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Malignant tumours of the minor salivary glands - a 20 year review
M.J. Strick. C. Kelly, J.V. Soames, N.R. McLean

Presented at the British Association of Plastic Surgeons, Birmingham, July 2000; and at the International Congress of Maxillofacial Surgeons, Edinburgh, may 2000.

The UK incidence of malignant disease of the minor salivary glands is only 0.6 per million per year. The tumours have a varied histology, can present in any age group and are frequently advanced if located in the sinonasal cavities.

In a 20-year review of 21 patients treated for minor salivary gland malignancy in a single institution, it was found that mucoepidermoid tumours were more common in the oral cavity and adenoid cystic carcinomas in the sinonasal tract (p = 0.002). Outcome was variable with sinonasal and adenoid cystic carcinoma having a poorer outcome. Kaplan-Meier curves showed that oral tumours had a higher probability of long term survival.

Radical surgery with reconstruction and post-operative adjuvant radiotherapy was effective in achieving loco-regional control. There were no local recurrences within 5 years and three after 5 years. Five patients developed metastatic disease within 10 years and a further two after 10 years. Late recurrences occurred and survival was mainly determined by the presence of systemic disease. 

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Malignant tumours of the minor salivary glands - a 20 year review
M.J. Strick (a,*), C. Kelly (b), J.V. Soames (c), N.R. McLean (a)

(a) Head and Neck Unit, Department of Plastic and Reconstructive Surgery, Royal Victoria Infirmary, Queen Victoria Rd, Newcastle-upon-Tyne, UK

(b) Department of Clinical Oncology, Northern Regional Centre for Cancer Treatment, Newcastle General Hospital, Newcastle-upon-Tyne, UK

(c) Department of Oral Pathology, The Dental School, Newcastle-Upon-Tyne, UK

Presented at the British Association of Plastic Surgeons, Birmingham, July 2000; and at the International Congress of Maxillofacial Surgeons, Edinburgh, may 2000.

KEYWORDS
Head and neck neoplasms; Malignant tumours; Minor salivary glands

Summary The UK incidence of malignant disease of the minor salivary glands is only 0.6 per million per year. The tumours have a varied histology, can present in any age group and are frequently advanced if located in the sinonasal cavities. In a 20-year review of 21 patients treated for minor salivary gland malignancy in a single institution, it was found that mucoepidermoid tumours were more common in the oral cavity and adenoid cystic carcinomas in the sinonasal tract (p = 0.002). Outcome was variable with sinonasal and adenoid cystic carcinoma having a poorer outcome. Kaplan-Meier curves showed that oral tumours had a higher probability of long term survival.

Radical surgery with reconstruction and post-operative adjuvant radiotherapy was effective in achieving loco-regional control. There were no local recurrences within 5 years and three after 5 years. Five patients developed metastatic disease within 10 years and a further two after 10 years. Late recurrences occurred and survival was mainly determined by the presence of systemic disease.

Minor salivary gland malignancies are uncommon accounting for between 10 and 15% of all salivary tumours, the incidence in the UK being only 0.6 per million per year. (1) Unlike the major salivary glands where approximately 80% of tumours are benign, (1,2)80% or more of minor salivary gland tumours are malignant (1.2) and they tend to have a great variation in presentation and histology. (1,3)

There are between 450 and 750 minor salivary glands in the head and neck region, (1) scattered throughout the sinonasal cavities, oropharynx, larynx (4) and trachea with the majority being found in the oral cavity. (1) Heterotopic minor salivary glands can also occur at unexpected sites including lymph nodes, the capsule of the thyroid gland, facial bones and the hypophysis. (1,5,6) All types of salivary tumours, both benign and malignant, can occur at any of these sites, including heterotopic locations (5,6) thus accounting for their varied presentation.

The mainstay of treatment of malignant minor salivary gland tumours is complete surgical resection, but there is controversy as to appropriate margins of excision, the role of radiotherapy and the management of the neck. (1,7) The purpose of this study was to review the management of all malignant minor salivary gland tumours presenting to the Head and Neck Oncology Clinic at Newcastle General Hospital over a 20-year period with a view to guiding future patient management.

