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Chapter 1 Surgical , Embryology, and Physiology of the Salivary Glands John D. Langdon, FKC, MB BS, BDS, MDS, FDSRCS, FRCS, FMedSci King’s College, London, UK

Outline Summary References Introduction The Embryology Introduction Anatomy Contents of the Parotid Gland There are three pairs of major salivary glands The consisting of the parotid, submandibular, and Auriculotemporal Nerve sublingual glands. In addition, there are numerous Retromandibular minor glands distributed throughout the oral cavity External Carotid within the mucosa and submucosa. Parotid Lymph Nodes k On average, about 0.5 liters of saliva are pro- k Parotid Duct duced each day but the rate varies throughout the Nerve Supply to the Parotid day. At rest, about 0.3 ml/min are produced but this The Submandibular Gland rises to 2.0 ml/min with stimulation. The contribu- Embryology Anatomy tion from each gland also varies. At rest, the parotid The Superficial Lobe produces 20%, the submandibular gland 65%, and The Deep Lobe the sublingual and minor glands 15%. On stimula- The Submandibular Duct tion, the parotid secretion rises to 50%. The nature Blood Supply and Lymphatic Drainage of the secretion also varies from gland to gland. Nerve Supply to the Submandibular Gland Parotid secretions are almost exclusively serous, the Parasympathetic Innervation submandibular secretions are mixed and the sublin- Sympathetic Innervation gual and minor gland secretions are predominantly Sensory Innervation mucinous. The Sublingual Gland Saliva is essential for mucosal lubrication, Embryology speech, and swallowing. It also performs an essen- Anatomy tial buffering role that influences demineralization Sublingual Ducts of teeth as part of the carious process. When Blood Supply, Innervation, and Lymphatic Drainage there is a marked deficiency in saliva produc- Minor Salivary Glands tion, xerostomia, rampant caries, and destructive Histology of the Salivary Glands periodontal disease ensues. Various digestive Control of Salivation enzymes – salivary amylase – and antimicrobial

Salivary Gland Pathology: Diagnosis and Management, Second Edition. Edited by Eric R. Carlson and Robert A. Ord. © 2016 John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc.

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agents – IgA, lysozyme, and lactoferrin – are also exocrine gland. In the adult, the gland is composed secreted with the saliva. entirely of serous acini. The gland is situated in the space between the posterior border of the mandibular ramus and the The Parotid Gland mastoid process of the temporal bone. The exter- nal acoustic meatus and the glenoid fossa lie above EMBRYOLOGY together with the zygomatic process of the tempo- ral bone (Figure 1.1). On its deep (medial) aspect The parotid gland develops as a thickening of the lies the styloid process of the temporal bone. Infe- epithelium in the cheek of the oral cavity in the riorly, the parotid frequently overlaps the angle of 15 mm Crown Rump length embryo. This thicken- the and its deep surface overlies the trans- ing extends backwards towards the in a plane verse process of the atlas vertebra. superficial to the developing facial nerve. The deep The shape of the parotid gland is variable. aspect of the developing parotid gland produces Often it is triangular with the apex directed inferi- bud like projections between the branches of the orly. However, on occasion it is more or less of even facial nerve in the third month of intra-uterine life. width and occasionally it is triangular with the These projections then merge to form the deep apex superiorly. On average, the gland is 6 cm in lobe of the parotid gland. By the sixth month of length with a maximum of 3.3 cm in width. In 20% intra-uterine life the gland is completely canalized. of subjects a smaller accessory lobe arises from Although not embryologically a bilobed structure, the upper border of the parotid duct approximately the parotid comes to form a larger (80%) superfi- 6 mm in front of the main gland. This accessory cial lobe and a smaller (20%) deep lobe joined by lobe overlies the . an isthmus between the two major divisions of the The gland is surrounded by a fibrous capsule facial nerve. The branches of the nerve lie between previously thought to be formed from the investing layer of deep cervical . This fascia passes these lobes invested in loose connective tissue. k up from the and was thought to split to k This observation is vital in the understanding of enclose the gland. The deep layer is attached to the the anatomy of the facial nerve and surgery in this mandible and the temporal bone at the tympanic region (Berkovitz, et al. 2003). plate and styloid and mastoid processes (McMinn, et al. 1984; Berkovitz and Moxham 1988; Williams ANATOMY 1995; Ellis 1997). Recent investigations suggest that the superficial layer of the parotid capsule is Theparotidisthelargestofthemajorsalivary not formed in this way, but is part of the superficial glands. It is a compound, tubuloacinar, merocrine, musculo-aponeurotic system (SMAS) (Mitz and

Figure 1.1. A lateral view of the skull showing some of the bony features related to the bed of the parotid gland. 1: Mandibular fossa; 1 2 2: Articular eminence; 3: Tympanic 9 4 plate; 4: Mandibular condyle; 5: Styloid process; 6: Ramus of 3 8 mandible; 7: Angle of mandible; 6 5 8: Mastoid process; 9: External acoustic meatus. Source: Surgical Management of the Infratemporal 7 Fossa. (J. Langdon, B. Berkovitz & B. Moxham). ISBN 9781899066797. Reproduced with permission of Taylor & Francis Books UK.

