The Tensor Tympani Tendon: A Hypothetical Site of Origin of Congenital Cholesteatoma

Abstract

Multiple theories have been discussed about the etiopathogenesis of congenital middle ear cholesteatoma (CMEC) and its specific site of origin. The intraoperative identification of the precise location of the keratinous mass is important to guarantee its complete removal, in order to reduce the risk of recurrence. This study proposes the tensor tympani tendon (TTT) as a possible site of origin of CMEC. All CMECs treated between 2013 and 2019 were reviewed. Only Potsic stage I lesions were included. Preoperative radiologic images were compared to intraoperative findings. Three removed TTT were sent for histologic evaluation. Seven patients were included (M:F = 3:4). Preoperative CT images were classified as type A in 2 cases (28.6%) and type B in 5 cases (71.4%). At intraoperative evaluation all CMEC sacs were found pedunculated on the TTT. The histologic examinations confirmed the connection between the cholesteatomatous sac and the TTT. According to the correlation of imaging, intraoperative findings and histology, we proposed that the TTT could be the primary site from which CMEC originates.

Introduction

Congenital middle ear cholesteatoma (CMEC) is defined as a keratinous mass located behind an intact tympanic membrane. CMEC accounts for only 0.2% to 1.5% of all intracranial tumors and approximately for 2% to 5% of all cholesteatomas, representing a rare entity [1].

Typically, CMEC may grow for years without symptoms, but if left untreated, it can extend to involve the epitympanum, the mastoid antrum, and the petrous portion of the temporal bone, causing conductive hearing loss, sensorineural hearing loss, vertigo, or tinnitus.

Multiple theories have been discussed about the etiopathogenesis of CMEC and its specific site of origin. The intraoperative identification of the precise location of the keratinous mass is important to guarantee its complete removal, in order to reduce the risk of recurrence.

The aim of this study is to report a cohort of pediatric patients surgically treated for early stage CMEC localized in the area of the tensor tympani tendon. The data supporting this specific localization as a hypothetical site of origin of CMEC and its possible implications are herein discussed.

Materials and Methods

A retrospective review of CMECs surgically treated at the Hospital of Carpi and University Hospital of Modena between 2013 and 2019 was performed. CMECs were diagnosed according to Levenson’s criteria: (1) presence of a white mass in the middle ear cavity, (2) normal pars flaccida and pars tensa of the tympanic membrane, (3) no past history of otorrhea and perforation, (4) no previous otological surgery, (5) the past history of otitis media or effusion should not be an exclusion criterion.

All reviewed cholesteatoma were staged according to Potsic classification (Table 1) [2, 3].

Table 1.

Potsic’s classification for congenital cholesteatoma

Stage I	Disease confined to a single quadrant
Stage II	Disease in multiple quadrants, but without involvement of ossicular chain or mastoid extension
Stage III	Disease involving the ossicular chain, without mastoid extension
Stage IV	Disease with mastoid extension

Among the 18 cases of CMEC operated in the considered time, 7 were Potsic stage I (early stage congenital cholesteatoma without involvement of ossicular chain or mastoid extension) and were included in the present study.

Preoperative Assessment

All patients underwent preoperative otoendoscopic evaluation, audiometric tests (pure tone audiometry and tympanometry) and temporal bone computed tomography (TBCT) [4].

Radiologic images were retrospectively reviewed, with particular attention to the relationship of the cholesteatoma with the cochleariform process and the tensor tympani tendon. The cholesteatoma extension was classified following the criteria of Lee et al. on TBCT [5].

Surgical Steps

Three patients underwent microscopic tympanoplasty through retroauricular approach and 4 patients underwent totally endoscopic transcanal tympanoplasty.

The surgical steps of microscopic tympanoplasty were: skin infiltration of the retroauricular region and of the external auditory canal (EAC), post-auricular incision, identification of the external auditory meatus, creation of the posterior vascular strip and access into the lumen of the canal, canaloplasty, elevation of the tympano-meatal flap, detachment of the tympanic membrane from the handle of the malleus, identification of the cholesteatoma.

The surgical steps of endoscopic tympanoplasty were: infiltration of the skin of the EAC with adrenaline solution, Rosen incision and elevation of the tympano-meatal flap, detachment of the tympanic membrane from the handle of malleus, identification of the cholesteatoma (Fig. 1).

Fig. 1.

a–d Endoscopic intraoperative appearance of four stage I congenital middle ear cholesteatomas and relevant surgical landmarks. cc congenital cholesteatoma, hm handle of the malleus, i incus, fn facial nerve, s stapes, rw round window

In both approaches, the removal of the cholesteatoma followed the resection of the tensor tympani tendon (Fig. 2). A thorough inspection of the middle ear through angled optics was performed and the region of the tensor tympani tendon was cauterized to eliminate any residual epithelial cells, in an attempt to reduce the risk of recurrence.