Patients and methods

In the 20-year period (1980-2000) the case notes of all patients treated for malignant tumours of the minor salivary glands at the Head and Neck Oncology Clinic were reviewed. Malignant tumours of the parotid, submandibular and sublingual salivary glands were excluded. Data were collected from the operating records and pathology database, the histological slides were examined and surviving patients reviewed in the head and neck clinic. The staging of all cases was based on the TNM classification of the American Joint Committee on Cancer (AJCC) and histological typing was according to the World Health Organisation classification of sali vary tumours.

Details of initial presentation, diagnostic inves tigations, histology, surgical and adjuvant treat ment, patterns of local, regional and systemic recurrence and survival were recorded and evaluated.

All patients had a standard work up including examination under anaesthesia, biopsy to achieve a tissue diagnosis prior to treatment and appropriate imaging detailing local and metastatic disease (Fig. 1).

The follow-up period was defined as the time from the first therapeutic intervention to date of most recent clinic review or death of the patient. Disease free interval was defined as the time from the first therapeutic intervention to diagnosis of recurrent disease whether local, regional or distant.

Statistical analysis of the results was carried out with standard statistical tests and the Kaplan-Meier method. Statistical computations were performed using the Statistical Package for Social Sciences (SPSS)-for-Windows software (SPSS Inc., USA). Survival rates and disease recurrence data were used to determine the significance of independent prognositic indicators against survival and recurrence.

image showing a biopsy to achieve a tissue diagnosis prior to treatment

Figure 1 CT Can showing advanced minor salivary gland tumour of the maxillary sinus

Results

In the 20-year period (1980-2000) 21 patients with minor salivary gland malignancies were seen (15 males and six femaLes), the median age at presen tation being 54 years of age (range 34-80 years).

The most common clinical presentation was a mass in the oral cavity (50%), followed by a blocked or bleeding nose (30%), infra orbital nerve anaes thesia (10%) and orbital pain. (10%).

There were five different histological tumour types found, the most common being adenoid cystic carcinoma (seven patients) followed by mucoepi dermoid carcinoma (Table 1). Three of the adenoid cystic tumours were of predominantly cribriform type and four of predominantly solid type. Three mucoepidermoid carcinoma were graded histo logically as low and three as high grade tumours. Five patients had polymorphous low-grade adenocarcinomas whilst two patients had carcinoma ex pleomorphic adenoma and one patient had an adenocarcinoma not otherwise specified (Fig. 2(A)- (C)).

Table 1: Histolgical Type
Adenoid cystic carcinoma 7
Mucoepidermoid carcinoma 6
Polymorphous low grade adenocarcinoma
 5
Carcinoma ex pleomorphic adenoma 2
Adenocarcinoma 1
image of figure 2a - 2c showing histology maging

Figure 2a - 2c : Histology (A) Adenoid cystic carcinoma showing cribiform pattern and perineural spread. (B) Muc0epidermoid carcinoma-well differentiated tumour. (C) Polymorphous low grade adenocarcinoma-variable morphology

Histological evidence of perineural spread was noted by the pathologist in six cases (four being adenoid cystic carcinoma, one mucoepidermoid carcimoma, and one adenocarcinoma not otherwise specified). Intravascular tumour was noted in two cases (one mucoepidermoid carcinoma and one adenocarcinoma not otherwise specified). Intra lymphatic tumour was present in one case of mucoepidermoid carcinoma.

The most common anatomical sites of these tumours were the hard and soft palate or the maxillary antrum (Table 2, Fig. 3). Mucoepidermoid tumours were more common in the oral cavity while adenoid cystic carcinomas appeared to have a predilection for the sinonasal tract. Polymorphous low-grade adenocarcinomas and the carcinoma ex pleomorphic adenomas occurred in the oral or oropharyngeal region. This difference in anatomical distribution for different tumour types attained statistical significance using the Mann-Whitney U test (p = 0.002).

All stages of disease were seen at presentation (Table 3). More than half of the patients presented with advanced disease in stages lll and IV Late presentation was attributed to tumours frequently occurring in anatomically inaccessible sites such as the maxillary antrum and ethmoid sinuses.

Table 2: sites of Occurrence
Hard and soft paLate 5
Maxillary antrum 5
Lip or buccaL mucosa 3
Nasal cavity 2
RetromoLar trigone 1
Tongue base
 1
Ethmoid sinus 1
Floor of mouth
 1
 Pharynx 1
image of figure 3 showing distribution of minor salivary gland malignancies

Figure 3 Distribution of minnor salivary gland malignancies showing anatomical locations of different histological types

Treatment of the primary disease consisted of a combination of surgery and radiotherapy. Che motherapy played no part in the treatment of primary disease, being considered only for pallia tion of widespread metastatic disease.

