Anat Sci Int DOI 10.1007/s12565-014-0247-9
ORIGINAL ARTICLE
The origin of the auriculotemporal nerve and its relationship to the middle meningeal artery George J. Dias • Joshua M. C. Koh Jon Cornwall
•
Received: 22 April 2014 / Accepted: 14 June 2014 Ó Japanese Association of Anatomists 2014
Abstract Knowledge of the anatomy of the auriculotemporal nerve (ATN) and middle meningeal artery (MMA) in the infratemporal fossa is necessary for assisting concise medical diagnosis and intervention. Current textbook descriptions describe a relationship between these structures that is not reported in previous studies. In addition, no previous studies have reported on symmetry or ethnicity affecting the relationship between these structures. This study aims to provide information on the relationship between the ATN and the meningeal artery in a specific ethnic group to further our understanding of normal morphology in this region. The infratemporal fossae of 19 Caucasian cadaveric heads were dissected bilaterally and the relationship between the ATN and MMA scrutinised. Twenty-five samples were included for analysis, including 6 bilateral (12 sides, 8 female) and 13 unilateral (9 female) specimens. Nerve root contributions to the ATN from the mandibular and inferior alveolar nerve included 8 specimens with 1 root, 12 with 2, 5 with 3, and 1 with 4. Three of six bilaterally dissected specimens had asymmetrical numbers of nerve roots. Two specimens were found with a ‘button hole’ arrangement of the ATN; these did not enclose the MMA. Variation was found both between and within specimens in relation to the relationship between the ATN and MMA. None of the specimens examined demonstrated a morphology that was consistent with common anatomical texts. Findings suggest modern texts require revision in order to accurately describe the relationship between these structures. G. J. Dias (&) J. M. C. Koh J. Cornwall (&) Department of Anatomy, University of Otago, PO Box 56, Dunedin 9013, New Zealand e-mail: [email protected] J. Cornwall e-mail: [email protected]
Keywords Auriculotemporal nerve Middle meningeal artery Variation Morphology
Introduction The origin of the auriculotemporal nerve (ATN), one of the sensory branches of the posterior division of the mandibular division of the trigeminal nerve (CN V3), is located within the infratemporal fossa. The posterior division gives rise to the lingual nerve, inferior alveolar nerve, and the ATN. Knowledge of the precise location of the proximal part of this nerve, and therefore its anatomical relationship with adjacent structures, is of importance during surgery in this region for space-occupying lesions such as perineural tumours of the ATN (Schmalfuss et al. 2002; Chan et al. 2013), aneurysms of the maxillary artery (Stephenson et al. 2011), and intervention for some temporomandibular joint pathologies. Iatrogenic injury or damage to the ATN can result in hypoesthesia, hyperesthesia, anaesthesia, and dysesthesia of the skin overlying the temporal region (Janis et al. 2010), as well as compromising the secretomotor fibres of the glossopharyngeal nerve (CN IX), which supplies the parotid gland (Loughner et al. 1990; Schmidt et al. 1998). The ATN is often described as arising from a single root that splits into two parts to encompass the middle meningeal artery (MMA) before rejoining, with this being commonly described as a ‘button hole’ or ‘encircling’ the passing MMA (Wilson 1857; Woodburne and Burkel 1988; Feneis and Dauber 1994; Chung 1995; Palastanga et al. 1995; Williams et al. 1995; Netter 1997; Abrahams et al. 1998; Agur and Lee 1999; Moore and Dalley 1999; Sauerland 1999; Sinnatamby 1999; Gosling et al. 2002; Schmalfuss et al. 2002; Snell 2004). Once the two parts of the
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nerve have rejoined, the ATN then passes deep, posterior to the lateral pterygoid muscle on the surface of the tensor veli palatini muscle, running between the sphenomandibular ligament and neck of the mandible. The nerve then passes laterally, deep to the temporomandibular joint, emerging posteriorly and ascending superficially to temporal vessels in the posterior aspect of the zygomatic arch. The ATN then splits into the auricular and temporal components; the auricular component supplies the external acoustic meatus, the surface of the tympanic membrane, and the skin of the upper half of the auricle while the temporal component supplies the skin of the temporal region. The MMA is the largest of 15 branches of the maxillary artery, typically arising as the third branch from the first (retromandibular) part of the maxillary artery from within the infratemporal fossa. It runs superiorly in the coronal plane between the sphenomandibular ligament and the lateral pterygoid muscle into the foramen spinosum, entering the middle cranial fossa with accompanying veins (Williams et al. 1995; Moore and Dalley 1999; Sinnatamby 1999). However, despite consistent textbook descriptions of the relationship between the ATN and MMA, some authors have suggested that such patterns of morphology are not representative of normal anatomy in this region. Baumel et al. (1971), Fernandes et al. (2003), and Gulekon et al. (2005) all describe patterns of the relationship between the ATN and MMA that are not consistent with most modern texts. Baumel et al. (1971) and Fernandes et al. (2003) suggest that the two roots of the ATN do not embrace the MMA, but in the majority of cases, they form a V-shaped arrangement within which the MMA is situated. In addition, Gulekon et al. (2005) describe the anatomy of the relationship between the ATN and MMA as highly variable, with the number of roots contributing to the formation of the ATN varying between one and four; none of their 32 dissections elicited a ‘button hole’ formation as described in many textbooks, and they were congruent with the descriptions of Baumel et al. (1971) and Fernandes et al. (2003). In addition to the disparity between scientific publications and textbook descriptions, it is unclear whether ethnic variation affects the relationship between the ATN and MMA or whether variation commonly exists between sides of the same individual. Variation in ethnicity and symmetry has been described as affecting the morphology and anatomical relationship between arterial structures in some instances (Toni et al. 2003, 2005). It is unclear whether these variables affect the ATN and its relationship with the MMA as previous studies do not detail the ethnicity of their specimens or address symmetry (Baumel et al. 1971; Fernandes et al. 2003; Gulekon et al. 2005). An understanding of such variations is important as clinicians are likely to encounter patient variation during surgical management.
