Available online at www.sciencedirect.

com

British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

Review

Focused review of investigation, management and outcomes

of salivary gland disease in specialty-specic journals
Rory OConnor a, , David A. Mitchell b , Peter A. Brennan c
a
b
c

Nottingham University Hospitals NHS Trust, City Hospital Campus, Hucknall Road, Nottingham NG5 1PB, United Kingdom
Mid Yorkshire Hospitals NHS Trust, Pinderelds General Hospital, Aberford Road, Wakeeld WF1 4EE, United Kingdom
Portsmouth Hospitals NHS Trust, Queen Alexandra Hospital, Southwick Hill Road, Cosham PO6 3LY, United Kingdom

Accepted 17 March 2014

Available online 29 April 2014

Abstract
We review papers on diseases of the salivary glands published in journals relating to the head and neck, which are commonly read by members
of our specialty. Most of the papers focus on the investigation and treatment of diseases of the parotid gland, which reflects the relative
prevalence of parotid lesions among salivary gland diseases. Minimally invasive surgery is increasingly of interest. There is a lack of clinical
trials that address the many controversies concerning salivary gland surgery, and much of the evidence for treatment is based on small case
series and expert opinion, partly because of the relative rarity of salivary disease and the disparate groups that treat it. This problem could be
addressed if regional and national oral and maxillofacial surgery (OMFS) units, and possibly other specialties, could collaborate more closely
and combine data.
2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Keywords: Salivary gland; Parotid; Benign, Malignant; Investigation; Review; Summary

Introduction
Diseases of the salivary glands and operations to treat them
are an important area in our specialty, but although such diseases are more common than oral cancer, fewer papers have
been published in this area.1,2 A previous review, which cited
papers from this journal only, focused on improvements in
imaging and the debate about aggressive and conservative
treatment of malignant lesions.3 We have tried to cover a
larger area of recently published material.
We found 118 papers on the salivary glands that had
been published between January 2011 and December 2012 in
closely related journals. Tables 1 and 2 summarise them by
category and type, respectively, and Table 3 outlines the focus

Corresponding author. Tel.: +44 0115 969 1169.

E-mail addresses: rory.oconnor@doctors.net.uk
(R. OConnor), david.mitchell@midyorks.nhs.uk
(D.A. Mitchell), peter.brennan@porthosp.nhs.uk (P.A. Brennan).

of each article according to the area of disease investigated.

If the article included more than one salivary gland or aspect
of disease, then these were all counted. All full-length publications have been included, but case reports have been cited
only when they add something new. We accept that it will
not be all-inclusive as general surgical and pathological journals, and other specialty-specific journals also include small
amounts of relevant material. This review is designed to be
educational and specialty-specific, and is not a systematic
attempt to answer a specific question.

Investigation of salivary gland disease

Ultrasound (US) combined with fine needle aspiration
cytology (FNAC) or core biopsy examination is useful in
diagnosing diseases of the major salivary glands.4 In their
review of methods of imaging, Burke et al. found that US
was a cheap, accurate, and accessible first-line investigation

http://dx.doi.org/10.1016/j.bjoms.2014.03.016
0266-4356/ 2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

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R. OConnor et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

Table 1
Number of articles in each category.
BJOMS

H&N

IJOMS

JCMFS

JOMS

Full length
Short communication
Technical note
Letter

13
2
3
1

29
3
0
0

15
10
3
3

1
2
1
0

5
23
1
3

Total

19

32

31

32

BJOMS British Journal of Oral and Maxillofacial Surgery.

H&N Head and Neck.
IJOMS International Journal of Oral and Maxillofacial Surgery.
JCMFS Journal of Cranio-Maxillo-Facial Surgery.
JOMS Journal of Oral and Maxillofacial Surgery.
Table 2
Type of article.
BJOMS

H&N

IJOMS

JCMFS

JOMS

3
1
7
1
5
2

6
1
18
4
3
0

0
1
10
3
15
2

1
0
0
0
2
1

0
0
1
4
24
3

19

32

31

32

Review
Clinical trial
Cohort study
Comparative study
Case report or series
Procedural note
Total

BJOMS British Journal of Oral and Maxillofacial Surgery.

