Injuries to the distal tibiofibular syndesmosis are challenging to treat. For syndesmotic injuries, screws have been used as the gold standard for fixation1. However, screw fixation results in limitation of the physiological mobility of the fibula, leading to complications such as screw breakage, malpositioning, and malreduction. Recently, suture-button fixation has become a promising and more physiologically sound alternative compared with screw fixation2–5. Irrespective of which fixation method is better for reducing syndesmotic injury, a precise understanding about the anatomy of the interosseous tibiofibular area is essential for the reduction and stabilization of the syndesmosis between the distal parts of the tibia and fibula.
The syndesmosis is thought to be stabilized by 4 ligamentous structures, namely, the anterior inferior tibiofibular ligament (AITFL), posterior inferior tibiofibular ligament (PITFL), transverse ligament, and interosseous ligament (IOL). In particular, anatomical knowledge about the IOL is very relevant to interosseous fixation (including fixation with use of positioned screws and suture buttons) because this structure could be a stabilizer, such as a pivot point for syndesmosis motion. The IOL is anatomically described as the most distal end of the interosseous membrane (IOM) and is pyramid-shaped. Although the IOL is widely attached to the interosseous tibiofibular area, its contribution to syndesmotic stability has been unclear because of the heterogeneity and ambiguity of its histological configuration, including fibrous structures and fatty tissues.
Bone is a highly adaptive structure when under mechanical stress load6,7. Previous reports have shown that high tensile stresses that are transmitted via dense connective tissues such as tendons, ligaments, and aponeuroses affect the morphology and cortical bone thickness of the attached structures8–10. Nonetheless, the morphological features of the interosseous tibiofibular area in relation to the tensile stress of the IOL have rarely been discussed. These morphological features can aid in understanding the precise location where the tensile stress of the IOL is loaded.
The purpose of the present study was to investigate the IOL between the tibia and the fibula on the basis of osseous surface morphology and macroscopic and histological anatomy. We hypothesized that the osseous surface of the interosseous tibiofibular area has a specific feature corresponding to the fibrous structure in the IOL.
Materials and Methods
Preparation of Cadaveric Specimens
Nineteen ankles (4 ankle pairs, 3 right ankles, and 8 left ankles) from 15 Japanese cadavers (9 male, 6 female) with a mean age (and standard deviation) of 79.3 ± 9.5 years (range, 61 to 94 years) at the time of death were obtained for this study. All cadavers had been donated to the Department of Anatomy of Tokyo Medical and Dental University. All cadaveric specimens were fixed in 8% formalin, preserved in 30% ethanol, and cut at the level of the distal third of the ankle with use of a diamond band pathology saw (EXAKT 312; EXAKT Advanced Technologies). For tibiofibular syndesmosis dissection, the skin and subcutaneous tissues were removed.
In all specimens, the osseous configuration of the medial side of the fibula and the lateral side of the tibia was examined with use of a micro-computed tomography (micro-CT) scanner (inspeXio SMX-100CT; Shimadzu). The micro-CT parameters were as follows: resolution, 200 μm; voltage, 100 kV; current, 80 μA; source-to-detector distance, 700 mm; source-to-rotation center distance, 500 mm; pitch, 0.179; slice thickness, 0.200 mm; field of view (xy), 91.55 mm; field of view (z), 45.0 mm; matrix, 512 × 512; and voxel size, 0.179 mm/voxel. Three-dimensional images were reconstructed with use of ImageJ software (version 1.52; National Institutes of Health). One ankle with osteoarthritis and deformity was excluded. Of the remaining 18 ankles (3 ankle pairs, 3 right ankles, and 9 left ankles), 15 and 3 were randomly assigned for macroscopic and histological analyses, respectively.