Fig. 2.

Microscopic intraoperative view of congenital middle ear cholesteatoma, before removal. a relationship between the cholesteatomatous sac and the tensor tympani tendon; b cutting the tensor tympani tendon before removing the cholesteatoma

Being uninvolved in any of the included cases, the ossicular chain was routinely preserved. The chorda tympani was sectioned in three patients, given the close proximity to the cholesteatoma.

Histological examination of the removed keratinous tissue and the adjacent tensor tympani tendon was performed in 3 cases, to confirm the diagnosis of CMEC and microscopically assess the relationships between these structures.

Post-operative Period

A standardized follow-up for CMEC was conducted at 1 and 6 months post-operatively. Thereafter, the follow-up visits were planned every 6–12 months, depending on the healing results and post-operative outcomes. At each follow-up, otoendoscopy and pure tone audiometry were performed and compared to the previous clinical images and audiograms. Given the limited extension of the pathology and the fact that the tympanic membrane was preoperatively intact and not reconstructed, clinical evaluation was considered sufficient for monitoring.

Results

A total of 7 patients were included (M:F = 3:4). Mean age at surgery was 7 (range 3–18).

In all cases, preoperative TBCT images showed the presence of a small (max diameter: 4.7 mm) isodense tissue located in the anterior epitympanum and mesotympanum, and according to Lee et al5 the cholesteatoma was classified as type A (no involvement of cochleariform process) in 2 cases (28,6%) and type B (involvement of cochleariform process) in 5 cases (71,4%) as shown in Fig. 3a, b. Consistently with the definition of Potsic I stage, none of our patients fell into group C. All mastoids were well pneumatized.

Fig. 3.

Comparison between preoperative temporal bone computed tomography of type I B congenital cholesteatoma (a) and intraoperative endoscopic view after elevation of the tympano-meatal flap (b). cp cochleariform process, tt tensor tympani tendon

In all cases intraoperative findings confirmed that the cholesteatomatous sac was pedunculated on the tensor tympani tendon, either close to the cochleariform process or in proximity of its insertion on the malleus handle. The surrounding middle ear mucosa was without signs of chronic inflammation and the ossicular chain intact.

Histologic examination of the sent specimens showed a cyst lined by keratinizing, multilayered, epidermoid cells, akin to epidermis, corresponding to cholesteatoma (Fig. 4a). A thin layer of small, cuboidal cells was localized around the tendon, and connected to the epithelium of cholesteatoma (Fig. 4b). Low-intermediate weight cytokeratins (MoAb MNF-116) strongly stained these cuboidal cells, whereas only faint staining was observed in basal layer of cholesteatoma (Fig. 4c and d). A tendon and a nerve, embedded in fibrous tissue surrounding the cyst wall were visible in all three cases (Fig. 5).

Fig. 4.

a Histologic evaluation of congenital middle ear cholesteatoma (CMEC). a Keratinizing, stratified epithelium lining CMEC (hematoxylin–eosin staining—H&E, 40×); b CMEC surrounded by fibrous tissue including a thin layer of cuboidal cells (H&E, 10×); c Cuboidal cell surrounding tendon (MNF-116); d cuboidal cells connecting to the wall of CMEC (MNF-116)

Fig. 5.

A 200 × hematoxylin–eosin staining showing the close relationship between the tensor tympani tendon and the congenital middle ear cholesteatoma

The median follow-up was 31 months (range 14–50). Neither intraoperative nor postoperative complications were reported. The post-operative audiometric examination at last follow-up did not report any case of sensorineural decline and the average ABG resulted 10 dB (range 5–15).

Discussion

According to the correlation of radiologic imaging, intraoperative findings and histological evaluation of the included cases, we proposed that the tensor tympani tendon could be the primary site of entrapped keratinized cells, from which CMEC originates.

Several theories have been developed debating on the etiology of CMEC and parallel to this, on the site of origin of the epidermoid cells. Michaels theorized that in normal individuals, an epidermoid formation of nonkeratinizing squamous epithelial cells is localized in the lateral wall of the Eustachian tube, near the anterior limb of the tympanic ring [6]. It seems to act as an organizer in the development of the tympanic membrane and middle ear in embryonic or early fetal live. According to his investigations, the epithelial formation disappears at 33 weeks’ gestation in all fetuses, but some may persist, holding the potential to become CMEC. The site of this epidermoid formation in the antero-superior and lateral part of tympanic cavity, as proposed by Michaels, corresponds to the most frequent site of CMEC reported in the literature [2, 7].