H&N Head and Neck.
IJOMS International Journal of Oral and Maxillofacial Surgery.
JCMFS Journal of Cranio-Maxillo-Facial Surgery.
JOMS Journal of Oral and Maxillofacial Surgery.

(with no ionising radiation)5 that differentiated malignant

from benign disease in 90% of cases, and also distinguished
between salivary stones and cystic and non-cystic disease.
They also mentioned that sialography has limitations in imaging the salivary ductal system as it is invasive and has a high
rate of failure. Magnetic resonance imaging (MRI) sialography, which is an alternative, needs further investigation.
A retrospective study of benign tumours of the superficial
lobe of the parotid found that US with FNAC was sufficient
for preoperative imaging.6 When US could not assess extension into the deep lobe or when there were features suspicious
of cancer, MRI or computed tomography (CT) confirmed
involvement of the deep lobe but added no further information
to indicate malignancy.
Lingam et al. recommended use of high-resolution US
and FNAC for pleomorphic adenoma, but found it difficult
to distinguish adenoid cystic carcinoma from polymorphous
Table 3
Summary of the focus of published articles by salivary gland.
Parotid Submandibular/sublingual Minor Total
Investigation
Treatment outcomes
Operative technique
Complicationsa

40
33
11
13

26
23
2
8

25
11
1
1

Total

97

59

38

Related to disease or its treatment.

91
67
14
22

low-grade adenocarcinoma.7 However the risk of tumour

seeding, that is associated with large bore needles and multiple passes, is small.8 Seager et al. reported a patient in whom
FNAC failed to identify malignant change in a pleomorphic
adenoma, and suggested that inconclusive results might be
improved by further aspirations.9
Nuclear scintigraphy and positron emission tomography
(PET) may be used to investigate parotid tumours when
FNAC is not diagnostic, but it is expensive and not routinely available.5 As an alternative, salivary lesions can be
investigated using core biopsy examination, which enables
histological and immunohistochemical analysis with a sensitivity of 94%, specificity of 100%, positive predictive value of
100%, and negative predictive value of 90%. Complications
are comparable to those of FNAC.10
US cannot be used to investigate tumours in the deep lobe
of the parotid because the mandible obstructs the waves; it
is also unable to demarcate the facial nerve, but does show
adjacent blood vessels. Despite a lack of consensus about
whether any imaging technique clearly shows the facial nerve
within the parotid, MRI is advised in these cases because it
is said to show perineural invasion of tumours.5,7 Clinical
assessment of the function of the nerve is the most sensitive,
pragmatic approach.
Despite the investigations available, diagnosis of rare presentations is difficult even with tissue samples for example,
Wegener granulomatosis can be misdiagnosed as chronic
inflammation.11

Sialolithiasis
Sialolithiasis has traditionally been treated by open removal
under general anaesthetic, but minimally invasive alternatives now exist. Using topical local anaesthetic and a carbon
dioxide laser to remove stones from the submandibular duct,
Yang and Chen reported that the coagulative effect of the
laser and protection of surrounding soft tissue by the hard
stone which scatters the beam, were advantages over the open
technique.12
Endoscopic investigation of ductal disease in the parotid
and submandibular glands is often useful. Gillespie et al.
identified chronic sialadenitis and ductal strictures in patients
with confirmed sialolithiasis. Retrieval of calculi and dilatation of the duct had a low complication rate (12%), and
symptoms improved in 84% of patients.13
Luers et al. endoscopically recovered calculi of less than
5 mm from the parotid and submandibular ducts using a
dormia basket or grasping forceps in 48% of patients.14 For
larger stones (more than 5 mm), or when a minimally invasive
approach has failed, endoscopically assisted sialolithectomy
can be done instead using the light of the endoscope in the
duct to guide the operation.15
Sialoendoscopy can also relieve obstructive symptoms in
Sjgren syndrome or systemic lupus erythematosus through

