Variations of the attachment of the superior head of human lateral pterygoid muscle

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Journal of Cranio-Maxillo-Facial Surgery xxx (2012) 1e7

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Variations of the attachment of the superior head of human lateralpterygoid muscle

Maria Antonopoulou a,*, Ioannis Iatrou b, Alexandros Paraschos a, Sophia Anagnostopoulou a

aDepartment of Anatomy, Medical School, University of Athens, GreecebDepartment of Oral and Maxillofacial Surgery, School of Dentistry, University of Athens, Greece

a r t i c l e i n f o

Article history:Paper received 5 April 2012Accepted 12 November 2012

Keywords:Lateral pterygoid muscleSuperior headAttachmentTemporomandibular jointArticular disc

* Corresponding author. Theomitoros 42, Ag DimiTel.: þ30 210 9944148/30 697 7438049; fax: þ30 210

E-mail address: [email protected] (M. Antonopo

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a b s t r a c t

Introduction: The superior head of the lateral pterygoid muscle (LPM), is closely related to the tempo-romandibular joint (TMJ) and plays a role in the aetiology of temporomandibular disorders. Increasedactivity of this muscle has been implicated in the anterior displacement of the TMJ disc. However, there isuncertainty about the manner of the LPM attachment to the discecondyle complex.Aim: The aim of this study was to investigate the exact anatomy of the attachment of the superior head ofthe LPM (SLPM) to the discecondyle complex of the TMJ.Material and methods: Thirty-six TMJs were examined e both sides of 18 Greek cadavers (eight males and10 females, mean age 79.6 years). Examination of the attachment of the SLPM was undertaken viewedunder the dissecting microscope.Results: Variation in the attachment of the SLPM was categorized into three types: in type I, the SLPMinserted into the condyle and the discecapsule complex (55.5%). In type II, the SLPM only inserted intothe condyle (27.8%). In type III, the SLPM inserted purely into the discecapsule complex (16.7%).Conclusions: This study demonstrates that there are three different attachment types of the SLPM tothe discecondyle complex. The type III variation could be involved in the TMJ pathology. The knowledge ofthe variations of the SLPM attachment could be useful for precise surgical and pharmaceutical approaches.

� 2012 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rightsreserved.

1. Introduction

The lateral pterygoid muscle (LPM) is considered to be involvedin the movement of the articular disc and to play a unique andcomplex role in the movement of the temporomandibular joint(TMJ) (Usui et al., 2008). The clinical opinion that a disturbance tothe activity of the LPM plays an important role in the aetiology oftemporomandibular disorders (TMD) is still widely accepted(Okeson,1998; Lund, 2000). The LPM, particularly its superior head,has been the focus of many reports investigating problems asso-ciated with the TMJ and the anterior displacement of the meniscusof the joint (Naidoo and Juniper, 1997).

The LPM is a short, thick muscle which conventionally isdescribed to consist of two parts or heads: the superior (upper)head and the inferior (lower) head. The superior head arises fromthe infratemporal surface and infratemporal crest of the greaterwing of the sphenoid bone. The inferior head arises from the lateral

trios, Athens 17342, Greece.9944148.ulou).

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lou M, et al., Variations of th12), http://dx.doi.org/10.1016

surface of the lateral pterygoid plate. From the two origins, thefibres converge, and pass backwards and laterally, to be insertedinto a depression on the front of the neck of the mandible and intothe articular capsule and disc of the TMJ (Salmons, 1995).

Early in the third month of intrauterine life the muscle insertsintomesenchyme that condenses around the developing condyle ofthe mandible, but part of its tendon sweeps backwards above thecondyle and inserts into the portion of Meckel’s cartilage that laterforms the head of the malleus (Harpman and Woollard, 1938). Thispart of the tendon becomes incorporated into the articular disc ofthe TMJ; its attachment to themalleus does not persist (Rees, 1954).

Classic textbooks describe that in adults the SLPM has its inser-tion in the articular disc and in the capsule of the TMJ. This has beenconfirmed by other researchers (Altruda Filho and Alves, 2006).

