Acta Oto-Laryngologica. 2015; Early Online, 1–7

ORIGINAL ARTICLE

Lesions involving the jugular foramen: clinical characteristics and surgical management

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WEI LI1,2 & CHUNFU DAI1,2 1

Otology & Skull Base Surgery Department and 2Hearing Medicine Key Laboratory of Ministry of Health, Eye Ear Nose & Throat Hospital, Fudan University, Shanghai, China

Abstract Conclusion: Lesions involving the jugular foramen (JF) present as various diagnoses. Pulsatile tinnitus is more common in glomus jugulare (GJ) tumors, whereas otalgia and facial nerve paresis are more prevalent in temporal bone malignancies (TBMs). Preoperative facial nerve electroneurography (ENoG) was significantly correlated with postoperative facial nerve function. Objective: To describe the diagnosis and surgical management of lesions involving the JF. Methods: The charts were reviewed for 38 patients who had lesions involving the JF, including 14 patients with TBMs, 11 with GJ tumors, 7 with cholesteatomas, 2 with facial nerve schwannomas, 2 with JF schwannomas, and 2 with cholesterol granulomas. The follow-up data were recorded. Results: The most frequent symptoms included hearing loss (89.47%), followed by otorrhea (47.37%) and pulsatile tinnitus (39.47%). With respect to TBMs, 57.14% of patients complained of otorrhea and otalgia, and 50.00% presented with facial nerve paresis. Among the 13 patients with facial nerve paresis, 53.85% were diagnosed with TBMs. Regarding GJ tumors, 81.82% had pulsatile tinnitus and hearing loss. Among the 25 patients with normal preoperative facial nerve function, the mean facial nerve ENoG reduction was 29.48 ± 29.15%, and the mean postoperative facial nerve score was 77.48 ± 33.13. The correlation coefficient was –0.973 (p = 0.000).

Keywords: Glomus jugulare tumors, temporal bone malignancies, schwannoma, electroneurography, cholesteatoma, cholesterol granuloma

Introduction The anatomy of the jugular foramen (JF) is complex. It contains the lower cranial nerves and major vascular structures. Lesions involving the JF exhibit significant diagnostic and surgical challenges. A large variety of lesions may develop or be identified in the JF. These lesions arise from structures within the foramen or from adjacent structures [1]. The most frequent intrinsic lesions are glomus jugulare (GJ) tumors, schwannomas of the lower cranial nerves, and meningiomas [2,3]. The extrinsic lesions include squamous cell carcinomas, chondrosarcomas, chordomas, and cholesteatomas, among other tumors [1]. Because many neural and vascular structures pass through the JF, the

lesions that develop in this area exhibit a wide clinical spectrum [4]. For intrinsic lesions involving the JF, previous studies demonstrated that GJ tumors account for approximately 60–80% of cases [5]. The estimated incidence is 1 in 1.3 million people [6]. These highly vascularized, aggressive lesions infiltrate the adjacent bone tissue, cranial nerves, and blood vessels [7]. The most common presenting symptoms include pulsatile tinnitus and hearing loss. A mesotympanic mass is characteristic but may be absent [8]. Temporal bone malignancies (TBMs) are the most common extrinsic lesions involving the JF. These lesions frequently originate from the external auditory canal or deep lobe of the parotid gland and extend into the middle ear. However, the lesions occasionally

Correspondence: Chunfu Dai, Department of Otology and Skull Base Surgery, Eye and ENT Hospital, Fudan University, 83 Fenyang Road, Shanghai, 200031, China. Tel: +86 02164377134. Fax: +86 02164377151. E-mail: [email protected]

(Received 13 October 2014; accepted 16 December 2014) ISSN 0001-6489 print/ISSN 1651-2251 online  2015 Informa Healthcare DOI: 10.3109/00016489.2014.1003094

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W. Li & C. Dai

Table I. Demographic characteristics of patients by lesion type. Total (n = 38)

GJ tumor (n = 11)

TBMs (n = 14)

CT (n = 7)

FNS (n = 2)

JFS (n = 2)

CG (n = 2)

Gender female (%)

55.26

54.55

57.14

28.57

50.00

100.00

100.00

Side, left (%)

55.26

72.73

62.86

42.86

50.00

100.00

50.00

Age (years)

47.05

47.18

55.36

36.71

40.50

43.50

34.50

PTA (dB)