R. OConnor et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

endoscopic dilatation of strictures, ductal irrigation, and

steroid injection, although repeated procedures are often
required.16

Diseases of the salivary glands in children

CT and MRI have been used in children with a parotid
swelling or sinus, despite the risk of radiation-induced
complications associated with CT, the need for general anaesthesia in younger children, and the fact that US is suitable.17
The authors admitted that CT was used early in the study
when MRI was not available, but US was used in only
one patient. An investigative algorithm that used MRI and
US was subsequently designed, and FNAC was reserved
for older, cooperative children, or those having a general
anaesthetic.
In children, neoplasms of the salivary glands are rare.
They account for 0.5% (0.8/million) of reported malignancies in this group, and mucoepidermoid and acinic
cell carcinomas are the most common.18 The stage and
grade of tumour was lower than in adults, which benefits survival (95% 5-year survival compared with 59% in
adults), but also reduces the need for adjuvant radiotherapy. For mucoepidermoid carcinoma, the grade, presence
of perineural invasion, and invaded surgical margins are
important prognostic factors, though most patients can be
treated with operation alone.19 Tumours in the minor salivary glands are even rarer although overall survival is
more favourable than in adults.20 Given that irradiation
in children may disturb facial growth and lead to secondary tumours, radiotherapy should be reserved for those
with high-grade disease, invaded margins, or multinodal
involvement.1820
Children with cerebral palsy sometimes drool because
saliva pools in the floor of the mouth. Tiigime-Saar et al.
injected botulinum neurotoxin type A into the major salivary glands to produce xerostomia.21 It reduced drooling
but required general anaesthesia and the benefits lasted for
only 2 months. Without larger studies it is difficult to justify repeated injections under general anaesthesia in these
patients.

Benign diseases of the salivary glands

Parotid gland
Recently, pleomorphic adenoma has been reaffirmed as the
predominant histological variant that accounts for two-thirds
of benign tumours.22 Partial superficial parotidectomy with
formal identification of the main trunk of the facial nerve and
excision of tumour with a surrounding cuff of salivary tissue
is widely used, and porcine dermal collagen (PermacolTM ,
Covidien, Dublin, Ireland) can be used to minimise Frey
syndrome.23 Human-derived grafts are also available, but

485

DermaMatrix (DePuy Synthes, Welwyn Garden City, UK)

seems to be associated with more postoperative complications, including formation of a sialocoele, than Alloderm
(LifeCell Corporation, Bridgewater, USA).24
Extracapsular dissection, in which only adjacent branches
of the facial nerve are dissected, can also be used to remove
benign parotid tumours.25 Although the tumour and facial
nerve are often closely related, a low recurrence rate is possible after minimal resection as parotid tissue attaches more
firmly to tumour than to nerve, so the nerve can be separated
from the surrounding gland.23
Most surgeons use an antegrade approach to dissect the
facial nerve, where the main trunk is located first.26 Kanatas
and McCaul used the branch to the posterior digastric muscle
as a marker to find the main nerve.27 A proximal marker is the
tympanomastoid fissure, which Bushey et al. found to be a
reliable and reproducible landmark in their cadaveric study.28
Many surgeons use a combination of anatomical landmarks,
and some rely on stimulation to identify the nerve and to
monitor dissection.
The facial nerve can also be dissected in a retrograde fashion. ORegan and Bharadwaj compared both approaches.29
The incidence of nerve injury was 10% higher in the retrograde group but all injuries recovered after 12 months in
both groups. Further work showed that recurrence after retrograde dissection for benign parotid lesions was 2%, which
was comparable to other studies, and that the incidence of
permanent injury was low.30 These findings suggest that the
retrograde approach is a safe alternative to the antegrade
approach.
Despite a meticulous technique, facial weakness still
occurs. In patients with unilateral facial palsy after parotidectomy for benign disease, Sforza et al. compared 7 common
facial movements with those of healthy controls using a threedimensional optoelectronic motion analyser.31 There were
differences in movements between each side of the face in
affected patients compared with controls, and distant parts of
the face compensated for weak areas. How the technology
will contribute to the treatment of facial palsy is yet to be
realised.
There is no consensus about how to prevent Frey syndrome
after parotidectomy. Torretta et al. reported an improvement
in symptoms after 4 patients with the syndrome had fat,
which had been harvested from the abdomen, injected into
the parotid region.32 Sanabria et al. reviewed the data from 12
studies on the use of a sternocleidomastoid flap to cover the
parotid defect, but could not recommend it because of a lack
of randomised controlled trials.33 These techniques do, however, improve aesthetics by restoring the parotid contour.32,34
Anecdotally an increased risk to the facial nerve has been
described.
A pigtail catheter can be used to drain a sialocoele, which
is a further complication of parotid surgery.35 Currently, the
most commonly used treatment is botulinum neurotoxin type
A and systemic hyoscine or propantheline bromide (ProBanthine , Concord). Other rare complications have been