Although there have been many studies of the anatomy of theLPM on cadavers, using various techniques (Table 3), there appearsto be no consensus regarding the nature of its insertion. Thedescription of the insertion has ranged from only inserting into thedisc, to being only inserted into the condyle, but most commonly ithas been described as inserting into the condyle, disc and capsule(Du Brul, 1980; Wilkinson and Chan, 1989).

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Table 1SLPM attachment type.

Type Frequency Percent (%)

Type I 20 55.5Type II 10 27.8Type III 6 16.7Total 36 100

SLPM: superior head of the lateral pterygoid muscle, type I: the SLPM inserted intothe condyle and the discecapsule complex, type II: the SLPM inserted into thecondyle, type III: the SLPM inserted purely into the discecapsule complex.

Table 2SLPM attachment type findings according gender.

Male (percent %) Female (percent %)

Type I 50 60Type II 37.5 20Type III 12.5 20Total 100 100

SLPM: superior head of the lateral pterygoid muscle, type I: the SLPM inserted intothe condyle and the discecapsule complex, type II: the SLPM inserted into thecondyle, type III: the SLPM inserted purely into the discecapsule complex.

Table 3Comparison of SLPM attachment type of various anatomic investigations.

Authors N Methods Type I Type II Type III

Porter,1970

42 Microscopicobservation

þ

Widmalmet al., 1987

10 Slices þ

Carpentieret al., 1988

10 Microscopicobservation

þ

Wilkinson, 1988 26 Macroscopic andmicroscopic study

þ

Wilkinson andChan, 1989

5 Dissectingmicroscope

þ

Naohara, 1989 25 Macroscopic andmicroscopic study

þ

Schmolke, 1994 5 Microscopicobservation

þ

Naidoo, 1996 40 Macroscopic andmicroscopicexamination

65% 27.5% 5%

Naidoo andJuniper, 1997

40 Morphologic andhistologicexamination

þ

Zhang et al.,1998

47 Macroscopic andmicroscopic study

þ

Fujita et al.,2001

20 Macroanatomicalmethod andhistologicalprocedure

þ

Christo et al.,2005

10 Serial sections at3e4 mm intervals,standardizedphotographs

þ

Usui et al.,2008

10 Macroscopic ex. þ

Akar Coskunet al., 2009

25 Macroscopic ex.Under 2.5 � loupemagnification

þ

Matsunagaet al., 2009

40 Under binoculardissectingmicroscope

þ

Kilic et al.,2010

49 Dissectingmicroscope

36.7% 26.5% 28.6%

Present study 36 Macroscopic ex.and dissectingmicroscope

55.5% 27.8% 16.7%

SLPM: superior head of the lateral pterygoidmuscle,N: number of specimens, type I:the SLPM inserted into the condyle and the discecapsule complex, type II: the SLPMinserted into the condyle, type III: the SLPM inserted purely into the discecapsulecomplex.

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Electromyographic studies have described the LPM as a musclecomposed of two heads that have reciprocal activation. The supe-rior head is active during the closing, retrusion and ipsilateral jawmovements and the inferior head is active during protrusion,opening and contralateral jaw movements (Grant, 1973;McNamara, 1973; Lipke et al., 1977; Juniper, 1983; Gibbs et al., 1984;Mahan et al., 1983). In these reports, the function of the superiorhead is based on the anatomical insertion of the head into thearticular disc. Murray et al. (2007) in contrast support the view thatthe superior head plays an important role in contralateral, protru-sive and jaw opening movements just like the inferior head andthere is evidence for functional heterogeneity within the superiorhead in order to generate specific movement directions (Murrayet al., 1999; Phanacet et al., 2003; Bhutada et al., 2008). The datafrom the previous studies do not support the notion that bothheads should be regarded as separate muscles. The LPM should beregarded as a system of fibres acting as one muscle, with varyingamounts of evenly graded activity throughout its entire range, withthe distribution of activity varied according to the biomechanicaldemands of the task (Hannam and Mc Millan, 1994; Murray et al.,2007).

The discrepancy between morphological studies and electro-myography studies might be due to the lack of precise informationof the origin and insertion of the muscle (Usui et al., 2008). Basedon such controversies, the aim of this study was to investigatethe exact attachment of the SLPM to the discecondyle complex ofthe TMJ.

