Presentation and surgical outcome of carotid body tumors in Upper Egypt: a retrospective study

 

Omar Abdelraheem♥ MSc, MD

Kamal A-A M Hassanein† MSc, FRCS, PhD

Ahmed Seif Al-Eslam‡ MSc, MD

Khaled N.Abokresha¶ MSc, MD

♥Department of Surgery; †Maxillofacial/Head and Neck Surgical Unit, Department of Surgery; ‡Department of Vascular Surgery;¶Department of Neurosurgery, Sohag Faculty of Medicine, the University of Sohag.

 

Corresponding author:

Omar Abdelraheem  MSc, MD, Department of Surgery, Sohag Faculty of Medicine, Sohag, the University of Sohag, Egypt

 

 

 

 

 

 

 

 

 

 

 

 

Abstract

Background and aims:

Carotid body tumors (CBTs) are rare, hypervascular neoplasms and are usually located at the carotid artery bifurcation.  However, surgery is the gold standard for curative treatment of CBTs it carries a high risk of mortality and morbidity. The aim of this study was to find out the pattern of presentation of CBTs in our locality and to evaluate the outcome of their surgical treatment.

Materials and methods:

A retrospective group of patients that presented with CBTs and subjected to surgical resection in the period from May 2006 to April 2011 were included in this study. All cases were evaluated clinically, radiologically before surgical treatment and diagnosis confirmed with postoperative histopathology. Surgical outcome was recorded. 

Results:

A total of 16 patients were presented in the study period and only 12 of them were subjected to surgical excision and they were 7 women and 5 men and their age ranged from 33 to 65 years (mean 46±13). Sex patients with Shamblin group I and II, subadventitial tumor excision was performed after ligation of the feeding vessels of the tumor and 3 of them were in need for ligation of the external carotid artery (ECA) and primary vascular repair of the internal carotid artery (ICA) was needed in another patient. The remaining 6 patients with Shamblin group III, ECA ligation was done in 5 patients, primary vascular repair of the ICA was needed in 3 patients and ICA reconstruction by saphenous vein graft in one patient. Postoperative hemiparesis occurred in 2 patients with Shamblin III, one of them improved in 3 months after surgery. Postoperative cranial nerve deficits occurred in 3 patients (2 cases with Shamblin III and one case with Shamblin II), 2 of them with transient hypoglossal paresis and the remaining one developed hoarseness of voice due to permanent vocal cord paralysis. There was no recurrences in the follow up period.

Conclusions:

Patients with CBTs in our locality are usually presented with an advanced stage. Early diagnosis and surgical resection of these tumors will minimize the morbidity and carry good surgical outcome. A team approach including head and neck and vascular surgeons are essential to achieve good surgical results.

 

 

 

Introduction

Carotid body tumors (CBTs) are hypervascular tumors arising from paraganglionic cells of the carotid body and are usually located at the carotid artery bifurcation. They are slowly growing tumors. The other head and neck paragangliomas are typically located in three main sites; the foramen jugulare (jugular paraganglioma), the middle ear cavity (tympanic paraganglioma), and along the cervical portion of the vagus nerve (vagal paraganglioma) (1).

CBT is a rare disease with an incidence of 0.012% from pathological studies (2). The sporadic form of CBT is common than the inherited variety and tends to occur slightly more often in women. It is seen more frequently in people living at high altitudes and is multicentric in approximately among 10% of cases (3). Bilateral and multicentric forms described (3-5%) with a higher incidence in familial forms (32%). Malignancy occurs in 6-12.5% of cases, which ranks carotid body paragangliomas as the most frequently occurring malignant head and neck paraganglioma (4, 5).

 

Surgery is the gold standard for curative treatment of CBTs. The first successful CBT excision was performed by Alber in 1889(6), and Gordon-Taylor (7) who described a safe, subadventitial dissection in 1940. Since the 1980s, devascularization of CBTs by ligation of feeding branches of the external carotid artery (ECA) during operation has been a common practical technique (8). Recently, Van der Bogt et al; (9) proposed a craniocaudal dissection technique that would minimize postoperative morbidity.