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Peyronie 1976; Jost and Levet 1983; Wassef 1987; and the parotid duct lie within a loose cellular Thaller, et al. 1989; Zigiotti, et al. 1991; Gosain, layer between these two sheets of fascia. This et al. 1993; Flatau and Mills 1995). Anteriorly, observation is important in parotid surgery. When the superficial layer of the parotid capsule is thick operating on the parotid gland, the skin flap can and fibrous but more posteriorly, it becomes a either be raised in the subcutaneous fat layer or thin translucent membrane. Within this fascia are deep to the SMAS layer. The SMAS layer itself can scant muscle fibers running parallel with those of be mobilized as a separate flap and can be used to the platysma. This superficial layer of the parotid mask the cosmetic defect following parotidectomy capsule appears to be continuous with the fascia by reattaching it firmly to the anterior border of the overlying the platysma muscle. Anteriorly, it forms sternocleidomastoid muscle as an advancement a separate layer overlying the , flap (Meningaud, et al. 2006). which is itself an extension of the deep cervical The superior border of the parotid gland fascia. The peripheral branches of the facial nerve (usually the base of the triangle) is closely molded

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2 2 3 Figure 1.2. The parotid gland and 4 associated structures. 1: Auriculotem- poralnerve;2:Superficialtemporal 8 vessels; 3: Temporal branch of facial nerve; 4: Zygomatic branch of facial 9 nerve; 5: Buccal branch of facial nerve; 5 6: Mandibular branch of facial nerve; 10 7: Cervical branch of facial nerve; 8: Parotid duct; 9: Parotid gland; 10: Mas- 6 seter muscle; 11: Facial vessels; 12: 11 Platysma muscle; 13: External jugular 11 vein; 14: Sternocleidomastoid muscle; 15 15: Great auricular nerve. Source: Sur- 14 gical Management of the Infratempo- 7 12 13 ral Fossa. (J. Langdon, B. Berkovitz & B. Moxham). ISBN 9781899066797. Reproduced with permission of Taylor & Francis Books UK.

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around the external acoustic meatus and the tem- poromandibular joint. An avascular plane exists between the gland capsule and the cartilaginous Medial pterygoid and bony acoustic meatus (Figure 1.2). The infe- muscle Superior pharyngeal rior border (usually the apex) is at the angle of constrictor muscle the mandible and often extends beyond this to overlap the digastric triangle where it may lie very close to the posterior pole of the submandibular salivary gland. The anterior border just overlaps the posterior border of the and Styloid process the posterior border overlaps the anterior border Middle pharyngeal Stylomandibular constrictor muscle of the sternocleidomastoid muscle. ligament The superficial surface of the gland is cov- Mandibulo-stylohyoid ered by skin and platysma muscle. Some terminal ligament Inferior pharyngeal constrictor muscle branches of the great auricular nerve also lie super- Masseter muscle Posterior border ficial to the gland. At the superior border of the of ramus

parotid lie the superficial temporal vessels with the and artery artery in front of the vein. The auriculotemporal Submandibular gland branch of the mandibular nerve runs at a deeper level just behind the superficial temporal vessels. The branches of the facial nerve emerge from the anterior border of the gland. The parotid duct also emerges to run horizontally across the Figure 1.3. The mandibulostylohyoid ligament and masseter muscle before piercing the buccinator surrounding anatomy. muscle anteriorly to end at the parotid papilla. The k transverse facial artery (a branch of the superficial k temporal artery) runs across the area parallel to the mandible. The mandibulostylohyoid ligament and approximately 1 cm above the parotid duct. (the angular tract) passes between the angle of the The anterior and posterior branches of the facial mandible and the stylohyoid ligament. Inferiorly, vein emerge from the inferior border. it usually extends down to the hyoid bone. These The deep (medial) surface of the parotid ligaments are all that separates the parotid gland gland lies on those structures forming the parotid anteriorly from the posterior pole of the superficial bed. Anteriorly, the gland lies over the masseter lobe of the submandibular gland. muscle and the posterior border of the mandibular ramus from the angle up to the condyle. As the gland wraps itself around the ramus it is related to CONTENTS OF THE PAROTID GLAND the at its insertion on to the deep aspect of the angle. More posteriorly, the The Facial Nerve parotid is molded around the styloid process and From superficial to deep, the facial nerve, the the , stylohyoid, and stylopharyngeus auriculotemporal nerve, the , muscles from below upwards. Behind this, the and the external carotid artery pass through the parotid lies on the posterior belly of the digas- substance of the parotid gland. tric muscle and the sternocleidomastoid muscle. The facial nerve exits the skull base at the The digastric and the styloid muscles separate stylomastoid foramen. The surgical landmarks are the gland from the underlying internal jugular important (Figure 1.4). To expose the trunk of the vein, the external and internal carotid facial nerve at the stylomastoid foramen the dissec- and the glossopharyngeal, vagus, accessory, and tion passes down the avascular plane between the hypoglossal nerves, and the sympathetic trunk. parotid gland and the external acoustic canal until The fascia that covers the muscles in the the junction of the cartilaginous and bony canals parotid bed thickens to form two named liga- can be palpated. A small triangular extension of the ments (Figure 1.3). The stylomandibular ligament cartilage points towards the facial nerve as it exits passes from the styloid process to the angle of the foramen (Langdon 1998b). The nerve lies about

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Pointer cartilage

Measurements to root of facial 3cm nerve: 4mm Parotid gland • 3cm from skin to root • 4mm from junction of SCM and PBDM to root Tip of the mastoid process Sternocleidomastoid muscle (SCM) Posterior belly of digastric muscle Anterior border of (PBDM) masseter muscle Styloid process (palpable through above lying parotid tissue) Figure 1.4. Anatomical landmarks of the extratemporal facial nerve.