59.79

53.73

60.71

85.29

42.00

42.00

33.00

Characteristic

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CG, cholesterol granuloma; CT, cholesteatoma; FNS, facial nerve schwannoma; GJ, glomus jugulare; JFS, jugular foramen schwannoma; PTA, pure-tone audiometry; TBM, temporal bone malignancy.

involve the JF while extending inferiorly. These patients may present with other symptoms, such as pulsatile tinnitus and progressive lower cranial nerve deficits, which are similar to those of GJ tumors. Differentiation of these tumors during the early stages is necessary. Although various histopathological categories exist, squamous cell carcinomas are the most commonly observed and account for 80% of cases [9]. Basal cell carcinoma, adenoid cystic carcinoma, adenocarcinoma, melanoma, and various sarcomas are among the other malignancies arising within the temporal bone [10]. Numerous studies concerning intrinsic JF lesions have been conducted, but few studies have addressed both intrinsic and extrinsic JF lesions. In this study, we retrospectively reviewed 38 patients who had lesions involving the JF. The clinical presentation, diagnoses, management, and outcome (including complications) are discussed.

Material and methods The charts of patients who had lesions involving the JF that were operated on by the senior author from May 2006 to December 2013 were reviewed. The data were reviewed specifically for age, sex, presenting symptoms, results of the neurologic examinations, location and extent of the lesions, surgical management, postoperative outcomes, and follow-up findings. The extent of lesion removal was determined by the intraoperative findings and radiologic follow-up. Postoperative complications were recorded. The preoperative clinical assessment included neurologic examinations, hearing tests, facial nerve electroneurography (ENoG), and assessment of vocal cord function. Temporal bone high-resolution computed tomography (HRCT) and magnetic resonance imaging (MRI) were performed for the radiologic diagnosis. Digital subtraction angiography (DSA) was performed for diagnosis and to guide the preoperative embolization in cases of highly vascularized lesions. Facial nerve function was graded according to the House-Brackmann (H-B) and Burres-Fisch

scales. Intraoperative facial nerve monitoring was conducted. The follow-up consisted of periodic clinical evaluations with pure-tone audiometry (PTA) and HRCT and/or MRI scans. Results Demographic characteristics The demographic characteristics are presented in Table I. The sample consisted of 38 patients diagnosed with lesions involving the JF. Among them, 14 patients had TBMs, 11 patients had GJ tumors, 7 patients had cholesteatomas, 2 patients had facial nerve schwannomas, 2 patients had JF schwannomas, and 2 patients had cholesterol granulomas. Among the 14 patients with malignancies, the pathological diagnoses were as follows: 9 cases of squamous cell carcinoma, 2 cases of adenoid cystic carcinoma, 2 cases of chondrosarcoma, and 1 case of ceruminous adenocarcinoma. The mean age of the 38 patients was 47.05 years (range 28–72 years). Twenty-one cases (55.26%) were left-sided and 17 cases (44.74%) were right-sided. There were 21 (55.26%) females and 17 (44.74%) males. Preoperative embolization was performed in 13 patients, including the 11 patients with GJ tumors, and 2 other patients with mimicked GJ tumors. Of the two patients with mimicked GJ tumors, one patient had a facial nerve schwannoma (Figure 1), and the other patient had squamous cell carcinoma, which is a highly vascularized tumor, as demonstrated by enhanced MRI and DSA (Figure 2). The mean follow-up time was 28 months (range 2–98 months). Clinical manifestations The most frequent symptoms included conductive hearing loss (n = 34, 89.47%) followed by otorrhea (n = 18, 47.37%), pulsatile tinnitus (n = 15, 39.47%), otalgia (n = 14, 36.84%), and facial nerve paresis (n = 13, 34.21%) (Table II). More specifically, among the 14 patients with TBMs, 11 patients (78.57%)

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Lesions involving the jugular foramen

Figure 1. A patient with a facial nerve schwannoma. A mass located in the jugular foramen exhibited marked contrast enhancement (star) on an MRI image with contrast. The jugular bulb was compressed (arrow).

