High rate of bilaterality in internal auditory canal metastases

AM ER IC AN JOURNAL OF OT OLA RYNGOLOGY– H E A D A N D NE CK M E D ICI N E AN D S U RGE RY 3 6 (2 0 1 5) 7 98 – 8 0 4

Available online at www.sciencedirect.com

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High rate of bilaterality in internal auditory canal metastases☆ Michael T. Chang, BS, Elias M. Michaelides, MD⁎ Yale University School of Medicine, Section of Otolaryngology, 800 Howard Ave, 4th Fl, New Haven, CT

ARTI CLE I NFO

A BS TRACT

Article history:

Purpose: Presentation of three cases of metastatic carcinoma to the internal auditory canal

Received 27 May 2015

bilaterally, as well as a systematic review of the literature regarding the characteristics of these lesions. Materials and methods: Using a MEDLINE Ovid search (1946–2015), we identified and reviewed 102 cases of metastatic carcinoma to the internal auditory canal. Metrics recorded include: patient age, sex, tumor type, laterality, past oncologic history, co-occurring metastatic sites, clinical findings, radiographic findings, therapy received, and outcome. Cases of unilateral versus bilateral IAC were compared. Results: Remarkably, 52.9% reported cases of internal auditory canal metastases have bilateral occurrence. The most common primary tumor sites for internal auditory canal metastases were lung (21.2%), skin (18.6%), and breast (16.7%), with lung and skin cancers having the highest rates of bilateral metastasis. Meningeal metastasis occurred at a much higher rate in bilateral cases (47.2%) versus unilateral cases (8.5%). Brain parenchymal metastasis also occurred at a higher rate in bilateral cases (38.2%) versus unilateral cases (19.2%). Outcomes for cases of internal auditory canal metastases are generally poor, with 56.3% of unilateral cases and 86.1% of bilateral cases reporting patient death within 5 years from diagnosis. Conclusions: In cases of internal auditory canal metastasis, clinicians should carefully assess for not only contralateral disease but also additional metastatic disease of the central nervous system. Rapid-onset hearing loss, tinnitus, vertigo, or facial palsy should raise suspicion for internal auditory canal metastasis, particularly in patients with a known oncologic history. Published by Elsevier Inc.

1.

Introduction

Metastatic carcinoma in the internal auditory canal (IAC) or cerebellopontine angle (CPA) is uncommon, representing only

☆

0.3%–0.7% of all lesions in this space [1,2]. However the IAC comprises roughly one quarter of metastatic sites in the temporal bone, second most after the petrous apex [3,4]. Metastasis from distant primary carcinomas to temporal bone

Funding source: none. ⁎ Corresponding author at: Yale Physicians Building, 800 Howard Ave, 4th Fl, New Haven, CT 06519. Tel.: +1 203 785 2593; fax: +1 203 785 3970. E-mail addresses: [email protected] (M.T. Chang), [email protected] (E.M. Michaelides).

http://dx.doi.org/10.1016/j.amjoto.2015.06.002 0196-0709/Published by Elsevier Inc.

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sites most frequently occurs by hematogenous spread, cerebrospinal fluid (CSF) dissemination, or extension from adjacent meninges [5]. Here we present a systematic review of the international literature on IAC metastases from distant primary sites as well as introduce three new cases of metastatic carcinomas to the IAC bilaterally from prostatic carcinoma, pulmonary adenocarcinoma, and malignant melanoma. We focus on unique attributes of carcinomas that have bilateral IAC involvement, including tumor type, clinical features, radiographic features, and co-occurring sites of metastases.

2.

Materials and methods

2.1.

Search strategy and criteria

profound sensorineural hearing loss bilaterally. Gadoliuniumcontrast magnetic resonance imaging (MRI) of the head revealed bilateral IAC enhancements, with a 29 × 4 mm lesion on the right and a 8 × 3 mm lesion on the left (Fig. 1A, B). Also of note was an extra-axial mass in the anterior fossa floor measuring 2.1 × 2.1 × 2.8 cm. CSF cytopathology revealed the presence of melanoma cells. The diagnosis of metastatic melanoma to bilateral IAC was made. Given the extent and growth rate of the lesion, the patient underwent whole brain radiation with chemotherapy and steroid treatment. While the patient gained some preservation of hearing on the left side, he experienced permanent loss of hearing on the right side. The patient continued to have a neurocognitive decline and ultimately died from complications related to extensive brain metastasis 4 months into treatment.

