An Evaluation of Color Duplex Scanning in the Primary Diagnosis and Management of Carotid Body Tumors M.J. Worsey, MB, BS, FRCS, A.L. Laborde, MD, T. Bower, MD, E. Miller, RVT, T.F. Kresowik, MD, W.J. Sharp, MD, J.D. Corson, MB, ChB, FRCS, FACS, Iowa City, Iowa
Carotid body tumors present a diagnostic challenge. Despite technologic diagnostic advances, misdiagnosis resulting in blind biopsy or exploration through a limited incision still occur. Color duplex scanning has recently been used to evaluate carotid body tumors in our institution. A characteristic feature of these tumors found with this modality is wide splaying of the carotid bifurcation by a hypervascuiar mass. Color duplex scanning is the noninvasive modality of choice for the primary diagnosis of carotid body tumors. Additionally, it may be of use in screening for familial carotid body tumors and sequential follow-up of nonoperatively managed tumors. (Ann Vasc Surg 1992;6:90-94). KEY WORDS:
Carotid body tumor; tumor; carotid artery; color duplex scanning.
The carotid body is located on the posteromedial aspect of the carotid bifurcation in the adventitia of the arterial wall. A paraganglioma of the carotid body progressively distorts the anatomy of the bifurcation and may eventually encase the carotid vessels and the adjacent cranial nerves. Carotid body tumors are highly vascular tumors with a blood supply derived primarily from the vasa vasorum of the carotid bifurcation and external carotid artery. Conventional management is surgical excision as these neoplasms generally enlarge to involve adjacent structures, have a variable rate of malignant change with metastases predominantly to the local lymph nodes [1,2]. However, concurrent disease,
especially in those of advanced age may encourage a nonoperative approach. Carotid body tumors have a classical arteriographic appearance and the surgical anatomy and blood supply can be clearly defined [3,4]. Hence it is recommended that clinically suspicious lesions be studied by arteriography, prior to a surgical procedure. Additionally the option of preoperative embolization is available for large tumors [5]. Five carotid body tumors were studied in four patients. An Acuson 128 color duplex scanner* with a 5MHz linear transducer was used to obtain longitudinal and transverse images. The characteristic diagnostic features of carotid body tumors on color duplex scanning will be discussed.
From the Department of Surgery, the Universio' of Iowa Hospitals and Clinics, Iowa City, Iowa. Presented at the 16th Annual Meeting of the Peripheral Vascular Surgery Society, June 2, 1991, Boston. Massachusetts. Reprint requests: M.J. Worsey, MD, Department of Surgery, Scaife Hall, University of Pittsburgh, Pittsburgh, Pennsylvania 15261.
CASE REPORTS Patient No. 1
A 45-year-old white man gave a two year history of a mass in the left neck, just below the angle of the jaw. *Acuson, Mountain View, California. 90
VOLUME6 No 1 - 1992
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Fig. 1. Transverse color duplex scan of carotid body tumor (CBT), widely separated internal (ICA) and external (ECA) carotid arteries and internal jugular vein (IJV).
Physical examination revealed the presence of a left-sided pulsatile mass+ 2 cm in diameter which was laterally but not vertically mobile. A color duplex scan showed a highly vascular mass splaying the carotid bifurcation (Fig. 1). The contralateral carotid system showed no abnormality. Transfemoral arch arteriography was highly suggestive of a carotid body tumor which derived its blood supply from the external carotid artery (Fig. 2). The tumor was excised with a segment of the external carotid and the internal carotid artery was preserved. Histology confirmed the preoperative diagnosis of a paraganglioma showing classical nests of epitheloid cells with granular eosinophilic cytoplasm separated by a vascularized connective tissue. Follow-up has been without clinical or color duplex evidence of recurrence at six months.
Patient No. 2 A 79-year-old white woman with controlled hypertension and stable angina presented with a one year history of a stable left neck mass. Physical examination was suspicious of a carotid body tumor and a computed tomographic (CT) scan with contrast was also consistent with this diagnosis (Fig. 3). Color duplex scan showed a vascular mass splaying the bifurcation. The dimensions of 3 cm x 2.5 cm x 2.5 cm correlated well with those estimated on CT. In view of her advanced age and coronary artery disease the patient declined surgery. Serial color duplex
Fig. 2. Subtraction arteriogram of left carotid body tumor (T) showing posteriorly displaced internal carotid (ic), external carotid (ec) and common carotid
(cc).