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We aim to investigate the origins of the ATN in order to further clarify the relationship between the ATN and the MMA in a Caucasian population. Such findings will likely assist diagnoses and treatment of pathologies in this region, improve our understanding of whether ethnic variations affect the location and morphology of this nerve, and assist with clarification of textbook descriptions of ATN, MMA, and infratemporal fossa anatomy.
Materials and methods Nineteen elderly New Zealand Caucasian, cadaveric heads from the Department of Anatomy, University of Otago, were dissected bilaterally. Exclusion criteria included damage to the ATN, MMA, or adjacent anatomical structures in the region of the infratemporal fossa that precluded positive identification of these structures. The study was performed in a manner that complied with the Declaration of Helsinki on medical protocol and ethics and met University of Otago ethical requirements. Sharp and blunt dissection was performed to remove the overlying tissues including the mandibular ramus (including the temporalis muscle attachment), lateral pterygoid muscle, and pterygoid venous plexus. Nerves were visualised with the assistance of a Schott MC500 microscope light source (Schott Inc., New York, NY) that was used over the dissection to facilitate identification of the ATN, MMA, and adjacent anatomical structures. Note was made of the number of nerve roots comprising the ATN, the origin of each root, whether any structure was contained within the roots of the ATN, and the identification of any structure contained with the roots of the ATN. Descriptions and data were entered into a Microsoft Excel spreadsheet (Microsoft Corp., Albuquerque, NM). Specimens were photographed during dissection using a Canon Powershot G10 14.7 megapixel camera (Canon Inc., Tokyo, Japan) to facilitate post-dissection classification and analysis. Analyses were performed using descriptive statistics.
Results Twenty-five samples were included in the final analysis, including 6 bilateral dissections (12 sides; 8 female, four male) and 13 unilateral dissections (9 female, 4 male). The number of roots contributing to the formation of the ATN ranged from one to four. They originated from the mandibular nerve and the inferior alveolar nerve; in some instances it was not possible to determine the origin of the nerve roots as they emerged from the foramen ovale
Auriculotemporal nerve middle meningeal artery
having already departed from a nerve prior to this point. In cases where there was more than one root, the roots were distinguished by the position from which they emerged and are referred to as either superior (closer to the foramen ovale) or inferior roots (further from the foramen ovale). Observations were grouped according to pattern and are described in Table 1 and illustrated in Fig. 1.
Table 1 Classification and description of auriculotemporal nerve roots and arterial structures identified by dissection in the infratemporal fossa of 19 Caucasian cadavers Cadaver
Specimen
Sex
No. roots
Origin of root(s)
Relationship to arterial structures
1
1
F
1
FO
Deep to MMA
1
2
F
1
PD
Superficial to MMA
2
3
F
2
PD, IAN
Encloses MA
One root
2
4
F
3
PD, IAN, IAN
Encloses MA, MMA
Eight specimens had only a single root. All but one of these specimens originated from the posterior division of the mandibular nerve just below the foramen ovale. The single case originated above the level of the foramen ovale in the middle cranial fossa, and its origin could not be precisely identified. Four of the ATNs passed superficial to the MMA while the other four passed deep.
3
5
F
1
PD (BH)
Superficial to MMA
3
6
F
3
PD, PD, IAN
Encloses MMA
4
7
F
3
PD, IAN, IAN
Encloses MMA
4
8
F
4
PD, PD, PD, IAN
Encloses MMA
5
9
M
2
FO, PD
Encloses MMA
5
10
M
2
FO, PD
Encloses MMA
6
11
M
2
PD, IAN
Encloses MMA
6
12
M
2
FO (BH), IAN
Encloses MMA
7
13
F
1
PD
Superficial to MMA
8
14
F
1
PD
Superficial to MMA
9
15
F
1
PD
Deep to MMA
10
16
F
2
FO, PD
Encloses MMA
11
17
F
3
PD, PD, IAN
Encloses MA
12
18
F
2
PD, IAN
Encloses MMA
13 14
19 20
F F
2 2
PD, PD PD, IAN
Encloses MMA Encloses MMA
15
21
F
3
PD, PD, PD
Encloses MMA
16
22
M
1
PD
Superficial to MMA
17
23
M
1
PD
Deep to MMA
18
24
M
2
FO, IAN
Encloses MMA
19
25
M
2
PD, IAN
Superficial to MMA
Two roots from the posterior division of the mandibular nerve Four specimens had two roots with both roots originating from the posterior division of the mandibular nerve. This included three samples with the superior root originating from above the level of the foramen ovale. One specimen had two roots originating from the main posterior division that merged together enclosing only connective tissue; the MMA was observed passing close to but outside the area enclosed by these two roots. One specimen displayed a ‘button hole’ formation where the nerve split before later rejoining; this did not enclose the MMA or any other arterial structures. Two roots originating from different nerves Seven samples had two roots with one originating from the main posterior division and the other from the inferior alveolar nerve. Most formed a basic triangle that was likely to enclose the MMA. One of these samples had roots enclosing both the maxillary artery and the MMA; another displayed a ‘button hole’ formation of the branch arising from the posterior division but this did not enclose the MMA or any other arterial structures. One specimen did not enclose the MMA and passed superficial to this artery (Fig. 2). Three roots The five samples with three roots (20 %) showed the most variation. From these five samples, one had all three roots originating from the main posterior division; two had two roots off the main posterior division origin and one root
PD posterior division of the mandibular division of the trigeminal nerve (CN V3); IAN inferior alveolar nerve; FO foramen ovale, where the nerve root origin could not be confirmed as the root emerged from the foramen and could not be visualised originating from the posterior division; MMA middle meningeal artery; MA maxillary artery; BH buttonhole structure of nerve, where the single nerve split into two then rejoined to form a single nerve; N/A not applicable
originating from the IAN; two had one root from the main posterior division and two roots from the IAN; From the five samples, two had roots that enclosed the entire maxillary artery as well as the MMA.
