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Carotid body tumors: Nonchromaffin paraganglioma of the cervical region
Carotid
Body Tumors:
Paraganglioma A Study of Fourteen
of the Cervical Patients Operated of the Tumor
JOHNM. HANFORD,M.D.,
From the Department of Surgery, Columbia Presbyterian Medical Center, New York, New York.
T
IS INTENDEDhere to emphasize certain factors of importance in the diagnosis and surgical treatment of carotid body tumors and especially the dangers associated with their excision. There is also an effort to evaluate the benefit of gradual rather than immediate complete carotid occlusion in those patients requiring carotid artery resection. Some years ago methods were devised for gradual occlusion of large arteries, notably of the common carotid artery, e.g., by Matas [I], Neff [Z], Halsted [3], and Kerr [a]. Both Halsted and Matas spent time and experiment with metallic materials for the occlusion of large arteries and for release if danger threatened. Neff [Z] and Kerr [4] appreciated the attempt at gradual or staged occlusion. More recently others have indicated the value of gradual occlusion as quoted here: “Where the patient is able to stand carotid compression for about ten minutes, ligation of the carotid can be carried out with a minimum of complications [51. ” “In those instances in which a carotid ligation is found desirable, it has been shown that if the carotid artery can be completely occluded for 5 or 10 minutes, the vessel can then be ligated, and in more than 90%, such ligation would be successful and without any untoward effects [6].” “It is now generally agreed that gradual ligation (sic) with a clamp such as the Crutchfield, Selverstone, or Poppen-Blalock clamp is safer than sudden
I
Nonchromaffin Region
upon for Removal
New York, New York
occlusion with a ligature [7].” “Part of the technic is gradual occlusion of the common carotid artery by the Selverstone clamp [8].” Indicative of its rarity, there were only fourteen patients who had removal of carotid body tumors at The Presbyterian Hospital, New York, between the years 1930 and 1964. The first postoperative patient with carotid body tumor seen by the author was a young woman presented at the New York Surgical Society some thirty years ago. She presented a complete unilateral hemiplegia. This serious postoperative complication is the key to operative removal of this tumor. The tumor often so entwines the bifurcation of the common carotid artery that complete removal of the tumor sometimes appears to be impossible without resection also of the bifurcation. (Fig. 1.) More significantly, the danger is interruption of the flow in the internal carotid artery which largely supplies the brain. Modern vascular surgery provides different methods of protecting the arterial flow to the brain when the internal carotid artery is sacrificed or is inadequate. Only one such method, namely, gradual occlusion of the common carotid artery, was used in this series. Disaster in the use of one artery graft is described. Of our fourteen patients operated upon for removal of the tumor, seven were subjected to simultaneous removal of the bifurcation. Seven tumors were removed without damage to the carotid arteries. In these seven the tumors either were not attached to the arteries or were safely dissected from them. 398
American
Joumal
of Suvgery
Carotid
Body
Of the seven arterial resections there were no deaths, but there were two cases of hemiplegia and one of hemiparesthesia. One patient (J. H.) had transitory hemiplegia due apparently to hypotension. She later completely recovered from the hemipltgia. One other patient suffered complete hemiplegia, \rith ultimate, almost complete recovery. This male patient (*I. G.), forty-one year> of age, after resection of the tumor with the bifurcation was provided with a homologous artery graft between the common and the internal carotid artery. It is thought that the stump of the internal carotid artery \ras so small as to induce thrombcjsis of its lumen due partly at least to the difficulty of anastomosing the very small internal carotid to the larger graft. It may be stated here that the operative findin:::, in eight of the fourteen operations included decrease in the size of the internal carotid artery. This presumably is due to compression by the tumor upon the arteries below, thus producing a gradual partial occlusion of the internal carotid artery as the tumor grows. In theory this should favor the safety of complete occlusion of the corresponding carotid artery system. None of our patients presented evidence of brain damage prior to operation. In four of the seven patients subjected to resection of the bifurcation with the tumor, gradual occlusion of the common carotid artery on the side of the tumor was carried out in stages. This started before operation by intermittent digital compression of the lower part of the common carotid artery over a period of several days. This tnaneuver, described by Matas [I], also tested the effect of the occlusion on the brain, if any. Then, if no evidence of brain damage had appeared by digital compression, operations were performed in two stages for gradual complete occlusion of the common carotid artery before excision of the tumor which then could be the third operation. During digital compression, the tumor mass decreased, in most cases, in size and its pulsation ceased. Such findings also favored the diagnosis of carotid body tumor. The first operation in each of the four patients preparatory to removal of the tumor with the bifurcation, consisted of an oblique transverse skin incision in the common carotid area for exploration of the tumor and its relation to the bifurcation ; and determination whether or not the bifurcation need be sacri-
Tumors
:lw!)
I:Ic. 1, I’:ttiwt .1 S C;trotirl body tumor encircling tllc l)ifurcatl~~n.