Surgical excision aimed for resection with at least a 1 cm margin of clearance and included maxillectomy or partial maxillectomy (10 patients), excision of orbit or orbital contents (two patients) with one patient requiring an access craniotomy, rim mandiblectomy (two patients) and partial excision of palate (three patients). In three patients complete resection was possible by means of wide local excision and direct closure (Table 4). Complete excision with histologically clear margins was achieved in nine cases all of these were in the oropharyngeal cavity. None of the eight cases of sinonasal tumours had clear excision margins on histology due to the advanced nature of the disease at presentation (stages III or IV) and the predomi nance of adenoid cystic carcinoma.

Five patients required neck dissections, indi cated by palpable neck disease or suspicious lymph nodes on CT/MRI scan. Four had primary neck dissections, only one of whom had positive lymph nodes on histology. One patient subsequently developed neck disease at 2 years and a neck dissection revealed positive Lymph nodes. In both positive cases the tumour type was mucoepider moid carcinoma (one high grade, the other low grade).

Table 3: Tumour stage at presentation
Stage I 5
Stage II 4
Stage III 6
Stage IV 6

Reconstructive surgery was required in the majority of patients, with seven patients having free flap reconstruction (four radial forearm flaps, and three rectus abdominis flaps). Local skin and buccal mucosal flaps were required in one patient and seven patients had split skin grafts and dental obturators.

Table 4: Tumour Excisions
Maxillectomy or partial maxillectomy 10
Partial excision of palate 3
 Rim mandibulectomy 2
Excision of orbit or orbital contents 2
Wide Local excision 4
images of figure 4 showing a kaplan-meier curve survival-all minor salivary gland malignancies
image of figure 5 showing a kaplan-Meier curve survival by anatomical site
image of figure 6 showing a kaplan-meier curve survival by mucoepider-moid vs adenoid cyctic carcinoma

Seventeen patients were treated with radio therapy. In two cases, the tumour was too advanced or the patient too unfit for surgery, and radiotherapy was used as the sole treatment. More commonly, (15 cases) patients had planned post-op radiotherapy, the indications for which included large tumour bulk, tumour at or close to the resection margin, histologically high grade tumours and evidence of perineural, intravascular or intralymphatic spread. Applying these criteria, all adenoid cystic tumours (7), both of the carcinomas ex pleomorphic adenoma, half of the mucoepidermoid tumours (3/6) and one of the polymorphous low-grade adenocarcinomas required radiotherapy. In 16 (of 17 cases), external beam radiotherapy was used. In 10 of these cases, 50 Gray was delivered in 20 fractions over 4 weeks, three patients had 50 Gray in 20 fractions over 6 weeks and two patients 63 Gray in 30 fractions over 6 weeks. One patient had 38 Gray in 19 fractions over 4 weeks in order to limit radiation to the globe in the orbit. One patient, who had radiotherapy as his initial treatment, had implantation of radioactive gold grains delivering a total of 70 Gray. During primary treatment all cases had radiotherapy delivered to the tumour bed and prophylactic radiotherapy of the neck was not undertaken.

Radiotherapy was also used for the treatment of recurrent disease. One had radiotherapy for the treatment of local recurrence, two for cerebral and two for spinal metastases.

Only one patient had chemotherapy, methotrexate and folinic acid being given for adenoid cystic brain metastasis in the region of the cavernous sinus.

Patients were followed for up to 13 years (range 1 -13 years) with a median of 5 years. Three patients developed local recurrences, (two adenoid cystic and one mucoepidermoid carcinoma). All three local recurrences occurred after 5 years. Seven patients (five adenoid cystic and two mucoeidermoid) developed distant disease most commonly in the brain (4) and Lung (3). Five patients developed metastatic disease within 10 years. A further two patients, with adenoid cystic carcinoma, developed late distant recurrences (after 11 years), justifying our policy of long term follow-up.

Twelve patients were clinically tumour free at last follow-up. Of these two had adenoid cystic carcinoma, three mucoepidermoid carcinoma, five polymorphous low grade adenocarcinoma and two carcinoma ex pleomorphic adenoma.

The overall crude 5-year survival was 78% which by 10 years had fallen to 40%.