3.2. We conducted a MEDLINE Ovid search (1946–2015) using the terms “metastasis” and “internal auditory canal” or “cerebellopontine angle.” By searching the references of the articles yielded by this search, we identified additional cases. Articles were included if they presented the original case descriptions of distant metastasis to the IAC or CPA. Articles were excluded if they were not written in the English language or if they were not available through a multiinstitutional library search. All cases of primary malignancy arising from the IAC were excluded. Because we wanted to focus on distant metastases, cases were excluded if the IAC metastasis occurred by contiguous spread from an adjacent primary site. Cases were also excluded if they involved distant carcinomas metastasizing to primary tumors, known as collision tumors.

2.2.

Data collection and analysis

Both authors independently reviewed relevant articles. The following metrics were recorded for each case when available: patient age, sex, tumor type, laterality, past oncologic history, co-occurring metastatic sites, clinical findings, radiographic findings, therapy received, and patient outcome. In addition to characterizing various properties of IAC metastases as a whole, we also compared characteristics between unilateral and bilateral cases of IAC metastasis. We used the student t test or chi-squared test to determine statistical significance, set at p < .05.

Case reports

3.1.

Case 1: metastatic melanoma

A 64 year-old male with a 20-year history of BRAF-mutant melanoma presented to an otolaryngologist after 10 days of acute onset bilateral hearing loss and 2 years of progressively worsening balance, headache, and tinnitus. Of note, ten years prior he had neck and axillary lymph node metastases requiring radical neck and axillary dissection with adjuvant chemotherapy and immunomodulatory agents. On exam he was noted to have severe difficulty with balance and decreased hearing bilaterally. Pure tone audiometry showed

Case 2: metastatic prostate carcinoma

A 76-year-old male with a 3-year history of metastatic prostate cancer to the paranasal sinuses presented to his otolaryngologist after acute onset of right-sided facial weakness, and progressively worsening bilateral deafness and tinnitus. At the time he was being treated for prostate cancer by chemotherapy and yearly androgen suppression therapy. On exam he was found to have right-sided facial weakness (House–Brackmann grade 5) and saccadic motions with right head thrust. Audiometry evaluation revealed profound hearing loss on the right and moderate hearing loss on the left. Videonystagmography showed reduced vestibular function bilaterally. Gadolinium-contrast MRI showed a 3.5 × 1.7 cm extra-axial lesion in the right IAC as well as a nodular enhancement in the left IAC. There was substantial infiltration of the facial nerve bilaterally. The diagnosis of metastatic prostate cancer to bilateral IAC was made. The patient subsequently underwent an orchiectomy to reduce tumor load. Because of the extent of his metastatic disease, a conservative approach was taken in management of his IAC metastases with steroids and palliative whole-brain radiation. The patient had mild hearing improvement on the left side but had no improvement in hearing or tinnitus on the right side. At 27-month follow up, the patient was alive and still undergoing systemic chemotherapy and androgen suppression therapy with no major radiographic changes in tumor size.

3.3.

3.

799

Case 3: metastatic lung adenocarcinoma

A 76-year-old female with a 20-pack year smoking history presented to her primary care physician after a fall. Upon further questioning, it was found that she was experiencing a rapid decline in balance and bilateral facial weakness. Physical examination by an otolaryngologist revealed sensorineural hearing deficit on the left side, bilateral facial weakness (House–Brackmann grade 3) delayed saccades bilaterally. Audiogram showed left profound sensorineural hearing loss with 0% speech discrimination and right normal hearing with 100% speech discrimination. Serial gadoliniumcontrast MRIs revealed rapid expansion of a left IAC mass from 0 × 0 cm to 6 × 6 × 11 cm over the course of three months. Additionally seen was a nodular enhancement