Cortical Thickness Mapping of Interosseous Tibiofibular Area
To visualize the distribution of cortical bone thicknesses on the medial side of the fibula and the lateral side of the tibia, we utilized 8-bit images of the 18 specimens, which were obtained as previously described. ImageJ software and the BoneJ plug-in8 were used to define the thickness at a point by measuring the diameter of the largest sphere that fit within the structure of interest11,12. Cortical bone thicknesses on the medial side of the fibula and the lateral side of the tibia were mapped in 3 dimensions; these areas were observed as well. Thicker points of the cortical bone were represented by brighter colors.
To quantify cortical bone thicknesses, we used the coronal section, which included the apex of the prominence on the medial aspect of the fibula, parallel to the plane between the tip of the medial and lateral malleoli. The cortical bones were divided into the proximal part of the tibia, distal part of the tibia, proximal part of the fibula, and distal part of the fibula using 3.0 × 12.0-mm rectangles bordering the fibular prominence. To determine intraobserver reproducibility, an observer (A.T.) randomly repeated the measurements 2 times. Furthermore, the means and standard deviations of the average cortical bone thicknesses of the quadrants were calculated.
Macroscopic Observation of Interosseous Tibiofibular Area
Fifteen ankles were analyzed macroscopically. All muscles and tendons were removed to expose the ankle syndesmosis, and the fibular artery and anterior branch artery, which perforate the IOM, were preserved. Initially, only the collateral ligaments of the ankle were removed to expose the edges of the fibula and tibia. The arteries were removed after observing the presence and location of the perforating branch of the fibular artery. To comprehensively observe entire structures in the interosseous tibiofibular area, we detached the IOM and IOL, which were interposed between the tibia and fibula (Fig. 1-A), as well as the AITFL, PITFL, and periosteum en bloc in the following order. First, we detached the AITFL and PITFL from the fibular side (Fig. 1-B) and subsequently took the fibula off by detaching the IOL and IOM to confirm their osseous attachment (Fig. 1-C). Second, to observe the tibial side, we detached the AITFL and PITFL from the tibia while preserving the connection between the periosteum, AITFL, and PITFL. Finally, we took the tibia off from the complex including the IOM, IOL, AITFL, PITFL, and periosteum (Fig. 1-D). The location of the osseous prominence was measured with use of a caliper with an accuracy of 0.1 mm.
Histological Analysis of Interosseous Tibiofibular Area
Histological examinations of the interosseous tibiofibular area were conducted on 3 randomly selected ankles. Using a diamond saw, we obtained 2 blocks (height, 5 mm) perpendicular to the axis of the leg at the level of the osseous prominence on the medial aspect of the fibula and at the middle level of the IOL. These regions were identified by 3-dimensional conformations of the micro-CT images. En bloc specimens were decalcified for 1 week with Plank-Rychlo solution (AlCl3:6H2O, 126.7 g/L; HCl, 85.0 mL/L; HCOOH, 50.0 mL/L) and were dehydrated. After fixation, the specimens were embedded in paraffin solution. Subsequently, the blocks were serially sectioned (thickness, 5 μm) and were stained according to the Masson trichrome staining protocol.
All data were expressed as the mean and the standard deviation. The Kruskal-Wallis 1-way analysis of variance (ANOVA) test was used to compare the cortical bone thicknesses of quadrants between the proximal part of the fibula, distal part of the fibula, proximal part of the tibia, and distal part of the tibia. When significant differences among quadrants were evident, comparisons were made between groups with use of the Steel-Dwass post hoc test. Intraobserver reliabilities were assessed with use of intraclass correlation coefficients (ICCs). A coefficient of >0.75 was considered to indicate excellent agreement. All ICCs were ≥0.96 (range, 0.96 to 0.98). All statistical analyses were performed with use of R for Windows (version 4.0.1; R Development Core Team), with the level of significance set at p < 0.05.