92
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Patient No. 4
A 27-year-old white woman presented to the ear, nose, and throat service with a several year history of a left-sided neck swelling which had enlarged over the preceding two months. She also complained of mild dysphagia. Physical examination revealed a firm 3 c m x 3 cm mass in the region of the carotid bifurcation which was slightly tender with transmitted pulsation. Preliminary diagnosis was of an enlarged lymph node and a fine needle aspiration was performed, taking two aspirates without incident. Cytology suggested a carotid body paraganglioma and subsequent carotid arteriography was also highly suggestive of this diagnosis. A vascular consult was obtained and a color duplex scan showed a 3 x 3 x 2 cm mass at the carotid bifurcation which splayed the internal and external carotid arteries. The classical tumor pattern as earlier described in both transverse and longitudinal sections was also seen (Fig. 5), The patient is awaiting tumor excision,
DISCUSSION
Fig. 3. Computed tomographic scan with contrast of left sided carotid body tumor (CBT).
scanning over a 30 month period has shown no increase in size.
Patient No. 3 A 35-year-old white man with a history of adrenal pheochromocytoma excision at nine years presented for screening as he had had a brother with bilateral carotid body tumors recently excised. Examination of his neck revealed asymptomatic bilateral masses at the level of both carotid bifurcations. He underwent arteriography which suggested bilateral carotid body tumors, the right being the larger and compressing the carotid vessels. Color duplex scanning showed the characteristic hypervascular carotid tumor pattern bilaterally with displacement and separation of the internal and external carotid arteries. Surgical excision of the right tumor necessitated removal of a segment of the internal carotid artery due to its close adherence to the tumor, and reconstruction of this vessel with a saphenous vein graft. This graft unfortunately occluded three days postoperatively and the patient suffered a right hemispheric cerebrovascular accident. The contralateral tumor was therefore treated with a course of radiotherapy and the patient was followed with interval color duplex scans. At three years the tumor remains stable and the color duplex scan suggests tumor encasement of the internal carotid artery and also tumor vessels arising from the internal carotid artery (Fig. 4).
Arteriography is regarded as the definitive test for the diagnosis and evaluation of carotid body tumors. Previous reports advocate it as an essential preoperative investigation [3,4]. The tumor has a classical arteriographic appearance and information is gained not only regarding its blood supply and extent, but also concurrent atheromatous disease of the cerebrovascular circulation. Most series report that the tumor blood supply is fairly constant, being from the external carotid artery and carotid bifurcation especially in small tumors, but contributions can also arise from the internal carotid, vertebral arteries and the thyrocervical trunk [6]. Arteriography has a recognized morbidity and is obviously not warranted as a first diagnostic step for all suspicious masses in this region. A variety of modalities have been used to study carotid body tumors as an aid to diagnosis as well as for sequential follow-up in cases where a conservative nonoperative approach is utilized. Computed tomographic scanning with contrast and rapid sequencing may be suggestive of a carotid body tumor though it may not differentiate these from carotid aneurysms at the bifurcation [7]. B-mode ultrasonography alone has been used in some institutions for screening of suspicious neck masses or sequential follow up of nonoperated carotid body tumors [8]. However, B-mode ultrasound does not define the vascularity of the tumor. The addition use of color flow imaging may increase sensitivity by detecting the vascularity of these tumors; however, this is dependent on the frequency of the transducer and standardized adjustment [9,10]. Magnetic resonance imaging (MRI) may also prove helpful. Both coronal and transverse images are available and the extent of the tumor is well seen. As yet MRI
VOt.UME 6 N o 1 - 1992
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Fig. 4. Color duplex scan of carotid body tumor (CBT) three years postirradiation showing encasement of internal carotid artery (ICA) and a probable tumor branch arising from this vessel (arrow).
