International Journal of Pediatric Otorhinolaryngology 75 (2011) 277–281

Development of the stapedius muscle canal and its possible clinical consequences

Ana Cisneros a,*, Jaime R. Whyte Orozco a, Jesus Angel Obon Nogues a, Carmen Yus Gotor b,Ana Whyte Orozco c, Miguel Angel Crovetto de la Torre d, Arturo Vera Gil a

a Department of Human Anatomy and Histology, School of Medicine, University of Zaragoza, C/ Domingo Miral, s/n, 50009 Zaragoza, Spainb Department of Pathology, Miguel Servet Hospital, Zaragoza, Spainc Department of Animal Pathology, School of Veterinary, University of Zaragoza, Spaind Department of Otorhinolaryngology, Basurto Hospital, Bilbao, Spain

A R T I C L E I N F O

Article history:

Received 27 October 2010

Accepted 13 November 2010

Available online 10 December 2010

Keywords:

Development

Human

Stapedius muscle canal

A B S T R A C T

Objective: To study the development of the stapedius muscle canal in human embryos and foetuses.

Materials and methods: 46 temporal bones with ages between 9 mm and new-borns were studied. The

preparations were dyed using Martins’ trichrome technique.

Results: Two areas of different embryological origin form the stapedius muscle canal, which contains

this muscle and the facial nerve. On the otic capsule, at 11 weeks an extension starts to grow from its

caudal part, which moves outwards and near to Reichert’s cartilage, forming the footplate and internal

wall. The pyramidal eminence comes from the mesenchyme that surrounds the muscle, forming a

partition to separate it from the laterohyale portion of Reichert’s cartilage.

Extensive connections are observed in its development between bone marrow and mesenchyme.

At 35 weeks the muscle and nerve start to separate by means of a bony partition. If this partition does

not form, there is going to be a dehiscence that could cause peripheral nerve pathology due to the

repeated contraction of the muscle, or the dissemination of infections from middle ear.

Conclusion: During the development of the stapedius muscle canal the presence of dehiscences between

the facial nerve and the muscle may have clinical repercussions.

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1. Introduction

The pyramid is a small bone eminence located on the rear wallof the tympanum, behind and outside the tympanic sinus, fromwhose anterior end the stapedius muscle tendon extends. A canalforms on the inside of the pyramid, called the stapedius musclecanal which houses the stapedius muscle; this canal extends to therear and to the bottom of the mastoid, with its upper part in front ofthe facial nerve and its caudal part within it.

There are few references to the development of the stapediusmuscle canal, and the majority of them limit themselves to statinghow the muscle is housed on the interior, and also the presence of asmall pyramidal eminence with a small foramen at its vertex thatpermits the passage of the muscle tendon and its close relationshipwith the facial nerve.

Hanson et al. [1] describe that the pyramidal eminence formsbased on the laterohyale process of Reichert’s cartilage; for Hough[2] the bone of the pyramidal eminence comes from theprecartilaginous cells of the second pharyngeal arch; Olszewskiand Antoszewska [3] highlights the close relationship between the

* Corresponding author. Tel.: +34 976 761688; fax: +34 976 761754.

E-mail address: aicisner@unizar.es (A. Cisneros).

0165-5876/$ – see front matter � 2010 Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.ijporl.2010.11.018

anlage of the stapedius muscle and the pyramidal eminence duringthe first phase of its development between weeks 13 and 20.Spector and Ge [4] observe how, between weeks 16 and 19, thepyramidal eminence presents a cartilaginous structure and itsossification process ends between development weeks 25 and 27,whilst for Rodriguez-Vazquez [5] the pyramidal eminence isformed by an anlage independent of Reichert’s cartilage, from themesenchymal tissue of the tympanic cavity which condensesaround the belly of the stapedius muscle after 12 weeks.

2. Materials and methods

46 series of histological preparations from human embryos andfoetuses have been studied. These specimens are from 9 mm tonewborn and belong to the collection of Human Anatomy andHistology Department.