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AM ER IC AN JOURNAL OF OT OLA RYNGOLOGY– H E A D A N D NE CK M E D ICI N E AN D S U RGE RY 3 6 (2 0 1 5) 7 98 – 8 0 4

Fig. 1 – Bilateral melanoma IAC metastases: (A) Axial and (B) coronal view of T1-weighted MRI with gadolinium contrast showing metastatic melanoma to the IAC bilaterally.

of the facial nerve in the right IAC. The tumor was initially thought to be a vestibular schwannoma, however, after PET scan revealed a right lung mass, the patient underwent a lung biopsy which revealed adenocarcinoma. CSF cytopathology was positive for malignant adenocarcinoma cells. A diagnosis of metastatic pulmonary adenocarcinoma to the meninges and bilateral IAC was made. At the time this manuscript was written, the patient was beginning a course of systemic chemotherapy.

4.

Results

A total of 122 cases of metastatic carcinoma to the IAC or CPA were found using our MEDLINE Ovid search criteria. Thirteen

articles were excluded because they were either not written in English or not available through a multi-institutional library search. Four cases of collision tumors were excluded. Six cases of contiguous spread from an adjacent primary site were excluded. Including the 3 cases we report here, a final number of 102 cases of IAC metastases were included in this review. Patient demographic information and oncologic histories are summarized in Table 1. The mean age of all reported cases was 54.0 years. Sixty-one percent of patients were male. Age and gender of patients did not have a statistically significant difference between unilateral and bilateral cases of IAC metastasis. Out of cases that reported previous oncologic history (N = 95), symptoms from IAC metastasis were the first sign of malignancy in 29 (30.5%) cases. Fifty-eight (61.5%)

Table 1 – Summary of patient demographic information and oncologic history for all cases of IAC/CPA metastasis and analysis of statistical significance between unilateral and bilateral groups.

Number of Cases Mean Age Sex Male n (%) Female n (%) Primary Tumor at Time of IAC Met Known, n (%) Unknown, n (%) Not reported, n (%) Mean Time from Diagnosis of Primary to Diagnosis of IAC Met (years)

All Cases

Unilateral Cases

Bilateral Cases

P Value

102 54.0

48 53.4

54 54.3

0.791

61 (59.8) 41 (40.2)

26 (54.2) 22 (45.8)

35 (64.8) 19 (35.2)

0.250 0.617

58 (56.9) 36 (38.3) 8 (7.8) 4.4

26 (54.2) 18 (37.5) 4 (8.3) 4.1

32 (59.3) 18 (33.3) 4 (7.4) 4.8

0.431 1.000 0.602

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Table 2 – Summary of primary sites (A) and tumor histological subtypes (B) seen in IAC metastases. A Primary Site

Total (%) cases

Unilateral

Bilateral

Lung Skin Breast Gastrointestinal Head & Neck Pancreas Kidney Prostate Thyroid Neural Lymphoma Reproductive Tract Bone Unknown

22 19 17 9 6 5 4 4 3 3 2 2 1 5

6 7 11 4 5 0 3 3 3 2 1 1 1 1

16 12 6 5 1 5 1 1 0 1 1 1 0 4

(21.6) (18.6) (16.7) (8.8) (5.9) (5.0) (3.9) (3.9) (2.9) (2.9) (2.0) (2.0) (1.0) (5.0)

%Bilateral 72.7% 63.2% 35.3% 55.6% 16.7% 100.0% 25.0% 25.0% 0.0% 33.3% 50.0% 50.0% 0.0% 80.0%

B Histological subtype

Total (%) cases

Unilateral

Bilateral

%Bilateral

Adenocarcinoma Malignant melanoma Squamous cell carcinoma Invasive ductal carcinoma Renal cell carcinoma Papillary thyroid Primitive neuroectodermal Other a

40 (39.2) 23 (22.5) 7 (6.9) 6 (5.8) 3 (2.9) 3 (2.9) 2 (2.0) 18 (17.6)