 

Shamblin et al; in 1971(10) proposed the classification of CBTs based on the tumor - vessel relationship. It has been widely used and maintained its usefulness in surgical techniques of resection. Shamblin group I: tumors are localized and do not involve the surrounding major vessels, group II: are adherent or partially surround the vessels, and group III: are large and encase the vessels.

The aim of this study was to find out the pattern of presentation of CBTs in our locality and to evaluate the outcome of their surgical treatment.

 

 

 

 

 

 

Patients and Methods

A retrospective study included patients with CBTs that had been presented to the Department of Surgery, at Sohag University Hospital in the period from May 2006 to April 2011. During this period, 16 patients diagnosed with CBTs, but 12 of them were treated by surgical excision after consenting. Three of the remaining 4 patients refused the consent as they did not accept the possible complications after surgery. One of them had bilateral and multicentric paraganglioma (Figure 1 a and b) and another one was referred to the Oncology Department, from the start, as the patient diagnosed histopathologically as a malignant CBT before his referral to our department. The remaining one was unfit for operation.

 

Data of this study included; demographic details, radiologic findings, surgical details and outcome during the follow up period. Five patients were referred from other hospitals    with an initial biopsy suggesting the diagnosis.  These cases were mismanaged as neck nodes in other places and the treating surgeons did perform open biopsies without proper preoperative evaluation.  The other cases diagnosed clinically and radiologically in our hospital and confirmed by postoperative histopathology. We avoided the need for preoperative biopsy. All patients were subjected to complete clinical evaluation, duplex scan, CT scan with angiography and selective angiography (Figure 2).

 

Our goal was to excise the tumor completely without neurovascular compromise. The surgical procedures are briefly described as follows (Figure 3a, b and c): the patient is under general anesthesia with endotracheal intubation. Wide transverse cervical incision was achieved to provide good exposure of the tumor and the carotid vessels controlled proximally and distally. Careful dissection to preserve the adjacent cranial nerves (vagus, hypoglossal, superior laryngeal and mandibular branch of the facial nerve). Certain precautions were applied to reduce the bleeding before tumor resection as using gentle blunt dissection in the adventitial plane, ligation of the feeding vessels supplying the tumor, ligation of ECA and use of electrocautery. Any undesirable lesions of the vessel wall are immediately managed by vascular surgeon via    primary vascular repair or vascular reconstruction. After complete haemostasis, wound closure with suction drain application. Clinical evaluation and follow up was accomplished to all patients. The patients were evaluated clinically and by douplex scan every 3 months for the first year and each 6 months later on in a regular outpatient visits

 

 

 

Results

A total of 16 patients were presented in the study period and they were 10 women and 6 men and their age ranged from 22 to 75 years (mean 42±19). All patients were presented with unilateral painless lump in the neck. In addition to that one case presented with bilateral and  multicenteric paragangelioma with no elevation of catecholamine secretion, which had been confirmed by laboratory investigations and another case, who presented with difficulty in deglutition, hypoglossal nerve paresis, and cervical lymphadenopathy in addition to neck swelling, who proved to be malignant CBT.

 

Twelve out of the sixteen cases accepted to have surgery and they were 7 women and 5 men and their age ranged from 33 to 65 years (mean 46±13). Five tumors (42%) were located in the right side and seven (58%) in the left side. None of the patients had a functioning CBT that presented with hypertension, palpitation and tachycardia due to elevated catecholamines level. Complete excision of the tumor was performed to all cases. According to Shamblin classification, it was found that Shamblin group1 included 2 patients, group II included 4 cases, and group III were 6 patients (table 1).

 

 Sex patients with Shamblin group I and II, subadventitial tumor excision was performed after ligation of the feeding vessels of the tumor and 3 of them were in need for ligation of the ECA and primary vascular repair of the internal carotid artery (ICA) was needed in another patient. The remaining 6 patients with Shamblin group III, ECA ligation was done in 5 patients, primary vascular repair of the ICA was needed in 3 patients and ICA reconstruction by saphenous vein graft was accomplished in another patient.

 

Postoperative hemiparesis occurred in 2 patients with Shamblin III, one of them improved in 3 months after surgery, while the other one was permanently affected. Postoperative cranial nerve complications occurred in 3 patients, 2 of them with transient hypoglossal paresis and the remaining one developed hoarseness of voice due to permanent vocal cord paralysis.