9 mm from the posterior belly of the digastric mus- cle and 11 mm from the bony external meatus (Holt 1996). The facial nerve then passes downwards and forwards over the styloid process and associated k muscles for about 1.3 cm before entering the sub- k stance of the parotid gland (Hawthorn and Flatau Figure 1.5. Clinical photograph of dissected facial nerve 1990). The first part of the facial nerve gives off following superficial parotidectomy. the posterior auricular nerve supplying the auricu- lar muscles and also branches to the posterior belly of the digastric and stylohyoid muscles. branch and adjacent branches. This explains why, On entering the parotid gland the facial when transient facial weakness follows facial nerve nerve divides into two divisions, temporofacial dissection, it is usually the mandibular branch that and cervicofacial, the former being the larger. The is affected. division of the facial nerve is sometimes called the pes anserinus due to its resemblance to the foot of a goose. From the temporofacial and cervico- Auriculotemporal Nerve facial divisions, the facial nerve gives rise to five The auriculotemporal nerve arises from the pos- named branches – temporal, zygomatic, buccal, terior division of the mandibular division of the mandibular, and cervical (Figure 1.5). The periph- trigeminal nerve in the infratemporal fossa. It runs eral branches of the facial nerve form anastomotic backwards beneath the lateral pterygoid muscle arcades between adjacent branches to form the between the medial aspect of the condylar neck parotid plexus. These anastomoses are important and the sphenomandibular ligament. It enters the during facial nerve dissection as accidental damage anteromedial surface of the parotid gland passing to a small branch often fails to result in any facial upwards and outwards to emerge at the superior weakness due to dual innervation from adjacent border of the gland between the temporomandibu- branches. Davis et al. (1956) studied these patterns lar joint and the external acoustic meatus. This following the dissection of 350 facial nerves in nerve communicates widely with the temporofacial cadavers. The anastomotic relationships between division of the facial nerve and limits the mobility adjacent branches fell into six patterns (Figure 1.6). of the facial nerve during surgery (Flatau and They showed that in only 6% of cases (type VI) Mills 1995). Further communications with the is there any anastomosis between the mandibular temporal and zygomatic branches loop around the

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ll 3 3 lV 1 4 2 2 4 l 3 3 5 5 1 1 2 Vl 2 4 4 5 3 lll V 3 5

4 4 5 5 Figure 1.6. The branching patterns of the facial nerve.

transverse facial and superficial temporal vessels auricular artery before ascending and dividing into (Bernstein and Nelson 1984). its terminal branches, the superficial temporal and maxillary arteries at the level of the condyle. The k superficial temporal artery continues vertically to k Retromandibular Vein emerge at the superior border of the gland and The vein is formed within the parotid gland by the crosses the zygomatic arch. Within the substance union of the superficial temporal vein and the max- of the parotid it gives off the transverse facial illary vein. The retromandibular vein passes down- artery, which emerges at the anterior border of the wards and close to the lower pole of the parotid gland to run across the face above the parotid duct. where it often divides into two branches passing The maxillary artery emerges from the deep aspect out of the gland. The posterior branch passes back- of the gland anteriorly to enter the infratemporal wards to unite with the on fossa. The maxillary artery gives off the deep auric- the surface of the sternocleidomastoid muscle to ular artery and the anterior tympanic artery within form the external . The anterior branch the substance of the parotid. All these branches passes forward to join the facial vein. from the external carotid also give off numerous The retromandibular vein is an important small branches within the parotid to supply the landmark during parotid gland surgery. The divi- gland itself. sion of the facial nerve into its temporofacial and cervicofacial divisions occurs just behind the retro- mandibular vein (Figure 1.7). The two divisions Parotid Lymph Nodes lie just superficial to the vein in contact with it. It Lymph nodes are found within the subcutaneous is all too easy to tear the vein whilst exposing the tissues overlying the parotid to form the preau- division of the facial nerve! ricular nodes and also within the substance of the gland. There are typically 10 nodes within the substance of the gland, the majority being within External Carotid Artery the superficial lobe and therefore superficial to the The external carotid artery runs deeply within the plane of the facial nerve. Only one or two nodes lie parotid gland. It appears from behind the poste- within the deep lobe (Marks 1984; McKean, et al. rior belly of the digastric muscle and grooves the 1985; Garatea-Crelgo, et al. 1993). All the parotid parotid before entering it. It gives off the posterior nodes drain into the upper deep cervical chain.

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Figure 1.7. The facial nerve and its relationship to the retromandibular vein within the parotid gland. Source: Surgical Management of the Infratemporal Fossa. (J. Langdon, B. Berkovitz & B. Moxham). ISBN 9781899066797. Reproduced with permission of Taylor & Francis Books UK.

Parotid Duct parts and the middle section corresponds to the The parotid duct emerges from the anterior border position of the parotid duct. The duct lies approxi- of the parotid gland and passes horizontally across mately 1 cm below the transverse facial vessels. The the masseter muscle. The surface markings of the accessory lobe of the parotid gland, when present, duct are obtained by drawing a line from the lowest drains into its upper border via one or two tribu- point of the alar cartilage to the angle of the mouth taries. Anastomosing branches between the buccal (Figure 1.8). This line is bisected and its midpoint is and zygomatic branches of the facial nerve cross joined with a straight line to the most anterior point the duct. At the anterior border of the masseter, the of the tragus. This line is divided into three equal duct bends sharply to perforate the buccal pad of fat

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the auriculotemporal nerve, which distributes the parasympathetic secretomotor fibers throughout the parotid gland. Some authorities suggest that there are also some parasympathetic innervations to the parotid from the chorda tympani branch of the facial nerve. The sympathetic nerve supply to the parotid arises from the superior cervical sympathetic gan- glion. The sympathetic fibers reach the gland via theplexusaroundthemiddlemeningealartery. They then pass through the otic ganglion without synapsing and innervate the gland through the auriculotemporal nerve. There is also sympathetic innervation to the gland arising from the plexuses that accompany the blood vessels supplying the gland. Sensory fibers arising from the connec- tive tissue within the parotid gland merge into the auriculotemporal nerve and pass proximally through the otic ganglion without synapsing. From there the fibers join the mandibular division of the trigeminal nerve. The sensory innervation of the parotid capsule is via the great auricular nerve. k The Submandibular Gland k

