Carotid
Body
Tumors
W. Frederiek McGuirt, MD, Lee A. Harker, MD
The anatomy, physiology, embryology, and pathology of the carotid body are reviewed, stressing the capability of the normal and neoplastic structure to produce pressor amines. Nine new cases of carotid body tumors are reported including a patient with a malignant tumor with a facial nerve paralysis and regional node metastases. The clinical presentation and management emphasize the preoperative catecholamine determinations and angiographic studies.
Most
active head and neck
sur¬
geons eventually encounter a patient with a carotid body tumor. If the correct diagnosis is not made pre¬
operatively, extraordinary judgment, knowledge, and skill may be required to avoid disastrous complications. This report discusses current knowl¬ edge of the structure and function of normal and neoplastic carotid body tissue, presents case summaries of nine patients with carotid body tu¬ mors encountered at the University of Iowa, and discusses current prin¬ ciples of evaluation and treatment of these lesions
Accepted for publication Aug 12, 1974. Read before the American Society for Head and Neck Surgery, Palm Beach, Fla, April 24, 1974. From the
Department of Otolaryngology and University of Iowa,
Maxillofacial Surgery, the
City. Reprint requests to the Department of Otolaryngology and Maxillofacial Surgery, University of Iowa, Iowa City, IA 52242 (Dr. McGuirt). Iowa
ANATOMY The carotid body is the largest of a group of homogeneous tissue masses called paraganglia that comprise the chemoreceptor system. It measures 5x3x2 mm and is located in the adventitia of the posterior medial sur¬ face of the common carotid artery, extending cephalically to the bifurca¬ tion. It has a fibrous capsule and is at¬ tached to the carotid bifurcation by the ligament of Mayer, through which it receives its blood supply and from which emanates a rich afferent nerve supply.1 Microscopically, nests of small uniform-sized epitheloid cells {Zellballen) are surrounded by a vascular stroma. Both argentaffin and chromaffin cells have been identified. PHYSIOLOGY
Modification of pulmonary ventila¬ tion is the primary function of the chemoreceptor system and the carotid body is the most important paraganglion, functionally. It responds primarily to hypoxia and reflexly causes an increased rate and depth of respiration and a slight increase in blood pressure and heart beat. To a lesser extent, increased blood levels of carbon dioxide and fixed acid cause similar effects.24 EMBRYOLOGY
The carotid body originates from mesoblastic and neural components. The neural components are derived from neural crest ectoderm as sympathogonia, which further differentiate
into sympathoblasts or chromaffinoblasts (Fig 1). In addition, sympa¬ thoblasts are forerunners of ganglion cell masses and the chromaffinoblasts are also seen in the adrenal me¬ dulla.' r' In the past all carotid body tumors were thought to be nonfunctional and were called nonchromaffin paragangliomas. It is now clear that this is not so. In both normal chemoreceptor tissue and carotid body tumors, neurosecretory granules have been identified by transmission electron microscopy'" and cytochemical tech¬ niques have definitely demonstrated epinephrine, norepinephrine, and ser¬ otonin.7 This should not be surpris¬ ing, since the adrenal medulla, with its similar neural ectodermal origin, normally elaborates these chemicals. Elevated urinary catecholamines have also been demonstrated in ca¬ "
rotid body tumors, and during surgi¬ cal excision and the immediate post¬ operative period, difficulties with blood pressure regulation and cardiac arrhythmias have been noted. Those functional tumors that secrete pressor substances and clinically re¬ semble pheochromocytomas are now classified as catechol secreting paragangliomas. The percentage of all ca¬ rotid body tumors that are clinically functional is not known, although it appears that all have the potential for
being
so.
PATHOLOGY
Neoplasia is the only pathologic
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affecting the carotid body, and resulting tumors are pinkish-gray brown, globular, homogeneous,
state
the or
firm masses of tissue that have welldefined capsules. They exhibit a strik¬ ing tendency to reproduce the normal architecture of the organ, and there is a minimum of cellular atypism or mytotic activity. Reticulum stains help accentuate the appearance of the Zellballen (Fig 2). REPORT OF CASES Case l.-In 1938, a 62-year-old white had an asymptomatic mass on the right side of the neck of one year's dura¬ tion. Under local anesthesia, the lesion was removed from the area of the angle of the mandible. Postoperatively, the patient de¬ veloped arrhythmias and died of ventricu¬ lar failure on the second postoperative day. woman
Comment.—Intra- and postopera¬ tive blood pressure abberations and cardiac arrhythmias occur commonly when large amounts of catecholamines are liberated into the blood stream during removal of pheochromocytomas or functional chemoreceptor tumors. This may have been related to this patient's death, though of course, it is impossible to prove, as the proper biochemical determinations were
not
Neural Crest Cells
\
-Sympathogonia Chromaffinoblasts
Sympathoblasts;
Ganglion Organ's
Cell Masses of Zuckerkandle
Carotid
Carotid
Nonchromaffin
Body
Tumors
Paragangliomas
—
Fig 1.—Flow body tissue.
chart
Adrenal Medulla
Body
·
showing neural
crest derivatives and their
Pheochromocytoma Catechol Secreting Paragangliomas relationship
to carotid
Fig 2.—Carotid body tumor metastatic to lymph node (case 8). Malignant tumor histo¬ logically very similar to normal carotid body structure. Nests of small, uniform-sized epitheloid cells accentuated by retlculin fibers. Minimal atypism and mitoses (reticulin, orig¬ inal magnification x430).
performed preoperatively at
that time.