 

All postoperative specimens diagnosed histopathologically to be benign paraganglioma except in one case that proved to be malignant CBT. This case was in need for intraoperative vascular reconstruction by saphenous vein graft and it was the case that complicated postoperatively with permanent hemiparesis. This patient transferred to oncology department for adjuvant postoperative radiotherapy. All patients were followed up from 6 - 46 months (mean 22 ± 12) with no local recurrence or mortality.

 

 

 

 

 

 

 

 

 

Table (1): Operative findings and posto[erative complications

 

Shamblin group

No.

 Tumor

size (cm)

Operative finding

Complications

ligation

of ECA

Primary

vascular repair

Saphenous

vein graft

Cerebral ischaemia

Hypoglossal paresis

Hoarseness

I

2

2-2.5

-

-

-

-

-

-

II

4

2.5-3.5

3

1

-

-

1

-

III

6

3.5-8

5

3

1

2

1

1

Total No.

12

 

8

4

1

2

2

1

 

 

 

 

 

 

 

 

 

Discussion

CBTs in the head and neck area impose a dilemma and their treatment is challenging for the surgeons. Most CBTs are benign and slow growing and surgical excision is the treatment of choice when the patient is young and fit. Some authors have found that radiotherapy is effective in inhibiting further growth of CBTs, However, it is often considered to be an alternative treatment modality for patients who can not undergo surgery due to extensive involvement (11).

CBTs tend to occur slightly more often in women (3); and that is parallel to the reported incidence in our cases. In this study 16 cases were diagnosed as CBTs in our department during the study period. Four of these patients did not have surgery due do different reasons. This does not seem to be surprising since many other studies showed cases that did not have surgical treatment for the same reasons(8,14).   

 

Five cases referred to us from other physicians with definite preoperative histological diagnosis after their misdiagnosis as neck nodes and they had been biopsied.  This is surprising since all these cases went for biopsy without prior neck ultrasound scan, which is an essential minimum prerequisite in management of these cases.  It is needless to say that preoperative open biopsy or even percutaneous needle biopsy are contraindicated (12) . These may cause intractable bleeding, pseudo aneurysm formation and carotid artery thrombosis.

 

The main purpose of the surgery is to remove all neoplastic tissue, saving the nearby important neurovascular structures of the neck. Surgical resection of CBTs was performed to all the studied cases with special maneuvers to facilitate and make the surgical procedure safer via wide transverse cervical incision, dissection and controlling the carotid vessels proximally and distally, and then subadventitial dissection of the carotid vessels and early ligation of the feeding vessels. These performed steps were reported in many other studies (8, 13- 14).

As CBTs are close to important vessels and nerves in the neck, so there is a risk of morbidity and mortality, which is variable. The incidence of ICA injury has been reported to be 2% to 23% with or without reconstruction (8,15-16). The sacrifice of ECA and ICA has been reported to be needed from 13-39% and 11% respectively (8,16). In our study, ligation of the ECA was done in 8 patients (67%), while primary vascular repair of ICA in 4 patients (33%) and reconstruction by using saphenous vein graft in one patient (8%). It was noticed that the incidence of vascular complications in our study was higher than the previous studies because this study included cases with more advanced tumors.

Postoperative cerebrovascular complications such as stroke can occur with or without manipulation of major neck vessels, and its incidence has been reported to be 0 to 11% (16-19). In our study, 2 patients developed postoperative cerebral ischaemia, one of them was transient and improved by conservative measures and the other case with permanent left sided hemiparesis (8%).

 

Postoperative neurological complications as cranial nerve deficits can occur, and the incidence of postoperative affection ranges from 6.9-42%. The hypoglossal and vagus nerve appeared to be the most vulnerable to injury from the sacrifice or retraction (8). Regarding to our postsurgical neurological complications; 2 cases showed temporary tongue deviation that may be due to retraction of the hypoglossal nerve and both cases improved spontaneously; while one patient developed permanent postoperative hoarseness (8%) due to vocal cord paralysis. These findings are parallel to the results of other studies(9,15,18,19). Postoperative mortality was not encountered in our cases. However, it is not unusual hazard after surgery especially in Shamblin III(8).