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Fig. 1 Schematic representation of the variation found in the origin of the auriculotemporal nerve (ATN). a, b One nerve root. Where there was only one nerve arising from the posterior division (a), four nerves passed superficial to the middle meningeal artery, and three passed deep. c Two nerve roots, with one root emerging through the foramen ovale. On one occasion the middle meningeal artery passed
through a ‘button hole’ formed by the nerve root from the foramen ovale. d–f Two nerve roots. g–i Three nerve roots. j Four nerve roots. EC external carotid artery, FO foramen ovale, IAN inferior alveolar nerve, LN lingual nerve, MMA middle meningeal artery, MA meningeal artery, PD posterior division of the mandibular division of the trigeminal nerve
ular nerve, immediately after its emergence from the foramen ovale, and the third further inferiorly. The other inferior root arose from the inferior alveolar nerve and both the inferior roots ran deep to the MMA. The two inferior roots joined to form one single branch, which then attached to both superior branches at the same point. The MMA passed between the superior and inferior roots. Symmetry between sides
Fig. 2 Photograph of a dissected infratemporal fossa and contents, viewed from the lateral aspect. Both roots of the auriculotemporal nerve can be seen passing superficial to the middle meningeal artery. The dashed line indicates the path of the maxillary artery toward the inside of the parotid gland (removed). 1 Root of the auriculotemporal nerve arising from the posterior division, 2 root of the auriculotemporal nerve arising from the inferior alveolar nerve, ATN auriculotemporal nerve, BN buccal nerve (severed), FO foramen ovale, GWS greater wing of the sphenoid, IAN inferior alveolar nerve, LN lingual nerve, LPP lateral pterygoid plate, MA maxillary artery, MMA middle meningeal artery, MN mandibular nerve, ZA zygomatic arch (cut)
Four roots One specimen had four roots; three of these originated from the main posterior division, and one arose from the IAN. In this specimen, the two superior roots originated from two separate locations adjacent to each other in the sagittal plane on the posterior division of the mandib-
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Three of the six bilaterally (four female) dissected heads had different numbers of roots on either side; this was found only on one female specimen out of the four. On one specimen the difference in the number of roots was one, and on two specimens it was two.
Discussion This study describes the variation in the anatomical relationship between the ATN and the MMA, with results suggesting that variation commonly exists not only between individuals but also within individuals. Furthermore, current textbook descriptions are not representative of observed patterns of relationship between the ATN and the MMA where the MMA is consistently described as being encompassed in a ‘button hole’ created by the roots of the ATN; we found no specimens displaying such patterns. In addition, the extent or degree of these variations is not addressed in current textbook descriptions.
Auriculotemporal nerve middle meningeal artery
Descriptive data Many anatomical textbooks describe the relationship between the ATN and MMA suggesting that a single root of the ATN forms a ‘button hole’ for the passage of the MMA or ‘encircling’ the MMA, after which the two parts of this single root converge and join (Wilson 1857; Woodburne and Burkel 1988; Feneis and Dauber 1994; Chung 1995; Palastanga et al. 1995; Williams et al. 1995; Netter 1997; Abrahams et al. 1998; Agur and Lee 1999; Moore and Dalley 1999; Sauerland 1999; Sinnatamby 1999; Gosling et al. 2002; Schmalfuss et al. 2002; Snell 2004). We found only 2 of the 25 specimens exhibited ‘button hole’ morphology of a nerve root, and on neither occasion did the MMA pass through this structure. The most common variation was for the formation of a triangle formed by the posterior division or inferior alveolar nerve (base) and the projecting roots (sides), through which the MMA was found to pass (Fig. 3). In 13 out of the 25 samples (52 %) this occurred to show the MMA running between the roots of the ATN in such a fashion. Previous publications (Baumel et al. 1971; Fernandes et al. 2003; Gulekon et al. 2005) also detail few MMAs piercing a ‘button hole’ formation of ATN roots. From the combined results of these studies it appears that such a description does not reflect normal textbook descriptions, including the latest edition of Gray’s Anatomy (Standring 2008), which show a ‘button hole’ auriculotemporal nerve with an MMA passing between the divided root. The most common relationship between the ATN and MMA is that when multiple nerve roots exist they form a triangle with the posterior root forming the base and the multiple branches the sides; in this study the MMA consistently pierces between the branches on 15 of 17 occasions (88.2 %). On the only occasions that it did not it was because the MMA had not yet originated from the maxillary artery (which itself had pierced the triangle formed by the nerve roots) or because the MMA passed under the nerve roots. Sometimes the maxillary artery also pierces this triangle, which occurred on three occasions.
Fig. 3 Schematic representation of current textbook descriptions of the relationship between the auriculotemporal nerve (ATN) and the middle meningeal artery (MMA) showing passage of the artery through the ‘button hole’ in the nerve (a) and the actual pattern that is most frequently found during dissection (b) where passage of the artery is through a triangle (broken lines) formed by the roots and the posterior division of the mandibular division of the trigeminal nerve (PD). EC external carotid artery, FO foramen ovale, IAN inferior alveolar nerve, LN lingual nerve, MMA middle meningeal artery, MA meningeal artery, PD posterior division of the mandibular division of the trigeminal nerve
formation of the ATN. Such variation needs to be considered when performing bilateral procedures of patients involving imaging, diagnoses, and surgery. Ethnicity It is difficult to reconcile ethnic variation between the few studies that have published comprehensive morphological data on the relationship between the ATN and the MMA. Baumel et al. (1971) stated the ethnicity of their cadavers as ‘mostly Caucasian, with a few American Indian and Negro specimens’ and did not state results by ethnicity; Fernandes et al. (2003) and Gulekon et al. (2005) do not state ethnicity. Rather, this present study perhaps provides a baseline on ethnic variations of the relationship between the ATN and MMA given all the cadavers were of Caucasian descent. Future studies may be able to use such information to provide further comparisons on ATN morphology between ethnicities.