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The preoperative examinations identified five patients with deficits of the lower cranial nerve, including one patient with a GJ tumor, two patients with TBM, one patient with JF schwannoma, and one patient with cholesterol granuloma. The patient with a GJ tumor had a chief complaint of hoarseness and tinnitus (not pulsatile) for 1 year. An examination revealed right-sided vocal cord palsy and tongue hemiatrophy, and the tongue was deviated to the right side. A patient with TBM presented with a 5-month history of hoarseness, facial nerve paresis, and dysphagia. Another patient with TBM presented with a 1-month history of hoarseness and facial nerve paresis, and her tongue was deviated to the left side. A patient with JF schwannoma complained of dysphagia for 4 months, and her tongue was deviated to the left side (Figure 3). The patient with cholesterol granuloma suffered paresthesia of the posterior portion of the tongue for 2 months. In these five patients, the most commonly affected nerves included the glossopharyngeal, vagal, and hypoglossal nerves. Treatment

experienced hearing loss, 8 patients (57.14%) complained of otorrhea and otalgia, and 7 patients (50.00%) presented with facial nerve paresis. Among the 11 patients with GJ tumors, 9 patients (81.82%) had pulsatile tinnitus and hearing loss. Of the 15 patients with pulsatile tinnitus, 9 (60%) patients were diagnosed with GJ tumors. Thirteen patients had preoperative facial nerve paresis (H-B grade III–VI), including seven cases of malignancy, four cases of cholesteatoma, one case of GJ tumor, and one case of facial nerve schwannoma.

Figure 2. A patient with squamous cell carcinoma. A mass located in the the jugular foramen exhibited marked contrast enhancement (star). The right cerebellar hemisphere appeared compressed by the mass (arrow).

All of the patients in this series were operated on by the senior author. Gross total removal of the lesions was achieved in 36 of the 38 cases (94.74%) and confirmed by postoperative serial radiological evaluation. Subtotal removal of the lesion was accomplished in one GJ tumor due to extensive bleeding during the operation, and one JF schwannoma due to the giant tumor. For all 11 patients with GJ tumors, preoperative angiography and embolization were performed. We applied the infratemporal fossa type A (IFT-A) approach with anterior facial nerve rerouting. The tumors were completely excised in 10 of the 11 patients (90.91%); subtotal removed was attained in 1 case due to extensive bleeding. The modified IFT-A approach was used in 6 of the 14 patients with TBMs, i.e. the fallopian canal bridge technique was applied. The other eight patients underwent the combined transmastoid-transcervical approach. Selective supraomohyoid neck dissection was performed in all cases. Nine patients underwent a superficial parotidectomy, whereas five patients underwent a total parotidectomy. Twelve cases (85.71%) received radiotherapy postoperatively. In addition, two patients with squamous cell carcinoma and chondrosarcoma received concomitant chemotherapy. We applied the combined transmastoidtranscervical approach [11,12] with the fallopian bridge technique to the seven patients with cholesteatoma and two patients with cholesterol granuloma.

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Table II. Symptoms and findings (% of patients) by lesion type. Total (n = 38)

GJ tumor (n = 11)

TBMs (n = 14)

CT (n = 7)

FNS (n = 2)

JFS (n = 2)

CG (n = 2)

Hearing loss (%)

89.47

81.82

78.57

100.00

50.00

50.00

50.00

Otorrhea (%)

47.37

27.27

57.14

85.71

50.00

0.00

0.00

Pulsatile tinnitus (%)

39.47

81.82

14.29

28.57

50.00

0.00

50.00

Otalgia (%)

36.84

36.36

57.14

0.00

0.00

50.00

50.00

FN paresis (%)

34.21

9.09

50.00

57.14

50.00

0.00

0.00

Hoarseness (%)

7.89

9.09

14.29

0.00

0.00

0.00

0.00

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Finding

Dysphagia (%)

5.36

0.00

7.14

0.00

0.00

50.00

0.00

Deviated tongue (%)

7.89

9.09

7.14

0.00

0.00

50.00

0.00

CG, cholesterol granuloma; CT, cholesteatoma; FN, facial nerve; FNS, facial nerve schwannoma; GJ, glomus jugulare; JFS, jugular foramen schwannoma; TBM, temporal bone malignancy.

For the two patients with JF schwannomas, we applied the IFT-A approach in patients with a JF schwannoma due to a giant tumor in the JF. For the two patients with facial nerve schwannomas, the combined transmastoid-transcervical approach was used. One of the patients had a preoperative ENoG reduction of 83%, although his facial nerve function was normal (H-B grade I) with occasional facial spasm. During the operation, the mass was found to surround the mastoid segment of the facial nerve. To achieve total tumor removal, the facial nerve was sacrificed, and then a greater auricular

Figure 3. A patient with jugular foramen (JF) schwannoma. An axial contrast-enhanced MR image showed a large tumor with a high, inhomogeneous signal in the left JF. The right hypoglossal nerve was clearly displayed (arrow), while the left hypoglossal nerve was compressed by the mass (star).

nerve graft was performed. We performed VII–XII nerve anastomosis on another patient.