To age the foetuses, we have used the O’Rahilly and Muller tableswhich are based on different measurements (maximum length,skull-heel length, biparietal diameter, abdominal circumference andcephalic circumference) as well as body weights. These measure-ments have been compared with the data provided by the clinicalhistory and by ultrasonography, when these data were available.

The whole head was secured in embryos and foetuses of less than12 weeks’ development, whilst in older ones a thorough and

A. Cisneros et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 277–281278

meticulous dissection of the complete temporal bones wasperformed. All the samples were fixed in 10% formol, decalcifiedwith 2% nitric acid at 25 8C. The average decalcification time variedbetween one and fifteen days depending on the size and thickness ofthe piece. After the decalcification process the acid was eliminatedby washing in water.

After dehydrating the samples in increasing concentrations ofalcohol, they were embedded in paraffin, cut with a Leitz

[()TD$FIG]

Fig. 1. Development of the stapedius muscle canal. (a) Anlage of the stapedius muscle (SM

7 weeks. (c) The mesenchymatous tissue starts to form between both structures. (d) Note

the canal footplate. (e) This extension (arrow) grows between the muscle (SM) and the

mesenchyme (***). (f) Note the osteogenic capacity of the footplate and internal wall of

organic matrix (****), whilst the extension still has a cartilaginous structure (large arro

ossification. (h) and (i) Both the muscle (SM) and the nerve (F) persist in their proximity w

19 weeks, (g) 25 weeks, (h) 30 weeks and (i) 38 weeks. Martins’ trichrome technique: (a),

(F), otic capsule (OC), Reichert’s cartilage (R), Sinus tympani (ST).

microtome in series at 7 mm and stained according to the Martins’trichrome technique.

3. Results

The anlage of the stapedius muscle is located between the oticcapsule and Reichert’s cartilage, in front of the facial nerve, fromwhich it is separated by a thin cellular layer that envelopes the

) and its close relationship with the facial nerve (F). (b) This relationship continues at

how, from the otic capsule (OC), an extension forms (arrow) that will be the anlage of

laterohyale portion of Reichert’s cartilage (R). It continues with the peri-muscular

the canal (small arrows) and how the mesenchyme is becoming transformed into

w). (g) The pyramidal eminence (arrows) and the canal have now completed their

ithin the canal. (a) 6 weeks, (b) 7 weeks, (c) 10 weeks, (d) 11 weeks, (e) 14 weeks, (f)

(b) and (c) 125�, (d), (e), (f), (g), (h), and (i) 24�. Stapedius muscle (SM), facial nerve

A. Cisneros et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 277–281 279

nerve; the muscle anlage is included in the mesenchyme of thesecond pharyngeal arch, as we can see after 6 weeks’ development(Fig. 1a). The otic capsule and the proximal mesenchyme will formone single canal around the stapedius muscle and the facial nerve,which will contain this muscle and the second segment of thefacial nerve.

The separation of the muscle and the nerve commencesbetween weeks 7 and 10, when mesenchymatous tissue formsbetween both elements (Fig. 1b and c).

In the 11-week old foetus, we have observed how a cartilagi-nous extension begins to grow from the caudal part of the oticcapsule, moving outwards and near to Reichert’s cartilage. Thisextension will initially form the footplate of the stapedius musclecanal (Fig. 1d).

The cartilaginous extension of the otic capsule progressesupward between weeks 12 and 18, inside Reichert’s cartilage untilit reaches the origin of the muscle. We underline how themesenchyme that surrounds the muscle and which is situatedabove the cartilaginous extension that we have mentioned, differsin osteoblasts, forming a partition that separates the stapediusmuscle from the laterohyale portion of Reichert’s cartilage, andwhich will be the anlage of the pyramidal eminence (Fig. 1e).

