Abdominal ultrasound in the detection of an incidental paraganglioma

Hsiao-Ting Chen; Yung-Yin Cheng; Teng-Fu Tsao; Cheng-Ming Peng; Jeng-Dong Hsu; Yeu-Sheng Tyan

doi:10.4103/JMU.JMU_25_20

CASE REPORT

Year : 2021 | Volume : 29 | Issue : 2 | Page : 119-122

Abdominal ultrasound in the detection of an incidental paraganglioma

Hsiao-Ting Chen¹, Yung-Yin Cheng¹, Teng-Fu Tsao², Cheng-Ming Peng³, Jeng-Dong Hsu⁴, Yeu-Sheng Tyan²
¹ Department of Medical Imaging, Chung Shan Medical University Hospital; Department of Medical Imaging and Radiological Sciences, Chung Shan Medical University, Taichung, Taiwan
² Department of Medical Imaging, Chung Shan Medical University Hospital; Department of Medical Imaging and Radiological Sciences; School of Medicine, Chung Shan Medical University, Taichung, Taiwan
³ School of Medicine, Chung Shan Medical University; Division of General Surgery, Department of Surgery, Chung Shan Medical University Hospital, Taichung, Taiwan
⁴ School of Medicine, Chung Shan Medical University; Department of Pathology, Chung Shan Medical University Hospital, Taichung, Taiwan

Date of Submission	14-Feb-2020
Date of Decision	29-Apr-2020
Date of Acceptance	15-May-2020
Date of Web Publication	14-Jul-2020

Correspondence Address:
Dr. Yung-Yin Cheng
Department of Medical Imaging, Chung Shan Medical University Hospital, No. 110, Sec. 1, Chien-Kuo N. Rd., Taichung 402
Taiwan

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/JMU.JMU_25_20

Abstract

Paraganglioma is a tumor that originates from neuroendocrine cells of the sympathetic or parasympathetic systems. Patients may suffer from headaches, palpitations, diaphoresis, and hypertension due to catecholamine excess or symptoms from the mass effect of the tumor. In the absence of typical symptoms of catecholamine excess, the diagnosis of a nonfunctional paraganglioma is often delayed. Herein, we report a case of a 63-year-old female patient with a nonfunctional paraganglioma which is an accidental finding during investigation of a fever. Abdominal ultrasonography incidentally detected this lesion as a complex, solid, cystic mass in the left suprarenal retroperitoneum.

Keywords: Paraganglioma, retroperitoneum, ultrasound

How to cite this article:
Chen HT, Cheng YY, Tsao TF, Peng CM, Hsu JD, Tyan YS. Abdominal ultrasound in the detection of an incidental paraganglioma. J Med Ultrasound 2021;29:119-22

How to cite this URL:
Chen HT, Cheng YY, Tsao TF, Peng CM, Hsu JD, Tyan YS. Abdominal ultrasound in the detection of an incidental paraganglioma. J Med Ultrasound [serial online] 2021 [cited 2023 Mar 26];29:119-22. Available from: http://www.jmuonline.org/text.asp?2021/29/2/119/299218

Introduction

Incidentaloma is a mass lesion that is discovered incidentally during a radiologic examination. Because of the widespread use of abdominal ultrasonography (US), computed tomography (CT), and magnetic resonance imaging (MRI), such imaging findings have been increasingly frequent.^[1],[2],[3] “Incidentaloma” is used to describe a wide and heterogeneous spectrum of pathologies, including benign or malignant tumors, hormonally active or inactive lesions, metastases, infections, granulomas, infiltrations, cysts and pseudocysts, and hemorrhages.^[1] We present the case of nonfunctional retroperitoneal paraganglioma discovered during investigation of a fever.