2. Materials & methods

2.1. The sample

Examination of the attachments of the SLPM was carried out inboth sides of eighteen cadavers (eight males and 10 females),yielding 36 specimens. The mean age was 79.6 years (range 52e93 years). The cadavers were donated to the Department ofAnatomy for educational and research purposes.

2.2. Dissection of the specimen

A horizontal incision was made along the zygomatic arch. Themasseter muscle which connects the zygomatic arch to themandible was located and reflected down by cutting the musclealong the inferior border of the zygomatic arch. A piece of thezygomatic arch was removed. The zygomatic arch was sectioned,using a bone saw, along the vertical axis just anterior to the condyleof the mandible. Another cut about 3 cm anterior to the first wasthen made. The cut piece of the zygomatic arch was removed andthe temporal fascia beneath it was observed. After section andreflection of the temporal fascia the temporalis musclewas exposed,which originates in the temporal fossa and inserts into the anteriorborder of the coronoid process and the anterior border of the ramusof the mandible. After osteotomy of the coronoid process, thetemporalis muscle was retracted upward. The mandible was thensectioned using the bone saw just anterior to the angle of themandible. The medial pterygoid muscle was located deep to wherethe mandible was. The following nerves were located: the inferioralveolar nerve, the mylohyoid nerve branches, the lingual nerve andthe buccal nerve. The LPMwas located approximately parallel to thepreviously removed zygomatic arch. During active contraction, theLPM was noted to be capable of pulling the jaw forward. The longbuccal nerve found between the heads of the LPM provided anexcellent landmark for the separation of the heads of the LPM(Fig. 1). The space between the two heads anteriorly was filled withfibrous adipose tissue. A dissecting microscope was used to aid


M. Antonopoulou et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2012) 1e7 3

further but minimal dissection. The muscle fibres of the SLPM wereseparated into those fibres inserting into the condyle and thoseinserting into the capsule and disc.

In some cases the insertion of the SLPM muscle fibres into thecondyle or into the capsule and disc were clear. When there weredoubts about the insertion of some fibres then the application oftension with artery forceps to the capsule and to the fibres, underthe dissecting microscope, clearly demonstrated their insertion.

The capsule was then incised from the temporal bone and fromthe condyle of the mandible, thus entering the upper and lowerjoint spaces of the TMJ. The muscle attachments of the joint werephotographed and recorded after macroscopic and microscopicexaminations.

2.3. Classification of the SLPM attachment type

Variation in the attachment of the SLPM was classified into thefollowing three different types:

type I: the superior head inserted into the condyle and the discecapsule complex;

Fig. 1. The LPM on the left side. (S: superior head, I: inferior head, M: medial head,DCC: disc capsule complex, BN: buccal nerve, MA: maxillary artery).

Fig. 2. (a): The LPM on the right side. (b): Schematic drawing


type II: the superior head only inserted into the condyle;type III: the superior head inserted purely into the discecapsule

complex.

2.4. Statistical analysis

The Pearson Chi-Square test was applied for statistical analysisusing SPSS software.

3. Results

3.1. Age and gender distribution

Themean age for all specimens examinedwas 79.6 years (range:52e93 years). The mean age for males was 85.75 years (range: 77e93 years), whereas the mean age for females was 74.8 years (range:52e90 years). This difference in ages between both genders wasnot statistically significant (P ¼ 0.06).

3.2. Investigation findings

The superior and inferior heads of the LPMs were seen in alldissections, whereas a third medial head was observed in eight ofthe 36 sides (22.2%) (Figs. 1 and 3). However the heads were notalways clearly distinguishable from each other by the positions ofthe origins. It was difficult to identify the border between the headsin all specimens. The insertion of these muscles to the condyle wasalways limited to the medial half of the condylar neck at the pter-ygoid fovea. The inferior LPM followed an upward, lateral andposterior course from its origin at the lateral pterygoid plate to itsinsertion at the pterygoid fovea. The SLPM was approximately one-third the size of the inferior LPM and ran inferiorly, laterally andposteriorly from its origin at the greater wing of the sphenoid andinfratemporal crest to a point under the crest of the articulareminence where it then took a more superior course. The medialhead originated on the surface of the greater wing of the sphenoidbone. Variation in the attachments of the SLPM is summarized inTable 1.