Complications Among the 25 patients with normal preoperative facial nerve function, 14 (56%) experienced facial nerve paresis postoperatively, including 10 patients with GJ tumors, 1 patient with a TBM, 1 patient with a facial nerve schwannoma, and 2 patients with JF schwannomas. Among the 10 GJ tumor patients, 3 patients had postoperative H-B grade II facial nerve function, and 7 had postoperative H-B grade III. The patient with TBM presented with postoperative H-B grade IV facial nerve function, and facial nerve grafting was not performed given his advanced age, postoperative radiotherapy, and poor prognosis. The two patients with a JF schwannoma had H-B grade II facial nerve function after 6 months. Another patient with a facial nerve schwannoma received a greater auricular nerve graft and displayed H-B grade III facial nerve function at the 1-year follow-up. For analysis purposes, we used the Burres-Fisch scale to grade the facial nerve function. Among the 25 patients with normal preoperative facial nerve function, the mean ENoG reduction was 29.48 ± 29.15%, and the mean postoperative facial nerve score was 77.48 ± 33.13. The distribution is presented in Figure 4. We used a bivariate Pearson’s correlation analysis (SPSS Statistics 16.0, Chicago, IL, USA) to determine whether the ENoG reduction was correlated with postoperative facial nerve function. The correlation coefficient was –0.973 (p = 0.000), and the correlation was statistically significant. Two patients, including a facial nerve schwannoma case and a TBM case, experienced postoperative cerebrospinal fluid leakage, which was managed successfully using a conservative strategy. No

Lesions involving the jugular foramen

5

100.00

Facial nerve score

80.00

60.00

40.00

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20.00

0.00 0.00

20.00

40.00

60.00

80.00

100.00

ENoG reduction (%) Figure 4. The scatter diagram of electroneurography reduction and the postoperative facial nerve score revealed a negative correlation between the two variables.

patients developed new lower cranial nerve palsy postoperatively. Prognosis During the follow-up period (mean 28 months, range 2–98 months), five patients died, including three squamous cell carcinoma cases, one adenoid cystic carcinoma case, and one ceruminous adenocarcinoma case. For the GJ tumor and JF schwannoma with subtotal removal, no obvious growth was revealed by clinical and radiological follow-up. No recurrence or death was noted in the other patients. Discussion A large variety of intrinsic or extrinsic lesions may develop or be identified in the JF, but the incidence is low. Numerous studies concerning intrinsic JF lesions have been published, but only a few studies address both intrinsic and extrinsic JF lesions. Most patients in our series had TBMs (n = 14, 36.84%); 11 patients had GJ tumors (28.95%), and 7 patients had cholesteatomas (18.42%). Two patients with facial nerve schwannoma, two patients with JF schwannoma, and two patients with cholesterol granuloma were included in this study. With regard to lesions involving the JF, GJ tumors are always considered in the diagnosis. According to the present study, other lesions such as TBMs, cholesteatomas, facial nerve schwannomas, JF schwannomas, or cholesterol granulomas (accounting for 71.05%) should be

considered. Differential diagnosis among these disorders should be carried out when a JF lesion is encountered. The clinical presentations of intrinsic JF lesions were nonspecific and included hearing loss, pulsatile tinnitus, and neuropathies affecting the cranial nerves [13], whereas the extrinsic lesions often exhibited a complex presentation and mimicked those of intrinsic JF lesions [1]. Our earlier study demonstrated that the misdiagnosis of malignancies involving the JF frequently occurs because of the lack of specific clinical manifestations during the early stages [14]. The growth of these lesions may cause facial paresis, vertigo, hoarseness, and paresis of the tongue. In more advanced cases, cerebellar symptoms and hemiparesis may occur. In this study, the most frequent symptoms included conductive hearing loss followed by otorrhea, pulsatile tinnitus, otalgia, and facial nerve paresis. For TBMs, 78.57% of patients experienced hearing loss, 57.14% of patients complained of otorrhea and otalgia, and 50.00% of patients presented with facial nerve paresis. Of the patients with GJ tumors, 81.82% of patients experienced pulsatile tinnitus and hearing loss, which is consistent with the Jackson study [8]. Nine (60%) of the 15 patients with pulsatile tinnitus were diagnosed with GJ tumors. Among the 13 patients with facial nerve paresis, 7 patients (53.85%) were diagnosed with TBMs. These lesions are frequently misdiagnosed because of the lack of specific clinical manifestations. According to our study, pulsatile tinnitus is more common in GJ tumors, whereas otalgia and facial