Case 2.—A 58-year-old white man had a 15-year history of a lump in the right side
of the neck with marked increase in size of the mass over the past year. At operation, a carotid body tumor was adherent to the carotid bifurcation and the internal, exter¬ nal, and common carotid arteries were all ligated during removal. The patient had an immediate postoperative cardiac arrest, but was resuscitated and had no further
complications.
Comment.—Ligation of the common
internal carotid artery without grafting or shunting carries a high mortality and morbidity,810 especially when this is done during head and neck tumor surgery as opposed to li¬ gation for control of intracranial an¬ eurysms. Today, this patient would have had reestablishment of his carotid arterial system with grafting. As in case 1, the possibility that cardiac ar¬ rest was due to arrhythmia related to catecholamine release at the time of surgical removal must be considered. or
Case 3.—A 68-year-old white, mentally retarded man was found to have an asymptomatic 7x8 cm mass on the right side of the neck that caused displacement of the right tonsil. The mass was firm and had transmitted carotid pulsations. An open biopsy was carried out and 450 ml of blood were lost. The patient was treated with 1,800 rads of 250 kv irradiation. He was last seen two years later with no change in tumor size. Comment.—This case, also treated some years ago, points out the dis¬ advantage of open biopsy as a means
of establishing the diagnosis, namely blood loss. Today, angiography is the preferred method. If radiation ther¬ apy is elected as a treatment modal¬ ity at our hospital now, 5,000 rads of
cobalt 60 is delivered, with the expec¬ tation that temporary or permanent cessation of tumor growth will be the optimum result. Marked regression of size has not been seen in benign tu¬ mors.1" Case 4.—A 38-year-old white man had an eight- to ten-year history of an asympto¬ matic swelling of the left side of his neck. A 2%-inch poorly demarcated, pulsatile, nonflxed mass was present just below the angle of the mandible. Under hypothermie anesthesia, a carotid body tumor was re¬ moved by subadventitial dissection with a 2,500 ml blood loss. Postoperatively there
left 12th nerve paralysis. Case 5.—A 73-year-old white woman had an 18-year history of an asymptomatic, slowly enlarging mass on the right side of
was a
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3.—Carotid
Fig
body
tumor metastatic to
lymph
node
(case 8).
Left, Well-encapsulated lymph node containing nests of epitheloid cells (hematoxylin-eosin, original magnification the neck. On examination it was 10 x 10 cm and pulsatile. A bruit and 12th nerve pa¬ ralysis were present. The mass could be re¬ duced by compression, but reformed rap¬ idly on release of the compression. The patient had a contralateral glomus jugu¬ lare tumor irradiated 17 years earlier with¬ out change in size. No treatment was insti¬ tuted to the carotid body tumor that did not increase further in size over the next five years.
illustrates the these le¬ long asymptomatic sions can exhibit.11 Also noteworthy is the concomitant second chemodecto¬ ma and its lack of marked radiosensitivity. Simultaneous chem¬ odectomas occur frequently as do medullary carcinomas of the thyroid, making a search for a second primary lesion imperative in all these pa¬ tients.1213
Comment.-This
case
course
Case 5.—A 53-year-old white woman was found to have a "wormy" 4x5 cm redu¬ cible mass in the area of the carotid bulb on the left with displacement of the lateral oropharyngeal wall nearly to the midline. The patient is being followed without treatment and has had no sequellae after two years. Case 6.—A 77-year-old white woman had a 6x3 cm hard, mass on the left side of the neck that had been present for many years, but which had increased in size over the past year. No bruit was noted. Biopsy results reported a carotid body tumor and no further treatment was given. There has
been
no
years.
change in size of the mass for four
Case 7.-A
53-year-old white woman had
40). Right,
Higher power showing nature of epitheloid cells to be chem¬ oreceptor tissue (hematoxylin-eosin, original magnification X100).
15-year history of a mass on the left side of the neck and a recent mass on the right side, both asymptomatic. Physical exami¬ nation revealed the masses to be nonten¬ der but pulsatile. Urinary catecholamines were slightly increased at 98 mg with a normal vanillymandelic acid value. She had a diminished ventilating response to a
breathing hypoxic
gases.
Angiogram
re¬
revealed bilateral carotid body tumors. Under hypothermie, hypotensive anesthesia, both tumors were excised subadventitially at the same sitting with preservation of the normal carotid sys¬ tems. She had paralysis of the left vocal cord and supine hypertension postopera¬ sults
tively.