Nevertheless, some critics have been moved against this theory. First of all, if the epithelial formation is supposed to be the cause of the mesotympanic cholesteatoma, it should primarily grow into the tympanic orifice of the Eustachian tube and then gradually expand into the tympanic cavity. Such types of cholesteatoma have never been described, and no connection between CMEC and the site of origin of the epidermoid formation has been found. Furthermore, there is no histological documentation that the cells of the epithelial formation mentioned by Michaels are keratinizing.

Sadé believed that CMEC could derive from a metaplastic transformation of middle ear mucosa into stratified squamous epithelium due to inflammation, which could form keratin [8]. Rüedi explained it as an invasion of the squamous epithelium by proliferation of the epithelial cones through a macroscopically intact, but microscopically injured, tympanic membrane [9]. Considering that CMEC were usually found near the tympanic isthmus, the junction of the first and second branchial arches, Aimi postulated that CMEC resulted from the migration of the ectoderm from the external ear into the middle ear, normally inhibited by the tympanic ring to induce the tympanic membrane in a proper position [10]. Tos assumed that CMEC could originate from retractions of the eardrum that may be repeatedly fixated to the malleus or incus and then loosened again. During these processes an inclusion of keratinized squamous epithelium may occur, leading in a few cases to cholesteatoma formation [11].

Similarly, several sites of congenital cholesteatoma have been described and for each of these, the proposed theories do not seem to be totally convincing. In Western countries the most frequent localization is at the level of the anterior quadrants of the tympanic membrane, as in all our cases, while in Eastern countries the localization posterior to the malleus handle seems to be more common. This latter site could be more frequently associated with ossicular chain anomalies, such as the absence of the long process of the incus, and/or the suprastructure of the stapes [12]. These findings suggest that the pathogenesis of CMEC cannot be adequately explained by one theory alone but probably combining elements from different theories.

Early diagnosis of CMEC is usually difficult and mostly accidental given the lack of symptoms. Nevertheless, when the cholesteatoma is diagnosed at early stage, it could be easier to unearth its primary site of origin, before the disease could cause erosion and infiltration of the neighbouring structures. In case of extensive cholesteatoma, it could also be difficult to establish confidently if the cholesteatoma is congenital rather than acquired.

For this reason, only patients with early stages congenital non-infiltrating sacked cholesteatoma were enrolled in the present case series, representing the most appropriate cohort of patients to investigate this topic. In all cases, after careful inspection of the middle ear, it was possible to identify the connection of the cholesteatoma with the tensor tympani tendon, which was dissected and in three cases sent for histologic examination.

The close relationship of CMEC with the cochleariform process has already been enlightened by previous studies, and has been used as a landmark to distinguish stage II from stage I CMEC [5]. However, neither the cochleariform process nor the tensor tympani tendon have never been considered as the primary site of CMEC.

According to the present authors, even in doubtful cases of cholesteatoma in which a congenital origin is suspected, the region of the tensor tympani tendon should be carefully explored and, in case of infiltration, the tendon should be removed and subsequently cauterized with the aim of eventually minimizing the recurrence rate. It is interesting to notice that according to postoperative audiometric results the removal of tensor tympani tendon did not impaired audiological outcomes.

In this study cohort a second-look tympanoplasty was not performed, given the small dimension and the sacked characteristic of cholesteatomas, and the surgical complete remediation, as confirmed by the final inspection of middle ear cavity through angled optics. Moreover, ossicular chain integrity did not require deferred ossiculoplasty.

It should be underlined that the role of the tensor tympani tendon as a site of origin of CMEC remains hypothetical and its validity is limited by the paucity of patients and histological confirmations collected. Moreover, the early stage of cholesteatoma, which intrinsically show a lower risk of recurrence, further limits the implications of tensor tympani tendon exploration and removal on long-term disease control.

To conclude, to date the etiopathogenesis of CMEC remains unclear and smoky. The theories formulated to explain its origin do not find unanimous approval and probably the real mechanism of development is not yet known. The histological finding of epithelial cells in connection with the tensor tympani tendon could pave the way for new research aimed at investigating defects in its development. This findings may also have a surgical implications, as the careful removal of keratinous remnants from this region and the removal of the tensor tympani tendon could lower the risk of recurrence, probably even in more advanced stages.

Further studies are necessary to confirm this theory and to verify the clinical implications of these surgical refinements.

Funding

None.

Declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this kind of retrospective investigation, our institutional review board does not perform a formal ethical assessment. This article does not contain any studies with animals performed by any of the authors.

Informed Consent

Informed consent was obtained from all individual participants included in the study.