The 55.5% of the specimens (20 of the 36 sides) showed type Iattachment. A small portion of the SLPM inserted into the ante-romedial part of the articular disc and the capsule (discecapsulecomplex). This portion arose from the most superomedial fibresof the muscle which corresponded to one-fifth of the total cross-sectional area of the SLPM. The remainder of the fibres from thesuperior head inserted into the pterygoid fovea directly or by

. (S: superior head, I: inferior head, C: condyle, D: disc).



tendon. The fibres of the superior and inferior head of the LPMfused in front of the pterygoid fovea of the condyle (Fig. 2).

The 27.8% of the specimens (10 of the 36 sides) showed type IIattachment. All the fibres of the superior head were attached to thepterygoid fovea. In these cases, the superomedial muscle fibrescould be separated from the capsule under the anterior part of thearticular disc, despite their close proximity. An upward and forwardtension on the anterior joint capsule demonstrated that thesemuscle fibres had direct insertion to the condyle at the pterygoidfovea or blended with the capsule and ran posteriorly to attach tothe condyle. The remainder of the fibres of the superior headtogether with fibres of the inferior head of the LPM was insertedinto the pterygoid fovea of the condyle (Fig. 3).

The 16.7% of the specimens (six of the 36 sides) showed type IIIattachment. The entire SLPM inserted into the discecapsulecomplex (Fig. 4).

No difference was observed between the left and right sides.Although it was more common to find the types I and III in femalesand type II in males, this gender difference was not statisticallysignificant (x2 ¼ 0.72, P ¼ 0.70, Table 2).

When the muscle fibres that inserted into the disc were pulledanteriorly with artery forceps, the tension was transmitted to thecondyle via the capsule and the disc was not pulled forwardindependently of the condyle. The condyle was pulled forward andlittle or no movement of the disc was produced either by themuscle acting on the condyle or the capsule, thus indirectlyaffecting the disc due to its attachment to both the capsule andcondyle. It was not possible to produce movement of the discindependent of the condyle, because of the fixed cadaver specimen.The manual traction of the superior head caused a forward shift ofthe whole complex, but in type III cases (entire SLPM attachment inthe discecapsule complex) the moving of the disc was moreprofound compared to the condyle.

Fig. 3. (a): The LPM on the right side. (b): Schematic drawing. (S: superior head, I: infer

Fig. 4. (a): The LPM on the right side. (b): Schematic drawing


4. Discussion

The majority of recent researchers and authors indicate that theSLPM inserts into the condyle and a small portion is frequentlyattached to the anteromedial part of the capsule and the articulardisc. This study showed that there are three different attachmenttypes of the SLPM to the discecondyle complex. The finding of thepresent study, that the entire SLPM is attached to the discecapsulecomplex (type III), although not described by the most recentanatomic studies, to our opinion is significant and should be takeninto consideration.

Anatomic studies of the tissues of the TMJ may be carried outusing histologic sections or by direct viewing under the dissectingmicroscope. The advantage of histologic sections is that it ispossible to selectively highlight different tissue types. The advan-tage of the dissecting microscope is that it allows a three-dimensional view of the specimen and more importantly allowsapplication of tension to different muscle and capsular fibres(Wilkinson and Chan, 1989).

There was wide anatomic variation between the specimensand this may explain some of the confusion in the literature inrelation to the nature of the SLPM. A cause of confusion in theliterature may be due to the fact that the true insertion of thismuscle is only made clear when the capsular and muscular fibresare lifted and stretched. The nature of the SLPM attachment alsovaries from the central to the medial part of the joint with the disc,capsule and SLPM fibres converging on the medial pole of thecondyle.

Many investigations about attachment of the LPM to the discecondyle complex have been reported already (Table 3). Most ofthese agree that the LPM consists of two heads, with the lower headattached to the pterygoid fovea, but there are controversiesbetween opinions regarding the attachment of the superior head.

ior head, M: medial head, C: condyle, D: disc, Caps: capsule, MA: maxillary artery).

. (S: superior head, I: inferior head, C: condyle, D: disc).