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R. OConnor et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

reported and include weakness of the accessory nerve, which

was caused by a suction drain.36

Malignant disease of the salivary glands

Parotid gland

Submandibular and sublingual glands

Currently, patients who have had excision of the submandibular gland are admitted over night to be monitored for
potential swelling and to use a suction drain. Laverick
et al. measured postoperative drainage, and concluded that
it stops after 68 h and amounts to less than 40 ml in 95%
of patients.37 Patients who drained over 40 ml were having
antiplatelet therapy that was not stopped, or were treated
as an emergency for acute infection of the gland. Patients
could therefore be treated as day cases if listed in the morning, as bleeding beyond 8 h seems to be negligible in most
cases.
De Virgilio et al. reported removal of the submandibular
gland through a modified facelift approach using robotic
assistance.38 The da Vinci robotic system (Intuitive Surgical,
Sunnyvale, USA) afforded more manoeuvrability, improved
visualisation, and removed the need for a scar in the neck
at the expense of a larger incision in the hairline. High costs
prohibit its widespread use at present.
A 10-year prospective study highlighted a small proportion of patients (8%) who require ipsilateral removal of the
sublingual gland after their original operation on the submandibular gland.39 This was related to sialadenitis of the
sublingual gland or stenosis of the remaining submandibular
duct, so-called submandibular stump syndrome. More conservative management of submandibular sialolithiasis may
reduce its incidence in future.
Severe keratoconjunctivitis sicca has been treated with
autotransplantation of the submandibular gland to replace the
lacrimal gland, but arterial, venous, and ductal resin models
of excised submandibular glands have shown a segmental distribution of vessels.40 This means that independent salivary
lobules could be transferred instead of the whole submandibular gland, thereby minimising epiphora, a side effect of the
procedure.
Minor salivary glands
While pleomorphic adenomas of the minor salivary glands
have a greater propensity for malignant transformation,
similar chromosomal changes have been found in benign
tumours of the major and minor salivary glands.41 On this
basis it is not possible to provide a cytogenetic explanation for the differences between these variants of the same
disease.
Chi et al. analysed a series of 1824 mucocoeles over
a 9-year period.42 Presentation tended to be in the first 3
decades of life, and over 80% were found on the lower labial
mucosa. Despite the large series, the reasons for this pattern
have still not been established, but may be because of the
greater density of minor salivary glands in the lower lip and
the higher risk of trauma from biting.