Comment.—Patients with one ca¬ rotid body tumor have a 3% to 4% chance of having a contralateral ca¬ rotid body tumor if the family history is negative for this lesion. If it is posi¬ tive, the chances of bilaterality are increased eightfold." The patient's postoperative supine hypertension is interesting. This is thought to be due to a lack of chemo- and baroreceptor influences postoperatively; when the patient stands and develops postural hypotension, renin is produced, which increases her blood pressure when she lies down. It would seem prudent to stage removal of bilateral tumors in order to attempt to avoid this unusual
complication.
Case 8.—A 42-year-old white man had a 12-year history of a lump in the neck be¬
neath the lobule of the ear. This remained asymptomatic and changed little for ten
was biopsied at a local hos¬ pital and found to be a carotid body tumor. Surgical removal was advised but the pa¬ tient deferred seeking further care until two years later, when after rapid increase in tumor size, the facial musculature on the right side became paralyzed and the pa¬ tient came for treatment. The patient's sister was known to have a carotid body tumor. On examination, the facial nerve was stimulatable at 1.33 ma but Bell phe¬ nomenon, and drooping of the corner of the mouth on the involved side, were pres¬ ent. Posterior cervical adenopathy, distinct from the tumor mass, was present. Angi¬ ography results revealed a large carotid body tumor. A lymph node biopsy was per¬
years, when it
formed and the results showed metastatic chemodectoma (Fig 3). The patient was treated with 5,000 rads of cobalt 60 with an approximate 50% reduction in the size of the primary tumor and improvement in fa¬ cial nerve function (Fig 4).
Comment.—This case accentuates the importance of a family history in patients with masses on the upper part of the neck.141" This case is most noteworthy because of the histologi¬ cally verified metastasis. This occurs in only 5% of these lesions.17 Histolog¬ ically, a malignant carotid body tu¬ mor cannot be reliably differentiated from a benign one at the primary site, and it is only the presence of mé¬ tastases that verify malignancy.'"·"' Because of the multicentric nature of paraganglionic foci, and the concomi¬ tant appearance of multiple lesions in areas of known chemoreceptor tissue,
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this criterion is often difficult to case 8, the intranodal pat¬ tern is, without question, a result of metastasis and not of a second focus of chemoreceptor tissue. The involve¬ ment of the facial nerve is extremely uncommon. Finally, this case also demonstrates limited radiosensitivity of a malignant chemodectoma. even
prove.2" In
COMMENT
The mor
diagnosis of a carotid body tu¬ suspected when a pa-
must be
tient has a slowly enlarging lateral neck mass that has no vertical mobil¬ ity, is firm and sometimes compres¬ sible, may be pulsatile or accom¬ panied by a bruit, and may feel warmer than the surrounding skin. Larger lesions displace the lateral pharyngeal wall and tonsillar fossa medially. The masses are usually asymptomatic but symptoms may re¬ sult from paralysis of the tenth or 12th nerve, or compression of the up¬ per air or food passages.21 Local pain
referred pain to the ear is some¬ times seen. To establish the diagnosis, open biopsy has been replaced by angiog¬ raphy unless rapid growth, bone de¬ struction, local invasion, or suspected metastasis suggests malignancy.22 Biopsy should never be attenipted or
transorally.2:' Arteriography results usually
dem¬
onstrate a circumscribed vascular blush at the carotid bifurcation with
displacement and separation of the
internal and external carotid arteries (Fig 5). The anatomic extension, feeding vessels, and degree of vascularity can be determined and all of these can aid in planning therapy. The vast majority of tumors are fed by the external carotid system, but larger lesions may receive contribu¬ tions from the thyrocervical trunk.
Generally, malignant tumors appear more vascular angiographically than benign ones. During arteriography it is also important to assess the status of the opposite carotid system and the intracerebral circulation if excision is
contemplated.21
If surgery or open biopsy is con¬ sidered, preoperative catecholamine
Fig 4.—Nerve paralysis on the right side of the face from malignant carotid body tumor (case 8). Left, Before treatment. Right, Eight months postirradiation—return of nasolabial crease and elevation of right corner of mouth with regression of tumor size.
Fig 5.—Angiograms (case 8). Left, Circumscribed tumor blush at carotid bifurcation. Right, Subtraction technique showing carotid displacement by a tumor fed by the exter¬ nal carotid system.