FIG. 2. A Matas-.Ulcn aluminum band, No. 20 gauge aluminum, Browr~ and Sharp gauge. All edges srnoothvtl by metal file. Six sclccted for the particular artcr!-.
ficed. If not, the tumor was then removed. Such a plan required preferably general anesthesia. If, however, it appeared that the bifurcation would need removal with the tumor, the common carotid artery was immediately partially occluded by a Matas-Allen aluminum band [I]. (Fig. 2.) MYthin five to ten days the second operation was performed. The intent here was to complete the occlusion by further compression of the band. In one patient (J. H.j at this stage (second operation) the common carotid artery was found completely occluded so that
400
Hanford
FIG. 3. Patient W. P. Plan of two stage occlusion by metal band. A, B, C, and D, section and ligation for removal of artery segments with tumor. (1) Partial occlusion by the band, January 20, 1938. (2) Complete occlusion by the band, January 24, 1938. (3) Excision of large recurrent tumor, January 29, 1938.
the tumor and bifurcation were then forthwith removed. This patient, a woman fifty years of age, lost much blood during the tumor removal. On the evening of the operative day, the blood pressure was found to have been 78/50 mm. Hg. A blood transfusion was given. Two days after the excisional operation, contralateral hemiplegia was noted. This could have been due to blood loss and hypotension, despite the transfusion. Later this patient completely recovered from the hemiplegia. In three other patients the occlusion was completed at the second operation and the wound closed, to await the third operation for removal of the tumor. Another of the four patients (A. E., fifty-six years of age), treated by the gradual occlusion method, suffered paresthesia of the contralateral limbs with transitory muscle weakness of the hand and face. Otherwise there was no motor weakness in this patient. This patient, who suffered the hemiparesthesia, was a generally healthy woman who had been aware of a swelling in the neck for one year. Six months before admission to the Presbyterian Hospital, an incisional biopsy of the tumor revealed it to
be a nonchromaffin paraganglioma, obviously, of the carotid body. The size of the tumor and its pulsation decreased by digital compression of the common carotid artery, without evidence of brain damage. Removal was performed in three stages, as described previously. After the second stage procedure, namely, complete occlusion of the common carotid artery, there was paresthesia of the contralateral upper limb, but no motor disturbance. This disappeared three days later. After the third operative stage (removal of the tumor with the bifurcation) paresthesia of both contralateral extremities was present. There was transitory weakness of the muscles of the contralateral face and of the hand but no other motor loss, and this weakness disappeared within a few days. From follow-up by letter ten months later, it was learned that the paresthesia had persisted but without any motor loss. There were two other patients treated by gradual common carotid occlusion, with no brain damage. R. S. K., a man, thirty-nine years of age, had postoperative temporary hoarseness due to trauma to the vagus nerve during operation, with no other complication. The other patient (W. P.), a man, fifty-five years of age, had been operated upon twice previously and on admission presented paralysis of the corresponding vocal cord. His tumor, then in existence at least twenty-three years, was very large and measured 8.5 by 4.5 cm. in size. Pressure upon the tumor induced cough. At two operations at the Presbyterian Hospital the aluminum band completely compressed the common carotid artery. At the third operation the tumor with the bifurcation was removed. The tumor did not occupy the bifurcation but the ninth, tenth, and twelfth nerves and the cervical sympathetic nerve, the internal jugular vein, and the internal carotid artery were all so adherent to the tumor as to require resection with it. It is thought that this tumor was primarily a vagus ganglion tumor, not a carotid body tumor, although it was a typical nonchromaffin paraganglioma. The external carotid artery was not involved but was ligated and divided during the excisional operation. (Fig. 3.) The patient recovered from the three operative procedures, with no evidence of brain damage. The internal carotid artery was found almost occluded at the time of tumor removal. Seven years later this patient returned with a mass in the corresponding posterior Amevican
Journal o.f Surgery
Carotid
Body
triangle of the neck. The mass was removed under endotracheal, general anesthesia. The man died of suffocation one hour after this operation apparently because the endotracheal tube had been removed before he had regained consciousness and due to the multiple nerve paralyses. The mass proved to be nonchromaffin paraganglioma representing incomplete removal of the primary tumor previously. This patient demonstrates the danger of allowing such a tumor to reach a very large size, and the inability of three separate surgeons to cure him. The three other patients of the seven subjected to removal of the bifurcation with the tumor were not treated by preliminary nor gradual operative occlusion of the common carotid artery. One, a man (A. S.) twenty-six years of age, was treated at operation by immediate, complete ligation of the common, external, and internal carotid arteries. The operation lasted four and one-quarter hours, made difficult by the continuous oozing from the vascular plexus around the tumor. This patient recovered from the operation with no evidence of brain damage during a follow-up period of nine years. He did have paralysis of the eleventh and twelfth cranial nerves. Another man (J. K.), thirty years of age, who was found before operation to have had a hyperactive carotid sinus reflex, was operated upon and the tumor with the bifurcation removed. This operation