In parotidectomy for malignant disease, sacrifice of a functioning facial nerve does not benefit survival. The broad
consensus is to preserve a nerve that is functioning before
excision, as the morbidity and impact on the quality of life
are serious, and no significant advantage in survival has been
seen. Microscopic remnants of tumour can be dealt with using
radiotherapy instead, although this depends on its type and
grade.4,43 Munir et al. reported that cortical mastoidectomy
or removal of the mastoid tip could uncover the intratemporal course of an extracranial facial nerve that is obscured by
tumour.44
Excision of parotid carcinomas with a selective or supraomohyoid neck dissection is needed when tumour has spread
to the cervical lymph nodes. However, Chisholm et al. found
that metastasis to the neck may be diffuse, affecting levels
IV of the ipsilateral neck, and they questioned whether a
neck dissection that did not include level V could capture
all of the disease.45 The role of neck dissection in malignant tumours of accessory parotid gland remains unclear
because of the small number of patients, but excision through
a facelift parotidectomy incision, rather than directly over
the lesion, is recommended to protect the facial nerve and
improve cosmesis.46
Complete removal of metastatic disease from around the
facial nerve from a primary on the skin can be difficult so adjuvant radiotherapy has been advocated to improve survival.47
Selective neck dissection may also be beneficial as the incidence of micrometastases in the clinically negative neck in
these patients is between 35% and 50%.
Mucosa-associated lymphoid tissue (MALT), which is
known to be associated with autoimmune diseases such
as Sjgren syndrome, has recently been found to have an
increased incidence of genetic aberrations, particularly trisomy 3.48
Duan et al. found an association between persistent (more
than 42 000 calls over 910 years) and heavy use of mobile
phones (at least 2.5 h/day), and parotid malignancy.49 However, their study suffered from recall bias and much of the
association was lost when other variables were incorporated.
Patients who lived in rural areas had a reduced incidence of
parotid carcinoma, perhaps because they could not afford a
mobile phone.

Submandibular and sublingual glands

Tumours of the sublingual gland are rare and often malignant,
but 5-year survival can be up to 80%.50 The most common
are adenoid cystic carcinomas.

R. OConnor et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

Minor salivary glands

The hard palate does not need to be resected in all patients
with low grade mucoepidermoid carcinoma, and one study
found that it was required only when bony involvement
was demonstrated on imaging or intraoperatively.51 Palatal
periosteum formed the deep margin, but there were no recurrences in 18 patients even when surgical margins had been
invaded.

General
Prognostic factors in salivary gland malignancy
The clinical features of parotid carcinoma associated with
poor prognosis include fixation and infiltration of tumour, and
cervical lymphadenopathy. However, Stodulski et al. found
that facial nerve palsy was the strongest predictor, reducing
survival by a factor of 9.7.52 Pain and the rate of tumour
growth were less reliable indicators.
Status of the surgical margin and extracapsular spread
were stronger predictors of disease-free survival than grade
and type of tumour in a series of 115 patients with primary parotid malignancies.53 In a series of 113 patients
with parotid mucoepidermoid carcinoma, histological grade
was the most important predictor of 5-year survival, falling
from 97% and 94% for low and moderate grade tumours,
respectively, to 73% for high-grade tumours.54 LequericaFernndez et al. found that the grade of tumour was a less
influential prognostic factor for all types of parotid carcinoma, 55 but increasing age and clinical stage, squamous cell
carcinomas, and immunoexpression of vascular endothelial
growth factor, had a negative effect on survival. For locally
advanced high-risk tumours, advanced nodal disease (higher
than N2) was the only significant predictor of recurrence and
survival.56 Similarly, the presence of metastasis to cervical
lymph nodes in acinic cell carcinoma, which occurs in 10%
of patients, significantly reduces 5-year survival from 77%
to 48%.57
Histological grade and site are also predictors of distant
spread in tumours of the major salivary glands, which mostly
metastasise to the lungs.58 Malignancies of the submandibular gland have the highest risk of spread, followed by
parotid and sublingual tumours.
In cancers of the minor salivary glands, prognosis is predicted by the size and grade of tumour, and by the status of
the lymph nodes and surgical margins,59 but in acinic cell
carcinoma, size seems to be the only significant determinant
of survival.60
For certain salivary gland tumours, the site of origin
affects the prognosis. Acinic cell carcinomas located in
the sinonasal, lacrimal, and tracheobronchial regions have
a worse outcome because they occur in anatomically confined areas and complete excision is difficult.61 Radiotherapy
reduces recurrence, but increasing age, grade and stage,

