuring 11 mm × 7 mm near the inferior pole of the left thyroid lobe with irregular form, unclear border, micro-calcification, a little blood. Elastography grade: 4. Other two nodules of very low suspicious.

Several hypoechoic and mixed echo thyroid nodules in both lobes. The biggest one in the right lobe was in size of 23 mm× 16 mm with irregular form, unclear border, arc-like calcification, a little blood.

 99mTc-MIBI or CT features

Cervical CT: Right lobe nodules, left side lesion suspicious series from parathyroid

99mTc-MIBI: Highly suspicious of left side parathyroid adenoma.

99mTc-MIBI: Suspicious of left side PHPT.Cervical CT: Nodule in the left lobe of malignant suspicious. Nodule inferior to the right lobe can not excepted the possibility of parathyroid original.

Cervical CT: Multiple nodules in both thyroid lobes.

Ultrasound

Among the 7 patients, totally 8 hypoechoic parathyroid nodules were observed by ultrasound, 5 of which were located on the right side of the patients’ necks. The result is similar in comparison with former studies [2]. The size of the nodules varied from the smallest one measuring 7.5 mm× 7.2 mm to the biggest measuring 32 mm× 22 mm× 15 mm. Among them, 2 of the 8 nodules, including 1 adenoma and 1 carcinoma, were observed to have calcification. 4 of the 7 patients were found to have multiple thyroid nodules including hypoechoic nodules, mixed-echo nodules and cysts; and at least one of them was considered malignant according to the guideline (Table 1, Fig. 1).
Fig. 1

Cervical ultrasonography of a 50-year-old female patient. a and b showed a hypoechoic thyroid nodule measuring 11 mm× 7 mm near the inferior pole of the left thyroid lobe with irregular form, unclear border, micro-calcification. Little blood signal was detected in CDFI mode. c and d showed a hypoechoic right superior parathyroid lesion. Rich color blood flow signal was detected. The pathological results were papillary thyroid micro-carcinoma and parathyroid adenoma respectively

CT and 99Tcm-MIBI SPECT

We have implemented 99Tcm-MIBI on 3 patients; the results showed suspicious or highly suspicious of parathyroid lesion. 3 patients underwent cervical CT, 2 of which prompted suspicious parathyroid lesions (Table 1). Moreover, by comparison of 3 imaging examinations, ultrasound is more efficient than cervical CT and 99Tcm-MIBI (Table 2).
Table 2

Comparisons of US, CT and 99mTc-MIBI

Patient

1

2

3

4

5

6

7

Characteristics

Th

Pth

Th

Pth

Th

Pth

Th

Pth

Th

Pth

Th

Pth

Th

Pth

Findinga

US

CT

×

MIBI

×

×

Diagnosisa

US

×

CT

Suspiciousb

Cannot except the possibilityc

×

MIBI

×

×

Suspicious

Abbreviations: Th Thyroid lesion, Pth Parathyroid lesion. a Finding: The lesion could be detected during or after the imaging scan; Diagnosis: The origin of the lesions (thyroid or parathyroid) can be correctly identified according to the imaging. bSuspicious: About 60% of the Possibilities. cCannot except the possibility: Lower than 50% of the Possibilities

Pathological results and surgical managements

Surgery was achieved in patients who met the criteria for parathyroidectomy; as there were other thyroid lesions suspicious for PTC, the thyroid specimen was sent for intraoperative frozen section pathologic examinations, which confirmed PTC. According to the intraoperative frozen results, which revealed all the suspected thyroid nodules in ultrasound were malignant; 2 patients underwent total thyroidectomies and 5 received lobectomies. Moreover, necessary exploration of recurrent laryngeal nerve and dissection of central cervical lymph nodes were also performed. The final pathological results revealed that the cause of PHPT was a single parathyroid adenomatous gland in 5 (71.4%) patients, two parathyroid adenomatous glands in 1 (14.3%) patient, and parathyroid carcinoma in 1 (14.3%) patient. Besides, the final pathology of the thyroid nodules was PTMC in 4 patients and PTC in other 3 patients, and 1 of the 7 patients was multi-focal PTC with metastasis of four cervical central lymph nodes (Table 3).
Table 3

