Carotid artery resection for head and neck cancer

Carotid artery resection for head and neck cancer Yoshitaka Okamoto, MD, Atsushi Inugami, MD, Zensei Matsuzaki, MD, Michinori Yokomizo, MD, Akiyoshi Konno, MD, Kiyoshi Togawa, MD, Ryousei Kuribayashi, MD, Toshihide Ogawa, MD, and Iwao Kanno, Phi), Akita, Japan Background. Carotid artery resection has been shown to yield a chance of cure in patients with advanced head and neck carcinoma involving the carotid artery. However, the criteria for the identification of those who are vulnerable to neurologic injury after resection have not been established. Interposition grafting may minimize the risk of neurologic morbidity, although it is technically difficult when there is involvement of the internal carotid artery close to the skull base. Methods. We studied 24 patients with head and neck tumor involvement of the carotid artery. We performed carotid artery resection in 16 of them, including 10 in whom the carotid artery was reconstructed with interposition grafts covered with muscle flaps. When it was thought that the reconstruction would be difficult, positron emission tomography was performed during balloon test occlusion of the internal carotid artery to assess the adequacy of hemispheric collateral blood flow before carotid resection. In one patient with interposition graft, carotid rupture occurred as a result of wound infection, but none of the other patients experienced perioperative death, persistent hemiplegia, or delayed stroke. Results. Twelve patients have survived longer than 8 months, and seven (43. 8 %) were alive without disease at 12 months after resection, whereas all four patients who could not be treated operatively died within 8 months as a result of local primary tumors. Conclusions. Carotid artery resection is the only therapy offering any potential for cure or palliation. Positron emission tomography is a rapid quantitative means of determining the cerebral blood flow, particularly when resection is planned without reconstruction. (Surgery 1996;120:54-9.) From the Departments of Otolaryngology and of Vascular Surgery, Akita University School of Medicine, and Department of Radiology and Nuclear Medicine, ResearchInstitute of Brain and Blood Vessels, Akita, Japan

PATIENTS WITH ADVANCEDCANCERo f the h e a d a n d neck may have involvement o f the carotid artery. Carotid artery resection is often the only therapy offering these patients any potential for cure o r palliation. 1 However, the criteria for the identification of those who are vulnerable to neurologic injury after resection have n o t yet b e e n established. 2' 3 A high incidence of neurologic complications is r e p o r t e d even in patients with good crossover or high carotid back pressure shown on preoperative arteriogram. 4, 5 Interposition grafting may minimize the risk of neurologic morbidity, 6, 7 although it is technically difficult when involvement o f the internal carotid artery occurs close to the skull base. This r e p o r t summarizes our experience with resection with a n d without r e p l a c e m e n t in patients with h e a d Accepted for publication Nov. 21, 1995. Reprint requests: YoshitakaOkamoto, MD, Department of Otolaryngology,Aldta UniversitySchool of Medicine, 1-1-1Hondo, Akita 010, Japan. Copyright 9 1996 by Mosby-YearBook, Inc. 0039-6060/96/$5.00 + 0 11/56/71953 54

SURGERY

a n d neck cancer, together with the use o f preresection positron emission t o m o g r a p h y (PET) 8 d u r i n g balloon test occlusion of the internal carotid artery to assess the adequacy o f hemispheric collateral b l o o d flow.

MATERIAL AND METHODS A total o f 24 patients were enrolled in this study. According to the site o f t u m o r involvement to the carotid artery, they were classified into two groups who underwent either carotid resection with r e p l a c e m e n t o r internal carotid artery balloon test occlusion. Carotid resection with replacement. Between 1982 a n d 1994 10 patients were diagnosed with h e a d and neck cancer a d h e r e n t to the carotid artery; these patients u n d e r w e n t en bloc resection of the t u m o r together with the internal a n d c o m m o n carotid arteries followed by r e p l a c e m e n t with autogenous saphenous vein grafts. T h e four m e n a n d six w o m e n r a n g e d in age from 52 to 81 years. All except the four patients with thyroid cancer received 60 Gy o f external radiotherapy before operation. In each patient a graft was interposed between the c o m m o n a n d internal carotid arteries with

Surgery Volume 120, Number 1

Okamoto et al.