Disease free survival was 89% at 2 years and 75% at 5 years. Four patients were followed up for longer than 10 years, of these two were disease free. One had adenoid cystic carcinoma and one carcinoma ex PSA.

Survival was evaluated by means of Kaplan Meier curves which plot survival probabilities (95% confidence interval). The curve for all tumours included in the study showed a steady decline over 14 years mainly due to metastatic disease (Fig. 4).

The Kaplan-Meier curve for all histological subtypes comparing survival for different anatomical sites showed that oral tumours had a significantly higher probability of long term survival than sinonasal tumours (95% confidence interval) (Fig. 5). The difference in survival over the follow-up period for oral tumours as compared to sinonasal tumours achieved a significance of p = 0.008 using the Mann-Whitney U test.

Similarly the Kaplan-Meier curve comparing mucoepidermoid with adenoid cystic tumours showed that over 6 years the survival for adenoid cystic tumours was poorer (95% confidence interval) (Fig. 6). Although on comparing equivalent TNM stages for mucoepidermoid and adenoid cystic tumours neither the difference in survivaL (p = 0.49 for stages Ill and IV) nor disease free interval (p = 0.37 for stages III and IV} achieved statisticaL significance.

There was no clear statistically significant correlation between type of tumour and gender (p = 0.09) or age of patients (p = 0.5), or survival for gender (p = 0.07) or age (p = 0.12). Tumour size (p 0.13), TNM stage (p = 0.08) and margin status (p = 0.12) did not achieve statistical significance as prognostic indicators. Histologically high grade tumours on (i.e. solid adenoid cystic carcinomas and high grade mucoepidermoid carcinomas) were not associated with a statistically significant poorer outcome possibly due to small sample size. Our previous study on adenoid cystic carcinoma in major and minor salivary glands did, however, show poorer survival for high grade adenoid cystic carcinoma. (8)

Discussion

This study confirms that minor salivary gland malignancies are uncommon and that adenoid cystic carcinoma and mucoepidermoid caricinoma are the most frequent histological types.(1,2,9) Mucoepidermoid carcinoma occurred most often in the oral cavity whereas adenoid cystic carcinoma had a propensity for the sinonasal tract, consistent with the series reported by Lopes. (7) Although Weber et al. reported that in lip and buccal mucosa a diagnosis of adenoid cystic carcinoma was the most likely, 10 Lopes and others have also reported that the most common intraoral site for minor salivary gland malignancies was the palate, usually the hard palate but also the soft palate, (2,3,7) as in the present series. Various authors have indicated that the proportion of minor salivary gland malignancies which are either adenoid cystic or mucoepidermoid tumours is higher than that for the parotid glands (3,11) and our results support this observation.

In this series, the median age at presentation was 54 years with the youngest patient being 34 years and the oldest patient 80 years. Bradley reported a peak incidence in the third and fourth decades (1) and also noted an equal sex distribution, whereas, in the present study there were more males than females (ratio of 3:1).

Although the most frequent clinical presentation was a swelling in the oral cavity, other symptoms such as nasal obstruction were related to the anatomical location of the tumour rather than histological type. In contrast, symptoms due to nerve involvement were associated with adenoid cystic carcinoma where perineural spread is common and associated with a poorer prognosis. (12,13,14)

Preoperative imaging is essential to delineate the extent of the tumour, particularly those located in inaccessible areas as such tumours are frequently advanced on presentation. (15) In the present series, some tumours had invaded into adjacent cavities such as the maxillary sinus and nasal cavity. Imaging by either CT or MRI scan was also helpful in identifying suspicious cervical lymph nodes although they cannot differentiate with certainty between reactive and metastatic nodes. (16) In the present series, surgical excision aimed at achieving complete clearance with a 1 cm margin, frequently requiring extensive surgery. A single procedure was carried out with a one-stage reconstruction, using a free flap if necessary. Wide local surgical clearance may be compromised by proximity to vital structures such as the brain and cranial nerves.15 Where histology showed tumour present at or close to the surgical resection margin, post-operative radiotherapy was given. Adjuvant radiotherapy appeared to improve the prognosis in these cases since incomplete excision did not achieve significance as a prognostic indicator.