remains under investigation with limited reported experience of its use [ 11]. Needle biopsy or surgical exploration of a mass at the carotid bifurcation is obviously dangerous and to be discouraged without appropriate work-up [12]. The role of fine-needle aspiration biopsy of such neck masses is controversial even if a carotid body tumor is suspected. A cytological diagnosis can usually be made but authorities debate the frequency and severity of subsequent morbidity. There are reports, however, of stroke and subsequent death following this procedure [13]. Color duplex scanning is a recent advance in diagnostic ultrasound. Steinke and associates were the first to suggest its use in the diagnosis of carotid body tumors and stressed its importance in the diagnosis of small tumors [14]. We have found that carotid body tumors have a characteristic duplex appearance using this modality. The typical scan shows a normal common carotid artery with the vascular tumor splaying the carotid bifurcation. This is especially well appreciated on a transverse
scan. The hypervascularity of the tumor is seen as irregular color signals between the abnormally widely separated internal and external carotid arteries. Additional information regarding concurrent carotid atheroma and compression or encasement by tumor can be obtained. Also the dimensions of the tumor can be accurately measured in three planes. The most important factor in making the diagnosis of a carotid body tumor is a high index of suspicion. These lesions initially present to a variety of services and are infrequently seen by most physicians due to their relative rarity [I5]. Color duplex scanning is an ideal modality for initial evaluation of such carotid bifurcation masses or screening of their relatives if a carotid body tumor is found. Sequential follow up of nonoperated or irradiated tumors is also easily performed. It is noninvasive, relatively inexpensive and avoids contrast or radiation exposure. Color duplex scanning plays a useful role in the initial diagnosis, assessment and sequential fol-
94
E V A L U A T I O N OF COLOR DUPLEX S C A N N I N G
ANNALS OF VASCULARS~RGER¥
Fig. 5. Transverse scan of carotid body tumor (CBT) showing hypervascularity and widely splayed carotid vessels.
6. CHAMBERS RG, MAHONEY WD, Carotid body tumors, Am J Surg 1968:II6:548-554. 7. SHUGAR MA. MAFEE MF. Diagnosis of carotid body tumors by dynamic computerized tomography. Head Neck Sur~,, 1982:4:518-52 I. 8. GOODING GA. Gray scale ultrasound detection of carotid body tumors. Radiology 1979:132:409-410, 9. TIHANSKY DP, PORTER PS, Pulsed Doppler-ultrasonic diagnosis of carotid body tumor. N Y St J Med 1989;580-582, 10, GRITZMAN N, HEROLD C, HALLER J, et al. Duplex sonography of tumors of the carotid body. Cardiovasc lntervent Radiol 1987;10:280-284. I I. OLSEN WL, DILLON WP, KELLY WM, et al. MR imaging of paragangliomas. Am J Radiol 1987;148:201. 12. CHUNG WB. The carotid body tumor. Can J Surg 1979;22: 319-322. 13. ENGZELL U, FRANZEN S, ZAJICEK J. Cytologic findings in t3 cases of carotid body tumors. Acta Cytologica 1971 :•5:25-30. 14. STEINKE W, HENNERICI M, AULICH A. Doppler color flow imaging of carotid body tumors. Stroke 1989;20:15741577. 15. BROWSE NL. Carotid body tumors. BMJ t982; 284:1507-1508.
low-up of carotid body tumors. This diagnostic modality may obviate the need for arteriography except in those cases where preoperative embolization is contemplated.
REFERENCES 1. MEYER FB, SUNDT TM, PEARSON BW. Carotid body tumors: a subject review and suggested surgical approach. J Neurosurg 1986;64:377-385. 2. MARTIN CE, ROSENFELD L. MC SWAIN B. Carotid body tumors. A 16 year follow up of seven malignant cases. South Med J 1973;66:1236-1243. 3. KRUPSKI WC, EFFERNEY DJ, EHRENFELD WK. et al. Cervical chemodectoma. Am J Surg 1982;144:215-220. 4. ROSEN IB, PALMER JA, GOLDBERG M, el al. Vascular problems associated with carotid body tumors. Am J Surg 1981 ;142:459-463. 5. SMITH RF, SHETTY PC, REDDY DJ. Surgical treatment of carotid paragangliomas presenting unusual technical difficulties. J Vasc Surg 1988;7:631-637.