determinations are imperative as are repeated blood pressure measure¬ ments. Blood sugar should also be measured since patients with func¬ tioning tumors show an inhibition of peripheral uptake of glucose and inhi¬ bition of insulin production by pan¬ creatic /5-cells.2' If a functioning tu¬ mor is detected preoperatively, the patient should be treated as though he had a pheochromocytoma; propranolol hydrochloride preopera¬ tively, and phenoxybenzamine hydro¬ chloride intraoperatively." Management options include obser¬ vation without treatment, surgical excision, and radiation therapy. For a number of years, complete re¬ moval was considered imperative, in part because of an early report sug¬ gesting that 50% of these tumors
histologically
were
malignant.2"
Later, because of high operative
mor¬
sion.9
sum¬
tality and morbidity, and because clinically the tumors rarely metasta¬ sized, others advised against exci¬ mary
-''
In Shamblin's1" recent
an
operative mortality
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of 7%
and a morbidity of 22% (hemiplegia) occurred in the cases undergoing sur¬ gery. Present opinion lies between these "all or nothing" approaches. Conley22 considers surgical resection when carotid body tumors: (1) are his¬ tologically malignant but resectable; (2) manifest an aggressive growth pattern; (3) are small or medium sized when in a person under age 50 years;
(4) interfere with speaking, swallow¬ ing, or breathing or cause severe
EF, Weinberg T: Carotid body tumors. Surgery 27:437-448, 1950. 2. Hewitt RL, et al: Chemodectomas. Surgery 71:275-282, 1972.
10. Shamblin WR, et al: Carotid body tumor. Am J Surg 122:732-739, 1971. 11. Keen WW, Funk J: Tumors of the carotid gland. JAMA 47:469-479, 566-570, 1906. 12. Cragg RW: Concurrent tumors of the left carotid body and Zuckerkandle bodies. Arch Pathol 18:635-645, 1934. 13. Albores-Saavedra J, Duran ME: Association of thyroid cancer and chemodectomas. Am J Surg 116:887-890, 1968. 14. Rush BF Jr: Familial bilateral carotid body tumors. Ann Surg 157:633-635, 1963. 15. Katz AD: Carotid body tumors in a large family group. Am J Surg 108:570-573, 1964. 16. Chase WH: Familial and bilateral tumors of the carotid body. J Pathol Bact 36:1-12,1933. 17. Javid H, et al: Surgical management of carotid body tumor. Arch Surg 95:771-779, 1967. 18. Rabbon AS, Elliott JL: Carotid body tumors with regional lymph node involvement. Surgery 42:381-385, 1957. 19. Turnbull FM, Jr: Malignancy in carotid body tumor with presentation of a proven case of metastasis to the lung. West J Surg Obstet Gynecol 62:382-390, 1954.
pain.
If surgery is chosen, hypothermie hypotensive anesthesia is preferred with close cardiopulmonary monitor¬
ing.
Subadventitial dissection with pres¬ ervation of the entire carotid system is preferred. This is based on Boyd's28
embryological demonstration that the carotid body lies in the carotid adventitia unrelated to the media. If pres¬ ervation is impossible, arterial graft¬ ing should be employed. If surgery is not deemed advisable, radiation ther¬ apy can provide useful palliation to patients who are symptomatic or have
rapidly growing
tumors.10
References 1. Lewison
3. Nelson WR: Carotid
51:326-335, 1962.
body
tumors.
Surgery
4. The carotid body in oxygen regulation, editorial. Lancet 1:79-80, 1972. 5. Pryse-Davies J, et al: Some morphological, histochemical and chemical observations on chemodectomas and normal carotid bodies. Cancer 17:185-202, 1964. 6. Grimsley PM, Glenner GG: Histology and ultrastructure of carotid body paragangliomas. Cancer 20:1473-1488, 1967. 7. Levit SA, et al: Catechol secreting paraganglioma of the glomus jugulare region resembling pheochromocytoma. N Engl J Med 281:805\x=req-\ 811, 1969. 8. Hamberger CA, et al: Malignant catecholamine producing tumor of the carotid body. Acta Pathol Microbiol Scand 69:489-492, 1967. 9. Monro RS: The natural history of carotid body tumors and their diagnosis and treatment. Br J Surg 37:445-453, 1950.
Kipkie GF: Simultaneous chromaffin tuof the carotid body and glomus jugulare. Arch Pathol 44:113-118, 1947. 21. Wilson H: Carotid body tumors. Surgery 59:483-493, 1966. 22. Wetzel N: Carotid angiography in the diagnosis and treatment of tumors of the head and neck. Arch Surg 74:954-958, 1957. 23. Conley JJ: The carotid body tumors. Arch Otolaryngol 81:187-193, 1965. 24. Bennett H: The value of angiography in the management of tumors of the head and neck. Radiology 84:1052-1058, 1965. 25. Brantigan CO, Katase RY: Clinical and pathological features of paragangliomas of the organ of Zuckerkandle. Surgery 65:989-905,1969. 26. Harrington SW, et al: Tumors of the carotid body. Ann Surg 114:820, 1941. 27. Reid MR: Adenomata of the carotid gland. Bull Hopkins Hosp 31:177-184, 1920. 28. Boyd JH: The development of the human carotid body, in Contributions in Embryology. Washington, DC, Carnegie Institute of Washington, W1 CO 778R, 1937, chapt 26. 20.
mors
Downloaded From: http://archotol.jamanetwork.com/ by a University of Arizona Health Sciences Library User on 06/06/2015
Body
Tumors
W. Frederiek McGuirt, MD, Lee A. Harker, MD
The anatomy, physiology, embryology, and pathology of the carotid body are reviewed, stressing the capability of the normal and neoplastic structure to produce pressor amines. Nine new cases of carotid body tumors are reported including a patient with a malignant tumor with a facial nerve paralysis and regional node metastases. The clinical presentation and management emphasize the preoperative catecholamine determinations and angiographic studies.