At 19 weeks in the area of the otic capsule that is going to formthe internal wall and the footplate of the canal, we can see how theperichondrium acquires an osteogenic capacity and enters the otic

[()TD$FIG]

Fig. 2. Development of the stapedius muscle canal. Existence of mesenchyme-bone marr

contacts, although they persist in some areas (arrows). (b) Separation by means of an in

foetus. (c) Absence of partition between both elements in a 35-week old foetus. (d) and (f

24 weeks, (b) 28 weeks, (c) 36 weeks, (d) 37 weeks, (e) 36 weeks and (f) 37 weeks. Martin

muscle (SM), facial nerve (F), otic capsule (OC), Reichert’s cartilage (R).

cartilage by means of the blood vessels. On the external wall, theosteoblastic cells of the partition (pyramidal eminence) segregateosteoid substance, on which the organic matrix (collagen fibresand ground substance) deposits, whilst the extension of the oticcapsule continues with its cartilaginous structure (Fig. 1f).

Between weeks 20 and 24, the canal cartilage becomes ossified,enveloping the muscle, facial nerve and stylomastoid vessels. Theossification of the internal wall and the footplate of the canal isendochondral, whilst the external wall has dual ossification; thatis, the ossification of the caudal portion originating from thecartilaginous extension is endochondral whilst the ossification ofthe cranial portion is membranous. Later both portions jointogether to form spicules and bone trabeculae.

This is when we observed the presence of extensive connectionsin the stapedius muscle canal between mesenchyme and the bonemarrow, which form in the endochondral bone (Fig. 2a).

At 25 weeks, the bone pyramid surrounds the stapedius muscleand the facial nerve. When the bone walls form, this eminenceremains open at the top in a foramen (vertex) through which thetendon emerges in search of the stapedius (Fig. 1g).

Once the canal formation has ended, its bone walls graduallybecome consolidated based on compact bone by means of theapposition mechanism. With this mechanism, the endochondralbone trabeculae fuse with the periosteum layer, forming smalllacunae, inside which active osteocytes can be seen. In this period,

ow contacts on the inside of the canal (arrows). (a) Progressive disappearance of the

complete partition of stapedius muscle (SM) and facial nerve (F) in a 35-week old

) Detail of the separation between both elements by epimysium and epineurium. (a)

s’ trichrome technique: (a) and (b) 125�, (c) and (d) 24�, (e) and (f) 125�. Stapedius

A. Cisneros et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 277–281280

foramina are still observed through which the bone marrowcontacts the mesenchyme that exists on the inside of the canal(Figs. 1h and 2b).

The muscle and the facial nerve are separated by a layer ofconnective tissue on the inside of the canal (Fig. 1h).

After 35 weeks’ development, both elements start to separateby means of the growth of a bony partition which forms on thebottom and internal part of the canal and moves towards theconjunctive tissue that separates the nerve muscle (Fig. 2c).

But this partition has not developed in all the cases studied byus. Proof of this are Figs. 2d and 1i belonging to a 37-week foetusand a 38-week foetus, respectively, where the absence of thepartition that separates the facial aqueduct from the stapediusmuscle can be observed.

Fig. 2e and f reflects the above in greater detail, showing howboth formations, nerve and muscle, are only separated by theirepineurium and epimysium, respectively.

4. Discussion

There is very little information about the development of thecanal and the eminence of the stapedius muscle. Some authorssimply mention how the laterohyale process intervenes in itsformation [1], which is discussed by Louryan [6] and Rodriguez-Vazquez [5], describing one the origin in the interhyale process andthe other as being based on the mesenchymal tissue of thetympanic cavity, whilst for Hough [2] the mesenchymal cells of thesecond pharyngeal arch intervene. The close relationship with thefacial nerve is also described [4] and how the stapedius muscle ishoused on its interior [3,7].

From the ontogenic viewpoint we have observed how thestapedius muscle canal is developed from two different embryo-logical origin anlages. The otic capsule intervenes in the footplateand internal wall, via indirect or endochondral ossification, and theexternal surface, which forms a protuberance on the tympanumbox, by two different ossifications; the caudal portion thatoriginates in the extension of the otic capsule is cartilaginous,whilst the cranial portion (pyramidal eminence) is direct ormembranous.