•"
i
I
Carotid body tumors present a diagnostic challenge. Despite technologic diagnostic advances, misdiagnosis resulting in blind biopsy or exploration through a limited incision still occur. Color duplex scanning has recently been used to evaluate carotid body tumors in our institution. A characteristic feature of these tumors found with this modality is wide splaying of the carotid bifurcation by a hypervascuiar mass. Color duplex scanning is the noninvasive modality of choice for the primary diagnosis of carotid body tumors. Additionally, it may be of use in screening for familial carotid body tumors and sequential follow-up of nonoperatively managed tumors. (Ann Vasc Surg 1992;6:90-94). KEY WORDS:
Carotid body tumor; tumor; carotid artery; color duplex scanning.
The carotid body is located on the posteromedial aspect of the carotid bifurcation in the adventitia of the arterial wall. A paraganglioma of the carotid body progressively distorts the anatomy of the bifurcation and may eventually encase the carotid vessels and the adjacent cranial nerves. Carotid body tumors are highly vascular tumors with a blood supply derived primarily from the vasa vasorum of the carotid bifurcation and external carotid artery. Conventional management is surgical excision as these neoplasms generally enlarge to involve adjacent structures, have a variable rate of malignant change with metastases predominantly to the local lymph nodes [1,2]. However, concurrent disease,
especially in those of advanced age may encourage a nonoperative approach. Carotid body tumors have a classical arteriographic appearance and the surgical anatomy and blood supply can be clearly defined [3,4]. Hence it is recommended that clinically suspicious lesions be studied by arteriography, prior to a surgical procedure. Additionally the option of preoperative embolization is available for large tumors [5]. Five carotid body tumors were studied in four patients. An Acuson 128 color duplex scanner* with a 5MHz linear transducer was used to obtain longitudinal and transverse images. The characteristic diagnostic features of carotid body tumors on color duplex scanning will be discussed.
From the Department of Surgery, the Universio' of Iowa Hospitals and Clinics, Iowa City, Iowa. Presented at the 16th Annual Meeting of the Peripheral Vascular Surgery Society, June 2, 1991, Boston. Massachusetts. Reprint requests: M.J. Worsey, MD, Department of Surgery, Scaife Hall, University of Pittsburgh, Pittsburgh, Pennsylvania 15261.
CASE REPORTS Patient No. 1
A 45-year-old white man gave a two year history of a mass in the left neck, just below the angle of the jaw. *Acuson, Mountain View, California. 90
VOLUME6 No 1 - 1992
E V A L U A T I O N OF COLOR D U P L E X S C A N N I N G
91
Fig. 1. Transverse color duplex scan of carotid body tumor (CBT), widely separated internal (ICA) and external (ECA) carotid arteries and internal jugular vein (IJV).
Physical examination revealed the presence of a left-sided pulsatile mass+ 2 cm in diameter which was laterally but not vertically mobile. A color duplex scan showed a highly vascular mass splaying the carotid bifurcation (Fig. 1). The contralateral carotid system showed no abnormality. Transfemoral arch arteriography was highly suggestive of a carotid body tumor which derived its blood supply from the external carotid artery (Fig. 2). The tumor was excised with a segment of the external carotid and the internal carotid artery was preserved. Histology confirmed the preoperative diagnosis of a paraganglioma showing classical nests of epitheloid cells with granular eosinophilic cytoplasm separated by a vascularized connective tissue. Follow-up has been without clinical or color duplex evidence of recurrence at six months.
Patient No. 2 A 79-year-old white woman with controlled hypertension and stable angina presented with a one year history of a stable left neck mass. Physical examination was suspicious of a carotid body tumor and a computed tomographic (CT) scan with contrast was also consistent with this diagnosis (Fig. 3). Color duplex scan showed a vascular mass splaying the bifurcation. The dimensions of 3 cm x 2.5 cm x 2.5 cm correlated well with those estimated on CT. In view of her advanced age and coronary artery disease the patient declined surgery. Serial color duplex
Fig. 2. Subtraction arteriogram of left carotid body tumor (T) showing posteriorly displaced internal carotid (ic), external carotid (ec) and common carotid
(cc).