Most
active head and neck
sur¬
geons eventually encounter a patient with a carotid body tumor. If the correct diagnosis is not made pre¬
operatively, extraordinary judgment, knowledge, and skill may be required to avoid disastrous complications. This report discusses current knowl¬ edge of the structure and function of normal and neoplastic carotid body tissue, presents case summaries of nine patients with carotid body tu¬ mors encountered at the University of Iowa, and discusses current prin¬ ciples of evaluation and treatment of these lesions
Accepted for publication Aug 12, 1974. Read before the American Society for Head and Neck Surgery, Palm Beach, Fla, April 24, 1974. From the
Department of Otolaryngology and University of Iowa,
Maxillofacial Surgery, the
City. Reprint requests to the Department of Otolaryngology and Maxillofacial Surgery, University of Iowa, Iowa City, IA 52242 (Dr. McGuirt). Iowa
ANATOMY The carotid body is the largest of a group of homogeneous tissue masses called paraganglia that comprise the chemoreceptor system. It measures 5x3x2 mm and is located in the adventitia of the posterior medial sur¬ face of the common carotid artery, extending cephalically to the bifurca¬ tion. It has a fibrous capsule and is at¬ tached to the carotid bifurcation by the ligament of Mayer, through which it receives its blood supply and from which emanates a rich afferent nerve supply.1 Microscopically, nests of small uniform-sized epitheloid cells {Zellballen) are surrounded by a vascular stroma. Both argentaffin and chromaffin cells have been identified. PHYSIOLOGY
Modification of pulmonary ventila¬ tion is the primary function of the chemoreceptor system and the carotid body is the most important paraganglion, functionally. It responds primarily to hypoxia and reflexly causes an increased rate and depth of respiration and a slight increase in blood pressure and heart beat. To a lesser extent, increased blood levels of carbon dioxide and fixed acid cause similar effects.24 EMBRYOLOGY
The carotid body originates from mesoblastic and neural components. The neural components are derived from neural crest ectoderm as sympathogonia, which further differentiate
into sympathoblasts or chromaffinoblasts (Fig 1). In addition, sympa¬ thoblasts are forerunners of ganglion cell masses and the chromaffinoblasts are also seen in the adrenal me¬ dulla.' r' In the past all carotid body tumors were thought to be nonfunctional and were called nonchromaffin paragangliomas. It is now clear that this is not so. In both normal chemoreceptor tissue and carotid body tumors, neurosecretory granules have been identified by transmission electron microscopy'" and cytochemical tech¬ niques have definitely demonstrated epinephrine, norepinephrine, and ser¬ otonin.7 This should not be surpris¬ ing, since the adrenal medulla, with its similar neural ectodermal origin, normally elaborates these chemicals. Elevated urinary catecholamines have also been demonstrated in ca¬ "
rotid body tumors, and during surgi¬ cal excision and the immediate post¬ operative period, difficulties with blood pressure regulation and cardiac arrhythmias have been noted. Those functional tumors that secrete pressor substances and clinically re¬ semble pheochromocytomas are now classified as catechol secreting paragangliomas. The percentage of all ca¬ rotid body tumors that are clinically functional is not known, although it appears that all have the potential for
being
so.
PATHOLOGY
Neoplasia is the only pathologic
Downloaded From: http://archotol.jamanetwork.com/ by a University of Arizona Health Sciences Library User on 06/06/2015
affecting the carotid body, and resulting tumors are pinkish-gray brown, globular, homogeneous,
state
the or
firm masses of tissue that have welldefined capsules. They exhibit a strik¬ ing tendency to reproduce the normal architecture of the organ, and there is a minimum of cellular atypism or mytotic activity. Reticulum stains help accentuate the appearance of the Zellballen (Fig 2). REPORT OF CASES Case l.-In 1938, a 62-year-old white had an asymptomatic mass on the right side of the neck of one year's dura¬ tion. Under local anesthesia, the lesion was removed from the area of the angle of the mandible. Postoperatively, the patient de¬ veloped arrhythmias and died of ventricu¬ lar failure on the second postoperative day. woman
Comment.—Intra- and postopera¬ tive blood pressure abberations and cardiac arrhythmias occur commonly when large amounts of catecholamines are liberated into the blood stream during removal of pheochromocytomas or functional chemoreceptor tumors. This may have been related to this patient's death, though of course, it is impossible to prove, as the proper biochemical determinations were
not
Neural Crest Cells
\
-Sympathogonia Chromaffinoblasts
Sympathoblasts;
Ganglion Organ's
Cell Masses of Zuckerkandle
Carotid
Carotid
Nonchromaffin
Body
Tumors
Paragangliomas
—
Fig 1.—Flow body tissue.
chart
Adrenal Medulla
Body
·
showing neural
crest derivatives and their
Pheochromocytoma Catechol Secreting Paragangliomas relationship
to carotid
Fig 2.—Carotid body tumor metastatic to lymph node (case 8). Malignant tumor histo¬ logically very similar to normal carotid body structure. Nests of small, uniform-sized epitheloid cells accentuated by retlculin fibers. Minimal atypism and mitoses (reticulin, orig¬ inal magnification x430).
performed preoperatively at
that time.