A low rate of cervical lymph node metastasis for minor salivary gland malignancies has been noted previously; Lopes et al. reported 3.8% incidence of neck node metastasis. 7. Of the 21 patients in the present study, five had indications for neck dissections with only two positive for metastatic disease (9.5%), both in patients with mucoepidermoid carcinoma. Our results were consistent with those of Matsuba et al. who found that cervical metastasis for adenoid cystic carcinoma of the major or minor salivary glands was rare. 9 However, adenoid cystic carcinoma has a tendency to spread by the vascular rather than lymphatic system. 6 In our series, pulmonary, cerebral and spinal metastases of adenoid cystic carcinoma were identified consist ent with a vascular mechanism of spread. In contrast there were no metastases to regional lymph nodes.

The outcome in this series was dependant on the anatomical site and the histological subtype. Sinonasal and adenoid cystic tumours had a poorer prognosis. Huang et al. similarly found that salivary maxillary antrum tumours had a poorer prognosis than palatal salivary tumours. (12) In the present study, there was a statistically significant difference in the anatomical location of the different tumour types with adenoid cystic carcinoma being more common in the sinonasal region (p = 0.002) and mucoepidermoid carcinoma more prevalent in the oral cavity. It may be that these two variables which independently predicted outcome were related i.e. adenoid cystic carcinoma (which had a poorer prognosis) occurs more frequently in the sinonasal cavities and sinonasal tumours tended to be advanced at the time of presentation. It can be hypothesised that adenoid cystic carcinoma has a predilection for the sinonasal cavities and a propensity to invade nerves and bone, which, coupled with the likelihood of late diagnosis for tumours hidden in the sinonasal cavities, leads to large tumours invading close to vital structures which are thus difficult to cure.

Several authors have reported that adenoid cystic carcinoma has a decreased recurrence free and overall survival, with tumour size, margin status and grade independently associated with decreased survival. (6,7,10,17) Cribriform adenoid cystic carcinomas are also reported to carry a better prognosis than solid types. (6,8,10,12,13) Using the Kaptan-Meier method our results concur that adenoid cystic carcinoma is associated with poorer survival. However, differences in outcome related to tumour size, TNM stage, margin status or histological grade did not achieve statistical significance, possibly due to small sampLe size.

The diagnosis of polymorphous low grade adeno carcinoma carried a good prognosis with no local or distant recurrences and no deaths. Polymorphous low grade adenocarcinomas have variable morphologies and may be mistaken for other tumours such as pleomorphic adenoma or adenocarci noma.(1,18) Generally, adenocarcinoma is aggressive and has a poor prognosis (18,19) and this was certainly the case with our single patient. Polymorphous low grade adenocarcinoma is a separate entity and follows a relatively indolent course (18) and differentiation from other histological types is essential for determining accurate prognosis and treatment.

In this series of patients late recurrences occurred, with a 10 year survival of only 40%. Many (57%) of the recurrences (locaL, pulmonary and cerebral metastases) occurred after 5 years with some (cerebral, pulmonary and spinal metastases) even appearing after 10 years (28%). Long term follow-up is essential in view of this tendency to late recurrence shown in this and other studies. (9,10)

Our management included radical surgery with reconstruction and radiotherapy as needed. Local control was usually achieved with only three of the 21 patients having locaL recurrence (14%), one of them had an ethmoid sinus tumour which was diagnosed late. Distant recurrences were more common. Our results suggest that our indications for surgery and adjuvant radiotherapy were effective in achieving local control. This is consistent with the suggestion of Weber et al. that combined therapy improves local and regional control. (10) Similarly Matsuba et aL. showed significantly better local control rates in patients with adenoid cystic carcinoma with combined treatment than in patients treated by surgery alone. (9) Adjuvant radiotherapy for salivary malignancy is advocated by several authors.(1,4,12,15,20)

The Kaplan-Meier curve for survival for minor salivary glands tumours for all tumour types in this study shows a steady decline in survival, mainly due to metastatic disease. Other authors have reported that distant metastases remain the principle cause for treatment failure. (6,21)

In conclusion, minor salivary gland malignancies are rare tumours with varied histology and can occur in any age group including younger patients. They may present late particularly when they occur hidden in the sinonasal cavities. Outcome is variabLe and is influenced by tumour type and anatomical location of the tumour, sinonasal and adenoid cystic carcinoma having a statistically poorer outcome. In our experience radical surgery with reconstruction and post-operative adjuvant radiotherapy in appropriate cases is effective in achieving loco-regional control. Local and systemic late recurrences occur. Long term survival outcome is determined mainly by systemic spread of disease.

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