Symmetry Limitations Within the six specimens that were dissected bilaterally (four females), three had variation in the number of roots comprising the ATN. From the specimens that exhibited varying numbers of nerve roots, the number of roots varied by only one on each occasion. Gulekon et al. (2005) found 7 of 16 specimens having asymmetry in the number of ATN nerve roots; on all but one occasion the number of nerve roots varied by one. This suggests that in practice a moderate to high proportion of the population will have an abnormal number of nerve roots contributing to the
In many cases the root of the ATN originated prior to its emergence from the foramen ovale. Even though positive identification could not take place, it is highly unlikely that these roots originated from any structure other than the posterior division of the mandibular nerve; these samples were therefore interpreted as having originated from this nerve. Small numbers in the sample also indicate that definitive conclusions cannot be drawn about differences between or within sexes, or within individuals. Despite
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this, it is possible to suggest trends for variations within individuals exist given that half the cases (three of six) included differences between sides.
Conclusion This study examines the relationship between the ATN and MMA in elderly Caucasian cadavers, indicating that variation in the origin and number or nerve roots consistently exists not only between but also within individuals. Variations observed in this study are similar to those of other dissection studies yet dissimilar to many textbook descriptions. It is proposed that in light of the consistency between descriptions in this and previous explorations of this region anatomical texts review their descriptions of ‘button-hole’ formation of the ATN and MMA relationship by instead highlighting the relationship between the MMA and the ‘triangle’ formed by the posterior division of the mandibular and inferior alveolar nerves and the ATN nerve roots (Fig. 3). These observations may assist in the identification of the ATN and MMA in the infratemporal fossa. Conflict of interest of interest.
The authors declare that there are no conflicts
References Abrahams PH, Hutchings RT, Marks SC (1998) McMinn’s colour atlas of human anatomy. Mosby International Ltd., Barcelona Agur AMR, Lee MJ (1999) Grant’s atlas of anatomy. Lippincott, Williams & Wilkins, Baltimore Baumel JJ, Vanderheiden JP, McElenney JE (1971) The auriculotemporal nerve of man. Am J Anat 130:431–440 Chan M, Dmytriw AA, Bartlett E, Yu E (2013) Imaging of auriculotemporal nerve perineural spread. Ecancermedicalscience 7:374 Chung KW (1995) Gross anatomy. Williams & Wilkins, Baltimore Feneis H, Dauber W (1994) Pocket atlas of human anatomy, 3rd edn. Thieme, London Fernandes PR, de Vasconselles HA, Okeson JP, Bastos RL, Maia ML (2003) The anatomical relationship between the position of the auriculotemporal nerve and mandibular condyle. Cranio 21:165–171
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Gosling JA, Harris PF, Whitmore I, Willan PLT (2002) Human anatomy: color atlas and text, 4th edn. Mosby, Maryland Heights Gulekon N, Anil A, Poyraz A, Peker T, Turgut HB, Karakosi M (2005) Variations in the anatomy of the auriculotemporal nerve. Clin Anat 18:15–22 Janis JE, Hatef DA, Ducic I, Ahmad J, Wong C, Hoxworth RE, Osborn T (2010) Anatomy of the auriculotemporal nerve: variations in its relationship to the superficial temporal artery and implications for the treatment of migraine headaches. Plast Reconstr Surg 125:1422–1428 Loughner BA, Larkin LH, Mahan PE (1990) Nerve entrapment in the lateral pterygoid muscle. Oral Surg Oral Med Oral Pathol Radiol Endod 69:299–306 Moore KL, Dalley AF (1999) Clinically oriented anatomy. Lippincott Williams & Wilkins, Baltimore Netter FH (1997) Atlas of human anatomy. Novartis, New Jersey Palastanga N, Field F, Soames R (1995) Anatomy and human movement. Butterworth Heinemann, London Sauerland EK (1999) Grant’s dissector. Lippincott, Williams & Wilkins, Baltimore Schmalfuss IM, Tart RP, Mukhevji S, Mancuso AA (2002) Perineural tumor spread along the auriculotemporal nerve. Am J Neuroradiol 23:303–311 Schmidt BL, Pogrel MA, Necoechea M, Kearns G (1998) The distribution of the auriculotemporal nerve around the temporomandibular joint. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 86:165–168 Sinnatamby CS (1999) Last’s anatomy. Churchill Livingstone, London Snell RS (2004) Clinical anatomy, 7th edn. Lippincott, Williams & Wilkins, Baltimore Standring S (ed) (2008) Gray’s anatomy, 40th edn. Churchill Livingstone, Edinburgh Stephenson JA, Panteleimonitis S, Choke E, Dennis M, Glasby M (2011) Endovascular treatment of a giant aneurysm of the maxillary artery. Case Rep Vasc Med. doi:10.1155/2011/818241 Toni R, Casa CD, Salvatore Mosca S, Malaguti A, Castorina S, Roti E (2003) Anthropological variations in the anatomy of the human thyroid arteries. Thyroid 13:183–192 Toni R, Casa CD, Castorinab S, Rotic E, Cedad G, Valentid G (2005) A meta-analysis of inferior thyroid artery variations in different human ethnic groups and their clinical implications. Ann Anat 187:371–385 Williams PL, Bannister LH, Berry MM, Collins P, Dyson M, Dussek JE, Ferguson MWJ (eds) (1995) Gray’s anatomy. Churchill Livingstone, New York Wilson W (1857) A system of human anatomy. Savill & Edwards, London Woodburne RT, Burkel WE (1988) Essentials of human anatomy, 8th edn. Oxford University Press, London
ORIGINAL ARTICLE
The origin of the auriculotemporal nerve and its relationship to the middle meningeal artery George J. Dias • Joshua M. C. Koh Jon Cornwall
•
Received: 22 April 2014 / Accepted: 14 June 2014 Ó Japanese Association of Anatomists 2014