Intraoperative course and pathological results

Characteristics

Patient

1

2

3

4

5

6

7

Intraoperative findings

Lesion A1 in the left thyroid lobe, toughLesion A2 (about 1 cm) posterior to the right thyroid lobe, soft

Lesion B1 (2x3cm) in the left thyroid zone, adherence to adjacent tissueLesion B2 inferior pole of the right thyroid lobeLesion B3 in the right thyroid lobe

Lesion C1 in the right thyroid lobe, toughLesion C2 posterior to the right thyroid lobe

Lesion D1 in the left thyroid lobe, toughLesion D2 (about 1 cm) posterior to the left thyroid lobe, soft

Several nodules in both thyroid lobe, toughMultiple enlarged lymph nodes in the cervical central regionLesion E posterior to the right thyroid lobe

Lesion F1 in the left thyroid lobe, toughLesion F2 (about 1 cm) posterior to the left thyroid lobe

Lesion G1 (2.5 cm) in the right thyroid lobe, toughLesion G2 (4 cm) in the left thyroid lobe

Section frozen results

Lesion A1: PTCLesion A2: Parathyroid adenoma

Lesion B1: Wait for final pathologic resultLesion B2: Parathyroid adenomaLesion B3: PTMC (about 0.3 cm)

Lesion C1: PTC (0.4 cm)Lesion C2: Highly suspected parathyroid adenoma, wait for final pathologic result

Lesion D1: PTC (1.3 × 1 × 0.6 cm)Lesion D2: Parathyroid adenoma

Lesion E: Parathyroid adenomaBoth thyroid lobe: Multi-focal PTC (3 in the left, 1 in the right)

Lesion F1: PTC(0.5 cm)Lesion F2: Parathyroid adenoma

Lesion G1: PTC(2 × 1.5x1cm)Lesion G2: Thyroid adenoma with cystic degeneration and interstitial fibrosis; Suspected parathyroid carcinoma, wait for final pathologic result

Surgical approach

Left thyroid lobectomy + Dissection of left central cervical lymph nodes + Exploration of left recurrent laryngeal nerve + Right parathyroidectomy

Bilateral parathyroidectomy+ Right thyroid lobectomy + Dissection of right central cervical lymph nodes + Exploration of bilateral recurrent laryngeal nerve

Right thyroid lobectomy + Dissection of right central cervical lymph nodes + Exploration of right recurrent laryngeal nerve + Right parathyroidectomy

Left thyroid lobectomy + Dissection of left central cervical lymph nodes + Exploration of left recurrent laryngeal nerve + Left parathyroidectomy

Total thyroidectomy + Dissection of central cervical lymph nodes + Right parathyroidectomy

Left thyroid lobectomy + Dissection of left central cervical lymph nodes + Exploration of left recurrent laryngeal nerve + Left parathyroidectomy

Total thyroidectomy + Exploration of bilateral recurrent laryngeal nerve + Dissection of right central cervical lymph nodes

Pathological results

Parathyroid

Parathyroid adenoma

Parathyroid adenoma (Lesion B1 & B3)

Parathyroid adenoma

Parathyroid adenoma

Parathyroid adenoma

Parathyroid adenoma

Parathyroid carcinoma

Thyroid

PTMC

PTMC

PTMC

PTC

Multi-focal PTC with metastasis of cervical lymph nodes

PTMC

PTC and Thyroid adenoma

Consistency with US

 Y

Y

Y

Y

Y

Y

Y/N*

Abbreviation: Y Consistent, N Inconsistent. * The results of US report did not mention parathyroid lesion, but it was described in the image features. So it can’t be considered simply to be consistent or inconsistent