EMBRYOLOGY The submandibular gland begins to form at the Figure 1.8. The surface markings for the parotid duct. 13 mm stage as an epithelial outgrowth into the mesenchyme forming the floor of the mouth in the linguogingival groove. This proliferates rapidly and the at the level of the upper giving off numerous branching processes, which molar teeth. The duct then bends again to pass for- eventually develop lumina. Initially the developing ward for a short distance before entering the oral gland opens into the floor of the mouth posteriorly, cavity at the parotid papilla. lateral to the . The walls of the groove into which it drains come together to form the Nerve Supply to the Parotid submandibular duct. This process commences The parasympathetic secretomotor nerve supply posteriorly and moves forwards so that ultimately comes from the inferior salivatory nucleus in the the orifice of the duct comes to lie anteriorly below brain stem (Figure 1.9). From there, the fibers run the tip of the tongue close to the midline. in the tympanic branch of the glossopharyngeal nerve contributing to the tympanic plexus in the ANATOMY middle ear. The lesser petrosal nerve arises from the tympanic plexus leaving the middle ear and The submandibular gland consists of a larger running in a groove on the petrous temporal bone superficial lobe lying within the digastric triangle inthemiddlecranialfossa.Fromhereitexits in the neck and a smaller deep lobe lying within through the foramen ovale to the otic ganglion, the floor of the mouth posteriorly (Figure 1.10). which lies on the medial aspect of the mandibu- The two lobes are continuous with each other lar branch of the trigeminal nerve. Postsynaptic around the posterior border of the mylohyoid mus- postganglionic fibers leave the ganglion to join cle.Asintheparotidgland,thetwo“lobes”are

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Trigeminal nerve

Motor root of facial nerve Sensory root of facial nerve Medulla oblongata

Auriculotemporal nerve Parotid gland Pons

1 Lingual nerve

V3

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Sublingual gland 5

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Tympanic nerve Vll lX Lesser petrosal nerve Chorda tympani nerve

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Mylohyoid muscle k V3= Mandibular nerve 1 Trigeminal ganglion k Vll= Facial nerve Submandibular gland lX= Glossopharyngeal 2 Facial nerve ganglion nerve 3 Inferior ganglion (lX) Parasympathetic nerve fibers 4 Tympanic plexus

5 Otic ganglion

6 Submandibular ganglion

Figure 1.9. The parasympathetic innervations of the salivary glands. The parasympathetic fibers are shown as blue lines.

not true lobes embryologically, as the gland arises is important to realize just how close the lower as a single epithelial outgrowth (Langdon 1998a). pole of the parotid is to the posterior pole of the However, surgically it consists of the two lobes as submandibular gland as confusion can arise if a described previously. It is a mixed seromucinous mass in the region is incorrectly ascribed to the gland. wrong anatomical structure (Figure 1.2). Superi- orly, the superficial lobe lies medial to the body of the mandible. Inferiorly, it often overlaps the The Superficial Lobe intermediate tendon of the digastric muscles and The superficial lobe lies within the digastric tri- the insertion of the . The lobe angle. Its anterior pole reaches the anterior belly is partially enclosed between the two layers of of the digastric muscle and the posterior pole the that arise from the greater reaches the stylomandibular ligament. This struc- cornu of the hyoid bone and is in intimate prox- ture is all that separates the superficial lobe of the imity of the facial vein and artery (Figure 1.11). submandibular gland from the parotid gland. It The superficial layer of the fascia is attached to

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Tongue

Submandibular gland, deep lobe

Mylohyoid muscle (a) Submandibular gland, superficial lobe

Anterior belly of digastric muscle

Platysma muscle

Submandibular gland, deep lobe k k

Facial vein Wharton duct (c)

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Submandibular gland, superficial lobe Anterior belly of digastric muscle Mylohyoid muscle (raphe) Figure 1.10. The relationship of the superficial and deep lobes of the submandibular gland. (a) cross-sectional anatomy. (b) The superficial lobe from outside. (c) The relationship of the deep and superficial lobes to the mylohyoid muscle.

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Figure 1.12. Deep dissection of the left submandibular Figure 1.11. Superficial dissection of the left submandibu- gland. With the submandibular gland retracted, the facial lar gland. The investing layer of the deep cervical fascia is artery is identified in proximity to the facial vein. elevated off of the submandibular gland and the facial vein is identified.

the lower border of the mandible and covers the of the lobe is related to muscle from inferior surface of the superficial lobe. The deep which it is separated by styloglossus muscle, the k layer of fascia is attached to the mylohyoid line lingual nerve, submandibular ganglion, hypoglos- k on the inner aspect of the mandible and therefore sal nerve, and deep lingual vein. More inferiorly, covers the medial surface of the lobe. the medial surface is related to the stylohyoid mus- The inferior surface, which is covered by skin, cle and the posterior belly of digastric. subcutaneous fat, platysma, and the deep fascia, is crossed by the facial vein and the cervical branch of the facial nerve, which loops down from the The Deep Lobe angle of the mandible and subsequently innervates The deep lobe of the gland arises from the superfi- the lower lip. The submandibular lymph nodes cial lobe at the posterior free edge of the mylohyoid lie between the salivary gland and the mandible. muscle and extends forward to the back of the Sometimes one or more lymph nodes may be sublingual gland (Figure 1.12). It lies between embedded within the salivary gland. mylohyoid inferolaterally, hyoglossus, and sty- The lateral surface of the superficial lobe is loglossus muscles medially, the lingual nerve related to the submandibular fossa, a concavity on superiorly, and the hypoglossal nerve and deep the medial surface of the mandible, and the attach- lingual vein inferiorly. ment of the medial pterygoid muscle. The facial artery grooves its posterior part lying at first deep to the lobe and then emerging between its lateral sur- The Submandibular Duct face and the mandibular attachment of the medial The submandibular duct is about 5 cm long in pterygoid muscle from which it reaches the lower the adult. The wall of the submandibular duct border of the mandible. is thinner than that of the parotid duct. It arises The medial surface is related anteriorly to the from numerous tributaries in the superficial lobe mylohyoid from which it is separated by the mylo- and emerges from the medial surface of this lobe hyoid nerve and submental vessels. Posteriorly, it is just behind the posterior border of the mylohy- related to styloglossus muscle, the stylohyoid liga- oid. It crosses the deep lobe, passing upwards ment, and the glossopharyngeal nerve separating it and slightly backwards for 5 mm before running from the pharynx. Between these, the medial aspect forwards between the mylohyoid and hyoglossus

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muscles. As it passes forward, it runs between the The parasympathetic secretomotor fibers orig- sublingual gland and to open into the inate in the superior salivatory nucleus and the pre- floor of the mouth on the summit of the sublingual ganglionic fibers then travel via the facial nerve, papilla at the side of the lingual frenum just below chorda tympani, and lingual nerve to the ganglion the tip of the tongue. It lies between the lingual via the posterior filaments connecting the ganglion and hypoglossal nerves on the hyoglossus. At the to the lingual nerve. They synapse within the gan- anterior border of hyoglossus muscle it is crossed glion and the postganglionic fibers innervate the by the lingual nerve. As the duct traverses the deep submandibular and sublingual glands (Figure 1.9). lobe of the gland it receives tributaries draining Some fibers are thought to reach the lower pole of that lobe. the parotid gland.