Most authors (classic textbooks) and earlier anatomical studieshave reported that the superior head of the muscle inserts into thearticular disc and the lower head inserts into the pterygoid fovea(Rees, 1954; Porter, 1970; Altruda Filho and Alves, 2006). Accordingto the results of the present study, the SLPMwas attached purely tothe disc (type III) only in three cadavers (six of the 36 sides, 16.7%).Naidoo (1996) reported the same finding in two out of 40 speci-mens examined (5%), and Kilic et al. (2010) in 14 specimens out of49 (28.6%).

More recent studies have reported that a small number ofmuscle fibres, the most upper and inner fibres of the SLPM areattached to the articular capsule and connected to the anteromedialaspect of the articular disc, while the remaining fibres of thesuperior head and the lower head are attached to the pterygoidfovea (Choukas and Sicher, 1960; Sicher, 1965; Meyenberg et al.,1986; Widmalm et al., 1987; Carpentier et al., 1988; Schmolke,1994; Naidoo, 1996; Naidoo and Juniper, 1997; Usui et al., 2008;Matsunaga et al., 2009; Akar Coskun et al., 2009).

In this study we found that in the majority of the specimens(55.5%), the main attachment of the SLPM was to the condyledirectly or by tendinous fibres. Only a few superomedial fibresappeared to insert into the discecapsule complex (type I).

However, other studies have not observed a direct muscle inser-tion into the disc. It has been described that the articular disc has nocontact with the LPM (Pinkert, 1984). Wilkinson (1988) reportedthat a small accessory insertion comprising the upper most 20% ofthe muscle, terminated under the foot of the disc. Then blendedwith the anterior ligament and run posteriorly to gain insertion intothe condyle. These muscle fibres did not pass through the capsuleand did not insert into the disc. Wilkinson and Chan (1989) too, re-ported that no muscle fibres were seen passing through the capsuleto insert into the body of the articular disc. Christo et al. (2005) alsoconcluded that a true muscle insertion of the superior head ofthe LPM to the disc was not observed. These studies support thatthe major insertion of the SLPM is to the condyle at the pterygoidfovea and are in accordance with our type II classification.

Kilic et al. (2010) described the same three types of attachmentsof the SLPM which were described in the present study. Anothertype was also described, where the superior head inserted into thediscecapsule complex and the inferior head inserted into thecomplex and condyle. This fourth type was described by Naohara(1989) and Fujita et al. (2001) too.

Most studies have not quantified the amount of fibres insertinginto the articular disc. Naohara (1989) found this attachment to bean area of 3 mm2 that corresponded to 30% of the area of thesuperior head and 3% of the total amount of the lateral pterygoidmuscle fibres. Naidoo and Juniper (1997) reported that approxi-mately 29.5% of the fibres of this muscle were inserted into themeniscus of the temporomandibular joint. Zhang et al. (1998) re-ported that 52% of the SLPM fibres insert to the condyle, 10% to thearticular disc, 24% to the capsule and 14% to the anterior attachmentof the disc. In our study in type I, the portion of fibres which wereinserted into the discecapsule complex relative to the amount of theSLPM was estimated macroscopically as approximately one-fifth.

This muscle is commonly thought to be responsible for theanterior disc displacement (Murray et al., 2001). Actually, despiteits functional heterogeneity it may allow the selective activation ofthe fibres that connect to the disc, without causing the whole discecondyle complex to be dragged anteriorly; studies on cadavericspecimens suggested that the manual traction of the superior headcauses a forward shift of the whole complex (Widmalm et al., 1987;Wilkinson, 1988; Christo et al., 2005).

Disc displacement of the TMJ is a common condition. Manyhypotheses have been proposed over the years in an attempt toexplain the pathogenesis of disc displacement, and many structural


factors were suspected as possible risk factors. According to theliterature, the roles of morphological (occlusal abnormalities andinclination of the eminence) and functional factors (hyperactivity ofthe LPM) appeared to be much less important than hypothesized inthe past (Manfredini, 2009). Efforts aremade in order to explain diskdisplacement (Kaya et al., 2010, Kim et al., 2012, Roh et al., 2012).