Osseous Surface Morphology of Interosseous Tibiofibular Area on Micro-CT
Micro-CT imaging revealed the osseous prominence on the medial side of the fibula in all specimens (Fig. 2-A and 2-C). No specific morphological features were identified on the lateral aspect of the tibia (Fig. 2-B and 2-C). Cortical thickness mapping with use of micro-CT data showed that the cortical bone on the medial side of the fibula proximal to the prominence was brightly colored, indicating thicker cortical bone (Fig. 3-A and 3-B). We compared the cortical bone thicknesses of 4 assigned rectangular areas––the area proximal to the fibular prominence (Fp), the tibial area corresponding to Fp (Tp), the area distal to the fibular prominence (Fd), and the tibial area corresponding to Fd (Td) (Figs. 3-C and 3-D). The cortical bone thicknesses of Fp, Tp, Fd, and Td were 1.4 ± 0.5, 0.8 ± 0.2, 0.7 ± 0.2, and 0.5 ± 0.1 mm, respectively. The cortical thickness of Fp was greater than that of other areas (p < 0.001) (Fig. 3-E).
Macroscopic Observation of Interosseous Tibiofibular Area
In all specimens, the perforating branch of the fibular artery passed from the posterior to the anterior aspect of the lower leg just distal to the IOM and proximal to the AITFL and PITFL (Figs. 4-A and 4-B). The IOM and IOL could be continuously detached from the tibia and fibula; the AITFL and PITFL were detached from the tibia while preserving the connection between the periosteum, AITFL, and PITFL (Figs. 5-A through 5-D). The IOL was observed as the distal extension of the IOM and fatty tissues located between the AITFL and PITFL. At the distal end of the IOM, the IOM anteriorly and posteriorly transitioned into the AITFL and PITFL, respectively. The perforating branch of the fibular artery ran through the proximal top of the IOL (i.e., proximal to the bifurcation of the IOM), which formed a thickened fiber (section mark [§] in Figure 5-A). In all specimens, the osseous prominence was observed on the medial aspect of the fibula, which corresponded to the thickened fibrous part of the IOL. The apex of the osseous prominence on the medial aspect of the fibula was located 51.3 ± 4.2 mm proximal to the tip of the lateral malleolus and 9.4 ± 2.0 mm posterior to the anterior ridge of the fibula (Fig. 5-B).
Histological Features of Interosseous Tibiofibular Ligament
At the level of the osseous prominence of the fibula, the thickened fibrous part of the IOL was densely stained and was widely attached to the medial aspect of the fibula via a fibrocartilaginous insertion (Figs. 6-A, 6-B, and 6-C). At the middle of the IOL, thin and fatty-like tissue was interposed between the tibia and fibula and was faintly stained (Figs. 6-A, 6-D, and 6-E).
The present study revealed that the osseous prominence on the medial aspect of the fibula provided an attachment point for the thickened part of the IOL, which was the bifurcation of the IOM into the AITFL and PITFL. The thickened proximal part of the IOL was consistently found in this location; we believe that this finding was related to the fact that the fibular artery perforated the adjacent distal part of the IOM (Fig. 7). Additionally, histological analysis indicated that the thickened part of the IOL attached to the prominence on the medial aspect of the fibula through the fibrocartilage. Therefore, based on the IOL attachment corresponding to the osseous prominence and fibrocartilage, these findings supported our hypothesis.
With respect to the anatomical knowledge of osseous morphology in the interosseous tibiofibular area, the crista interossea tibiae and fibularis have been regarded as the distal margin of the IOM attachment13. Furthermore, the fibular notch of the tibia has been known to be concave, in contrast to the convex shape of the fibula in the syndesmosis13. However, the morphological characteristics of the transition zone between the crista and the notch have not been recognized14. The current study revealed the osseous prominence distal to the crista fibularis of the medial part of the fibula, which corresponded to the attachment of the thickened fibrous part of the IOL via tissue with fibrocartilaginous histology. These findings were validated by the fact that cortical bone thickening was limited to the osseous prominence and the medial side of the fibula proximal to the prominence, as analyzed with BoneJ11. As previously described8, these osseous morphological features, particularly cortical bone thickening, could correspond to the high tensile stress from dense connective tissues (i.e., the IOM and the thickened fibrous part of the IOL in the present study).