Blood Supply and Lymphatic Drainage Sympathetic Innervation The arterial blood supply arises from multiple The sympathetic root is derived from the plexus branches of the facial and lingual arteries. Venous on the facial artery. The postganglionic fibers blood drains predominantly into the deep lingual arise from the superior cervical ganglion and vein. The lymphatics drain into the deep cervical pass through the submandibular ganglion without group of nodes, mostly into the jugulo-omohyoid synapsing. They are vasomotor to the vessels sup- node, via the submandibular nodes. plying the submandibular and sublingual glands. Five or six branches from the ganglion supply the submandibular gland and its duct. Others pass Nerve Supply to the Submandibular Gland back into the lingual nerve via the anterior fila- Parasympathetic Innervation ment to innervate the sublingual and other minor The secretomotor supply to the submandibular salivary glands in the region. gland arises from the submandibular (sublingual) k ganglion. This is a small ganglion lying on the k upper part of the hyoglossus muscle. There are Sensory Innervation additional ganglion cells at the hilum of the gland. Sensory fibers arising from the submandibular and The submandibular ganglion is suspended from the sublingual glands pass through the ganglion with- lingual nerve by anterior and posterior filaments out synapsing and join the lingual nerve, itself a (Figure 1.13). branch of the trigeminal nerve.

The Sublingual Gland

EMBRYOLOGY The sublingual gland arises in 20 mm embryos as a number of small epithelial thickenings in the linguogingival groove and on the outer side of the groove. Each thickening forms its own canal and so many of the sublingual ducts open directly onto the summit of the sublingual fold. Those that arise within the linguogingival grove end up draining into the submandibular duct.

ANATOMY The sublingual gland is the smallest of the major salivary glands. It is almond shaped and weighs Figure 1.13. Clinical photograph showing the relationship approximately 4 g. It is predominantly a mucous of the lingual nerve to the submandibular gland. gland. The gland lies on the mylohyoid and is

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Surgical Anatomy, Embryology, and Physiology of the Salivary Glands 13

covered by the mucosa of the floor of the mouth, Histology of the Salivary Glands whichisraisedasitoverliestheglandtoformthe sublingual fold. Posteriorly, the sublingual gland is The salivary glands are composed of large num- in contact with the deep lobe of the submandibular bers of secretory acini, which may be tubular or gland. The sublingual fossa of the mandible is globular in shape. Each acinus drains into a duct. located laterally and the genioglossus muscle is These microscopic ducts coalesce to form lobular located medially. The lingual nerve and the sub- ducts. Each lobule has its own duct and these then mandibular duct lie medial to the sublingual gland merge to form the main ducts. The individual lobes between it and the genioglossus. and lobules are separated by dense connective tis- sue which is continuous with the gland capsule. Sublingual Ducts The ducts, blood vessels, lymphatics, and nerves run through and are supported by this connective The gland has a variable number of excretory ducts tissue. ranging from 8 to 20. The majority drain into the The acini are the primary secretory organs floor of the mouth at the crest of the sublingual fold. but the saliva is modified as it passes through the A few drain into the submandibular duct. Some- intercalated, striated, and excretory ducts before times, a collection of draining ducts coalesce ante- being discharged into the mouth and oropharynx riorly to form a major duct (Bartholin’s duct) which opens with the orifice of the submandibular duct at (Figure 1.14). The lobules also contain signifi- the sublingual papilla. cant amounts of adipose tissue particularly in the parotid gland. The proportion of adipose tissue relative to excretory acinar cells increases with age. Blood Supply, Innervation, and Lymphatic In the human parotid, the excretory acini Drainage are almost entirely serous. In the submandibular The arterial supply is from the sublingual branch gland, again, the secretory units are mostly serous k of the and also the submental branch but there are additional mucous tubules and acini. k of the facial artery. Innervation is via the sublingual In some areas the mucinous acini have crescentic ganglion as described above. The lymphatics drain “caps” of serous cells called serous demilunes. In to the submental nodes. the sublingual gland the acini are almost entirely mucinous, although there are occasional serous acini or demilunes. Minor Salivary Glands The serous cells contain numerous proteina- ceous secretory (zymogen) granules. These gran- Minor salivary glands are distributed widely in the ules contain high levels of amylase. In addition, the oral cavity and oropharynx. They are grouped as secretory cells produce kallikrein, lactoferrin, and labial, buccal, palatoglossal, palatal, and lingual lysozyme. In mucous cells, the cytoplasm is packed glands. The labial and buccal glands contain both with large pale secretory droplets. mucous and serous acini, whereas the palatoglos- Initially the secretory acini drain into inter- sal glands are mucous secreting. The palatal glands calated ducts. These function mainly to conduct that are also mucous secreting occur in both the the saliva but they may also modify the elec- hard and soft palates. The anterior and posterior trolyte content and secrete immunoglobulin A. The lingual glands are mainly mucous. The anterior intercalated ducts drain into striated ducts, which glands are embedded within the muscle ventrally coalesce into intralobular and extralobular col- and they drain via four or five ducts near the lecting ducts. The intercalated duct cells are very lingual frenum. The posterior lingual glands are active metabolically and they transport potassium located at the root of the tongue. The deep pos- and bicarbonate into saliva. They reabsorb sodium terior lingual glands are predominantly serous. and chloride ions so that the resulting saliva is Additional serous glands (of von Ebner) occur hypotonic. They also secrete immunoglobulin A, around the circumvallate papillae on the dorsum lysozyme, and kallikrein. The immunoglobulin is of the tongue. Their watery secretion is thought to produced by plasma cells adjacent to the striated be important in spreading taste stimuli over the duct cells and it is then transported through the taste buds. epithelial lining into the saliva. The main collecting