Case 2.—A 58-year-old white man had a 15-year history of a lump in the right side
of the neck with marked increase in size of the mass over the past year. At operation, a carotid body tumor was adherent to the carotid bifurcation and the internal, exter¬ nal, and common carotid arteries were all ligated during removal. The patient had an immediate postoperative cardiac arrest, but was resuscitated and had no further
complications.
Comment.—Ligation of the common
internal carotid artery without grafting or shunting carries a high mortality and morbidity,810 especially when this is done during head and neck tumor surgery as opposed to li¬ gation for control of intracranial an¬ eurysms. Today, this patient would have had reestablishment of his carotid arterial system with grafting. As in case 1, the possibility that cardiac ar¬ rest was due to arrhythmia related to catecholamine release at the time of surgical removal must be considered. or
Case 3.—A 68-year-old white, mentally retarded man was found to have an asymptomatic 7x8 cm mass on the right side of the neck that caused displacement of the right tonsil. The mass was firm and had transmitted carotid pulsations. An open biopsy was carried out and 450 ml of blood were lost. The patient was treated with 1,800 rads of 250 kv irradiation. He was last seen two years later with no change in tumor size. Comment.—This case, also treated some years ago, points out the dis¬ advantage of open biopsy as a means
of establishing the diagnosis, namely blood loss. Today, angiography is the preferred method. If radiation ther¬ apy is elected as a treatment modal¬ ity at our hospital now, 5,000 rads of
cobalt 60 is delivered, with the expec¬ tation that temporary or permanent cessation of tumor growth will be the optimum result. Marked regression of size has not been seen in benign tu¬ mors.1" Case 4.—A 38-year-old white man had an eight- to ten-year history of an asympto¬ matic swelling of the left side of his neck. A 2%-inch poorly demarcated, pulsatile, nonflxed mass was present just below the angle of the mandible. Under hypothermie anesthesia, a carotid body tumor was re¬ moved by subadventitial dissection with a 2,500 ml blood loss. Postoperatively there
left 12th nerve paralysis. Case 5.—A 73-year-old white woman had an 18-year history of an asymptomatic, slowly enlarging mass on the right side of
was a
Downloaded From: http://archotol.jamanetwork.com/ by a University of Arizona Health Sciences Library User on 06/06/2015
3.—Carotid
Fig
body
tumor metastatic to
lymph
node
(case 8).
Left, Well-encapsulated lymph node containing nests of epitheloid cells (hematoxylin-eosin, original magnification the neck. On examination it was 10 x 10 cm and pulsatile. A bruit and 12th nerve pa¬ ralysis were present. The mass could be re¬ duced by compression, but reformed rap¬ idly on release of the compression. The patient had a contralateral glomus jugu¬ lare tumor irradiated 17 years earlier with¬ out change in size. No treatment was insti¬ tuted to the carotid body tumor that did not increase further in size over the next five years.
illustrates the these le¬ long asymptomatic sions can exhibit.11 Also noteworthy is the concomitant second chemodecto¬ ma and its lack of marked radiosensitivity. Simultaneous chem¬ odectomas occur frequently as do medullary carcinomas of the thyroid, making a search for a second primary lesion imperative in all these pa¬ tients.1213
Comment.-This
case
course
Case 5.—A 53-year-old white woman was found to have a "wormy" 4x5 cm redu¬ cible mass in the area of the carotid bulb on the left with displacement of the lateral oropharyngeal wall nearly to the midline. The patient is being followed without treatment and has had no sequellae after two years. Case 6.—A 77-year-old white woman had a 6x3 cm hard, mass on the left side of the neck that had been present for many years, but which had increased in size over the past year. No bruit was noted. Biopsy results reported a carotid body tumor and no further treatment was given. There has
been
no
years.
change in size of the mass for four
Case 7.-A
53-year-old white woman had
40). Right,
Higher power showing nature of epitheloid cells to be chem¬ oreceptor tissue (hematoxylin-eosin, original magnification X100).
15-year history of a mass on the left side of the neck and a recent mass on the right side, both asymptomatic. Physical exami¬ nation revealed the masses to be nonten¬ der but pulsatile. Urinary catecholamines were slightly increased at 98 mg with a normal vanillymandelic acid value. She had a diminished ventilating response to a
breathing hypoxic
gases.