was difficult because of the extreme vascularity around the tumor. During attempt at removal of the tumor, with preservation of the arteries, a tear occurred at the bifurcation. Since the internal carotid artery was “so compressed and atrophic,” immediate complete ligation of the common carotid was carried out and the tumor with the bifurcation removed. During the operation, this patient was connected with an auditory and visual electrocardiographic machine. Frequently during the dissection about the carotid bulb extra systoles, bradycardia, and hypotension would occur, despite local infiltration of 1 per cent Xylocainem at the carotid sinus. Blood transfusion of 2,500 cc. was used during the operation and a prophylactic tracheostomy completed the procedure. After operation no brain damage appeared. He did have headache and felt faint on examination of the side of the neck operated on. He presented Horner’s syndrome on that side. This case shows the possible Vol. 110. Sr~temher
1965
Tumors
401
hazard of attempting to remove the tumor and save the arteries. The third patient (A. G.) in this group was the forty-one year old man referred to previously, with the homologous artery graft. The internal carotid artery was estimated to have been one-third the normal size. During the dissection a tear occurred in the wall of the internal carotid artery. In this patient also there was a large vascular mass around the tumor like a large cavernous hemangioma, with large veins feeding it. Immediate complete ligation of the three main arteries with removal of the tumor and bifurcation was performed, and the homologous artery graft sutured in place. The patient had a stormy postoperative course, with dysarthria, dysphagia, hoarseness, pneumonia, and on the twelfth day, a hemiplegia of face-armleg pattern while under heparin. On the fourteenth day, a tracheostomy was performed under local anesthesia and removal of the graft followed by thrombolectomy of the internal carotid artery remnant, and ligation of the internal and common carotid arteries. He required a nasogastric tube for feeding. There was paralysis of the tenth and twelfth nerves. He steadily improved; and in a follow-up letter from Pakistan, it appeared that most of the paralysis had subsided. Again, the hazards of carotid body tumor excision are emphasized. It is thought that this patient would have been better without the graft and with gradual occlusion of the common carotid artery before the tumor excision. (Table I.) COMMENTS
There is evidence as given above that gradual occlusion is safer than immediate complete occlusion of the common carotid artery [5-g]. At the present time gradual carotid occlusion, together with testing of the brain circulation, would be performed in one operation by the use of the Selverstone, Crutchfield, or Poppen-Blalock clamp in place of the aluminum band [g-11]. In view of reports of operations for removal of carotid body tumors, the results in this series of cases may be considered good, despite considerable nerve damage and two (temporary) hemiplegias, with no deaths. These good results are attributable in part to the fact that all of the fourteen patients were operated on by surgeons skilled in surgery of the neck, and to the gradual or staged occlusion of the common
Hanford
40”
lIAT.4 ON THE FOCRTEEN
I\
s
‘l!l:w
\I
\\’
.,‘
R
one stage IP
nr,rles?
PATlEST!:
lixcrllent
moral of tumr,r with bifurca tion. immediate lijiation of :4 art&es
L’!i
x
I’
stageopera-
Satisfactrll-y
Nel
tion: removal i,f turn<,! with hi fut-cation
w. I’
damage
l)ied flam sui location not due t(, arter? damage
(2nd 0y.j
R.S
\‘I?
partly at pre vious operations; probably a ganglion nodw sum? tumor: reCL,,-,enre
K
cI
!Ci!l) s<,tbtntcd :(!I
:i itagr
o&x,-a
lirrrllrnt
tion
.\I,
Irounded bifurcatiun, internal car<,tid small
/ l!l:i!o I’. :x5
‘l‘hyr,,id nrrrlule?
.I- l{
A. IE.
cIWO) I’. .i(i
Previous biopsy proved diaynosia
Simple excisiran
Tumor 3.4 x 3 cm., Yeryvaxw lx, annoying bleedinc.. blwd loss + + +; internal carotid compress?d
3 stage planned, Z-stage done. bifurcation w moved with tumor
Hypotension 78/50 mm. Hg; transfusion; hemiplegia
Vascularity not stated. .X11 nerve adhet-ent; inter-nal carotid smL+ll
3 stage, bifurcation I-emoved: -XII “erYe rrsected
After 2nd op euation (corn plete occlusion) ccmtralateral “aresthesis slight motet loss
tumor
1 stage: arterie< taped during I c
Excellent
Ic
G cm.
I<. A.. s. I3
C. A.
Tumor 3.5 x L cm easily dissected from vebSKIS. nut ver> \~arcillal
sur-
rounded bifurcation; veryvase cular; internal carotid small, vagu? adherent (1953)
I?. Rl
Unknown; carotid body not suspected
Vascularity about tumor; vagus tumor, arteries not in V”lWd
l’utbably an ertopic carotid bc,d.v tum,rl
Not per*;, nent
Hemiplegia due? tu hyp,>m trnsion and hl<,i,d loss, t-e covely complete in .i months
h-\Xle?
None
Well IS months aftrt- operation
.x
h-one
Probably tumor of ganglion nodosum?
None
moval
Removal from “agus nerve
“er”e
paralysis corn plete; anonchromaffin paraganglioma
American
Journal of Suvgery
Carotid
I’reliminal I)iagnosis
A.
I)
(1954) nI, :t4
y
Findings
Unknown; carotid body not suspectrd, elsewhel-e, lymph nc,de
biopsy
A.
c:.
Opel-ative
(1957) 31. _I1
Body
Operation
:3 x 5 cm. tumor. vascularity, fibers of vagus spread out “vet tumor like patient C. A.
Excision of tumor and resection of vag”s and internal jugular vein
Hysteria due to complete paralysis; Homer‘s hy”~ drome
Large vascular mass and smaller mass at bifurcation; internal carotid size
il) Immediate ligation of 3 arteries of bifurcation with tumor; artery homolgraft in lab 6 x 5 Y 2.5 cm.; (2) removal of graft; tracheostomy thrombolectomy of internal carotid
Stormy; dysphagia, dysphonia: Hor“IX’S %y”drome; hemi plegia on 12th day yostoperative; pneumonia, nasogastric tube
usual
’5
ogous tumor
;
J. K.
c1859) Iv, :30
Cal-&d body tumor suspetted; hyperactive carotid sinus reflex
Profuse venous plexus surrounded tumor 4 x 3.5 cm.; internal carotid 2 to 3 mm.