Abstract Knowledge of the anatomy of the auriculotemporal nerve (ATN) and middle meningeal artery (MMA) in the infratemporal fossa is necessary for assisting concise medical diagnosis and intervention. Current textbook descriptions describe a relationship between these structures that is not reported in previous studies. In addition, no previous studies have reported on symmetry or ethnicity affecting the relationship between these structures. This study aims to provide information on the relationship between the ATN and the meningeal artery in a specific ethnic group to further our understanding of normal morphology in this region. The infratemporal fossae of 19 Caucasian cadaveric heads were dissected bilaterally and the relationship between the ATN and MMA scrutinised. Twenty-five samples were included for analysis, including 6 bilateral (12 sides, 8 female) and 13 unilateral (9 female) specimens. Nerve root contributions to the ATN from the mandibular and inferior alveolar nerve included 8 specimens with 1 root, 12 with 2, 5 with 3, and 1 with 4. Three of six bilaterally dissected specimens had asymmetrical numbers of nerve roots. Two specimens were found with a ‘button hole’ arrangement of the ATN; these did not enclose the MMA. Variation was found both between and within specimens in relation to the relationship between the ATN and MMA. None of the specimens examined demonstrated a morphology that was consistent with common anatomical texts. Findings suggest modern texts require revision in order to accurately describe the relationship between these structures. G. J. Dias (&) J. M. C. Koh J. Cornwall (&) Department of Anatomy, University of Otago, PO Box 56, Dunedin 9013, New Zealand e-mail: [email protected] J. Cornwall e-mail: [email protected]
Keywords Auriculotemporal nerve Middle meningeal artery Variation Morphology
Introduction The origin of the auriculotemporal nerve (ATN), one of the sensory branches of the posterior division of the mandibular division of the trigeminal nerve (CN V3), is located within the infratemporal fossa. The posterior division gives rise to the lingual nerve, inferior alveolar nerve, and the ATN. Knowledge of the precise location of the proximal part of this nerve, and therefore its anatomical relationship with adjacent structures, is of importance during surgery in this region for space-occupying lesions such as perineural tumours of the ATN (Schmalfuss et al. 2002; Chan et al. 2013), aneurysms of the maxillary artery (Stephenson et al. 2011), and intervention for some temporomandibular joint pathologies. Iatrogenic injury or damage to the ATN can result in hypoesthesia, hyperesthesia, anaesthesia, and dysesthesia of the skin overlying the temporal region (Janis et al. 2010), as well as compromising the secretomotor fibres of the glossopharyngeal nerve (CN IX), which supplies the parotid gland (Loughner et al. 1990; Schmidt et al. 1998). The ATN is often described as arising from a single root that splits into two parts to encompass the middle meningeal artery (MMA) before rejoining, with this being commonly described as a ‘button hole’ or ‘encircling’ the passing MMA (Wilson 1857; Woodburne and Burkel 1988; Feneis and Dauber 1994; Chung 1995; Palastanga et al. 1995; Williams et al. 1995; Netter 1997; Abrahams et al. 1998; Agur and Lee 1999; Moore and Dalley 1999; Sauerland 1999; Sinnatamby 1999; Gosling et al. 2002; Schmalfuss et al. 2002; Snell 2004). Once the two parts of the
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nerve have rejoined, the ATN then passes deep, posterior to the lateral pterygoid muscle on the surface of the tensor veli palatini muscle, running between the sphenomandibular ligament and neck of the mandible. The nerve then passes laterally, deep to the temporomandibular joint, emerging posteriorly and ascending superficially to temporal vessels in the posterior aspect of the zygomatic arch. The ATN then splits into the auricular and temporal components; the auricular component supplies the external acoustic meatus, the surface of the tympanic membrane, and the skin of the upper half of the auricle while the temporal component supplies the skin of the temporal region. The MMA is the largest of 15 branches of the maxillary artery, typically arising as the third branch from the first (retromandibular) part of the maxillary artery from within the infratemporal fossa. It runs superiorly in the coronal plane between the sphenomandibular ligament and the lateral pterygoid muscle into the foramen spinosum, entering the middle cranial fossa with accompanying veins (Williams et al. 1995; Moore and Dalley 1999; Sinnatamby 1999). However, despite consistent textbook descriptions of the relationship between the ATN and MMA, some authors have suggested that such patterns of morphology are not representative of normal anatomy in this region. Baumel et al. (1971), Fernandes et al. (2003), and Gulekon et al. (2005) all describe patterns of the relationship between the ATN and MMA that are not consistent with most modern texts. Baumel et al. (1971) and Fernandes et al. (2003) suggest that the two roots of the ATN do not embrace the MMA, but in the majority of cases, they form a V-shaped arrangement within which the MMA is situated. In addition, Gulekon et al. (2005) describe the anatomy of the relationship between the ATN and MMA as highly variable, with the number of roots contributing to the formation of the ATN varying between one and four; none of their 32 dissections elicited a ‘button hole’ formation as described in many textbooks, and they were congruent with the descriptions of Baumel et al. (1971) and Fernandes et al. (2003). In addition to the disparity between scientific publications and textbook descriptions, it is unclear whether ethnic variation affects the relationship between the ATN and MMA or whether variation commonly exists between sides of the same individual. Variation in ethnicity and symmetry has been described as affecting the morphology and anatomical relationship between arterial structures in some instances (Toni et al. 2003, 2005). It is unclear whether these variables affect the ATN and its relationship with the MMA as previous studies do not detail the ethnicity of their specimens or address symmetry (Baumel et al. 1971; Fernandes et al. 2003; Gulekon et al. 2005). An understanding of such variations is important as clinicians are likely to encounter patient variation during surgical management.