Angiogram
re¬
revealed bilateral carotid body tumors. Under hypothermie, hypotensive anesthesia, both tumors were excised subadventitially at the same sitting with preservation of the normal carotid sys¬ tems. She had paralysis of the left vocal cord and supine hypertension postopera¬ sults
tively.
Comment.—Patients with one ca¬ rotid body tumor have a 3% to 4% chance of having a contralateral ca¬ rotid body tumor if the family history is negative for this lesion. If it is posi¬ tive, the chances of bilaterality are increased eightfold." The patient's postoperative supine hypertension is interesting. This is thought to be due to a lack of chemo- and baroreceptor influences postoperatively; when the patient stands and develops postural hypotension, renin is produced, which increases her blood pressure when she lies down. It would seem prudent to stage removal of bilateral tumors in order to attempt to avoid this unusual
complication.
Case 8.—A 42-year-old white man had a 12-year history of a lump in the neck be¬
neath the lobule of the ear. This remained asymptomatic and changed little for ten
was biopsied at a local hos¬ pital and found to be a carotid body tumor. Surgical removal was advised but the pa¬ tient deferred seeking further care until two years later, when after rapid increase in tumor size, the facial musculature on the right side became paralyzed and the pa¬ tient came for treatment. The patient's sister was known to have a carotid body tumor. On examination, the facial nerve was stimulatable at 1.33 ma but Bell phe¬ nomenon, and drooping of the corner of the mouth on the involved side, were pres¬ ent. Posterior cervical adenopathy, distinct from the tumor mass, was present. Angi¬ ography results revealed a large carotid body tumor. A lymph node biopsy was per¬
years, when it
formed and the results showed metastatic chemodectoma (Fig 3). The patient was treated with 5,000 rads of cobalt 60 with an approximate 50% reduction in the size of the primary tumor and improvement in fa¬ cial nerve function (Fig 4).
Comment.—This case accentuates the importance of a family history in patients with masses on the upper part of the neck.141" This case is most noteworthy because of the histologi¬ cally verified metastasis. This occurs in only 5% of these lesions.17 Histolog¬ ically, a malignant carotid body tu¬ mor cannot be reliably differentiated from a benign one at the primary site, and it is only the presence of mé¬ tastases that verify malignancy.'"·"' Because of the multicentric nature of paraganglionic foci, and the concomi¬ tant appearance of multiple lesions in areas of known chemoreceptor tissue,
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this criterion is often difficult to case 8, the intranodal pat¬ tern is, without question, a result of metastasis and not of a second focus of chemoreceptor tissue. The involve¬ ment of the facial nerve is extremely uncommon. Finally, this case also demonstrates limited radiosensitivity of a malignant chemodectoma. even
prove.2" In
COMMENT
The mor
diagnosis of a carotid body tu¬ suspected when a pa-
must be
tient has a slowly enlarging lateral neck mass that has no vertical mobil¬ ity, is firm and sometimes compres¬ sible, may be pulsatile or accom¬ panied by a bruit, and may feel warmer than the surrounding skin. Larger lesions displace the lateral pharyngeal wall and tonsillar fossa medially. The masses are usually asymptomatic but symptoms may re¬ sult from paralysis of the tenth or 12th nerve, or compression of the up¬ per air or food passages.21 Local pain
referred pain to the ear is some¬ times seen. To establish the diagnosis, open biopsy has been replaced by angiog¬ raphy unless rapid growth, bone de¬ struction, local invasion, or suspected metastasis suggests malignancy.22 Biopsy should never be attenipted or
transorally.2:' Arteriography results usually
dem¬
onstrate a circumscribed vascular blush at the carotid bifurcation with
displacement and separation of the
internal and external carotid arteries (Fig 5). The anatomic extension, feeding vessels, and degree of vascularity can be determined and all of these can aid in planning therapy. The vast majority of tumors are fed by the external carotid system, but larger lesions may receive contribu¬ tions from the thyrocervical trunk.
Generally, malignant tumors appear more vascular angiographically than benign ones. During arteriography it is also important to assess the status of the opposite carotid system and the intracerebral circulation if excision is
contemplated.21
If surgery or open biopsy is con¬ sidered, preoperative catecholamine
Fig 4.—Nerve paralysis on the right side of the face from malignant carotid body tumor (case 8). Left, Before treatment. Right, Eight months postirradiation—return of nasolabial crease and elevation of right corner of mouth with regression of tumor size.