COz(Hypercepnia)

55

CO: (Hypercapnia)

Balloon Occlusion Test

9 Time (min.)

-'=5 t

-;o t

o s

fi

t

t

k t

55

75

t

t

PET study Fig. 1. Protocol of [150]H20 PET cerebral blood flow study.

T a b l e I. Clinical features a n d outcome in patients who u n d e r w e n t carotid resection with saphenous vein interposition grafting

Patient Age (yr)/ no. Gender Primary site

Histologic findings

Prior Neurologic radiation Reconstruction Infection morbidity

1 2 3 4 5

71/M 56/M 52/F 69/M 73/F

Epipharynx Maxilla Tongue Thyroid Hypopharynx

SCC SCC SCC Adenocarcinoma SCC

Yes Yes Yes No Yes

PMMC PMMC PMMC -LDMC

No No No No No

No No No No No

6 7 8 9 10

54/M 71/M 56/M 74/F 81/F

Larynx Thyroid Thyroid Thyroid Larynx

SCC Adenocarcinoma Adenocarcinoma Adenocarcinoma SCC

Yes No No No Yes

PMMC SMMC PMMC LDMC PMMC

No No No Yes No

No No No No No

Outcome 14 mot (lung metastasis) 26 mot (lung metastasis)* 39 mo NED 123 mo NED 18 dayst (diabetes mellitus coma) 9 mot (double cancer) 63 mo NED 4 mo t (double cancer) 18 dayst (carotid rupture) 10 mot (lung metastasis)

SCC, Squamous cell carcinoma; PMMC, pectoralis major myocutaneous flap; LDMC, latissimus dorsis myocutaneous flap; SMMC, sternocleidomastoid myocutaneous flap; NED, no evidence of disease. *Alive without disease 12 months after operation. tDied.

5-0 nylon suture over a Javid shunt. The s h u n t was removed before the completion of the proximal anastomosis. The graft in every patient except patient 4 was covered with a muscle flap. Internal carotid artery balloon test occlusion. In the 14 patients with suspected t u m o r involvement of the internal carotid artery close to the skull base, it was considered too difficult to apply an interposition graft; these patients u n d e r w e n t angiographic a n d clinical evaluations by means of internal carotid artery balloon test occlusion between 1991 a n d 1994. The 12 m e n a n d two w o m e n ranged in age from 24 to 75 years. All except one patient with parotid gland adenocarcinoma received radiotherapy. Twelve patients who showed n o clinical deficit (patients treated with balloon occlusion) then underwent [150] H 2 0 PET cerebral blood flow studies including cerebral blood flow determinations obtained first without a n d then with balloon test occlusion of the internal carotid artery. The methods of internal carotid artery balloon test occlusion a n d of [150] H 2 0 PET

cerebral blood flow studies have b e e n reported previously.9,10 Briefly, PET cerebral blood flow studies were performed by using the Headtome IV (Shimadzu Medical, Kyoto,Japan), a three-ring five-plane PET apparatus for whole body imaging. After transmission scanning for attenuation correction, an intravenous bolus of 1.1 to 1.5 MBq of [150] H 2 0 was administered. The cumulative brain tracer time-activity curve was recorded for 90 seconds after radioactivity was first detected in the scann e r field of view. Arterial blood was continually sampled to measure the arterial tracer time-activity curve, and it was taken as a measure of CO2 tension. Cerebral blood flow determination was conducted first before the carotid occlusion a n d then six more times at intervals of at least 15 minutes d u r i n g a n d after the occlusion. For occlusion the balloon was inflated u p to 45 minutes (Fig. 1). The carotid back-pressure was d e t e r m i n e d in some patients by using a d o u b l e - l u m e n balloon catheter as reported previously. 1] I n f o r m e d consent was obtained from all patients.

Okamoto et al.

56

Surgery July 1996

Fig. 2. S e l e c t e d i m a g e s f r o m P E T c e r e b r a l b l o o d flow s t u d y w i t h a n d w i t h o u t i n t e r n a l c a r o t i d a r t e r y ball o o n test o c c l u s i o n s h o w n o a l t e r a t i o n i n c e r e b r a l b l o o d flow.