Discussion

The coexistence of primary hyperparathyroidism and papillary thyroid cancer is a known entity over the years. From the initial report by Ogburn and Black in 1960s to the recent discussions over these years, a series of relevant clinical studies were conducted. According to their findings, it has been reported with a rate of 2~11% patients underwent surgery for PHPT [2]. As for the data we summarized, the average rate is about 3.5% of thyroid cancer among patients with PHPT undergoing parathyroidectomy (ranging 1.7 to 15%, 313 thyroid carcinoma cases among 9051 patients with PHPT) (Table 4). The largest cohort was described by Linos et al., who found 2.5% (51 of 2058) patients with surgically proved PHPT had associated NMTC [7]. Furthermore, the incidence rate of concurrence of PTC and PHPT in 5 big clinical series (the total number of patients with PHPT was over 500) is relatively stable of 2.1 to 3.3% [2, 8, 9, 10]. However, it was of great fluctuations in the small clinical series especially when the total number of patients being reviewed were less than 100 [11, 12, 13] (Table 4). The reason we analyzed from a statistic perspective is the high false positive rate caused by selection bias of small sample which also occurred in our data (6.25%). Combining with statistic experience, the data from relevant big sample is more convincing due to the low incidence of synchronous PHPT and PTC. On the other hand, the synchronous PTC and PHPT has a concurrence rate between 2.6 to 4.5% in the patients firstly admitted for thyroid operation, and Niedźwiecki et al. considered that there was no significant difference of PHPT incidence between various type of goiter [14].
Table 4

Papillary thyroid cancer among patients with PHPT undergoing parathyroidectomy

Author

Year

Number of patients with PHPT

Number of patients with NMTC

Incident rate(%)

Linos et al. [4]

1982

2058

51

2.5

Lehwald et al. [2]

2013

1464

41

2.8

Attie and Vardhan [8]

1993

948

31

3.3

Burmeister et al. [9]

1997

700

18

2.6

Bentrem et al. [10]

2002

580

12

2.1

Hedman and Tisell [21]

1984

426

25

5.8

Nishiyama et al. [22]

1979

420

13

3.1

Strichartz and Giuliano [23]

1990

388

11

2.8

Prinz et al. [24]

1982

351

16

4.6

Krause et al. [25]

1996

322

9

2.8

LiVolsi et al. [26]

1976

272

31

11.4

Ogburn and Black [1]

1956

230

4

1.7

Phillips et al. [27]

2014

217

5

2.3

Morita et al. [28]

2008

200

12

6.0

Xue et al. [29]

2016

155

12

7.7

Beus et al. [30]

2004

101

3

3.0

Arciero et al. [11]

2012

94

6

6.4

Sidhu and Campbell [12]

2000

65

4

6.2

Gul et al. [13]

2010

60

9

15.0

Total

9051

313

3.5

The mechanisms underlying the relationship between PHPT and PTC have still left to be unknown; most of the published studies claimed this relationship is still considered as coincidental. Previous head and neck irradiation in childhood appears to be an increased risk for the development of both PHPT and NMTC [3, 15, 16, 17]. However, many patients included in the previous clinical series did not have a radiation exposure or treatments; neither did we found in the patients in our study. Thus, it may not be an essential risk for the concurrence of PHPT and PTC. Beebeejaun et al. suggested a possible hypothesis for the correlation based on shared embryological origin and genes (i.e. Eya 1), high parathyroid hormone (PTH), low 1,25 hydroxyl vitamin D, hypercalcemia resulting in high levels of angiogenic growth factors (i.e. bFGF) [18]. Hypotheses have been presented, but no firm conclusions exist at this time regarding the etiology of synchronous thyroid and parathyroid disease.

Over the past years, more and more articles related to coexistence of PHPT and NMTC were reported, but the specific treatment strategy in guidelines has not been established. For PHPT, modern surgical management has transitioned from the traditional bilateral neck exploration to minimally invasive parathyroidectomy. This surgical approach allows for smaller incisions, lower morbidity, but less exposure of the thyroid glands, which leads to concerns about missing coexistent thyroid pathology. As for NMTC, total thyroidectomy or lobectomy with necessary cervical lymph nodes dissection is consensus according to the American Thyroid Association (ATA) guideline. Based on above, minimally invasive parathyroidectomy for PHPT with selective total thyroidectomy or lobectomy for thyroid nodules seems to be the main way currently.