Fig 5.—Angiograms (case 8). Left, Circumscribed tumor blush at carotid bifurcation. Right, Subtraction technique showing carotid displacement by a tumor fed by the exter¬ nal carotid system.
determinations are imperative as are repeated blood pressure measure¬ ments. Blood sugar should also be measured since patients with func¬ tioning tumors show an inhibition of peripheral uptake of glucose and inhi¬ bition of insulin production by pan¬ creatic /5-cells.2' If a functioning tu¬ mor is detected preoperatively, the patient should be treated as though he had a pheochromocytoma; propranolol hydrochloride preopera¬ tively, and phenoxybenzamine hydro¬ chloride intraoperatively." Management options include obser¬ vation without treatment, surgical excision, and radiation therapy. For a number of years, complete re¬ moval was considered imperative, in part because of an early report sug¬ gesting that 50% of these tumors
histologically
were
malignant.2"
Later, because of high operative
mor¬
sion.9
sum¬
tality and morbidity, and because clinically the tumors rarely metasta¬ sized, others advised against exci¬ mary
-''
In Shamblin's1" recent
an
operative mortality
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of 7%
and a morbidity of 22% (hemiplegia) occurred in the cases undergoing sur¬ gery. Present opinion lies between these "all or nothing" approaches. Conley22 considers surgical resection when carotid body tumors: (1) are his¬ tologically malignant but resectable; (2) manifest an aggressive growth pattern; (3) are small or medium sized when in a person under age 50 years;
(4) interfere with speaking, swallow¬ ing, or breathing or cause severe
EF, Weinberg T: Carotid body tumors. Surgery 27:437-448, 1950. 2. Hewitt RL, et al: Chemodectomas. Surgery 71:275-282, 1972.
10. Shamblin WR, et al: Carotid body tumor. Am J Surg 122:732-739, 1971. 11. Keen WW, Funk J: Tumors of the carotid gland. JAMA 47:469-479, 566-570, 1906. 12. Cragg RW: Concurrent tumors of the left carotid body and Zuckerkandle bodies. Arch Pathol 18:635-645, 1934. 13. Albores-Saavedra J, Duran ME: Association of thyroid cancer and chemodectomas. Am J Surg 116:887-890, 1968. 14. Rush BF Jr: Familial bilateral carotid body tumors. Ann Surg 157:633-635, 1963. 15. Katz AD: Carotid body tumors in a large family group. Am J Surg 108:570-573, 1964. 16. Chase WH: Familial and bilateral tumors of the carotid body. J Pathol Bact 36:1-12,1933. 17. Javid H, et al: Surgical management of carotid body tumor. Arch Surg 95:771-779, 1967. 18. Rabbon AS, Elliott JL: Carotid body tumors with regional lymph node involvement. Surgery 42:381-385, 1957. 19. Turnbull FM, Jr: Malignancy in carotid body tumor with presentation of a proven case of metastasis to the lung. West J Surg Obstet Gynecol 62:382-390, 1954.
pain.
If surgery is chosen, hypothermie hypotensive anesthesia is preferred with close cardiopulmonary monitor¬
ing.
Subadventitial dissection with pres¬ ervation of the entire carotid system is preferred. This is based on Boyd's28
embryological demonstration that the carotid body lies in the carotid adventitia unrelated to the media. If pres¬ ervation is impossible, arterial graft¬ ing should be employed. If surgery is not deemed advisable, radiation ther¬ apy can provide useful palliation to patients who are symptomatic or have
rapidly growing
tumors.10
References 1. Lewison
3. Nelson WR: Carotid
51:326-335, 1962.
body
tumors.
Surgery
4. The carotid body in oxygen regulation, editorial. Lancet 1:79-80, 1972. 5. Pryse-Davies J, et al: Some morphological, histochemical and chemical observations on chemodectomas and normal carotid bodies. Cancer 17:185-202, 1964. 6. Grimsley PM, Glenner GG: Histology and ultrastructure of carotid body paragangliomas. Cancer 20:1473-1488, 1967. 7. Levit SA, et al: Catechol secreting paraganglioma of the glomus jugulare region resembling pheochromocytoma. N Engl J Med 281:805\x=req-\ 811, 1969. 8. Hamberger CA, et al: Malignant catecholamine producing tumor of the carotid body. Acta Pathol Microbiol Scand 69:489-492, 1967. 9. Monro RS: The natural history of carotid body tumors and their diagnosis and treatment. Br J Surg 37:445-453, 1950.
Kipkie GF: Simultaneous chromaffin tuof the carotid body and glomus jugulare. Arch Pathol 44:113-118, 1947. 21. Wilson H: Carotid body tumors. Surgery 59:483-493, 1966. 22. Wetzel N: Carotid angiography in the diagnosis and treatment of tumors of the head and neck. Arch Surg 74:954-958, 1957. 23. Conley JJ: The carotid body tumors. Arch Otolaryngol 81:187-193, 1965. 24. Bennett H: The value of angiography in the management of tumors of the head and neck. Radiology 84:1052-1058, 1965. 25. Brantigan CO, Katase RY: Clinical and pathological features of paragangliomas of the organ of Zuckerkandle. Surgery 65:989-905,1969. 26. Harrington SW, et al: Tumors of the carotid body. Ann Surg 114:820, 1941. 27. Reid MR: Adenomata of the carotid gland. Bull Hopkins Hosp 31:177-184, 1920. 28. Boyd JH: The development of the human carotid body, in Contributions in Embryology. Washington, DC, Carnegie Institute of Washington, W1 CO 778R, 1937, chapt 26. 20.
mors
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