Table

II. Clinical features and outcome

in patients who underwent

internal carotid artery balloon test occlusion

studies

Patient Age (yr)/ no. Gender Primary site

Histologic findings

Stump Collateral P~ior Matas pressure flow En bloc Carotid Neurologic radiation test (mm Hg) (PET) operation resection morbidity

Outcome

11

69/M

Hypopharynx

SCC

Yes

•

--

--

No

--

--

8 mot (primary)

12

75/F

Larynx

SCC

Yes

x

--

--

No

--

--

13

64/F

Oropharynx

SCC

Yes

O

41 m m

$

No

--

--

3 mot (primary) 3 mot (primary)

14

51/F

Hypopharynx

SCC

Yes

O

--

---)

No**

--

--

6 mot (primary)

15 16 17 18

54/F 50/F 51/F 59/F

Oropharynx Oropharynx Hypopharynx Parotid g l a n d

Yes Yes Yes No

O O O O

54 m m --68 m m

~# --* ---) ---)

Yes Yes Yes Yes

No No No No

-----

21 24 12 11

19

69/F

Unknown

SCC SCC SCC Adenocarcinoma SCC

Yes

O

--

--)

Yes

Yes

No

24 m o t ( l u n g metastasis) *

20

71/F

Larynx

SCC

Yes

O

--

---)

Yes

Yes

Yes

21

48/F

Hypopharynx

SCC

Yes

O

--

---)

Yes

Yes

No

22

24/M

Tongue

SCC

Yes

O

55 m m

---)

Yes

Yes

No

23 24

73/F 62/F

Hypopharynx Parotid g l a n d

SCC SCC

Yes Yes

O O

73 m m 46 m m

--> --~

Yes Yes

Yes Yes

No No

19 m o t ( l u n g metastasis) * 6 m o t (local recurrence ) 15 m o t (local recurrence) 12 m o N E D 13 m o alive (bone metastasis)

mo mo mo mo

NED NED NED NED

All four patients who could not be treated operatively because of inadequate collateral flow died within 8 months. Five of six patients treated with carotid resection survived at least 6 months, and 2 (33.3%) were alive without disease at 12 months after operation. SCC, Squamous cell carcinoma; Matas, internal carotid artery balloon occlusion; PET, PET during balloon test occlusion; primary, died with primary neck tumor; NED, no evidence of disease; O , no neurologic symptoms and good crossover shown by arteriography; x, neurologic symptoms or poor crossover shown by arteriography; $, decrease in blood flow to 20 ml/100 ml per minute during balloon test; -% no change or decrease in cerebral blood flow amounting to less than 10 ml/100 ml per minute in comparison with value obtained without occlusion; ,1,#, very slow decrease was seen in this patient during balloon occlusion, although blood flow was 40 ml/100 ml at end of occlusion test. *Alive without disease at 12 months after operation. tDied. **Tumor was fixed to both internal carotid arteries close to skull base and it was necessary to leave it.

Surgery Volume 120, Number I

Okamoto et al.

80-

5,7

---O~CBL

ACAterritory A ---~-

e-

E

PCAterritory white matter

SO

m

E 0 0

40

E IJ. r (,1

20

0 -40

-'2o

6

2'0

4'0

~o

8'o

Tirne(rnin)

%

9

ACA

I~1

MCA territory

territory territory

[]

PCA

[]

white matter

150 v O~ eco

100" >

r o Og

50,

Before Occlusion

Hypercepnhl (Befor Occlusion)

S rain AftlH Occl~Lon

30 rain Aher Occlusi~

Hyplrcacmill After Oecluliml

30 rain Aher Open

Fig. 3. Change of cerebral blood flow in patient 15. During occlusion the blood flow decreased slowly and response to hypercapnia was poor compared with that observed before occlusion. Lower part shows relative change of cerebral flow in same patient. CBF, Cerebral blood flow; CBL, cerebellum; ACA, anterior cerebral artery; MCA, middle cerebral artery; PCA, posterior cerebral artery.