The IOL15,16 or interosseous tibiofibular ligament17–19 has been described as the most distal-end thickening of the IOM and the pyramidal network, which is located in the tibiofibular interosseous area and comprises adipose tissue. Because of histological heterogeneity15, ambiguity between the fibrous and fatty parts, and continuity with surrounding structures15, the IOL has never been comprehensively understood. Another reason why the IOL has never been comprehensively understood could be the difficulty in visualizing the narrow interosseous area from the outside. Using macroscopic and histological methods, we revealed that the IOL could be interpreted as the thickened fibrous part that we observed in the present study. This fibrous part, which corresponded to the distal end of the IOM, was located distal to the fibular artery perforation and proximal to the bifurcation into the AITFL and PITFL, and it gradually transitioned distally into the pyramidal adipose membrane. Based on the osseous morphological and histological discrepancies between the 2 parts (i.e., the thickened fibrous part and the pyramidal adipose membrane), the tensile stress of the interosseous area could be mainly transmitted by the proximal part of the IOL to the medial side of the fibula proximal to the prominence.
The perforating branch of the fibular artery is an anatomically well-known structure that penetrates the distal part of the IOM and runs across the AITFL beneath the peroneus tertius muscle13,18,20,21. Similarly, the perforating branch of the fibular artery was confirmed in all specimens in the current study. Given that the perforating branch of the fibular artery originates from the axial artery during the developmental period, the consistent persistence of the perforating branch of the fibular artery can be understood. Additionally, the consistency of the proximal fibrous part of the IOL could be embryologically supported by the consistent persistence of the perforating branch of the fibular artery, which divides the proximal fibrous part of the IOL from the IOM.
Our findings highlight a few important clinical insights. There has been no consensus on the optimal screw positioning for syndesmotic injury, and several locations, including 2 to 5 cm proximal to the tibial plafond or tibiotalar joint, have been recommended on the basis of clinical experience22,23. While biomechanical and finite-element modeling studies24,25 have been conducted to optimize screw locations, the anatomical knowledge of the interosseous tibiofibular area has not been reflected in the hypothetical background. The current study suggests that the location of the prominence on the medial aspect of the fibula could be a helpful clue as to the ideal location for syndesmotic fixation in relation to the proximal thickened fiber of the IOL because it could act as a stabilizing structure for motion of the syndesmosis. Furthermore, identification of the prominence could prevent intraoperative injury to the perforating branch of the fibular artery, which passes through the IOM proximal to the prominence.
The present study had some limitations. First, this study was purely anatomical and was limited to uninjured specimens; therefore, we could not prove the actual tensile stress in the interosseous tibiofibular area, and our explanations remain speculative. Second, this study was limited to Japanese specimens; therefore, there could be inter-ethnic variations in the location of the prominence on the medial aspect of the fibula. Third, the cadavers in this study were those of elderly adults with a mean age of >70 years; therefore, there is an age discrepancy between the cadavers used in the present study and younger patients with traumatic syndesmotic injury. However, elderly osteoporotic patients with ankle fractures also have syndesmotic injuries that require fixation; therefore, this limitation may not be a basic weakness. Fourth, the investigated samples were few in number, were not fully paired, and had differences in terms of sex (with 9 specimens from male donors and 6 from female donors) and side (with 3 ankle pairs, 3 right ankles, and 9 left ankles). To validate our findings, additional larger studies including biomechanics or clinical case imaging are required.
In conclusion, we observed the osseous prominence on the medial aspect of the fibula corresponding to the proximal thickened part of the IOL via the fibrocartilaginous attachment. The perforating branch of the fibular artery was relevant to the consistency of the proximal thickened part of the IOL, which was differentiated from the IOM.
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