Case Report

A 63-year-old female with a history of hypertension under medication control for 3 years went to the emergency department of our hospital because of fever and chills for 2 days. She went to the emergency department of our hospital because of fever and chills for two days. Physical examination disclosed a soft abdomen without flank knocking pain. Blood examination showed elevated C-reactive protein (14.8 mg/dL; normal < 0.7 mg/dL). Urinalysis was positive for leukocyte esterase and bacteria. The remaining systemic inquiry was unremarkable. There was no leukocytosis at presentation.

Abdominal US was performed to evaluate the urinary system and showed a mass lesion with cystic contents in the left upper retroperitoneum behind the pancreas and just lateral to the abdominal aorta [Figure 1]. Bilateral kidneys showed no hydronephrosis. The patient underwent abdominal CT that confirmed a mass lesion in the left retroperitoneal location that was very close to the left adrenal gland [Figure 2]. An incidentaloma was considered.

Figure 1: A retroperitoneal incidentaloma in a 63-year-old female patient with a urinary tract infection. (a) Transverse sonogram of the upper abdomen shows a mass lesion (arrows) with central cystic change in the left upper retroperitoneum, behind the pancreas (p). (b) Color Doppler (left panel, velocity setting of 53 cm) and corresponding gray-scale (right panel) transverse sonograms at the level of the celiac artery (CA) show the mass (m) in the left lateral to the abdominal aorta (AA). The mass lesion is thought to be in the left adrenal fossa. No detectable Doppler flow signal within the lesion. (c) Color Doppler (left panel) and corresponding gray-scale (right panel) longitudinal sonograms reveal that the mass (marked by + cursors) is posterior to the splenic vein (SV) and caudal (distal) to the splenic artery (SA) and between the liver (l), spleen (s), and left kidney (LK). HA, hepatic artery; IVC, inferior vena cava; PV, portal vein; VB, vertebral body

Click here to view

Figure 2: The transverse views of nonenhanced (a) and contrast-enhanced (b) computed tomography scan confirm the location of the mass (arrowheads) behind the pancreas (p) and left lateral to the abdominal aorta (AA). The mass is composed of an enhancing solid part peripherally and a nonenhancing cystic part centrally (open star). The mass is very close to the left adrenal gland (arrow) and the fat plane between them is not clearly visible. Note that some areas with poor contrast enhancement in the left renal parenchyma (stars) are consistent with acute pyelonephritis, which is not obvious on the sonogram. L, liver; LK, left kidney

Click here to view

Antibiotic treatment was prescribed for the urinary tract infection, fever, and chills subsided. One month later, the patient underwent laparoscopic surgery, and the retroperitoneal incidentaloma about 6.4 cm Ö 5.5 cm was excised totally. Neither ascites nor retroperitoneal lymph node was noted. The left adrenal gland was free of the tumor. The pathology showed a paraganglioma [Figure 3]. The postoperative course was uneventful. There was no tumor recurrence at the 2-year follow-up on CT.

Figure 3: Histopathology of the paraganglioma. (a) Gross view of the specimen shows a yellowish to brownish elastic and encapsulated mass. (b and c) Histopathological views show the paraganglioma composed of sheet, zellballen growth of epithelioid, polygonal, tumor cells with amphophilic, finely granular, cytoplasm, and centralized nuclei with conspicuous nucleoli (b: [H and E, ×40] and c: [H and E, ×100]). The immunostains (images not shown) show synaptophysin (+), chromogranin (+), and Melan A (-) in tumor cells. The S100 highlights sustentacular cells. The PHH3 shows a mitotic rate <1 mitosis/10 HPF in tumor cells

Click here to view

Discussion

Paraganglioma is a tumor that originates from the neuroendocrine cells of the sympathetic or parasympathetic systems.^[4],[5],[6] These tumors can occur at the skull base, neck, chest, and abdomen.^[7] When the lesion occurs in the abdomen, the most common site is the adrenal gland, and it is then specifically called a “pheochromocytoma.” The term, “paraganglioma,” refers to a tumor that is outside the adrenal gland.^[8]