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W. Li & C. Dai

nerve paresis are more prevalent in TBMs. These findings can be important cues in the differential diagnosis of JF lesions. When approaching JF lesions, the facial nerve serves as a significant obstacle for adequately exposing and removing the lesions while preserving facial function. The facial nerve may be subclinically involved in the lesions, but the preoperative evaluation of facial nerve involvement may be difficult when the facial function is normal based on the H-B grading system. In the present study, among the 25 patients in this series with normal preoperative facial nerve function, the preoperative facial nerve ENoG was significantly correlated with postoperative facial nerve function. The correlation coefficient was –0.973 (p = 0.000). Similarly, Esslen [15] reported that slowly progressive tumors may cause degeneration of up to half the nerve fibers before facial nerve paresis becomes apparent. Bendet et al. [16] reported that even when the facial function is clinically intact in cases with malignant tumors, a low preoperative ENoG response may predict facial nerve involvement by the tumor. Combined with our results that suggest that the preoperative ENoG reduction was significantly correlated with postoperative facial nerve function, it is essential to predict potential facial nerve involvement and estimate the postoperative facial nerve function. A number of neurologic surgical approaches to the lateral skull base have been advocated for removing lesions involving the JF. The IFT-A approach is the predominant technique described in the literature. This technique allows the surgeon to control the JF area and surrounding vital structures, such as the internal carotid artery and jugular vein, but necessitates sacrifice of the middle ear structures and anterior transposition of the facial nerve [17,18]. Some authors have described a fallopian bridge technique, in which the facial nerve may remain within its bony canal and may not require anterior transposition [19]. In our experience, IFT-A is the best approach for resecting a greater number of vascular tumors, such as GJT tumors and some TBMs. When managing nonvascular tumors (i.e. cholesteatomas, JF schwannomas, cholesterol granulomas, and certain TBMs), a more conservative approach may be used. In such cases, we chose the combined transmastoidtranscervical approach. This approach involves performing a complete mastoidectomy. The dissection is extended more inferiorly toward the upper cervical neck to identify the vasculature and lower cranial nerves. For nonvascular or noninvasive tumors with normal facial nerve function, we performed the fallopian bridge technique. Thus, the exact surgical plan should be tailored to the individual

patient. The optimal surgical approach should be individualized and based on the lesion size and location, structures involved, level of hearing loss, lower cranial nerves, patient status, and surgeon’s experience. Despite their proximity to the lower cranial nerves, most JF lesions cause lower cranial nerve deficits late and are therefore detected at an advanced stage. In the present study, preoperative examinations revealed that only five patients (13.16%) had deficits of the lower cranial nerve, and the most commonly affected nerves included the glossopharyngeal, vagal, and hypoglossal nerves. No postoperative lower cranial nerve deficits were noted in this series of patients. In our experience, the tumor is coagulated with a bipolar cautery and carefully dissected from the pars nervosa while preserving the plane of dissection between the tumor and the medial wall of the jugular bulb. By keeping the medial wall of the jugular bulb intact intraoperatively, the lower cranial nerves at the JF are at less risk for injury. This technique can only be performed when the lesion has not invaded the medial wall of the jugular bulb or infiltrated the lower cranial nerves.

Conclusions Lesions involving the JF present as various diagnoses. Pulsatile tinnitus is more common in GJ tumors, whereas otalgia and facial nerve paresis are more prevalent in TBMs. Preoperative facial nerve ENoG was significantly correlated with the postoperative facial nerve function.

Acknowledgments This study was supported by the project on Advanced and Frontier Techniques for Shanghai Municipal Hospital (SHDC12010119) and the Shanghai Talent Program-08-039. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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Lesions involving the jugular foramen: clinical characteristics and surgical management.

Lesions involving the jugular foramen (JF) present as various diagnoses. Pulsatile tinnitus is more common in glomus jugulare (GJ) tumors, whereas ota...
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