Immediate ligation of 3 arteries; much blood loss; 2,500 cc. blood transfusion; tracheostomy
Good but frontal headache and slight dizziness
J. V.
(1959) F, 67
Branchial
Tumor deep to many veins; froze” section; carotid body tumor
Tumor dissected away from arteries
lixcellent
H. C., Negress
(1963) F. -18
Carotid body tumor; arteriogram
Tumor completely surrounded internal carotid; YOSCI~. larity around tumor; internal carotid not resected
Excision; tumor dissected away from arteries
G”“d
cyst
carotid artery in four patients of the seven in whom this artery was resected. It may be presumed that the general surgeon not familiar with surgery of the neck, who encounters a mass of vessels around a tumor in the neck not previously diagnosed and not considered beforehand as a possible carotid body tumor, finds himself embarassed and inept. This may result in great loss of blood and in undue rough handling of the tissues, especially of the arteries, so as to predispose to arterial thrombosis and to immediate complete occlusion of the arteries supplying the brain. A practiced “head and neck” surgeon of today would be more likely to succeed. The automatic decrease in size of the internal v/01. 1IO.Scplembev 1965
cc1:s
Tumors
Nr,“chl-omaflin paraganglioma of ganglia” ndosum? persistent Homer’s
None
carotid artery by tumor growth conceivably encourages collateral circulation to the brain, at least in some patients, and thereby decreases the hazard of arterial occlusion when the bifurcation is removed. There is always the yuestion in a patient who survives carotid artery occlusion whether a collateral circulation can be established or encouraged or whether the patient has already the capacity to nourish the brain by means of the favorable arterial arrangement with which he was born. One can try for the former and hope for the latter. Also, the small internal carotid artery makes the use of a graft or prosthesis difficult and dangerous. It is worthy of note that in eight of the fourteen patients there was operative damage to
Hanford ganglion of the vagus nerve. In some cases the tumor so encircled the carotid bifurcation that complete removal required arterial resection. Seven such resections were carried out. In four of these, gradual occlusion of the common carotid artery was performed. Except for some damage to nerves, no serious damage ultimately resulted. There were no deaths attributable to the arterial occlusions. Newer instruments are available for the procedure of gradual arterial occlusion in one operation. There is occasionally a hazard in attempting removal of a tumor from the arteries because an inadvertent nick in a large artery may require unexpected arterial resection. The maintenance of normal blood pressure and an adequate airway with oxygen, during and after operation, are to be emphasized. None of these tumors showed evidence of malignancy. FIG. 4. A percutaneous arteriogram showing the outline of the tumor and much dye in the vessels of the neck. Diagnosis later proved by biopsy. Tumor not removed.
one or more cervical nerves. In twelve of the fourteen patients there was a mass of blood vessels surrounding the tumor. The age-old diagnostic sign of the carotid body tumor being immovable vertically is invalid. Any mass attached to the carotid sheath is fixed, such as tuberculous nodes or metastatic cancer. The most valuable diagnostic measure is the (usually percutaneous) arteriogram. (Fig. 4.) Because most of the dye is caught in the vessels of and around the tumor, the collateral circulation of the brain, unfortunately, is rarely depicted. An arteriogram of the contralateral side might show the collateral circulation. In view of the surrounding vascular plexus, an incisional biopsy of the tumor is difficult and dangerous. An aspiration biopsy usually will bring only blood. Decrease in size of the tumor and the absence of pulsation upon digital compression of the common carotid artery point to the presence of a carotid body tumor. SUMMARY
The removal of a nonchromaffin paraganglioma from the neck of fourteen patients is reported. Eleven were carotid body tumors. Three originated presumably in the jugular
REFERENCES
Occlusion of large surgical arteries with removable metallic bands to test the efficiency of the collateral circulation. J.A.M.A., 56~233, 1911. NEPF, J. M. A method of gradual automatic occlusion of the large blood vessels at one operation. J.A.M.A., 57: 700, 1911. HALSTED, W. S. Surgical Papers, p. 309. Baltimore. 1924. The lohns Hopkins Press. KERR, %I. H. Fractional ligation of the common carotid artery in the treatment of pulsating exophthalmos. Surg. Gynec. 6” Obst., 41: 565,1925. GURDJIAN, E. S., WEBSTER, J. E., MARTIN, F. A., and HARDY, W. G. Carotid compression in the neck-results and significance in carotid ligation. J.A.M.A., 163:1030, 1957. GURDJIAN, E. S., HARDY, W. G., and LINDER, D. W. The surgical consideration of 258 patients with carotid artery occlusion. Surg. Gynec. b Obst., 110: 327, 1960. ODOM, G. L., WOODHALL, B., TINDALL, G. T., and JACKSON, J. R. Changes in intravascular pressure and size of intracranial aneurism following common carotid ligation. J. Neurosurg., 19: 41, 1962. SMITH, F. P. Differential carotid ligation for supraclinoid arterial cerebral aneurism. J. Neurosurg., 19: 787, 1962. SELVERSTONE, B. and WHITE, J. C. A new technique for gradual occlusion of the carotid artery. Arch. Neurol. & Psychiat., 66: 246, 1951. CRUTCHFIELD, W. G. Instruments for use in the treatment of certain intracranial vascular lesions. J. Neurosurg., 16:471, 1959. FAGER, C. A. and POPPEN, J. L. Observations on controlled ligation of the internal carotid artery. S. Clin. North America, 36: 567, 1956.
1. MATAS, R. and ALLEN, C. W.
2.
3. 4.
5.