123
We aim to investigate the origins of the ATN in order to further clarify the relationship between the ATN and the MMA in a Caucasian population. Such findings will likely assist diagnoses and treatment of pathologies in this region, improve our understanding of whether ethnic variations affect the location and morphology of this nerve, and assist with clarification of textbook descriptions of ATN, MMA, and infratemporal fossa anatomy.
Materials and methods Nineteen elderly New Zealand Caucasian, cadaveric heads from the Department of Anatomy, University of Otago, were dissected bilaterally. Exclusion criteria included damage to the ATN, MMA, or adjacent anatomical structures in the region of the infratemporal fossa that precluded positive identification of these structures. The study was performed in a manner that complied with the Declaration of Helsinki on medical protocol and ethics and met University of Otago ethical requirements. Sharp and blunt dissection was performed to remove the overlying tissues including the mandibular ramus (including the temporalis muscle attachment), lateral pterygoid muscle, and pterygoid venous plexus. Nerves were visualised with the assistance of a Schott MC500 microscope light source (Schott Inc., New York, NY) that was used over the dissection to facilitate identification of the ATN, MMA, and adjacent anatomical structures. Note was made of the number of nerve roots comprising the ATN, the origin of each root, whether any structure was contained within the roots of the ATN, and the identification of any structure contained with the roots of the ATN. Descriptions and data were entered into a Microsoft Excel spreadsheet (Microsoft Corp., Albuquerque, NM). Specimens were photographed during dissection using a Canon Powershot G10 14.7 megapixel camera (Canon Inc., Tokyo, Japan) to facilitate post-dissection classification and analysis. Analyses were performed using descriptive statistics.
Results Twenty-five samples were included in the final analysis, including 6 bilateral dissections (12 sides; 8 female, four male) and 13 unilateral dissections (9 female, 4 male). The number of roots contributing to the formation of the ATN ranged from one to four. They originated from the mandibular nerve and the inferior alveolar nerve; in some instances it was not possible to determine the origin of the nerve roots as they emerged from the foramen ovale
Auriculotemporal nerve middle meningeal artery
having already departed from a nerve prior to this point. In cases where there was more than one root, the roots were distinguished by the position from which they emerged and are referred to as either superior (closer to the foramen ovale) or inferior roots (further from the foramen ovale). Observations were grouped according to pattern and are described in Table 1 and illustrated in Fig. 1.
Table 1 Classification and description of auriculotemporal nerve roots and arterial structures identified by dissection in the infratemporal fossa of 19 Caucasian cadavers Cadaver
Specimen
Sex
No. roots
Origin of root(s)
Relationship to arterial structures
1
1
F
1
FO
Deep to MMA
1
2
F
1
PD
Superficial to MMA
2
3
F
2
PD, IAN
Encloses MA
One root
2
4
F
3
PD, IAN, IAN
Encloses MA, MMA
Eight specimens had only a single root. All but one of these specimens originated from the posterior division of the mandibular nerve just below the foramen ovale. The single case originated above the level of the foramen ovale in the middle cranial fossa, and its origin could not be precisely identified. Four of the ATNs passed superficial to the MMA while the other four passed deep.
3
5
F
1
PD (BH)
Superficial to MMA
3
6
F
3
PD, PD, IAN
Encloses MMA
4
7
F
3
PD, IAN, IAN
Encloses MMA
4
8
F
4
PD, PD, PD, IAN
Encloses MMA
5
9
M
2
FO, PD
Encloses MMA
5
10
M
2
FO, PD
Encloses MMA
6
11
M
2
PD, IAN
Encloses MMA
6
12
M
2
FO (BH), IAN
Encloses MMA
7
13
F
1
PD
Superficial to MMA
8
14
F
1
PD
Superficial to MMA
9
15
F
1
PD
Deep to MMA
10
16
F
2
FO, PD
Encloses MMA
11
17
F
3
PD, PD, IAN
Encloses MA
12
18
F
2
PD, IAN
Encloses MMA
13 14
19 20
F F
2 2
PD, PD PD, IAN
Encloses MMA Encloses MMA
15
21
F
3
PD, PD, PD
Encloses MMA
16
22
M
1
PD
Superficial to MMA
17
23
M
1
PD
Deep to MMA
18
24
M
2
FO, IAN
Encloses MMA
19
25
M
2
PD, IAN
Superficial to MMA
Two roots from the posterior division of the mandibular nerve Four specimens had two roots with both roots originating from the posterior division of the mandibular nerve. This included three samples with the superior root originating from above the level of the foramen ovale. One specimen had two roots originating from the main posterior division that merged together enclosing only connective tissue; the MMA was observed passing close to but outside the area enclosed by these two roots. One specimen displayed a ‘button hole’ formation where the nerve split before later rejoining; this did not enclose the MMA or any other arterial structures. Two roots originating from different nerves Seven samples had two roots with one originating from the main posterior division and the other from the inferior alveolar nerve. Most formed a basic triangle that was likely to enclose the MMA. One of these samples had roots enclosing both the maxillary artery and the MMA; another displayed a ‘button hole’ formation of the branch arising from the posterior division but this did not enclose the MMA or any other arterial structures. One specimen did not enclose the MMA and passed superficial to this artery (Fig. 2). Three roots The five samples with three roots (20 %) showed the most variation. From these five samples, one had all three roots originating from the main posterior division; two had two roots off the main posterior division origin and one root
PD posterior division of the mandibular division of the trigeminal nerve (CN V3); IAN inferior alveolar nerve; FO foramen ovale, where the nerve root origin could not be confirmed as the root emerged from the foramen and could not be visualised originating from the posterior division; MMA middle meningeal artery; MA maxillary artery; BH buttonhole structure of nerve, where the single nerve split into two then rejoined to form a single nerve; N/A not applicable
originating from the IAN; two had one root from the main posterior division and two roots from the IAN; From the five samples, two had roots that enclosed the entire maxillary artery as well as the MMA.