The view that the SLPM can cause an anteriorly displaced disc isvery simplistic. Some parts of the superior head do appear to beactive during intercupsal clenching, but the joint must be unloadedfor this to have an affect on the disc (Phanacet et al., 2003; Christoet al., 2005). Carpentier et al. (1988) demonstrated that the maininsertions of the SLPM are to the condyle. They concluded that inconsidering the anatomical organization of the SLPM, the expla-nation of anterior displacement of the disc due to a spastic activityof this muscle alone is not probable. However Wongwatana et al.(1994) reported that since other factors (e.g., trauma) can resultin disc displacement, the SLPM can maintain disc displacementonly when it inserts directly into the disc.

Some authors claim that internal derangement of the TMJ is theresult of LPM hyperactivity or hypoactivity, poor coordinationbetween the two heads of the muscle, and/or a disturbance in thenormal role of the muscle in the control or stabilization of the TMJ(Scapino and Mills, 1997; Okeson, 1998; Hiraba et al., 2000; Murrayet al., 2001). Some literature reports state that there is no goodscientific evidence that the lateral pterygoid muscles of patientswith TMD are functionally disturbed. The role of the lateral ptery-goid muscle in normal function and TMDs remains controversialand needs re-evaluation (Murray et al., 2004, 2007).

Other studies evaluated the relationship between the LPMattachment type and internal derangement of the TMJ basedon MRI observations. Taskaya-Yilmaz et al. (2005) concluded thatsince the SLPM only attached to the disc, the disc may displaceanteriorly very easily and this situation will reduce the functionof this muscle which may cause muscle atrophy. There was nostatistically significant difference between the type of muscleattachment and the presence or absence of disc displacement butthere was a statistically significant difference between the type ofmuscle attachment and the presence of muscle atrophy and muscledegeneration. Mazza et al. (2009) published a study close to theprevious one and concluded that when the SLPMwas inserted onlyinto the disk, the percentage of disk dislocation without reductionwas greater. This study supported that it is possible to impute tothis attachment type a negative prognostic value for a long-termimprovement of disc pathology and to consider the possibilitythat this muscle may contribute to dislocating the disc when itsinsertion is directed only on the disc itself. However Degrin et al.(2011) concluded that there was no statistically significant corre-lation between the LPM attachment types and TMJ abnormalities.

The findings in the present study, which are similar with thoseof Kilic et al. (2010), may also lead to the assumption that the typeof LPM attachment may determine the tendency for TMJ disordersand may guide clinicians to use preventive treatment methods inthose patients who are identified as high-risk patients.

Botulinum toxin (BTX-A) injections in the LPM are more recenttreatment for patients with severe clicking of the TMJ associatedwith anterior disc displacement. Although the precise mechanismis unclear, this treatment seems to reduce the action of the muscle,to improve the discecondyle relationship and to eliminate theclicking (Bakke et al., 2005; Yoshida and Iizuka, 2006; Majid, 2010).In cases of therapeutic failure of suchmethods the cause could lie inthe presence of an entire SLPM attachment to the discecapsulecomplex (type III of our study).

The knowledge of the variable attachments of the SLPM to thediscecondyle complex of the TMJ may ensure more precise surgicaland pharmaceutical approaches.



5. Conclusion

By examining 36 specimens from 18 human cadavers we wereable to clear up the exact attachment of the SLPM to the discecondyle complex of the TMJ. Our principal findings are:

� there is a variable attachment of the SLPM. We found threedifferent SLPM attachment types;

� in the majority of cases (55.5%), the main insertion of the SLPMwas to the condyle at the pterygoid fovea. Only a few super-omedial fibres of the superior head were inserted into themedial aspect of the capsule and the disc;

� in 27.8% of cases the SLPM inserted directly into the condyle;� in 16.7% of cases the SLPM attachment was into the discecapsule complex. This variation is in our opinion significantand should be taken into consideration by surgeons and otherclinicians;

� in all joints, the application of forward tension to SLPMmuscle fibres was always transmitted to the condyle and didnot move the disc forward independently of the condyle. Themanual traction of the superior head causes a forward shiftof the whole complex, but with an interesting observation thatin type III cases (entire SLPM attachment in the discecapsulecomplex) the moving of the disc was more profoundcompared to the condyle.

We hope that these findings are useful to Oral and Maxillofacialsurgeons and other clinicians who manage temporomandibulardisorders.

Role of funding sourceNone.

Conflict of interestNone.

Acknowledgements

None.

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Variations of the attachment of the superior head of human lateral pterygoid muscle

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