6.
7.
8.
9.
10.
11.
American
Jouvnel of Suwry
Body Tumors:
Paraganglioma A Study of Fourteen
of the Cervical Patients Operated of the Tumor
JOHNM. HANFORD,M.D.,
From the Department of Surgery, Columbia Presbyterian Medical Center, New York, New York.
T
IS INTENDEDhere to emphasize certain factors of importance in the diagnosis and surgical treatment of carotid body tumors and especially the dangers associated with their excision. There is also an effort to evaluate the benefit of gradual rather than immediate complete carotid occlusion in those patients requiring carotid artery resection. Some years ago methods were devised for gradual occlusion of large arteries, notably of the common carotid artery, e.g., by Matas [I], Neff [Z], Halsted [3], and Kerr [a]. Both Halsted and Matas spent time and experiment with metallic materials for the occlusion of large arteries and for release if danger threatened. Neff [Z] and Kerr [4] appreciated the attempt at gradual or staged occlusion. More recently others have indicated the value of gradual occlusion as quoted here: “Where the patient is able to stand carotid compression for about ten minutes, ligation of the carotid can be carried out with a minimum of complications [51. ” “In those instances in which a carotid ligation is found desirable, it has been shown that if the carotid artery can be completely occluded for 5 or 10 minutes, the vessel can then be ligated, and in more than 90%, such ligation would be successful and without any untoward effects [6].” “It is now generally agreed that gradual ligation (sic) with a clamp such as the Crutchfield, Selverstone, or Poppen-Blalock clamp is safer than sudden
I
Nonchromaffin Region
upon for Removal
New York, New York
occlusion with a ligature [7].” “Part of the technic is gradual occlusion of the common carotid artery by the Selverstone clamp [8].” Indicative of its rarity, there were only fourteen patients who had removal of carotid body tumors at The Presbyterian Hospital, New York, between the years 1930 and 1964. The first postoperative patient with carotid body tumor seen by the author was a young woman presented at the New York Surgical Society some thirty years ago. She presented a complete unilateral hemiplegia. This serious postoperative complication is the key to operative removal of this tumor. The tumor often so entwines the bifurcation of the common carotid artery that complete removal of the tumor sometimes appears to be impossible without resection also of the bifurcation. (Fig. 1.) More significantly, the danger is interruption of the flow in the internal carotid artery which largely supplies the brain. Modern vascular surgery provides different methods of protecting the arterial flow to the brain when the internal carotid artery is sacrificed or is inadequate. Only one such method, namely, gradual occlusion of the common carotid artery, was used in this series. Disaster in the use of one artery graft is described. Of our fourteen patients operated upon for removal of the tumor, seven were subjected to simultaneous removal of the bifurcation. Seven tumors were removed without damage to the carotid arteries. In these seven the tumors either were not attached to the arteries or were safely dissected from them. 398
American
Joumal
of Suvgery
Carotid
Body
Of the seven arterial resections there were no deaths, but there were two cases of hemiplegia and one of hemiparesthesia. One patient (J. H.) had transitory hemiplegia due apparently to hypotension. She later completely recovered from the hemipltgia. One other patient suffered complete hemiplegia, \rith ultimate, almost complete recovery. This male patient (*I. G.), forty-one year> of age, after resection of the tumor with the bifurcation was provided with a homologous artery graft between the common and the internal carotid artery. It is thought that the stump of the internal carotid artery \ras so small as to induce thrombcjsis of its lumen due partly at least to the difficulty of anastomosing the very small internal carotid to the larger graft. It may be stated here that the operative findin:::, in eight of the fourteen operations included decrease in the size of the internal carotid artery. This presumably is due to compression by the tumor upon the arteries below, thus producing a gradual partial occlusion of the internal carotid artery as the tumor grows. In theory this should favor the safety of complete occlusion of the corresponding carotid artery system. None of our patients presented evidence of brain damage prior to operation. In four of the seven patients subjected to resection of the bifurcation with the tumor, gradual occlusion of the common carotid artery on the side of the tumor was carried out in stages. This started before operation by intermittent digital compression of the lower part of the common carotid artery over a period of several days. This tnaneuver, described by Matas [I], also tested the effect of the occlusion on the brain, if any. Then, if no evidence of brain damage had appeared by digital compression, operations were performed in two stages for gradual complete occlusion of the common carotid artery before excision of the tumor which then could be the third operation. During digital compression, the tumor mass decreased, in most cases, in size and its pulsation ceased. Such findings also favored the diagnosis of carotid body tumor. The first operation in each of the four patients preparatory to removal of the tumor with the bifurcation, consisted of an oblique transverse skin incision in the common carotid area for exploration of the tumor and its relation to the bifurcation ; and determination whether or not the bifurcation need be sacri-
Tumors
:lw!)
I:Ic. 1, I’:ttiwt .1 S C;trotirl body tumor encircling tllc l)ifurcatl~~n.