Properly surgical approach depends on accurate preoperative imaging, several imaging procedures have been described for the preoperative localization of parathyroid tumors in the present era of minimally invasive parathyroidectomy. Among these methods, 99Tcm-sestamibi is usually recommended as the first choice [19], while ultrasound seems just as a supplement without enough attention. Reviewing previous studies listed in Table 3, it has barely mentioned the role of ultrasound before operation; however, as an inexpensive and noninvasive technique, ultrasound acts as the perfect diagnostic tool to detect concomitant thyroid and parathyroid nodules. For the patients ready for the operation of PHPT, as ultrasound screening was routinely performed, thyroid nodules are not easy to missed diagnosis [11]. Here comes another question: If the patient is admitted for NMTC for the first time as the patients in our study, what we could do to avoid missing the parathyroid lesion as much as possible?

In most previous reports like Lehwald et al., PHPT was usually diagnosed before the identification of the thyroid carcinoma that was usually diagnosed in pathology specimen as an incidental finding after the surgery [2]; however, in our study, most of the cases were admitted by annual thyroid nodule examination, while the parathyroid lesion was not prompted until taking an ultrasound screening before the surgery. In this current study, 6 of 7 patients were discovered of suspected parathyroid lesion as described in the ultrasound reports, of which 5 patients did not perform serum PTH test before ultrasound. The following high level of serum PTH basically certified our suspicion before the operation. Among the patients, only 1 of them had the main complaint of bone pain, and her serum PTH level was in normal during two tests before surgery. One interesting case is one of the patients was not prompted parathyroid lesion in the ultrasound results; but this patient was asymptomatic hyperparathyroidism and there was no evidence supporting abnormal serum PTH level before ultrasound. By summarizing the clinical data of this female patient and comparing intraoperative findings and ultrasound reports, we found the lesion in the same position was misdiagnosed as PTC without the reminder of high level of PTH (Tables 1 and 3). Furthermore, Nam et al., who had analyzed 7 parathyroid cancers and 32 parathyroid adenomas, noted that the significant ultrasound features of parathyroid carcinoma includes: large size, heterogeneous echotexture, irregular shape, non-circumscribed margin, intra-nodular calcifications, and local invasion [20]. All of the imaging features of parathyroid carcinomas are similar to those of PTCs’. Although accurate diagnosis was not given, we succeeded to find out the malignant lesion at least. We thought more accurate diagnosis would have arrived if the PTH level was in unusual level before the ultrasound exam.

Conclusion

In conclusion, our study illustrates the need for clinical awareness of concomitant hyperparathyroidism and non-medullary thyroid cancer and is substantiated with published case reviews. The coexistence of PHPT and NMTC is rare but it does happen. This study, together with other findings, concluded that there is some relationship during the concurrence procedure of PHPT and PTC; moreover, comprehensive preoperative ultrasound of both thyroid and parathyroid glands is necessary for patients with PHPT. To date, there is still no specific guidelines for the management of patients with synchronous PHPT and PTC, so the treatment that which one of the two is dominant to deal with is still controversial; early detection maybe can do something to promote the process of the management coming to a consensus.

Different from previous opinions that considering 99Tcm-sestamibi as the first choice, we think that ultrasound seems a more efficient and necessary option for preoperative localization, for it can simultaneously screen the thyroid and parathyroid lesion. If combined with biochemical tests, the rate of missing diagnosis or misdiagnosis will be sharply reduced. All of these will help to contribute for a precise surgery.

Notes

Acknowledgements

Not applicable.

Funding

This work was funded by National Natural Science Foundation of China (No.81671700, No.81701706), Natural Science Foundation of Shanghai (No.16ZR1426000), Shanghai key discipline of medical imaging (No.2017ZZ02005). These four parties have provided funding financial support for this research.

Availability of data and materials

The dataset used and analysed during the current study are available from the corresponding author on reasonable request.

Authors’ contributions

JS was a major contributor in writing the manuscript and QW reviewed. The ultrasonography was provided by YW. All authors have read and approved the final manuscript.

Ethics approval and consent to participate

The study was approved by Ethics Committee of Shanghai Sixth People’s Hospital. All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional research committee and the declaration of Helsinki. Formal consent is not required for this type of study.

Consent for publication

Written informed consent was obtained from patients for publication of this article and accompanying images. A copy of the written consent is available for review by Editor-in Chief of this journal.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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© The Author(s). 2019

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Authors and Affiliations

  1. 1.Department of Ultrasound in MedicineShanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai Institute of Ultrasound in MedicineShanghaiChina

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