92
E V A L U A T I O N OF COLOR DUPLEX S C A N N I N G
ANNALS OF VASCULAR SURGERY
Patient No. 4
A 27-year-old white woman presented to the ear, nose, and throat service with a several year history of a left-sided neck swelling which had enlarged over the preceding two months. She also complained of mild dysphagia. Physical examination revealed a firm 3 c m x 3 cm mass in the region of the carotid bifurcation which was slightly tender with transmitted pulsation. Preliminary diagnosis was of an enlarged lymph node and a fine needle aspiration was performed, taking two aspirates without incident. Cytology suggested a carotid body paraganglioma and subsequent carotid arteriography was also highly suggestive of this diagnosis. A vascular consult was obtained and a color duplex scan showed a 3 x 3 x 2 cm mass at the carotid bifurcation which splayed the internal and external carotid arteries. The classical tumor pattern as earlier described in both transverse and longitudinal sections was also seen (Fig. 5), The patient is awaiting tumor excision,
DISCUSSION
Fig. 3. Computed tomographic scan with contrast of left sided carotid body tumor (CBT).
scanning over a 30 month period has shown no increase in size.
Patient No. 3 A 35-year-old white man with a history of adrenal pheochromocytoma excision at nine years presented for screening as he had had a brother with bilateral carotid body tumors recently excised. Examination of his neck revealed asymptomatic bilateral masses at the level of both carotid bifurcations. He underwent arteriography which suggested bilateral carotid body tumors, the right being the larger and compressing the carotid vessels. Color duplex scanning showed the characteristic hypervascular carotid tumor pattern bilaterally with displacement and separation of the internal and external carotid arteries. Surgical excision of the right tumor necessitated removal of a segment of the internal carotid artery due to its close adherence to the tumor, and reconstruction of this vessel with a saphenous vein graft. This graft unfortunately occluded three days postoperatively and the patient suffered a right hemispheric cerebrovascular accident. The contralateral tumor was therefore treated with a course of radiotherapy and the patient was followed with interval color duplex scans. At three years the tumor remains stable and the color duplex scan suggests tumor encasement of the internal carotid artery and also tumor vessels arising from the internal carotid artery (Fig. 4).
Arteriography is regarded as the definitive test for the diagnosis and evaluation of carotid body tumors. Previous reports advocate it as an essential preoperative investigation [3,4]. The tumor has a classical arteriographic appearance and information is gained not only regarding its blood supply and extent, but also concurrent atheromatous disease of the cerebrovascular circulation. Most series report that the tumor blood supply is fairly constant, being from the external carotid artery and carotid bifurcation especially in small tumors, but contributions can also arise from the internal carotid, vertebral arteries and the thyrocervical trunk [6]. Arteriography has a recognized morbidity and is obviously not warranted as a first diagnostic step for all suspicious masses in this region. A variety of modalities have been used to study carotid body tumors as an aid to diagnosis as well as for sequential follow-up in cases where a conservative nonoperative approach is utilized. Computed tomographic scanning with contrast and rapid sequencing may be suggestive of a carotid body tumor though it may not differentiate these from carotid aneurysms at the bifurcation [7]. B-mode ultrasonography alone has been used in some institutions for screening of suspicious neck masses or sequential follow up of nonoperated carotid body tumors [8]. However, B-mode ultrasound does not define the vascularity of the tumor. The addition use of color flow imaging may increase sensitivity by detecting the vascularity of these tumors; however, this is dependent on the frequency of the transducer and standardized adjustment [9,10]. Magnetic resonance imaging (MRI) may also prove helpful. Both coronal and transverse images are available and the extent of the tumor is well seen. As yet MRI
VOt.UME 6 N o 1 - 1992
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93
Fig. 4. Color duplex scan of carotid body tumor (CBT) three years postirradiation showing encasement of internal carotid artery (ICA) and a probable tumor branch arising from this vessel (arrow).