FIG. 2. A Matas-.Ulcn aluminum band, No. 20 gauge aluminum, Browr~ and Sharp gauge. All edges srnoothvtl by metal file. Six sclccted for the particular artcr!-.
ficed. If not, the tumor was then removed. Such a plan required preferably general anesthesia. If, however, it appeared that the bifurcation would need removal with the tumor, the common carotid artery was immediately partially occluded by a Matas-Allen aluminum band [I]. (Fig. 2.) MYthin five to ten days the second operation was performed. The intent here was to complete the occlusion by further compression of the band. In one patient (J. H.j at this stage (second operation) the common carotid artery was found completely occluded so that
400
Hanford
FIG. 3. Patient W. P. Plan of two stage occlusion by metal band. A, B, C, and D, section and ligation for removal of artery segments with tumor. (1) Partial occlusion by the band, January 20, 1938. (2) Complete occlusion by the band, January 24, 1938. (3) Excision of large recurrent tumor, January 29, 1938.
the tumor and bifurcation were then forthwith removed. This patient, a woman fifty years of age, lost much blood during the tumor removal. On the evening of the operative day, the blood pressure was found to have been 78/50 mm. Hg. A blood transfusion was given. Two days after the excisional operation, contralateral hemiplegia was noted. This could have been due to blood loss and hypotension, despite the transfusion. Later this patient completely recovered from the hemiplegia. In three other patients the occlusion was completed at the second operation and the wound closed, to await the third operation for removal of the tumor. Another of the four patients (A. E., fifty-six years of age), treated by the gradual occlusion method, suffered paresthesia of the contralateral limbs with transitory muscle weakness of the hand and face. Otherwise there was no motor weakness in this patient. This patient, who suffered the hemiparesthesia, was a generally healthy woman who had been aware of a swelling in the neck for one year. Six months before admission to the Presbyterian Hospital, an incisional biopsy of the tumor revealed it to
be a nonchromaffin paraganglioma, obviously, of the carotid body. The size of the tumor and its pulsation decreased by digital compression of the common carotid artery, without evidence of brain damage. Removal was performed in three stages, as described previously. After the second stage procedure, namely, complete occlusion of the common carotid artery, there was paresthesia of the contralateral upper limb, but no motor disturbance. This disappeared three days later. After the third operative stage (removal of the tumor with the bifurcation) paresthesia of both contralateral extremities was present. There was transitory weakness of the muscles of the contralateral face and of the hand but no other motor loss, and this weakness disappeared within a few days. From follow-up by letter ten months later, it was learned that the paresthesia had persisted but without any motor loss. There were two other patients treated by gradual common carotid occlusion, with no brain damage. R. S. K., a man, thirty-nine years of age, had postoperative temporary hoarseness due to trauma to the vagus nerve during operation, with no other complication. The other patient (W. P.), a man, fifty-five years of age, had been operated upon twice previously and on admission presented paralysis of the corresponding vocal cord. His tumor, then in existence at least twenty-three years, was very large and measured 8.5 by 4.5 cm. in size. Pressure upon the tumor induced cough. At two operations at the Presbyterian Hospital the aluminum band completely compressed the common carotid artery. At the third operation the tumor with the bifurcation was removed. The tumor did not occupy the bifurcation but the ninth, tenth, and twelfth nerves and the cervical sympathetic nerve, the internal jugular vein, and the internal carotid artery were all so adherent to the tumor as to require resection with it. It is thought that this tumor was primarily a vagus ganglion tumor, not a carotid body tumor, although it was a typical nonchromaffin paraganglioma. The external carotid artery was not involved but was ligated and divided during the excisional operation. (Fig. 3.) The patient recovered from the three operative procedures, with no evidence of brain damage. The internal carotid artery was found almost occluded at the time of tumor removal. Seven years later this patient returned with a mass in the corresponding posterior Amevican
Journal o.f Surgery
Carotid
Body
triangle of the neck. The mass was removed under endotracheal, general anesthesia. The man died of suffocation one hour after this operation apparently because the endotracheal tube had been removed before he had regained consciousness and due to the multiple nerve paralyses. The mass proved to be nonchromaffin paraganglioma representing incomplete removal of the primary tumor previously. This patient demonstrates the danger of allowing such a tumor to reach a very large size, and the inability of three separate surgeons to cure him. The three other patients of the seven subjected to removal of the bifurcation with the tumor were not treated by preliminary nor gradual operative occlusion of the common carotid artery. One, a man (A. S.) twenty-six years of age, was treated at operation by immediate, complete ligation of the common, external, and internal carotid arteries. The operation lasted four and one-quarter hours, made difficult by the continuous oozing from the vascular plexus around the tumor. This patient recovered from the operation with no evidence of brain damage during a follow-up period of nine years. He did have paralysis of the eleventh and twelfth cranial nerves. Another man (J. K.), thirty years of age, who was found before operation to have had a hyperactive carotid sinus reflex, was operated upon and the tumor with the bifurcation removed. This operation