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Mucous cell A Production and secretion of proteinaceous Tight junctions and enzymatic materials within secretory vesicles

Intercalated duct cell Flattened E Dense apical basal nucleus microfilaments

Desmosomes B Myoepithelial cell

Cytoplasmic Actin myofilaments processes Junctions between intercalated duct cells Cholinergic and cholinergic axon axons Large, spherical, Junctions between centrally located strated duct cells and nucleus cholinergic axon E’ Serous A’ demilune

Striated duct cell Production and D Secretory endpiece, secretion with adrenergic and of -amylase, cholinergic nerve perioxidase, terminals prolone-rich B’ proteins D’ C’ k k C Serous cell Adrenergic + Na axons Microvilli Cl Secretory granules Intercellular secretory Arteriole canaliculus Lysozyme with adrenergic Centrally Kallikrein nerve terminals Spherical nucleus located K+ nucleus Rough ER Basal invaginations Immunoglobulin and mitochondria Mitochondria yield striated appearance

To interlobular excretory ducts

Basal infoldings- increase surface area

Figure 1.14. Diagram showing the histology of the major components of the salivary glands.

ducts are simple conduits for saliva and do not surround the serous acini as basket cells. Those modify the composition of the saliva. associatedwiththeductcellsaremorefusiform Myoepithelial cells are contractile cells closely and are aligned along the length of the ducts. The related to the secretory acini and also much of the cytoplasm of the myoepithelial cells contains actin duct system. The myoepithelial cells lie between myofilaments which contract as a result of both the basal lamina and the epithelial cells. Numer- parasympathetic and sympathetic activity. Thus, ous cytoplasmic processes arise from them and the myoepithelial cells “squeeze” the saliva out

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Surgical Anatomy, Embryology, and Physiology of the Salivary Glands 15

of the secretory acini and ducts and add to the Summary salivary secretory pressure. • Although embryologically the parotid consists of a single lobe, anatomically the facial nerve Control of Salivation lies in a distinct plane between the anatomical superficial and deep lobes. There is a continuous low background saliva pro- • There are fixed anatomical landmarks indicat- duction, which is stimulated by drying of the oral ing the origin of the extracranial facial nerve as and pharyngeal mucosa. A rapid increase in the it leaves the stylomastoid foramen. resting levels occurs as a reflex in response to mas- • The lower pole of the parotid gland is sepa- ticatory stimuli including the mechanoreceptors rated from the posterior pole of the subman- and taste fibers. Other sensory modalities such as dibular gland by only thin fascia. This can lead smell are also involved. The afferent input is via to diagnostic confusion in determining the ori- the salivatory centers, which are themselves influ- gin of a swelling in this area. enced by the higher centers. The higher centers • The relationship of the submandibular salivary may be facilitory or inhibitory, depending on the duct to the lingual nerve is critical to the safe circumstances. The efferent secretory drive to the removal of stones within the duct salivary glands passes via the parasympathetic and • Great care must be taken to identify the lin- sympathetic pathways. There are no peripheral gual nerve when excising the submandibular inhibitory mechanisms. gland. The lingual nerve is attached to the Cholinergic nerves (parasympathetic) often gland by the parasympathetic fibers synapsing accompany ducts and branch freely around the in the submandibular (sublingual) ganglion. secretory endpieces (acini). Adrenergic nerves • The sublingual gland may drain into the sub- (sympathetic) usually enter the glands along the mandibular duct or it may drain directly into the floor of the mouth via multiple secretory k arteries and arterioles and ramify with them. k Within the glands, the nerve fibers intermingle ducts. such that cholinergic and adrenergic axons fre- quently lie in adjacent invaginations of a single Schwann cell. Secretion and vasoconstriction are References mediated by separate sympathetic axons whereas a single parasympathetic axon may, through serial Berkovitz BKB, Langdon JD, Moxham BJ. 2003. The facial terminals, result in vasodilatation, secretion, and nerve and the parotid gland. In: Langdon, JD, Berkovitz, constriction of myoepithelial cells. BKB, Moxham, BJ (eds), Surgical Anatomy of the Infratemporal Fossa. London, Martin Dunit, pp. 181–206. Secretory endpieces are the most densely Berkovitz BKB, Moxham BJ. 1988. A Textbook of Head and innervated structures in the salivary glands. Indi- Neck Anatomy.London,Wolfe. vidual acinar cells may have both cholinergic and Bernstein L, Nelson RH. 1984. Surgical anatomy of the extra- adrenergic nerve endings. The secretion of water parotid distribution of the facial nerve. Arch Otolaryngol and electrolytes, which accounts for the volume 110:177–183. of saliva produced, results from a complex set of Davis RA, Anson BJ, Budinger JM, Kurth LE. 1956. Sur- stimuli which are largely parasympathetic. The gical anatomy of the facial nerve and parotid gland active secretion of proteins into the saliva depends based on 350 cervicofacial halves. Surg Gynecol Obstet upon the relative levels of both sympathetic and 102:385–412. parasympathetic stimulation. Ellis H. 1997. Clinical Anatomy, 9th edn. Oxford, Blackwell. Although the ducts are less densely inner- Flatau AT, Mills PR. 1995. Regional anatomy. In: Norman JE Color Atlas and Text of the Salivary vated than secretory acini, they do influence the deB, McGurk M (eds), Glands. London, Mosby Wolfe, pp. 13–39. composition of the saliva. Adrenal aldosterone Garatea-Crelgo J, Gay-Escoda C, Bermejo B, Buenechea- promotes resorption of sodium and secretion of Imaz R. 1993. Morphological studies of the parotid lymph potassium into the saliva by striated ductal cells. nodes. J Cranio-Maxillo-Facial Surg 21:207–209. Myoepithelial cell contraction is stimulated pre- Gosain AK, Yousif NJ, Madiedo G, et al. 1993. Surgical dominantly by adrenergic fibers, although there anatomy of the SMAS: a reinvestigation. Plast Reconstr may be an additional role for cholinergic axons. Surg 92:1254–1263.