The classical presentation of a paraganglioma is excess catecholamine production.^[6],[9],[10] Paragangliomas produce, store, synthesize, and metabolize catecholamines.^[11] A value three times the upper range of normal is a positive result.^[6] However, because of fluctuating release of catecholamines, a false negative may occur in the presence of low catecholamine level.^[11] Urine and plasma metanephrines, which are the metabolites of catecholamines, last more consistent in the body, so measurement of these metabolites in plasma is now considered the more accurate test.^[12],[13] There is another biochemical marker called chromogranin A (CgA) that is used in patients with paraganglioma. CgA is a polypeptide commonly secreted by chromaffin cells, typically with catecholamines.^[14] In the absence of typical symptoms of catecholamine excess, diagnosis of a nonfunctional paraganglioma is often delayed.^[15],[16]

Diagnostic imaging plays a critical role in paragangliomas [Table 1]. On US imaging, paragangliomas in the neck usually appear as hypoechoic, well-defined, inhomogeneous, hypervascular masses in the area of the carotid bifurcation, which separates the internal and external carotid arteries.^[17],[18] However, there are few reports of US imaging of abdominal paragangliomas. Hashimoto et al. revealed eight abdominal paragangliomas (size range: 2.3–11.9 cm; median: 6.5 cm) and showed that six of eight were in contact with the inferior vena cava or pancreas.^[19] They found that all eight lesions had distinct boundaries with near-spherical (six of eight), polygonal (one of eight), or irregular (one of eight) shapes. Half of the lesions (four of eight) had predominantly cystic components, and seven of eight showed blood flow signals. In our case, the tumor was close to the pancreas and exhibited a well-defined margin and cystic change. We did not detect Doppler flow signals within the lesion, which may have been because of the high-velocity scan setting (53 cm) for which a high-flow vessel, such as the abdominal aorta [Figure 1]b, is not contaminated with aliasing artifacts, but the sensitivity to low blood flow within a tumor declines.

Table 1: Imaging characteristics of paragangliomas

Click here to view

On contrast-enhanced CT, these tumors appear as paraaortic soft-tissue masses with either homogeneous contrast enhancement or central areas of low attenuation, as in our case.^[20] Compared with larger tumors, smaller ones are more likely to be homogeneous in attenuation and sharply marginated. Punctate calcification or focal areas of high attenuation caused by acute hemorrhage are seen in some tumors.^[20] On MRI, these tumors are usually hypointense or isointense compared with the liver parenchyma on T1-weighted images and are markedly hyperintense on T2-weighted images.^{[21],[22],[23]} Either CT or MRI images may exhibit similar appearances between functioning and nonfunctioning paragangliomas.^[21]

The diagnosis of malignant paraganglioma has stringent criteria according to the World Health Organization (WHO) classification in 2004 and requires evidence of metastases at nonchromaffin sites distant from the primary tumor, such as lymph nodes, bones, liver, and lung.^[24] However, the WHO classification changed in 2017. Currently, the term metastatic paraganglioma has replaced malignant paraganglioma.^[25],[26] Previous reports have shown that the malignant rate of paragangliomas range from 7% to 50%^{[27],[28],[29]} and tumor malignancy can be diagnosis at the first presentation or during follow-up. In addition, Hamidi et al. reported that approximately 21% of malignant paragangliomas are nonfunctional tumors.^[30] The clinical, biochemical, and radiological features alone are inadequate to predict malignancy.^[10] Some biochemical data are thought to be a factor to predict malignancy, but they remain controversial.^{[31],[32],[33]}

Concerning treatments for paraganglioma, patients with biochemically active paraganglioma should immediately be placed on antihypertensive medications to control symptoms and reduce the risk of hypertensive crises. After antihypertensive medications, treatment options are surgical resection, radiofrequency ablation, radiotherapy, chemotherapy, and molecular-targeted therapies; however, surgical resection remains the only curative treatment for patients with paraganglioma.^{[11],[29],[34]} A previous report described apparently benign disease that returned with metastases ≤15 years after resection,^[27] so life-long follow-up of patients with resected paragangliomas is imperative.^[29]