In this study it has been noticed that all patients with permanent postoperative neurovascular complications and 80% of patients who had carotid artery reconstruction were referred to Shamblin group III .These results also support the reports that the Shamblin classification can be used to predict the possible postoperative neurovascular complications (10,15-22).

 

 

Conclusions:

Patients with CBT in our locality are usually presented with an advanced stage. Early diagnosis and surgical resection of these tumors will minimize the morbidity and carry good surgical outcome. A team approach including head and neck and vascular surgeons are essential to achieve good surgical results.

 

 

 

 

 

 

 

 

 

 

 

 

References

1-Persky MS, Setton A, Niimi Y, Hartman J, Frank D, Berenstein A. Combined endovascular and surgical treatment of head and neck paragangliomas: a team approach. Head Neck 2002; 24(5):423-431.

2-Lack  EE, Cubilla AL, Woodruff JM, Farrar HW. Paragangliomas of the head and neck region.Cancer 1977;39: 397-409.

3- Saldana MJ, Salem LE, Travezan R. High altitude hypoxia and chemodectomas. Hum Pathol 1973; 4:251–263.

4- Fanning JR, Woods FM, Christian HJ. Metastatic carotid body tumour. Report of the case with the review of literature. J Am Med Assoc 1963;185: 49.

5- Patetsios P, Gable DR, Garrett WV, et al. Management of carotid body paragangliomas and review of a 30 years experience. Ann Vasc Surg 2002;16: 331–338.

6-Muhm M, Polterauer P, Gstottner W, et al. Diagnostic and therapeutic approaches to carotid body tumors: review of 24 patients. Arch Surg. 1997; 132(3):279-284.

7-Gordon-Taylor G. On carotid tumours. Br J Surg 1940; 28(110): 163-172.

8- Lim J-Y, Kim J, Kim SH, et al. Surgical Treatment of Carotid Body aragangliomas: Outcomes and Complications According to the Shamblin  Classification. Clinic Experiml Otorhinolaryngol 2010; 3(2):91-95.

9-Van der Bogt KE, Vrancken Peeters MP, van Baalen JM, Hamming JF. Resection of carotid body tumors: results of an evolving surgical technique. Ann Surg 2008; 247(5):877-884.

10-Shamblin WR, ReMine WH, Sheps SG, Harrison EG Jr. Carotid body tumor (chemodectoma): clinicopathologic analysis of ninety cases. Am J Surg 1971; 122(6):732-739.

11-Voorda AL, Jacobson N, Anttmen J. Slowely growing pulmonary metastases

of malignant cervical chemodectomas. Acta Oncol 1994; 34:77–78.

12-Zaharopoulos P. Diagnostic challenges in the fine-needle aspiration diagnosis of carotid body paragangliomas: report of two cases. Diagn Cytopathol 2000;23:202-7.

13- Biassi GM, Mingazzini PM, Miani S, Ruberti U. Carotid body tumor Mediterranean Leaque of Angiology and Vascular Surgery March 1996;31-37.

14- Singh D, Pinjala RK, Reddy RC, et al. Management for carotid body paragangliomas_Interact CardioVasc Thorac Surg 2006; 5: 692–695

15-Makeieff M, Raingeard I, Alric P, Bonafe A, Guerrier B, Marty-Ane C. Surgical management of carotid body tumors. Ann Surg Oncol. 2008;15(8): 2180-2186.

16-. Luna-Ortiz K, Rascon-Ortiz M, Villavicencio-Valencia V, Herrera- Gomez A. Does Shamblin’s classification predict postoperative morbidity in carotid body tumors? A proposal to modify Shamblin’s classification. Eur Arch Otorhinolaryngol 2006; 263(2):171-175.

17- Carroll W, Stenson K, Stringer S. Malignant carotid body tumor. Head Neck 2004;26(3): 301-306.

18-. Wang SJ, Wang MB, Barauskas TM, Calcaterra TC. Surgical management of carotid body tumors. Otolaryngol Head Neck Surg 2000; 123(3):202-206.

19-. Sajid MS, Hamilton G, Baker DM. A multicenter review of carotid body tumour management. Eur J Vasc Endovasc Surg 2007; 34(2): 127-130.