487

invaded margins, nodal disease, and tumours that express

Ki-67, carry a poorer prognosis.61,62 Ki-67, which is a
biomarker associated with cellular proliferation, has been validated as a marker of biological aggressiveness in acinic cell
carcinoma, and high expression is associated with reduced
survival.4,63 Loss of RB1-inducible coiled-coil 1, a positive
regulator for the retinoblastoma tumour suppressor pathway
and salivary gland tumour marker, is also associated with a
poorer prognosis and reduced survival.64
The approach to treatment affects the prognosis of rare
salivary gland-like carcinomas that occur in the nasopharynx,
and surgery with postoperative radiotherapy are preferred
over radiotherapy alone.65 Metastasis to the lymph nodes,
surgical treatment, histological subtype, and distant spread,
are independent predictors of survival.
Chemotherapy in salivary gland malignancy
There is no level I evidence for chemotherapy in salivary
malignancy with or without involvement of the facial nerve,
nodal spread, high histological grade, or invaded surgical
margins. In 15 patients with locally advanced salivary gland
cancer who were treated with chemotherapy and concomitant radiotherapy with or without operation, disease-free
survival and overall survival at 2 years was 44% and 67%,
respectively.66 However, as most patients had large tumours
(stage IV), outcomes would be expected to be poor regardless
of treatment.
Ghosal et al. published a phase II clinical trial using imatinib and cisplatin for acinic cell carcinoma;67 imatinib inhibits
the tyrosine kinase receptor KIT, which is over-expressed
in this disease.4,63 In 22 of 28 (79%) patients with progressive, locally recurrent, or metastatic disease, there was partial
response or stabilisation for at least 6 months, but only 3
(11%) showed an objective improvement in disease morphology and activity on CT, MRI and PET, respectively. Cisplatin
and imatinib were beneficial in some patients, but the authors
could not recommend routine adoption of this combination
because the responses of patients varied.
Papaspyrou et al. reviewed chemotherapy with single and
combined agents for non-resectable, recurrent, or metastatic
acinic cell carcinoma, but could not make any recommendations, as response was minimal and short lived.68 Given
that the disease follows an indolent and protracted course
they advised that functional molecular imaging such as FDGPET or dynamic contrast-enhanced MRI should be used to
measure activity.
Radiation-induced xerostomia
Xerostomia can be caused by radioiodine treatment for thyroid carcinoma as it is concentrated in the salivary glands and
causes ductal inflammation and subsequent constriction.69
The submandibular glands are responsible for the production of over 60% of resting saliva so their preservation,
where possible, will reduce xerostomia after treatment.

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R. OConnor et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 483490

During neck dissection the submandibular gland is routinely

excised although it does not contain any nodes. A prospective and retrospective study, and a review have reported that
unless there is gross disease, it is usually possible to clear
all the nodes in the region without sacrificing the gland, as it
rarely harbours occult tumour.7072
Transposition of the submandibular gland out of the radiotherapy field has significantly reduced xerostomia, improved
quality of life, and has resulted in an objective increase in
salivary flow compared with control groups.73,74 However,
quality of life was significantly lower during the first month
after radiotherapy and the incidence of dysphagia was unaffected, which suggests that the acute insult on the oral mucosa
cannot be overcome with this approach alone. Nonetheless,
Rieger et al. found that transfer of the submandibular gland
improved swallowing and gave better quality of life scores
compared with pilocarpine, an oral sialogogue.75
Future treatment of xerostomia may lie in the cultivation
of human salivary gland cells, which could be implanted into
patients who have had radiotherapy. Chan et al. described a
successful and straightforward method to isolate and culture
selected salivary gland cell lines, which may evolve into a
clinically applicable technique to restore salivary function in
patients with xerostomia.76
Conclusion
Many more publications relate to diseases of the parotid gland
than to diseases of the other salivary glands. As with all
research involving the salivary glands, the main constraint is
the recruitment of enough patients to produce robust results.
A solution would be for head and neck units to collaborate and
combine patients data, which would generate larger numbers
to study.
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