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given her consent for her images and other clinical information to be reported in the journal. The patient understands that her name and initials will not be published and due efforts will be made to conceal identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1.	Mirilas P, Skandalakis JE. Benign anatomical mistakes: Incidentaloma. Am Surg 2002;68:1026-8.
2.	Chojniak R. Incidentalomas: Managing risks. Radiol Bras 2015;48:9-10.
3.	Young WF Jr. Clinical practice. The incidentally discovered adrenal mass. N Engl J Med 2007;356:601-10.
4.	Asa SL, Ezzat S, Mete O. The diagnosis and clinical significance of paragangliomas in unusual locations. J Clin Med 2018;7:280.
5.	Lack EE. Atlas of tumor pathology. In: Tumors of the Adrenal Gland and Extraadrenal Paraganglia. Armed Forces Institute of Pathology. Vol. 8. Washington, DC, USA: American Registry of Pathology Press; 2007.
6.	Alrezk R, Suarez A, Tena I, Pacak K. Update of Pheochromocytoma Syndromes: Genetics, Biochemical Evaluation, and Imaging. Front Endocrinol (Lausanne) 2018;9:515.
7.	Rha SE, Byun JY, Jung SE, Chun HJ, Lee HG, Lee JM. Neurogenic tumors in the abdomen: Tumor types and imaging characteristics. Radiographics 2003;23:29-43.
8.	Rindi G, Klimstra DS, Abedi-Ardekani B, Asa SL, Bosman FT, Brambilla E, et al. A common classification framework for neuroendocrine neoplasms: An International Agency for Research on Cancer (IARC) and World Health Organization (WHO) expert consensus proposal. Mod Pathol 2018;31:1770-86.
9.	Stein PP, Black HR. A simplified diagnostic approach to pheochromocytoma. A review of the literature and report of one institution's experience. Medicine (Baltimore) 1991;70:46-66.
10.	Bravo EL. Pheochromocytoma: New concepts and future trends. Kidney Int 1991;40:544-56.
11.	Martucci VL, Pacak K. Pheochromocytoma and paraganglioma: Diagnosis, genetics, management, and treatment. Curr Probl Cancer 2014;38:7-41.
12.	Lenders JW, Duh QY, Eisenhofer G, Gimenez-Roqueplo AP, Grebe SK, Murad MH, et al. Pheochromocytoma and paraganglioma: An endocrine society clinical practice guideline. J Clin Endocrinol Metab 2014;99:1915-42.
13.	Grossman A, Pacak K, Sawka A, Lenders JW, Harlander D, Peaston RT, et al. Biochemical diagnosis and localization of pheochromocytoma: Can we reach a consensus? Ann N Y Acad Sci 2006;1073:332-47.
14.	Eiden LE, Iacangelo A, Hsu CM, Hotchkiss AJ, Bader MF, Aunis D. Chromogranin A synthesis and secretion in chromaffin cells. J Neurochem 1987;49:65-74.
15.	Sclafani LM, Woodruff JM, Brennan MF. Extraadrenal retroperitoneal paragangliomas: Natural history and response to treatment. Surgery 1990;108:1124-9.
16.	Lack EE, Cubilla AL, Woodruff JM, Lieberman PH. Extra-adrenal paragangliomas of the retroperitoneum: A clinicopathologic study of 12 tumors. Am J Surg Pathol 1980;4:109-20.
17.	Demattè S, Di Sarra D, Schiavi F, Casadei A, Opocher G. Role of ultrasound and color Doppler imaging in the detection of carotid paragangliomas. J Ultrasound 2012;15:158-63.
18.	Tong Y. Role of duplex ultrasound in the diagnosis and assessment of carotid body tumour: A literature review. Intractable Rare Dis Res 2012;1:129-33.