RESULTS

T h e perioperative a n d postoperative morbidity a n d o u t c o m e in each of the 10 patients who u n d e r w e n t carotid artery resection with interposition grafting are shown in Table I. N o n e of these patients showed any intraoperative neurologic complications. Patient 9 h a d partial necrosis of the muscle flap used for coverage of the graft a n d died as a result of carotid r u p t u r e caused by ensuing w o u n d infection. T h e o t h e r patients did n o t have skin necrosis, m u c o c u t a n e o u s fistula, carotid rup-

ture, or w o u n d infection. O f the seven patients who died, three h a d local-regional recurrence a n d four d i e d of distant metastasis. T h e clinical features o f the 14 patients who underwent balloon test occlusion studies o f cerebral b l o o d flow without a n d with internal carotid balloon test occlusion are shown in Table II. T e n o f the patients either h a d no change in cerebral b l o o d flow on occlusion with the internal carotid artery balloon test or showed a decrease in b l o o d flow a m o u n t i n g to less than 10 m l /

58

Okamoto et al.

100 ml per minute in comparison with values obtained before occlusion. The cerebral blood flow remained above 35 ml/100 ml per minute throughout the bilateral cortex (Fig. 2). In one of the 12 patients who underwent PET studies, the cerebral blood flow decreased slowly during balloon occlusion, although the blood flow was 40 m l / 100 ml per minute at the end of occlusion test (Fig. 3). Another patient had a decrease in blood flow to 20 m l / 100 ml per minute during the balloon test. En bloc tumor resection was performed in the 10 patients in whom PET showed good cerebral blood flow that was maintained during the vessel occlusion. In four of the 10 patients the tumor could be separated from the carotid artery and the artery could be salvaged. In patient 4 the tumor was fixed to bilateral carotid arteries close to the skull base and it was necessary to leave it unresected. In six patients the internal and c o m m o n carotid arteries were resected without replacement. Neither persistent hemiplegia nor delayed stroke occurred, and one patient who had mild hemiplegia immediately after operation showed complete recovery within 7 days. This patient had shown temporary hypotension (50 m m Hg) for a 10-minute period during resection of the carotid artery. All four patients who could not undergo en bloc resection because of inadequate collateral blood flow died within 8 months. Four in whom the tumor could be separated from the carotid artery are alive without disease. Of six patients who underwent carotid resection, two had local recurrence and three had distant metastasis, although five patients have survived longer than 8 months.

DISCUSSION The therapy offering the greatest promise of cure in patients with advanced head and neck carcinoma involving the carotid artery is reportedly radical extirpation with ablative surgery in the form of en bloc resection of the primary lesion and the involved carotid artery, although even then the prognosis is generally poor. 12-14This was also the case in our patients. It seems certain that the survivors would have died if they had been treated only by nonoperative means, and even in patients who undergo resection only to die of distant metastases, the local control at the neck substantially decreases their discomfort and serves to improve the quality of their lives. Lor~ and Boulos 15 issued the first report of a study showing that resection and carotid replacement improved survival. However, the many reports about the risk of postoperative carotid graft thrombosis or rupture in patients with interposition grafts indicate highly variable morbidity rates for ligation and replacement. 17' 12-16 The serious complicating factors are poor recipient tissue bed as a result of intensive irradiation, secondary infection, oral fistula, and inadequate tissue flap covering.