remains under investigation with limited reported experience of its use [ 11]. Needle biopsy or surgical exploration of a mass at the carotid bifurcation is obviously dangerous and to be discouraged without appropriate work-up [12]. The role of fine-needle aspiration biopsy of such neck masses is controversial even if a carotid body tumor is suspected. A cytological diagnosis can usually be made but authorities debate the frequency and severity of subsequent morbidity. There are reports, however, of stroke and subsequent death following this procedure [13]. Color duplex scanning is a recent advance in diagnostic ultrasound. Steinke and associates were the first to suggest its use in the diagnosis of carotid body tumors and stressed its importance in the diagnosis of small tumors [14]. We have found that carotid body tumors have a characteristic duplex appearance using this modality. The typical scan shows a normal common carotid artery with the vascular tumor splaying the carotid bifurcation. This is especially well appreciated on a transverse
scan. The hypervascularity of the tumor is seen as irregular color signals between the abnormally widely separated internal and external carotid arteries. Additional information regarding concurrent carotid atheroma and compression or encasement by tumor can be obtained. Also the dimensions of the tumor can be accurately measured in three planes. The most important factor in making the diagnosis of a carotid body tumor is a high index of suspicion. These lesions initially present to a variety of services and are infrequently seen by most physicians due to their relative rarity [I5]. Color duplex scanning is an ideal modality for initial evaluation of such carotid bifurcation masses or screening of their relatives if a carotid body tumor is found. Sequential follow up of nonoperated or irradiated tumors is also easily performed. It is noninvasive, relatively inexpensive and avoids contrast or radiation exposure. Color duplex scanning plays a useful role in the initial diagnosis, assessment and sequential fol-
94
E V A L U A T I O N OF COLOR DUPLEX S C A N N I N G
ANNALS OF VASCULARS~RGER¥
Fig. 5. Transverse scan of carotid body tumor (CBT) showing hypervascularity and widely splayed carotid vessels.
6. CHAMBERS RG, MAHONEY WD, Carotid body tumors, Am J Surg 1968:II6:548-554. 7. SHUGAR MA. MAFEE MF. Diagnosis of carotid body tumors by dynamic computerized tomography. Head Neck Sur~,, 1982:4:518-52 I. 8. GOODING GA. Gray scale ultrasound detection of carotid body tumors. Radiology 1979:132:409-410, 9. TIHANSKY DP, PORTER PS, Pulsed Doppler-ultrasonic diagnosis of carotid body tumor. N Y St J Med 1989;580-582, 10, GRITZMAN N, HEROLD C, HALLER J, et al. Duplex sonography of tumors of the carotid body. Cardiovasc lntervent Radiol 1987;10:280-284. I I. OLSEN WL, DILLON WP, KELLY WM, et al. MR imaging of paragangliomas. Am J Radiol 1987;148:201. 12. CHUNG WB. The carotid body tumor. Can J Surg 1979;22: 319-322. 13. ENGZELL U, FRANZEN S, ZAJICEK J. Cytologic findings in t3 cases of carotid body tumors. Acta Cytologica 1971 :•5:25-30. 14. STEINKE W, HENNERICI M, AULICH A. Doppler color flow imaging of carotid body tumors. Stroke 1989;20:15741577. 15. BROWSE NL. Carotid body tumors. BMJ t982; 284:1507-1508.
low-up of carotid body tumors. This diagnostic modality may obviate the need for arteriography except in those cases where preoperative embolization is contemplated.
REFERENCES 1. MEYER FB, SUNDT TM, PEARSON BW. Carotid body tumors: a subject review and suggested surgical approach. J Neurosurg 1986;64:377-385. 2. MARTIN CE, ROSENFELD L. MC SWAIN B. Carotid body tumors. A 16 year follow up of seven malignant cases. South Med J 1973;66:1236-1243. 3. KRUPSKI WC, EFFERNEY DJ, EHRENFELD WK. et al. Cervical chemodectoma. Am J Surg 1982;144:215-220. 4. ROSEN IB, PALMER JA, GOLDBERG M, el al. Vascular problems associated with carotid body tumors. Am J Surg 1981 ;142:459-463. 5. SMITH RF, SHETTY PC, REDDY DJ. Surgical treatment of carotid paragangliomas presenting unusual technical difficulties. J Vasc Surg 1988;7:631-637.
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