was difficult because of the extreme vascularity around the tumor. During attempt at removal of the tumor, with preservation of the arteries, a tear occurred at the bifurcation. Since the internal carotid artery was “so compressed and atrophic,” immediate complete ligation of the common carotid was carried out and the tumor with the bifurcation removed. During the operation, this patient was connected with an auditory and visual electrocardiographic machine. Frequently during the dissection about the carotid bulb extra systoles, bradycardia, and hypotension would occur, despite local infiltration of 1 per cent Xylocainem at the carotid sinus. Blood transfusion of 2,500 cc. was used during the operation and a prophylactic tracheostomy completed the procedure. After operation no brain damage appeared. He did have headache and felt faint on examination of the side of the neck operated on. He presented Horner’s syndrome on that side. This case shows the possible Vol. 110. Sr~temher
1965
Tumors
401
hazard of attempting to remove the tumor and save the arteries. The third patient (A. G.) in this group was the forty-one year old man referred to previously, with the homologous artery graft. The internal carotid artery was estimated to have been one-third the normal size. During the dissection a tear occurred in the wall of the internal carotid artery. In this patient also there was a large vascular mass around the tumor like a large cavernous hemangioma, with large veins feeding it. Immediate complete ligation of the three main arteries with removal of the tumor and bifurcation was performed, and the homologous artery graft sutured in place. The patient had a stormy postoperative course, with dysarthria, dysphagia, hoarseness, pneumonia, and on the twelfth day, a hemiplegia of face-armleg pattern while under heparin. On the fourteenth day, a tracheostomy was performed under local anesthesia and removal of the graft followed by thrombolectomy of the internal carotid artery remnant, and ligation of the internal and common carotid arteries. He required a nasogastric tube for feeding. There was paralysis of the tenth and twelfth nerves. He steadily improved; and in a follow-up letter from Pakistan, it appeared that most of the paralysis had subsided. Again, the hazards of carotid body tumor excision are emphasized. It is thought that this patient would have been better without the graft and with gradual occlusion of the common carotid artery before the tumor excision. (Table I.) COMMENTS
There is evidence as given above that gradual occlusion is safer than immediate complete occlusion of the common carotid artery [5-g]. At the present time gradual carotid occlusion, together with testing of the brain circulation, would be performed in one operation by the use of the Selverstone, Crutchfield, or Poppen-Blalock clamp in place of the aluminum band [g-11]. In view of reports of operations for removal of carotid body tumors, the results in this series of cases may be considered good, despite considerable nerve damage and two (temporary) hemiplegias, with no deaths. These good results are attributable in part to the fact that all of the fourteen patients were operated on by surgeons skilled in surgery of the neck, and to the gradual or staged occlusion of the common
Hanford
40”
lIAT.4 ON THE FOCRTEEN
I\
s
‘l!l:w
\I
\\’
.,‘
R
one stage IP
nr,rles?
PATlEST!:
lixcrllent
moral of tumr,r with bifurca tion. immediate lijiation of :4 art&es
L’!i
x
I’
stageopera-
Satisfactrll-y
Nel
tion: removal i,f turn<,! with hi fut-cation
w. I’
damage
l)ied flam sui location not due t(, arter? damage
(2nd 0y.j
R.S
\‘I?
partly at pre vious operations; probably a ganglion nodw sum? tumor: reCL,,-,enre
K
cI
!Ci!l) s<,tbtntcd :(!I
:i itagr
o&x,-a
lirrrllrnt
tion
.\I,
Irounded bifurcatiun, internal car<,tid small
/ l!l:i!o I’. :x5
‘l‘hyr,,id nrrrlule?
.I- l{
A. IE.
cIWO) I’. .i(i
Previous biopsy proved diaynosia
Simple excisiran
Tumor 3.4 x 3 cm., Yeryvaxw lx, annoying bleedinc.. blwd loss + + +; internal carotid compress?d
3 stage planned, Z-stage done. bifurcation w moved with tumor
Hypotension 78/50 mm. Hg; transfusion; hemiplegia
Vascularity not stated. .X11 nerve adhet-ent; inter-nal carotid smL+ll
3 stage, bifurcation I-emoved: -XII “erYe rrsected
After 2nd op euation (corn plete occlusion) ccmtralateral “aresthesis slight motet loss
tumor
1 stage: arterie< taped during I c
Excellent
Ic
G cm.
I<. A.. s. I3
C. A.
Tumor 3.5 x L cm easily dissected from vebSKIS. nut ver> \~arcillal
sur-
rounded bifurcation; veryvase cular; internal carotid small, vagu? adherent (1953)
I?. Rl
Unknown; carotid body not suspected
Vascularity about tumor; vagus tumor, arteries not in V”lWd
l’utbably an ertopic carotid bc,d.v tum,rl
Not per*;, nent
Hemiplegia due? tu hyp,>m trnsion and hl<,i,d loss, t-e covely complete in .i months
h-\Xle?
None
Well IS months aftrt- operation
.x
h-one
Probably tumor of ganglion nodosum?
None
moval
Removal from “agus nerve
“er”e
paralysis corn plete; anonchromaffin paraganglioma
American
Journal of Suvgery
Carotid
I’reliminal I)iagnosis
A.
I)
(1954) nI, :t4
y
Findings
Unknown; carotid body not suspectrd, elsewhel-e, lymph nc,de
biopsy
A.
c:.
Opel-ative
(1957) 31. _I1
Body
Operation
:3 x 5 cm. tumor. vascularity, fibers of vagus spread out “vet tumor like patient C. A.
Excision of tumor and resection of vag”s and internal jugular vein
Hysteria due to complete paralysis; Homer‘s hy”~ drome
Large vascular mass and smaller mass at bifurcation; internal carotid size
il) Immediate ligation of 3 arteries of bifurcation with tumor; artery homolgraft in lab 6 x 5 Y 2.5 cm.; (2) removal of graft; tracheostomy thrombolectomy of internal carotid
Stormy; dysphagia, dysphonia: Hor“IX’S %y”drome; hemi plegia on 12th day yostoperative; pneumonia, nasogastric tube
usual
’5
ogous tumor
;
J. K.
c1859) Iv, :30
Cal-&d body tumor suspetted; hyperactive carotid sinus reflex
Profuse venous plexus surrounded tumor 4 x 3.5 cm.; internal carotid 2 to 3 mm.