Surgery July 1996 In our patients treated with reconstruction we attributed the low rates ofperioperative mortality and morbidity to the use of myocutaneous flaps, which allow coverage of the arterialized vein and replacement of excised mucosal defects in the u p p e r respiratory and digestive tracts with healthy well-vascularized tissue. However, one patient died of carotid rupture as a result of the wound infection caused by partial necrosis of the flap used for coverage. The rate of perioperative morbidity after carotid resection may be minimized by covering the interposition graft with a well-vascularized flap. However, such carotid artery replacement is not always technically or physiologically possible, particularly when the locus of tumor involvement of the internal carotid artery is close to the skull base. Adequate perfusion of the brain after internal carotid artery resection without replacement depends on cross flow from the contralateral carotid artery. For the preoperative assessment of the adequacy of cerebral collateral flow, several internal carotid artery test occlusion techniques have been developed. Matas 17 described the application of pericutaneous digital carotid pressure, together with clinical observation of the patient's neurologic features and the angiographic assessment of collateral flow at the circle of Willis. Other reported methods 18-22 include intraoperative test occlusion with electroencephalographic monitoring and preoperative intracranial balloon test occlusion of the internal carotid artery with a combination of neurologic and neuropsychological testing, electroencephalographic monitoring, and internal carotid artery stump pressure measurement. However, n o n e has been confirmed to be adequate for the accurate prediction of morbidity after permanent occlusion. Recently incorporation of cold xenon computed tomography techniques or of single p h o t o n emission computed tomography with technetium 99m hexamethyl-propyleneamine oxide single p h o t o n emission during balloon test occlusion was reported as a m e t h o d for the quantitative determination of cerebral blood flow. 22 However, xenon has anesthetic effect and itself activates the cerebral blood flow, and the results obtained by these methods are qualitative rather than quantitative. For these reasons we routinely use a [150] H20 and PET technique for rapid quantitative determination of cerebral blood flow throughout the entire brain during internal carotid artery balloon test occlusion. The occlusion time of up to 45 minutes is used to assess the likelihood of adequate collateral circulation after perm a n e n t internal carotid artery occlusion. We f o u n d that PET was quite useful in this assessment, and we observed neither persistent hemiplegia nor delayed stroke after carotid resection. A m o n g the several additional interesting observations we noted that, in the patient who showed very slow decrease of the cerebral collateral flow examined with PET during bal-

Surgery Volume 120, Number I

loon test occlusion, the flow was nevertheless still more than 40 m l / 1 0 0 ml per minute at the end of occlusion, which is higher than the cut-off flow for induction of neurologic complication (less than 20 m l / 1 0 0 ml per minute). Arteriogram in this patient revealed g o o d crossover and high carotid back pressure. However, we think that delayed stroke might have occulted if this patient had been treated with carotid resection without replacement. The risk of delayed stroke in patients undergoing carotid ligation has been reported by numerous authors.18, 23, 24 Moore and Baker 23 reported that, of 88 patients who underwent carotid ligafion for neck carcinoma, 19 exhibited cerebral complication between 8 hours and 5 days after operation. Thrombus formation in the internal carotid stump with propagation into the circle of Willis and embolizafion by collateral flow has been suggested to be a cause of delayed stroke. However, this is probably not very likely because in fatal delayed stroke the autopsy findings fail to show a thrombus. 23 In addition, although the internal carotid artery was resected at the carotid canal in our patients, none of them experienced delayed stroke or visual disturbance. Slow decrease of collateral cerebral blood flow, as observed in one of our patients, may contribute to the development of delayed stroke. Of the patients in whom PET study had indicated that good collateral flow could be obtained after operation, one immediately experienced mild and nonpersistent hemiplegia because of hypotension during the operation. The correction and prevention ofhypotension are thought to be the most important factors in preventing cerebral ischemia, even when PET study has been performed. The outcome in the patients who underwent carotid resection was poor, but all four of those treated nonoperatively because of inadequate collateral blood flow died within 8 months as a result of local primary tumors. Of the patients treated with resection, 12 (75.0%) have survived longer than 8 months and seven (43.8%) were alive without disease at 12 months after operation. We believe carotid artery resection is the only therapy offering any potential for cure or palliation. If possible, the carotid artery should be reconstructed with interposition grafts covered with nonirradiated well-vascularized tissue as a prophylactic measure against undesirable events that may occur after carotid resection. When carotid artery resection without reconstruction is planned, it is necessary to perform an internal carotid artery balloon test occlusion procedure. If no clinical deficit develops, quantitative assessment of cerebral blood flow should be considered as an aid in reducing the risk of the development of cerebral infarction because of inadequate collateral flow. The use of PET with the intravenous administration of [150] H 2 0 permits the rapid quantitative determination of cerebral blood flow throughout the entire brain and pro-

Okamoto et al.