20-Westerband A, Hunter GC, Cintora I, et al. Current trends in the detection and management of carotid body tumors. J Vasc Surg 1998; 28(1):84-92.

21- Arora M, Kohli A, Singh G. Surgical management of carotid body tumors: GOVT. medical college jammu experience. Ind J Thorac Cardiovasc Surg 2011; 27(2):  88-90.

22- Sanh A, Oz K, Ayduran E, et al., Carotid body tumors and our surgical approaches .Ind J Otolaryngol Head Neck Surg 2012; 10: 1007.

 

 

 

 

Figure (1 a): Bilateral carotid body tumor as shown by CT angiography

 

 

Figure (1 b): Abdominal paraganglioma of the same patients as shown by CT angiography of the abdomen confirming the multicenteric nature of the case.

 

 

Figure (2): Digital subtraction angiography of the right carotid artery showing a huge hyypervascular CBT.

 

Figure (3 a): Intraoperative photo showing the tumor mass and controlling the CCA and the ICA.

 

 

Figure (3 b): Intraoperative photo after complete resection of the CBT and primary repair of the ICA.

 

 

Figure (3 c): Post operative CBT measuring about 7 cm, Shamblin III.

 

 

 

 

 

 

 

 

 

 

 

الملخص العربى

 

 

العوارض الإكلينكية  ونتائج الجراحة لاورام الجسم السباتى فى صعيد مصر:دراسة استرجاعية

عمر عبد الرحيم, كمال عبد العال حسانين,أحمد  سيف الإسلام , خالد ناصر

 

جراحة عامة ,جراحة الوجه والفكين ,  جراحة الاوعية الدموية، جراحة المخ والاعصاب

 

كلية طب سوهاج جامعة سوهاج

 

تعد أورام الجسم السباتى من أورام الرقبة النادرة , وحيث أنها تنشا عند ملتقى الشريان السباتى بالرقبة وقريبة من الأعصاب المخية, ولهذا  يمثل التدخل الجراحى لإستئصالها خطورة على حياة المريض وكذلك فى حدوث مضاعفات ما بعد العملية.وقد هدف هذا البحث لدراسة  اعراض هذه الاورام وتقييم نتائج العلاج الجراحى لها .

وقد تناول هذا البحث دراسة استرجاعية للعوارض الاكلينيكية لهذه الأورام وطرق تشخيصها والطرق الجراحية التى تم اجراؤها لاستئصال هذه الاورام  وقد تم تسجيل  النتائج الجراحية والمضاعفات اثناء و ما بعد العملية .

 

وقد اشتمل البحث على عدد 16 مريضا ممن يعانون من ورم الجسم السباتى بعد التشخيص الاكلينكى وبواسطة الاشعة التشخيصية  وقد تم عمل العلاج الجراحى لإثنى عشرة حالة فقط  ممن وافقوا على إجراء العملية .

وبعد دراسة المضاعفات الناتجة  من عمليات إستئصال أورام الجسم السباتى , وجد أن حالتين تعرضوا لشلل نصفى منهم حالة تحسنت بالعلاج التحفظى, والأخرى لم يطرأ عليها  أى تحسن ملحوظ, وحالتين تعرضوا لشلل مؤقت للعصب المخى الثانى عشر والحالة الأخيرة تعرضت لخشونة مستديمة فى الصوت نتيجة لإصابة العصب الحنجرى المرتجع أثناء العملية. وقد لوحظ أن أغلب هذه المضاعفات,حدثت نتيجة  للعلاج الجراحى للحالات المتأخرة والتى لم يتم تشخيصها مبكرا .

وبمتابعة المرض لفترة تتراوح من 6-46 شهر لم تحدث هناك أى حالات إرتجاع للورم أو أى حالات وفيات .

ونستنتج من هذه الدراسة:

-التشخيص الاكلينيكى لحالات أورام الجسم السباتى فى صعيد مصر عادة ما تكون فى مراحل متأخرة.

-التشخيص المبكر لمثل هذه الحالات يقلل من مخاطر التدخل الجراحى.

-لابد من تعاون  فريق عمل يضم جراح الوجه والرقبة وجراح الأوعية الدوية والشرايين للحصول على نتائج جراحية جيدة.