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Hawthorn R, Flatau A. 1990. Temporomandibular joint McMinn RMH, Hutchings RT, Logan BM. 1984. A Colour anatomy. In: Norman JE deB,BramleyP(eds),AText- Atlas of Applied Anatomy.London,Wolfe. book and Colour Atlas of the Temporomandibular Joint. Meningaud J-P, Bertolus C, Bertrand J-C. 2006. Parotidec- London, Mosby Wolfe, pp. 1–51. tomy: Assessment of a surgical technique including Holt JJ. 1996. The stylomastoid area: anatomic-histologic facelift incision and SMAS advancement. JCranio- study and surgical approach. Laryngoscope 106:396–399. Maxillofacial Surg 34:34–37. Jost G, Levet Y. 1983. Parotid fascia and face lifting: a crit- Mitz V, Peyronie M. 1976. The superficial musculo- ical evaluation of the SMAS concept. Plast Reconstr Surg aponeurotic system (SMAS) in the parotid and cheek 74:42–51. area. Plast Reconstr Surg 58:80–88. Langdon JD. 1998a. Sublingual and submandibular gland Thaller SR, Kim S, Patterson H, et al. 1989. The submuscular excision. In: Langdon JD, Patel MF (eds), Operative Max- aponeurotic system (SMAS): a histologic and comparative illofacial Surgery. London, Chapman & Hall, pp. 376–380. anatomy evaluation. Plast Reconstr Surg 86:691–696. Langdon JD. 1998b. Parotid surgery. In: Langdon JD, Wassef M. 1987. Superficial fascia and muscular layers in Patel MF (eds), Operative Maxillofacial Surgery.London, the face and neck: a histological study. Aesthetic Plast Chapman & Hall, pp. 386–388. Surg 11:171–176. Marks NJ. 1984. The anatomy of the lymph nodes of the Williams PL. 1995. (ed.). Gray’s Anatomy, 38th edn. parotid gland. Clin Otolaryngol 9:271–275. New York, Churchill Livingstone. McKean ME, Lee K, McGregor IA. 1984. The distribution of Zigiotti GL. Liverani MB, Ghibellini D. 1991. The relation- lymph nodes in and around the parotid gland: an anatom- ship between parotid and superficial fasciae. Surg Radiol ical study. Br J Plast Surg 38:1–5. Anat 13:293–300.

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Chapter 2 Diagnostic Imaging of Salivary Gland Pathology Pradeep K. Jacob, MD, MBA1 and J. Michael McCoy, DDS 2 1Department of Radiology, University of Tennessee at Chattanooga, College of Medicine, Chattanooga, TN, USA 2Departments of Oral and Maxillofacial Surgery, Pathology, and Radiology, University of Tennessee Medical Center, Knoxville, TN, USA

Outline Pathology of the Salivary Glands Vascular Lesions Introduction Lymphangioma (Cystic Hygroma) Imaging Modalities Hemangioma Computed Tomography (CT) Acute Sialadenitis CT Technique Chronic Sialadenitis Advanced Computed Tomography HIV−Lymphoepithelial Lesions Magnetic ResonanceImaging(MRI) Mucous Escape Phenomena MRI Technique Sialadenosis (sialosis) k k Spin Echo T1 Sialolithiasis Sjogren Syndrome Spin Echo T2 Sarcoidosis Proton Density Images (PD) Congenital Anomalies Gradient Recalled Echo Imaging (GRE) of the Salivary Glands Short Tau Inversion Recovery (STIR) First Branchial Cleft Cyst Gadolinium (Gd) Contrast Neoplasms – Salivary, Epithelial Fluid Attenuation Inversion Recovery (FLAIR) Benign Diffusion Weighted Images (DWI) Pleomorphic Adenoma MR Spectroscopy (MRS) Warthin Tumor Dynamic Contrast Enhanced Magnetic Resonance Oncocytoma Imaging Malignant Other Magnetic Resonance Imaging Techniques Mucoepidermoid Carcinoma Ultrasonography (US) Adenoid Cystic Carcinoma Ultrasound Technique Neoplasms – Non-Salivary Sialography Benign Radionuclide Imaging (RNI) Lipoma Positron Emission Neurogenic Tumors Tomography (PET) Positron Emission Tomography/ Malignant Computed Tomography (PET/CT) Lymphoma Metastases Diagnostic Imaging Anatomy Parotid Glands Summary Submandibular Glands References Sublingual Glands Minor Salivary Glands

Salivary Gland Pathology: Diagnosis and Management, Second Edition. Edited by Eric R. Carlson and Robert A. Ord. © 2016 John Wiley & Sons, Inc. Published 2016 by John Wiley & Sons, Inc.