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Fig. 1 Schematic representation of the variation found in the origin of the auriculotemporal nerve (ATN). a, b One nerve root. Where there was only one nerve arising from the posterior division (a), four nerves passed superficial to the middle meningeal artery, and three passed deep. c Two nerve roots, with one root emerging through the foramen ovale. On one occasion the middle meningeal artery passed
through a ‘button hole’ formed by the nerve root from the foramen ovale. d–f Two nerve roots. g–i Three nerve roots. j Four nerve roots. EC external carotid artery, FO foramen ovale, IAN inferior alveolar nerve, LN lingual nerve, MMA middle meningeal artery, MA meningeal artery, PD posterior division of the mandibular division of the trigeminal nerve
ular nerve, immediately after its emergence from the foramen ovale, and the third further inferiorly. The other inferior root arose from the inferior alveolar nerve and both the inferior roots ran deep to the MMA. The two inferior roots joined to form one single branch, which then attached to both superior branches at the same point. The MMA passed between the superior and inferior roots. Symmetry between sides
Fig. 2 Photograph of a dissected infratemporal fossa and contents, viewed from the lateral aspect. Both roots of the auriculotemporal nerve can be seen passing superficial to the middle meningeal artery. The dashed line indicates the path of the maxillary artery toward the inside of the parotid gland (removed). 1 Root of the auriculotemporal nerve arising from the posterior division, 2 root of the auriculotemporal nerve arising from the inferior alveolar nerve, ATN auriculotemporal nerve, BN buccal nerve (severed), FO foramen ovale, GWS greater wing of the sphenoid, IAN inferior alveolar nerve, LN lingual nerve, LPP lateral pterygoid plate, MA maxillary artery, MMA middle meningeal artery, MN mandibular nerve, ZA zygomatic arch (cut)
Four roots One specimen had four roots; three of these originated from the main posterior division, and one arose from the IAN. In this specimen, the two superior roots originated from two separate locations adjacent to each other in the sagittal plane on the posterior division of the mandib-
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Three of the six bilaterally (four female) dissected heads had different numbers of roots on either side; this was found only on one female specimen out of the four. On one specimen the difference in the number of roots was one, and on two specimens it was two.
Discussion This study describes the variation in the anatomical relationship between the ATN and the MMA, with results suggesting that variation commonly exists not only between individuals but also within individuals. Furthermore, current textbook descriptions are not representative of observed patterns of relationship between the ATN and the MMA where the MMA is consistently described as being encompassed in a ‘button hole’ created by the roots of the ATN; we found no specimens displaying such patterns. In addition, the extent or degree of these variations is not addressed in current textbook descriptions.
Auriculotemporal nerve middle meningeal artery
Descriptive data Many anatomical textbooks describe the relationship between the ATN and MMA suggesting that a single root of the ATN forms a ‘button hole’ for the passage of the MMA or ‘encircling’ the MMA, after which the two parts of this single root converge and join (Wilson 1857; Woodburne and Burkel 1988; Feneis and Dauber 1994; Chung 1995; Palastanga et al. 1995; Williams et al. 1995; Netter 1997; Abrahams et al. 1998; Agur and Lee 1999; Moore and Dalley 1999; Sauerland 1999; Sinnatamby 1999; Gosling et al. 2002; Schmalfuss et al. 2002; Snell 2004). We found only 2 of the 25 specimens exhibited ‘button hole’ morphology of a nerve root, and on neither occasion did the MMA pass through this structure. The most common variation was for the formation of a triangle formed by the posterior division or inferior alveolar nerve (base) and the projecting roots (sides), through which the MMA was found to pass (Fig. 3). In 13 out of the 25 samples (52 %) this occurred to show the MMA running between the roots of the ATN in such a fashion. Previous publications (Baumel et al. 1971; Fernandes et al. 2003; Gulekon et al. 2005) also detail few MMAs piercing a ‘button hole’ formation of ATN roots. From the combined results of these studies it appears that such a description does not reflect normal textbook descriptions, including the latest edition of Gray’s Anatomy (Standring 2008), which show a ‘button hole’ auriculotemporal nerve with an MMA passing between the divided root. The most common relationship between the ATN and MMA is that when multiple nerve roots exist they form a triangle with the posterior root forming the base and the multiple branches the sides; in this study the MMA consistently pierces between the branches on 15 of 17 occasions (88.2 %). On the only occasions that it did not it was because the MMA had not yet originated from the maxillary artery (which itself had pierced the triangle formed by the nerve roots) or because the MMA passed under the nerve roots. Sometimes the maxillary artery also pierces this triangle, which occurred on three occasions.
Fig. 3 Schematic representation of current textbook descriptions of the relationship between the auriculotemporal nerve (ATN) and the middle meningeal artery (MMA) showing passage of the artery through the ‘button hole’ in the nerve (a) and the actual pattern that is most frequently found during dissection (b) where passage of the artery is through a triangle (broken lines) formed by the roots and the posterior division of the mandibular division of the trigeminal nerve (PD). EC external carotid artery, FO foramen ovale, IAN inferior alveolar nerve, LN lingual nerve, MMA middle meningeal artery, MA meningeal artery, PD posterior division of the mandibular division of the trigeminal nerve
formation of the ATN. Such variation needs to be considered when performing bilateral procedures of patients involving imaging, diagnoses, and surgery. Ethnicity It is difficult to reconcile ethnic variation between the few studies that have published comprehensive morphological data on the relationship between the ATN and the MMA. Baumel et al. (1971) stated the ethnicity of their cadavers as ‘mostly Caucasian, with a few American Indian and Negro specimens’ and did not state results by ethnicity; Fernandes et al. (2003) and Gulekon et al. (2005) do not state ethnicity. Rather, this present study perhaps provides a baseline on ethnic variations of the relationship between the ATN and MMA given all the cadavers were of Caucasian descent. Future studies may be able to use such information to provide further comparisons on ATN morphology between ethnicities.