We have observed two aspects in the formation of the stapediusmuscle canal that we wish to underline due to their clinicalrepercussion.

The first is the presence of transitory mesenchyme-bonemarrow contacts of the endochondral bone; we believe that theseconnections may play an important role in the phagocytosis of themesenchymal remains and join the elimination mechanisms ofdetritus produced during its regression, as described at the time byLinthicum et al. [8], in all the walls of the tympanum box as aprotection mechanism against acute ear infections in new borns,and recently by Miura et al. [9] who has described it in the facialrecess.

The second aspect is how the stapedius muscle and the facialnerve are housed in a common compartment and until 35 weeks’development, these two elements do not start to separate bymeans of a bone partition. This fact does not always occur, as wehave observed in our material, as a dehiscence may remainbetween the muscle and the nerve.

Way back in 1894, Politzer described the presence ofdehiscences or congenital foramina in the Fallopian canal,especially in its tympanic segment. This tympanic segment ofthe facial nerve presents a thin bone wall and frequentlydehiscences, above all in the supra-adjacent region of the ovalwindow niche.

The frequency of dehiscences is variable. Clinical studies, withdiagnosis during a surgical event, describe a prevalence of 6–35%[10], whilst anatomic studies show them from 29% to 57% [11–14].

We believe that the dehiscence develops due to deficientossification in the formation of the bone partition that separatesthe facial nerve from the stapedius muscle, which means that bothelements are only separated by a conjunctive tissue partition, anddirect contact may even be established between the muscleepimysium and the nerve epineurium. This close connectionbetween facial nerve and stapedius muscle suggests possibleclinical repercussions that we will comment below.

Facial palsy is the most frequent cranial neuropathy [15] ofwhich 70% correspond to forms of Bell’s palsy or idiopathic facialpalsy because, although a viral aetiology has been suggested thatincriminates herpes simplex, there is no definite proof about thatrelationship [16], anti-viral treatment of herpes does not appear tobe efficient, either [17]. However, there appears to be proof thattreatment with corticoids is appropriate and beneficial in thetreatment of Bell’s facial palsy [18]. Another form of facial palsy isthat associated with acute otitis media (AOM) whose physiopa-thology is somewhat controversial [19], as its development hasbeen related to different causes, including the presence ofdehiscenses of the Fallopian canal, which, exposing the nerve tothe infection of the supra-adjacent mucous, facilitate its neuritis[20]. The existence of a dehiscence between the facial nerve andthe canal that houses the stapedius muscle in some individuals, aswe have found in this work, has not been connected to the origin ofany of these forms of facial palsy. However, in our opinion, it opensup the door to future investigations for two reasons: on the onehand, the repeated contraction of the stapedius muscle, when itsfibres enter into the epineurium of the mastoid facial, couldrepresent a repeated microtraumatism of unknown reach, whichcould be the cause of neuritis such as that produced in Bell’s palsy.On the other hand, with acute otitis media, the existence ofdehiscences between the middle ear and the facial nerve, throughthe stapedius muscle canal, could provide a dissemination channelfor the infection, especially when there are no other obviousdehiscences of the Fallopian canal that explain the neuritis. Theseetiopathogenic hypotheses have not been proved but they open upnew ways of analysing these forms of facial palsy.

Acknowledgements

We are grateful to Aragon Government (DGA) and EuropeanSocial Fund for financial support in the framework of the project213-69.

References

[1] J.R. Hanson, B.J. Anson, E.M. Strickland, Branchial sources of the auditory ossiclesin man. Part II. Observations of embryonic stages from 7 mm to 28 mm (CRlength), Arch. Otolaryngol. 76 (1962) 200–215.

[2] J.V.D. Hough, Congenital malformations of the middle ear, Arch. Otolaryngol. 78(1963) 335–343.