Immediate ligation of 3 arteries; much blood loss; 2,500 cc. blood transfusion; tracheostomy
Good but frontal headache and slight dizziness
J. V.
(1959) F, 67
Branchial
Tumor deep to many veins; froze” section; carotid body tumor
Tumor dissected away from arteries
lixcellent
H. C., Negress
(1963) F. -18
Carotid body tumor; arteriogram
Tumor completely surrounded internal carotid; YOSCI~. larity around tumor; internal carotid not resected
Excision; tumor dissected away from arteries
G”“d
cyst
carotid artery in four patients of the seven in whom this artery was resected. It may be presumed that the general surgeon not familiar with surgery of the neck, who encounters a mass of vessels around a tumor in the neck not previously diagnosed and not considered beforehand as a possible carotid body tumor, finds himself embarassed and inept. This may result in great loss of blood and in undue rough handling of the tissues, especially of the arteries, so as to predispose to arterial thrombosis and to immediate complete occlusion of the arteries supplying the brain. A practiced “head and neck” surgeon of today would be more likely to succeed. The automatic decrease in size of the internal v/01. 1IO.Scplembev 1965
cc1:s
Tumors
Nr,“chl-omaflin paraganglioma of ganglia” ndosum? persistent Homer’s
None
carotid artery by tumor growth conceivably encourages collateral circulation to the brain, at least in some patients, and thereby decreases the hazard of arterial occlusion when the bifurcation is removed. There is always the yuestion in a patient who survives carotid artery occlusion whether a collateral circulation can be established or encouraged or whether the patient has already the capacity to nourish the brain by means of the favorable arterial arrangement with which he was born. One can try for the former and hope for the latter. Also, the small internal carotid artery makes the use of a graft or prosthesis difficult and dangerous. It is worthy of note that in eight of the fourteen patients there was operative damage to
Hanford ganglion of the vagus nerve. In some cases the tumor so encircled the carotid bifurcation that complete removal required arterial resection. Seven such resections were carried out. In four of these, gradual occlusion of the common carotid artery was performed. Except for some damage to nerves, no serious damage ultimately resulted. There were no deaths attributable to the arterial occlusions. Newer instruments are available for the procedure of gradual arterial occlusion in one operation. There is occasionally a hazard in attempting removal of a tumor from the arteries because an inadvertent nick in a large artery may require unexpected arterial resection. The maintenance of normal blood pressure and an adequate airway with oxygen, during and after operation, are to be emphasized. None of these tumors showed evidence of malignancy. FIG. 4. A percutaneous arteriogram showing the outline of the tumor and much dye in the vessels of the neck. Diagnosis later proved by biopsy. Tumor not removed.
one or more cervical nerves. In twelve of the fourteen patients there was a mass of blood vessels surrounding the tumor. The age-old diagnostic sign of the carotid body tumor being immovable vertically is invalid. Any mass attached to the carotid sheath is fixed, such as tuberculous nodes or metastatic cancer. The most valuable diagnostic measure is the (usually percutaneous) arteriogram. (Fig. 4.) Because most of the dye is caught in the vessels of and around the tumor, the collateral circulation of the brain, unfortunately, is rarely depicted. An arteriogram of the contralateral side might show the collateral circulation. In view of the surrounding vascular plexus, an incisional biopsy of the tumor is difficult and dangerous. An aspiration biopsy usually will bring only blood. Decrease in size of the tumor and the absence of pulsation upon digital compression of the common carotid artery point to the presence of a carotid body tumor. SUMMARY
The removal of a nonchromaffin paraganglioma from the neck of fourteen patients is reported. Eleven were carotid body tumors. Three originated presumably in the jugular
REFERENCES
Occlusion of large surgical arteries with removable metallic bands to test the efficiency of the collateral circulation. J.A.M.A., 56~233, 1911. NEPF, J. M. A method of gradual automatic occlusion of the large blood vessels at one operation. J.A.M.A., 57: 700, 1911. HALSTED, W. S. Surgical Papers, p. 309. Baltimore. 1924. The lohns Hopkins Press. KERR, %I. H. Fractional ligation of the common carotid artery in the treatment of pulsating exophthalmos. Surg. Gynec. 6” Obst., 41: 565,1925. GURDJIAN, E. S., WEBSTER, J. E., MARTIN, F. A., and HARDY, W. G. Carotid compression in the neck-results and significance in carotid ligation. J.A.M.A., 163:1030, 1957. GURDJIAN, E. S., HARDY, W. G., and LINDER, D. W. The surgical consideration of 258 patients with carotid artery occlusion. Surg. Gynec. b Obst., 110: 327, 1960. ODOM, G. L., WOODHALL, B., TINDALL, G. T., and JACKSON, J. R. Changes in intravascular pressure and size of intracranial aneurism following common carotid ligation. J. Neurosurg., 19: 41, 1962. SMITH, F. P. Differential carotid ligation for supraclinoid arterial cerebral aneurism. J. Neurosurg., 19: 787, 1962. SELVERSTONE, B. and WHITE, J. C. A new technique for gradual occlusion of the carotid artery. Arch. Neurol. & Psychiat., 66: 246, 1951. CRUTCHFIELD, W. G. Instruments for use in the treatment of certain intracranial vascular lesions. J. Neurosurg., 16:471, 1959. FAGER, C. A. and POPPEN, J. L. Observations on controlled ligation of the internal carotid artery. S. Clin. North America, 36: 567, 1956.
1. MATAS, R. and ALLEN, C. W.
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American
Jouvnel of Suwry