17 7 5 5 3 3 2 6

23 16 2 1 12

57.5% 69.6% 28.6% 16.7% 0% 0% 0% 66.7%

a

Other includes cases of unreported histology (N = 11) or single case reports of papillotubular breast carcinoma, signet ring cell pancreatic carcinoma, myxopapillary ependymoma, undifferentiated nasopharyngeal carcinoma, histiocytic lymphoma, malignant fibrous xanthoma, and sarcoma.

patients that developed IAC metastases had a known history of malignancy, with 50 of these patients having undergone prior oncologic treatment prior to development of IAC metastasis. The mean time interval from diagnosis of primary tumor to IAC metastasis was 4.4 years. IAC metastases were discovered as early as 2 months after initial diagnosis of primary carcinoma [6] and as late as 20 years after diagnosis of a primary carcinoma as presented in our patient with metastatic melanoma. The mean interval from diagnosis of primary to IAC metastasis did not differ significantly between unilateral and bilateral groups. The most common sites of a primary tumor (Table 2A) were lung (21.2%), skin (18.6%), and breast (16.7%). Overall, tumors from 21 different primary sites have been reported as metastatic to the IAC. Additionally there have been 5 cases of IAC metastasis from an unknown primary [7–11]. The most common tumor histological subtypes to metastasize to the IAC (Table 2B) were adenocarcinoma (39.2%) and malignant melanoma (22.5%). Remarkably, 54 of 102 (52.9%) cases of IAC metastases occurred bilaterally, including all 3 cases we report here. The primary sites with the highest rate of bilateral metastasis included lung (16 of 22, 72.7%) skin (7 of 12, 63.2%), pancreas (5 of 5, 100%), and carcinomas of unknown primary (4 of 5, 80%). The tumor histological subtypes with the highest rate of bilaterality included malignant melanoma (16 of 23, 69.6%) and adenocarcinoma (23 of 40, 57.5%).

A summary of reported metastases co-occurring with IAC metastases is provided in Table 3. Overall, 63 (61.7%) patients with IAC metastasis were found to have metastatic disease at other sites at the time of presentation, with approximately equal rate of other metastatic disease in bilateral (50.9%) and unilateral (47.4%) cases. Notably, cases of bilateral IAC metastasis had a higher rate of co-occurring metastatic disease in the CNS than unilateral cases. Meningeal metastasis occurred at a much higher rate in bilateral IAC cases (47.2%) versus unilateral cases (8.5%). Of 30 patients with known leptomeningeal carcinomatosis, 26 (86.6%) had bilateral disease. Brain parenchymal metastasis also occurred at a higher rate in bilateral cases (38.2%) versus unilateral cases (19.2%). The most common reported metastatic sites outside of the CNS include lymph node (10.8%), lung (10.8%), vertebra (9.8%), liver (8.8%), and adrenal gland (8.8%). The IAC was the solitary metastatic site in 38.2% cases. The signs and symptoms present at the time of initial evaluation are summarized in Table 4. Almost all reported cases of IAC metastases were symptomatic (96.1%). The most common presenting symptoms were hearing loss (77.5%), facial nerve palsy (50.0%), vertigo (33.3%), tinnitus (27.5%), and balance difficulty (17.6%). Hearing loss was the most common symptom on initial presentation in both bilateral (85.5%) and unilateral (66.7%) lesions.

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Table 3 – Co-occurring sites of metastatic disease present in cases of IAC metastases. Metastatic Site CNS Meninges Brain Parenchyma Spinal Cord Bone Vertebra Skull (excluding IAC) Long Bone Pelvis Other Lymph Node Lung Liver Adrenal Gland Kidney Spleen Heart Small Intestine Thyroid Skin Sinus Pancreas Testes Retroperitoneum Colon Bladder No Other Known Mets

N (%) cases

Unilateral IAC Met

Bilateral IAC Met

31 (30.4) 30 (29.4) 4 (3.9)

5 9 1

26 21 3

10 (9.8) 6 (5.9) 3 (2.9) 2 (2.0)