19.	Hashimoto M, Miyakishi M, Nakatani T, Nakajima Y, Kobayashi S, Itou T, et al., Study of ultrasound images of paragangliomas. Jpn. J Med Ultrasound Technol 2017;42:24-35.
20.	Hayes WS, Davidson AJ, Grimley PM, Hartman DS. Extraadrenal retroperitoneal paraganglioma: Clinical, pathologic, and CT findings. AJR Am J Roentgenol 1990;155:1247-50.
21.	Lee KY, Oh YW, Noh HJ, Lee YJ, Yong HS, Kang EY, et al. Extraadrenal paragangliomas of the body: Imaging features. AJR Am J Roentgenol 2006;187:492-504.
22.	van Gils AP, Falke TH, van Erkel AR, Arndt JW, Sandler MP, van der Mey AG, et al. MR imaging and MIBG scintigraphy of pheochromocytomas and extraadrenal functioning paragangliomas. Radiographics 1991;11:37-57.
23.	Quint LE, Glazer GM, Francis IR, Shapiro B, Chenevert TL. Pheochromocytoma and paraganglioma: Comparison of MR imaging with CT and I-131 MIBG scintigraphy. Radiology 1987;165:89-93.
24.	DeLellis RA, Lloyd RV, Heitz PU, Eng C. WHO Classification of Tumours: Pathology and Genetics of Tumours of Endocrine Organs. 3^rd ed. Lyon, France: International Agency for Research on Cancer (IARC); 2004. p. 159-60.
25.	Lloyd RV, Osamura RY, Kloppel G, Rosai J. WHO Classification of Tumours: Pathology and Genetics of Tumours of Endocrine Organs. 4^th ed. Lyon, France: International Agency for Research on Cancer (IARC); 2017. p. 179-206.
26.	Lam AK. Update on adrenal tumours in 2017 World Health Organization (WHO) of Endocrine Tumours. Endocr Pathol 2017;28:213-27.
27.	Goldstein RE, O'Neill JA Jr, Holcomb GW 3^rd, Morgan WM 3^rd, Neblett WW 3^rd, Oates JA, et al. Clinical experience over 48 years with pheochromocytoma. Ann Surg 1999;229:755-64.
28.	Pommier RF, Vetto JT, Billingsly K, Woltering EA, Brennan MF. Comparison of adrenal and extraadrenal pheochromocytomas. Surgery 1993;114:1160-5.
29.	van Heerden JA, Roland CF, Carney JA, Sheps SG, Grant CS. Long-term evaluation following resection of apparently benign pheochromocytoma(s)/paraganglioma(s). World J Surg 1990;14:325-9.
30.	Hamidi O, Young WF Jr., Iñiguez-Ariza NM, Kittah NE, Gruber L, Bancos C, et al. Malignant pheochromocytoma and paraganglioma: 272 patients over 55 years. J Clin Endocrinol Metab 2017;102:3296-305.
31.	Eisenhofer G, Lenders JW, Siegert G, Bornstein SR, Friberg P, Milosevic D, et al. Plasma methoxytyramine: A novel biomarker of metastatic pheochromocytoma and paraganglioma in relation to established risk factors of tumour size, location and SDHB mutation status. Eur J Cancer 2012;48:1739-49.
32.	Eisenhofer G, Goldstein DS, Sullivan P, Csako G, Brouwers FM, Lai EW, et al. Biochemical and clinical manifestations of dopamine-producing paragangliomas: Utility of plasma methoxytyramine. J Clin Endocrinol Metab 2005;90:2068-75.
33.	Poirier É, Thauvette D, Hogue JC. Management of exclusively dopamine-secreting abdominal pheochromocytomas. J Am Coll Surg 2013;216:340-6.
34.	Andersen KF, Altaf R, Krarup-Hansen A, Kromann-Andersen B, Horn T, Christensen NJ, et al. Malignant pheochromocytomas and paragangliomas - the importance of a multidisciplinary approach. Cancer Treat Rev 2011;37:111-9.