[3] J. Olszewski, M. Antoszewska, Development of the stapedius muscle in humanfetuses, Folia Morphol. 46 (1–2) (1987) 25–27.

[4] J.G. Spector, X. Ge, Ossification patterns of the tympanic facial canal in the humanfetus and neonate, Laryngoscope 103 (9) (1993) 1052–1065.

[5] J.F. Rodriguez-Vazquez, Development of the stapedius muscle and pyramidaleminence in humans, J. Anat. 215 (2009) 292–299.

[6] S. Louryan, Le developpement des osselets de l’ouie chez l’embryon humain:correlations avec les donnees recueillies chez la souris, Bulletin de l’Associationdes Anatomistas 77 (236) (1993) 29–32.

[7] J. Whyte, A. Cisneros, C. Yus, J. Blasco, A. Torres, R. Sarrat, Contribution to thedevelopment of the stapedius muscle structure in human fetuses, Anat. Histol.Embriol. 30 (2001) 175–178.

[8] F.H. Linthicum, Q. Tian, W. Slattery, Marrow-mesenchyme connections in the fetaland newborn tympanum, Ann. Otol. Rhinol. Laryngol. 106 (1997) 466–470.

[9] T. Miura, C. Suzuki, I. Otani, K. Omori, Marrow-tympanum connections in fetusesand infants, Nippon Jibiinkoka Gakkai Kaiho 111 (1) (2008) 14–20.

[10] S. Harvey, M. Fox, Relevant issues in revision and canal-wall-down mastoidecto-my, Otolaryngol. Head Neck Surg. 121 (1) (1999) 18–22.

[11] S.H. Selesnick, A.G. Lynn-Macrae, The incidence of facial nerve dehiscence atsurgery for cholesteatoma, Otol. Neurotol. 22 (2001) 129–328.

A. Cisneros et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 277–281 281

[12] E.H. Moreano, M.M. Paparella, D. Zelterman, M.V. Goycoolea, Prevalence of facialcanal dehiscence and persistent stapedial artery in the human middle ear: areport of 1,000 temporal bones, Laryngoscope 104 (3 Pt 1) (1994) 309–320.

[13] B. Perez, M.E. Campos, J. Rivero, D. Lopez, D. Lopez-Aguado, Incidence of dehis-cences in the fallopian canal, Int. J. Pediatr. Otorhinolaryngol. 40 (1997) 51–60.

[14] E. Di Martino, B. Sellhaus, J. Haensel, J.G. Schlegel, M. Westhofen, A. Prescher,Fallopian canal dehiscences: a survey of clinical and anatomical findings, Eur.Arch. Otorhinolaryngol. 262 (2) (2005) 120–126.

[15] J.M. Gilchrist, Seventh cranial neuropathy, Semin. Neurol. 29 (1) (2009) 5–13.[16] M. Kanerva, A.J. Jaaskelainen, M. Suvela, H. Piiparinen, A. Vaheri, A. Pitkaranta,

Human herpesvirus-6 and -7 DNA in cerebrospinal fluid of facial palsy patients,Acta Otolaryngol. 128 (4) (2008) 460–464.

[17] P. Lockhart, F. Daly, M. Pitkethly, N. Comerford, F. Sullivan, Antiviral treatment forBell’s palsy (idiopathic facial paralysis), Cochrane Database Syst. Rev. 7 (4) (2009)CD001869.

[18] R.A. Salinas, G. Alvarez, F. Daly, J. Ferreira, Corticosteroids for Bell’s palsy (idio-pathic facial paralysis), Cochrane Database Syst. Rev. 17 (3) (2010) CD001942.

[19] L.O. Redaelli de Zinis, P. Gamba, C. Balzanelli, Acute otitis media and facial nerveparalysis in adults, Otol. Neurotol. 24 (1) (2003) 113–117.

[20] K. Tschiassny, Is facial palsy, when complicating cases of acute otitis media,indicative for immediate mastoid operation? Cincinnati J. Med. 25 (1944)262–266.