4 3 2 1

6 3 1 1

5 6 2 5 0 1 1 0 1 1 1 0 0 0 1 1 25

6 5 7 4 5 2 2 2 1 1 1 1 1 1 0 0 14

11 (10.8) 11 (10.8) 9 (8.8) 9 (8.8) 5 (4.9) 3 (2.9) 3 (2.9) 2 (2.0) 2 (2.0) 2 (2.0) 2 (2.0) 1 (1.0) 1 (1.0) 1 (1.0) 1 (1.0) 1 (1.0) 39 (38.2)

Management of IAC metastases varied widely depending on tumor type, extent of metastatic disease, patient comorbidities, prior therapy, and treatment goals. In cases where management decisions were reported (N = 78), 39 patients (50.0%) underwent therapy involving some combination of surgery, chemotherapy, whole brain radiation (WBRT), and stereotactic radiosurgery (SRS). Twenty-four patients (30.8%) underwent combination therapy of surgery with radiation (WBRT or SRS or both). Five patients (6.4%) underwent surgery with both chemotherapy and radiation [12–16]. Fifteen (19.2%) patients underwent surgery only, 3 (3.8%) underwent chemotherapy only [16,17], 4 (5.1%) underwent WBRT only [3,16–18], and 2 (2.6%) underwent SRS only [19,20]. 16 (21.6%) patients did not undergo any therapy because either they elected not to or they died before therapy could be initiated. Outcomes for patients with IAC metastasis were generally poor. In 68 cases where patient follow up was reported, 48.6% of all patients with IAC metastasis died within 6 months, 61.4% within 1 year, and 71.4% within 5 years. Cases of bilateral metastasis had a much higher rate of death compared with cases of unilateral metastasis at 6 months (66.7% vs 31.3%), 1 year (77.8% vs 46.9%), and 5 years (56.3% and 86.1%). Given the high variation in tumor type and management strategies, it is difficult to draw conclusions from this data set with respect to efficacy of various treatment strategies.

5.

Discussion

Diagnosis of IAC metastasis can be difficult for multiple reasons. IAC metastasis can often go unrecognized because

Table 4 – Signs and symptoms present at initial otolaryngology evaluation in reported cases of IAC/CPA metastasis. Symptom

N (%) cases

Unilateral IAC Met

Bilateral IAC Met

Hearing loss Facial palsy Vertigo Tinnitus Balance difficulty Headache Facial pain Visual disturbance Otalgia Otorrhea Asymptomatic

79 (77.5) 51 (53.4) 34 (33.3) 28 (27.5) 18 (17.6) 12 (11.8) 9 (8.8) 8 (7.8) 3 (2.9) 2 (2.0) 4 (3.9)

32 28 16 13 6 7 6 4 1 2 2

47 23 18 15 12 5 3 4 2 0 2

temporal bone imaging is not routinely included in metastatic workup. Additionally the diagnosis may be overlooked as symptoms can be overshadowed in the setting of more widespread metastatic disease. Furthermore, clinical and radiographic features of unilateral IAC lesions can mimic vestibular schwannomas [21,22] or meningiomas [13] while bilateral IAC lesions can mimic neurofibromatosis type 2 [23–27]. Nonetheless metastatic carcinoma should be considered in the differential diagnosis because of its potentially dire outcomes. Remarkably, we found that IAC metastases occur bilaterally in over half of cases. While we acknowledge that this high rate may in part reflect a reporting bias, similar rates of bilateral occurrence have been found in smaller reviews of temporal bone metastases [3,28]. The mechanism of bilateral spread is likely attributed to the distribution of malignant cells throughout the meninges and cerebrospinal fluid (CSF) [29,30]. We found a remarkably higher rate of CNS metastatic disease in bilateral cases compared with unilateral cases. One study of 33 temporal bone specimens noted that 100% of patients with meningeal metastasis also had metastatic disease at the IAC [30]. Bilateral disease often occurs with leptomeningeal carcinomatosis, evidence that adjacent meningeal spread may play a key role in disseminating tumor cells bilaterally [29]. In this review, 86.6% of patients with meningeal disease had bilateral IAC metastasis. Malignant cells in the CSF may be a predictor of bilateral metastasis, however CSF cytology has a false negative rate of 10%–50% for predicting leptomeningeal carcinomatosis [11,31]. In the cases that reported CSF cytopathology, 66.7% of patients with bilateral disease had presence of malignant cells in CSF. Past reviews suggest that the most common cancers that metastasize to the IAC are those with a propensity for bone invasion, including breast, lung, prostate, kidney, and colon [3]. This review confirms that breast and pulmonary carcinomas are among the most frequent tumors that metastasize to the IAC, and additionally introduces melanoma as another major cancer that metastasizes to the IAC. Importantly, however, we also find that tumors of several types from almost any primary site can metastasize to the IAC.