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Introduction or local spread from the orthogonal projections or 3-D rendering. The ability to manipulate images Anatomic and functional diagnostic imaging plays is critical when assessing pathology in complex a central role in modern medicine. Virtually all anatomy, such as evaluation of parotid gland specialties of medicine to varying degrees depend masses to determine deep lobe involvement, facial on diagnostic imaging for diagnosis, therapy, and nerve involvement, or extension into the skull follow-up of treatment. Because of the complexity base. Images in the coronal plane are important of the anatomy, treatment of diseases of the head in evaluating the submandibular gland in relation and neck, including those of the salivary glands, to the floor of mouth. Lymphadenopathy and its are particularly dependent on quality medical relationship to the carotid sheath and its contents imaging and interpretation. Medical diagnostic and other structures are also well delineated. CT is imaging is divided primarily into two major cat- also superior to MRI in demonstrating bone detail egories, anatomic and functional. The anatomic and calcifications. CT is also the fastest method of imaging modalities include computed tomogra- imaging . Other advantages phy (CT), magnetic resonance imaging (MRI), include widespread availability of scanners, high and ultrasonography (US). Although occasionally resolution images, and speed of image acquisition obtained, plain film radiography for the head and also reduces motion artifacts. Exposure to ionizing neck, including salivary gland disease, is mostly radiation and the administration of IV contrast are of historical interest. In a similar manner, the use the only significant disadvantages to CT scanning. of sialography has been significantly reduced, although both plain films and sialography are of some use in imaging sialoliths. Functional diagnos- CT Technique tic imaging techniques include planar scintigraphy, The CT scanner contains a gantry, which holds an single photon emission computed tomography X-ray tube and a set of detectors. The X-ray tube (SPECT), positron emission tomography (PET), is positioned opposite the detectors and is physi- k k and magnetic resonance spectroscopy (MRS), all of cally coupled. A “fan beam” of X-rays is produced which are promising technologies. Recently, the use and passes through the patient to the detectors as of a combined anatomic and functional modality in the tube and detector rotate around the patient. In the form of PET/CT has proved invaluable in head newer generation of scanners, the multiple rows of and neck imaging. Previously widely employed detectors are fixed around the gantry and only the procedures including gallium radionuclide imaging tube rotates. A table carries the patient through the are less important today than in the past. gantry. The detectors send signals, dependent on the degree of X-ray attenuation, to a computer that uses this data to construct an image using complex Imaging Modalities algorithms. For most CT studies (especially in the head COMPUTED TOMOGRAPHY (CT) and neck) intravenous contrast is administered. IV contrast is a solution consisting of organic com- CT has become indispensable in the diagnosis, pounds bonded with Iodine molecules. Iodine is a treatment and follow-up of diseases of the head dense atom with an atomic weight of 127, which and neck. The latest generation of multiple-row is good at absorbing X-rays and is biocompatible. detector CT (MDCT) provides excellent soft-tissue IV contrast readily attenuates the X-ray beam at and osseous delineation. The rapid speed with concentrations optimal for vascular and soft tissue which images can be obtained along with the “enhancement,” but short of causing attenuation high spatial resolution and tissue contrast makes related artifacts. Streak artifacts, however, can CT the imaging modality of choice in head and occur if the concentration is too high, as seen occa- neck imaging. True volumetric data sets obtained sionally at the thoracic inlet and supraclavicular from multidetector row scanners allow for excel- region from dense opacification of the subclavian lent coronal, sagittal or oblique reformation of vein during rapid bolus injection of IV contrast. images as well as a variety of 3-D renderings. This CT of the neck should be performed with allows the radiologist and surgeon to characterize intravenous contrast whenever possible to opti- a lesion, assess involvement of adjacent structures mize delineation of masses, inflammatory or

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Figure 2.1. Axial CT of the neck in soft tissue window with- Figure 2.2. Axial CT of the neck in soft tissue window with out contrast demonstrating poor definition between soft IV contrast demonstrates improved visualization of struc- tissue structures. The blood vessels are unopacified and tures with enhancement of tissues and vasculature. Note cannot be easily distinguished from lymph nodes. Note the the small lipoma (arrow) anterior to the left submandibular sialolith (arrow) in the hilum of the left submandibular gland. gland, which distorts the anterior aspect of the gland with k slight posterior displacement. k

infectious changes in the tissues, and enhance vascular structures. Imaging is obtained from the level of the orbits through the aortic arch in the axial plane with breath hold. The images are recon- structed using a computer algorithm to optimize soft tissue delineation, and displayed in soft tissue window and level settings (Figures 2.1 and 2.2). In a similar manner images are reconstructed using a computer algorithm to optimize bone details as more sharp and defined (Figure 2.3). The lung apex is often imaged in a complete neck evalu- ation and displayed using lung window settings (Figure 2.4a). Dedicated CT scans of the chest are beneficial in the postoperative evaluation of patients with salivary gland malignancies as lung nodules can be observed, possibly indicative of metastatic disease (Figure 2.4b). Multiplanar refor- matted images of the neck are obtained typically in the coronal and sagittal planes, (Figures 2.5 and 2.6), although they may be obtained in virtually any plane desired or in a 3-D rendering. The Hounsfield unit (H) (named after Godfrey Figure 2.3. Axial CT of the skull base reconstructed in Hounsfield, inventor of the CT scanner) is the unit a sharp algorithm and in bone window and level display of density measurement for CT. These units are demonstrating sharp bone detail. Note the sharply defined assigned based on the degree of attenuation of normal right stylomastoid foramen (arrow).

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(a) Figure 2.5. Coronal CT reformation of the neck in soft tissue window at the level of the submandibular glands. Orthogonal images with MDCT offer very good soft tissue detail in virtually any plane of interest in order to assess anatomic and pathologic relationships. k k

(b) Figure 2.4. Axial CT of the neck at the thoracic inlet in lung windows demonstrating lung parenchyma (a). Axial image of dedicated CT of chest demonstrating cannon ball lesions in a patient previously treated for adenoid cystic carcinoma of the palate (b). These lesions are represen- tative of diffuse metastatic disease of the lungs, but not pathognomonic of adenoid cystic carcinoma.

the X-ray beam by tissue in a given voxel (volume Figure 2.6. Sagittal CT reformation of the neck in soft element) and are assigned relative to water (0 H) tissue window at the level of the parotid gland. Note (Table 2.1). The scale ranges from −1024 H for air, the accessory parotid gland (black arrow) sitting atop to +4000 H for very dense bone. The images are the parotid (Stensen) duct (thin white arrow). Also note the created based on a grayscale from black (−1024 retromandibular vein (large white arrow) and external audi- H) to white (+4000 H) and shades of gray. Despite tory canal.

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