Symmetry Limitations Within the six specimens that were dissected bilaterally (four females), three had variation in the number of roots comprising the ATN. From the specimens that exhibited varying numbers of nerve roots, the number of roots varied by only one on each occasion. Gulekon et al. (2005) found 7 of 16 specimens having asymmetry in the number of ATN nerve roots; on all but one occasion the number of nerve roots varied by one. This suggests that in practice a moderate to high proportion of the population will have an abnormal number of nerve roots contributing to the
In many cases the root of the ATN originated prior to its emergence from the foramen ovale. Even though positive identification could not take place, it is highly unlikely that these roots originated from any structure other than the posterior division of the mandibular nerve; these samples were therefore interpreted as having originated from this nerve. Small numbers in the sample also indicate that definitive conclusions cannot be drawn about differences between or within sexes, or within individuals. Despite
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this, it is possible to suggest trends for variations within individuals exist given that half the cases (three of six) included differences between sides.
Conclusion This study examines the relationship between the ATN and MMA in elderly Caucasian cadavers, indicating that variation in the origin and number or nerve roots consistently exists not only between but also within individuals. Variations observed in this study are similar to those of other dissection studies yet dissimilar to many textbook descriptions. It is proposed that in light of the consistency between descriptions in this and previous explorations of this region anatomical texts review their descriptions of ‘button-hole’ formation of the ATN and MMA relationship by instead highlighting the relationship between the MMA and the ‘triangle’ formed by the posterior division of the mandibular and inferior alveolar nerves and the ATN nerve roots (Fig. 3). These observations may assist in the identification of the ATN and MMA in the infratemporal fossa. Conflict of interest of interest.
The authors declare that there are no conflicts
References Abrahams PH, Hutchings RT, Marks SC (1998) McMinn’s colour atlas of human anatomy. Mosby International Ltd., Barcelona Agur AMR, Lee MJ (1999) Grant’s atlas of anatomy. Lippincott, Williams & Wilkins, Baltimore Baumel JJ, Vanderheiden JP, McElenney JE (1971) The auriculotemporal nerve of man. Am J Anat 130:431–440 Chan M, Dmytriw AA, Bartlett E, Yu E (2013) Imaging of auriculotemporal nerve perineural spread. Ecancermedicalscience 7:374 Chung KW (1995) Gross anatomy. Williams & Wilkins, Baltimore Feneis H, Dauber W (1994) Pocket atlas of human anatomy, 3rd edn. Thieme, London Fernandes PR, de Vasconselles HA, Okeson JP, Bastos RL, Maia ML (2003) The anatomical relationship between the position of the auriculotemporal nerve and mandibular condyle. Cranio 21:165–171
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Gosling JA, Harris PF, Whitmore I, Willan PLT (2002) Human anatomy: color atlas and text, 4th edn. Mosby, Maryland Heights Gulekon N, Anil A, Poyraz A, Peker T, Turgut HB, Karakosi M (2005) Variations in the anatomy of the auriculotemporal nerve. Clin Anat 18:15–22 Janis JE, Hatef DA, Ducic I, Ahmad J, Wong C, Hoxworth RE, Osborn T (2010) Anatomy of the auriculotemporal nerve: variations in its relationship to the superficial temporal artery and implications for the treatment of migraine headaches. Plast Reconstr Surg 125:1422–1428 Loughner BA, Larkin LH, Mahan PE (1990) Nerve entrapment in the lateral pterygoid muscle. Oral Surg Oral Med Oral Pathol Radiol Endod 69:299–306 Moore KL, Dalley AF (1999) Clinically oriented anatomy. Lippincott Williams & Wilkins, Baltimore Netter FH (1997) Atlas of human anatomy. Novartis, New Jersey Palastanga N, Field F, Soames R (1995) Anatomy and human movement. Butterworth Heinemann, London Sauerland EK (1999) Grant’s dissector. Lippincott, Williams & Wilkins, Baltimore Schmalfuss IM, Tart RP, Mukhevji S, Mancuso AA (2002) Perineural tumor spread along the auriculotemporal nerve. Am J Neuroradiol 23:303–311 Schmidt BL, Pogrel MA, Necoechea M, Kearns G (1998) The distribution of the auriculotemporal nerve around the temporomandibular joint. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 86:165–168 Sinnatamby CS (1999) Last’s anatomy. Churchill Livingstone, London Snell RS (2004) Clinical anatomy, 7th edn. Lippincott, Williams & Wilkins, Baltimore Standring S (ed) (2008) Gray’s anatomy, 40th edn. Churchill Livingstone, Edinburgh Stephenson JA, Panteleimonitis S, Choke E, Dennis M, Glasby M (2011) Endovascular treatment of a giant aneurysm of the maxillary artery. Case Rep Vasc Med. doi:10.1155/2011/818241 Toni R, Casa CD, Salvatore Mosca S, Malaguti A, Castorina S, Roti E (2003) Anthropological variations in the anatomy of the human thyroid arteries. Thyroid 13:183–192 Toni R, Casa CD, Castorinab S, Rotic E, Cedad G, Valentid G (2005) A meta-analysis of inferior thyroid artery variations in different human ethnic groups and their clinical implications. Ann Anat 187:371–385 Williams PL, Bannister LH, Berry MM, Collins P, Dyson M, Dussek JE, Ferguson MWJ (eds) (1995) Gray’s anatomy. Churchill Livingstone, New York Wilson W (1857) A system of human anatomy. Savill & Edwards, London Woodburne RT, Burkel WE (1988) Essentials of human anatomy, 8th edn. Oxford University Press, London