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Patients suspected of having IAC lesions should undergo full neurotologic evaluation. Clinically, rapidly progressive cochleovestibular or facial nerve complaints reflecting a rapidly expanding tumor should raise suspicion of IAC metastasis, particularly in patients with a known history of malignancy [32]. While metastasis to the IAC frequently occurs in patients with a known history of malignancy, initial clinical presentation can be caused by an IAC metastasis before an occult primary or another metastatic site [11,17,28,33,34], as described in one of our cases here. Thus metastatic carcinoma should always be a consideration when working up a cochleovestibular or facial nerve complaint. Even if a primary tumor has been treated, IAC metastasis can arise several months or years after treatment of a primary tumor [15,35,36]. MRI with gadolinium contrast is the imaging modality of choice in detecting IAC lesions as they frequently enhance on T1-weighted images. Though IAC metastases on MRI appear similar to vestibular schwannomas, metastases may be distinguished by the presence of adjacent extranodular extension while schwannomas typically have contrast enhancement confined to the mass [37]. Computed tomography (CT) evaluation of the temporal bone may not show any abnormal findings [19,38]. Biopsy may be required to definitively differentiate between vestibular schwannoma and metastatic tumor [32]. Given the high rate of bilateral occurrence, evidence of IAC metastasis on one side should warrant careful workup of the contralateral side. Unilateral symptoms are not necessarily indicative of unilateral disease, as patients with bilateral metastases may also have only unilateral symptoms [16]. IAC metastasis should also raise suspicion of metastatic lesions in the brain parenchyma and meninges, particularly in the presence of bilateral IAC lesions. Patients should undergo thorough neurological testing and imaging when an IAC lesion in found. Additionally, because IAC metastasis often co-occurs with other metastatic sites, patients should undergo total body imaging to detect additional metastatic sites. We find here that some of the most common metastatic sites outside of the CNS include vertebrae, lungs, liver, and adrenal glands. In many cases, however, we find that metastasis to the IAC is solitary without other distant metastatic sites [33,39,40], as in the patient with lung cancer presented here. Outcomes of IAC metastasis are generally poor, likely attributed to their anatomic proximity to critical neurologic structures as well as their propensity to occur late in a patient’s oncological course when there is already extensive metastatic disease. Patients with bilateral IAC metastases had a remarkably higher percentage of deaths at 6-months, 1year, and 5-years compared with unilateral IAC metastases. Bilateral IAC metastases may indicate a high load of malignant cells in the CSF, as additional metastatic disease can arise at other CNS sites several months after resection of the IAC lesion [17,22]. Additionally, a second metastasis can arise on the contralateral side several months after resection of an initial IAC metastatic tumor, as demonstrated in two cases [25,38]. The management of IAC metastasis is a multifactorial decision based on the type of cancer, extent of metastatic disease, patient comorbidities, and treatment goals.

6.

803

Conclusion

Though uncommon, metastatic carcinoma should be an important consideration in the diagnosis of IAC lesions as they can cause potentially devastating symptoms. Any rapidly progressive cochleovestibular or facial symptom should raise suspicion for IAC metastasis, especially in patients with a prior history of malignancy. Involvement of both sides should be considered in the workup as many IAC metastases occur bilaterally. IAC metastases should prompt extensive full body workup given its tendency to co-occur with other metastatic sites. In particular, IAC metastases frequently occur with metastatic disease at other CNS sites, thus warranting thorough clinical and radiographic neurological workup.

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