59

vides essential information that aids in assessing the safety and feasibility of carotid resection. REFERENCES

1. East CA, Adseshiah M, Grant HR. Resection of the extracranial artery in head and neck cancer. J Otolaryngol 1989;68:206-10. 2. Kennedy JT, Krause GJ, Lovey S. The importance of tumor attachment to the carotid artery. Arch Otolaryngo11977;103:70-3. 3. Martis C, Karabouta I, Lazarids N. The internal carotid artery in the surgery of extensive oral cancer. IntJ Oral Maxillofac Surg 1986;15:113-8. 4. Urkim M, Billet HF, Laeson W. Salvage surgery for recurrent neck carcinoma after mulfimodality therapy. Head Neck Surg 1986;8:332-42. 5. Meleca RJ, Marks SC. Carotid artery resection for cancer of the head and neck. Arch Otolaryngol Head Neck Surg 1994;120:974-8. 6. Karam F, Schaefer S, Cherryhohnes D, Dagher FJ. Carotid artery resection and replacement in patients with head and neck malignant tumors. J Cardiovasc Surg 1990;31:697-701. 7. Billet HF, Urken M, Lawson W, Haimov M. Carotid artery rese.ction and bypass for neck carcinoma. Laryngoscope 1988;98:181-.3. 8. Fox PT, Mintun MA, Raichle ME, Herscovitch P. A non-invasive approach to quantitative functional brain mapping with H2 150 and positron emission tomography. J Cereb Blood Flow Metab 1984;4:329-33. 9. Kanno K, Iida H, Miura S, et al. A system for cerebral blood flow measurement using H215Oautoradiographic method and positron emission tomography. J Cereb Blood Flow Metab 1987;7:143-53. 10. Yamamoto S, Amano M, Miura S, lida H, Kanno I. Deadtime correction m e t h o d using r a n d o m coincidence for PET. J Nucl Med 1986;27:1925-8. 11. Enzmann DR, Miller DC, Olcott C, Mehigan JT. Carotid back pressure in conjunction with cerebral angiogTaphy. Radiology 1980;134:415-22. 12. McCready RA, Miller SK, Hanlaker RC, Singer MI, Herod GT. What is the role of carotid arterial resection in the management of advanced cervical cancer? J Vase Surg 1989;10:274-80. 13. Atkinson DP, Jacobs LA, Weaver AW. Elective carotid resection and bypass for neck carcinoma. Laryngoscope 1988;98:181-3. 14. Hiranandani LH. Management of cervical metastases in head and neck cancers. J Laryngol Otol 1971;85:1097-126. 15. Lor~JM, Boulos EJ. Resection and reconstruction of the carotid artery in metastatic squamous cell carcinoma. Am J Surg 1981; 141:437-47. 16. Koopman CH Jr, Coulthard SW, Malone JM, Weinstein PR. Complication of carotid artery replacement in head and neck neoplasms. Otolaryngol Head Neck Surg 1982;90:561-6. 17. Matas R. Testing the efficiency of the collateral circulation.JAMA 1914;63:1441-7. 18. James NJ, Stuteville OH, Tasche C. Elective carotid artery ligatinn in the treatment of advanced cancer of the head and neck. Plast Reconstr Surg 1971;47:243-5. 19. Hays RJ, Levinson SA, Wylie EJ. Intraoperative management of carotid back pressure as a guide to operative management fi)r carotid endarterectomy. Surgery 1972;72:953-60. 20. Gee W, MehiganJJ, Wylie EJ. Measurement of collateral cerebral hemispheric blood pressure by ocular pneumoplethysmography. A m J Surg 1975;130:121-7. 21. Cotton LR, Horrocks M. Involvement of the carotid artery in tumours of the head and neck. Clin Otolaryngol 1978;3:37-t2. 22. De Vfies EJ, Sekhar LN, Janecka IP, Schramm VL, Horton JA, Eibling DE. Elective resection of the internal carotid artery without reconstruction. Laryngoscope 1988;98:960-6. 23. Moore O, Baker HW. Carotid artery ligation in surgery of the head and neck. Cancer 1955;8:712-5. 24. Moore OS, Karlan M, Siglar L. Factors influencing the safety of carotid ligation. Am J Surg 1969;118:666-8.