Injuries to the distal tibiofibular syndesmosis are challenging to treat. For syndesmotic injuries, screws have been used as the gold standard for fixation1 2–5
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 8–10
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 11 , 12
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.
Fig. 1: Figs. 1-A through 1-D Images illustrating the method for detaching the IOL in the interosseous tibiofibular area. AITFL = anterior inferior tibiofibular ligament, PITFL = posterior inferior tibiofibular ligament, Ant = anterior, Dist = distal, Lat = lateral, Post = posterior, and Prox = proximal. Fig. 1-A Axial CT image showing the parts of the IOL that were detached from the tibia and fibula as indicated by blue dotted lines. Fig. 1-B Photograph showing the posterior aspect of the right leg following removal of the surrounding muscles. The IOL and the interosseous membrane (IOM) are detached from the fibular side as shown by the blue dotted lines. The asterisks show the detached part of the fibula and the corresponding part of the IOL. Fig. 1-C Photograph showing the tibia with the residual IOL (left side of image) and the medial side of the fibula (right side of image). The asterisks show the detached part of the fibula and the corresponding part of the IOL. Fig. 1-D Photograph showing that the residual IOL is detached from the tibial side. The daggers show the detached part of the tibia and the corresponding part of the IOL.
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 :6H2 O, 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.
Statistical Analyses
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.
Results
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 ).
Fig. 2: Figs. 2-A, 2-B, and 2-C Micro-CT scans illustrating the osseous morphology of the interosseous tibiofibular area of the distal part of the left leg. Prox = proximal, Ant = anterior, Med = medial, and Post = posterior. Fig. 2-A Three-dimensional imaging of the medial surface of the distal part of the fibula; the yellow dotted area indicates the prominence on the medial surface of the fibula, and the red dotted lines indicate the level of sectioning as shown in Figure 2-C. Fig. 2-B Three-dimensional imaging of the lateral surface of the tibia; the red dotted lines indicate the level of sectioning as shown in Figure 2-C. Fig. 2-C Coronal section at the middle level of the tibia and fibula. The yellow arrowhead indicates the apex of the prominence.
Fig. 3: Figs. 3-A through 3-E Evaluation of cortical bone thickening in the interosseous tibiofibular area. The cortical thickening maps of the left leg in Figure 2 are shown after image processing. The thicker the cortical bone at a given point, the brighter the color of the point. Prox = proximal, Ant = anterior, and Post = posterior. Fig. 3-A The medial surface of the distal part of the fibula. Fig. 3-B The lateral surface of the distal part of the tibia. Fig. 3-C Coronal section including the apex of the prominence (yellow arrowhead) on the medial aspect of the fibula. The interosseous tibiofibular area (the area indicated by the white rectangle) is magnified in Figure 3-D. Fig. 3-D The cortical bones are quartered into the proximal part of the tibia (Tp), distal part of the tibia (Td), proximal part of the fibula (Fp), and distal part of the fibula (Fd) as the equivalent rectangles, which are separated by the fibular prominence. The color bar on the right side of the image (which ranges from black, to navy blue, to blue, to purple, to red, to orange, to yellow, to white) indicates cortical thickness. Fig. 3-E Scatterplot showing the cortical bone thickness of the quadrants. Cortical bone thicknesses are displayed as the mean and the standard deviation. The cortical thickness of Fp (red asterisk) was greater than that of other areas (Kruskal-Wallis test and Steel-Dwass post hoc test, p < 0.001).
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 ).
Fig. 4: Figs. 4-A and 4-B Photographs showing the perforating branch of the fibular artery in the distal part of the right leg following muscle removal. Med = medial, Lat = lateral, and Dist = distal. Fig. 4-A Posterior aspect. The fibular artery runs behind the syndesmosis. The red arrowheads indicate the perforating branch of the fibular artery. Fig. 4-B Anterior aspect. The perforating branch of the fibular artery (red arrowheads) passes distal to the interosseous membrane (IOM) and proximal to the anterior and posterior inferior tibiofibular ligaments (AITFL and PITFL, respectively).
Fig. 5: Figs. 5-A through 5-D Photographs showing the separated IOL and osseous attachments. Ant = anterior, Post = posterior, Dist = distal, AITFL = anterior tibiofibular ligament, and PITFL = posterior tibiofibular ligament. Fig. 5-A The fibular aspect of the IOL. The interosseous membrane (IOM) distally transitions into the anterior and posterior inferior tibiofibular ligaments (AITFL and PITFL, respectively). The fibular artery runs through the fibrous part (section mark [§]), which is the distal edge of the IOM and proximal edge of the AITFL and PITFL. The red arrow indicates the running path of the perforating branch of the fibular artery. Fig. 5-B The medial aspect of the fibula from which the IOL is detached. The fibrous part in Figure 5-A corresponds to the osseous prominence (yellow dotted area). The location of the apex of the osseous prominence (yellow arrowhead) is shown as the maximum length from the tip of the lateral malleolus and anterior ridge of the fibula to the apex of the osseous prominence. The asterisk (*) indicates the corresponding attachment as indicated in Figure 5-A. Fig. 5-C The tibial aspect of the IOL is indicated by the dagger (†). Fig. 5-D The lateral aspect of the tibia. The dagger (†) indicates the corresponding attachment as indicated in Figure 5-C.
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 ).
Fig. 6: Figs. 6-A through 6-E Histological analysis of the interosseous tibiofibular ligament. Ant = anterior, Prox = proximal, and Lat = lateral. Fig. 6-A Micro-CT scan showing the levels of the section. Fig. 6-B Histological section at the level of the osseous prominence on the medial aspect of the fibula (Masson trichrome stain). Fig. 6-C Magnified image of the black square shown in Figure 6-B. Fig. 6-D Histological section at the middle level of the interosseous tibiofibular ligament. Fig. 6-E Magnified image of the black square shown in Figure 6-D.
Discussion
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.
Fig. 7: Schematic illustration of the interosseous tibiofibular ligament and attachment on the medial aspect of the fibula. The fibula is detached from the IOL of the right ankle. The IOL is approximately divided into the proximal fibrous part and the distal fatty part. The proximal and distal parts and corresponding attachments on the medial aspect of the fibula are indicated as section marks (§) and asterisks (*), respectively. AITFL = anterior tibiofibular ligament, PITFL = posterior tibiofibular ligament, IOM = interosseous membrane, Ant = anterior, Dist = distal, Lat = lateral, Post = posterior, and Prox = proximal.
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 13 14 11 8
The IOL15 , 16 17–19 15 15
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
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 24 , 25
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.
References
1. Van Heest TJ, Lafferty PM. Injuries to the ankle syndesmosis. J Bone Joint Surg Am. 2014 Apr 2;96(7):603-13.
2. Seyhan M, Donmez F, Mahirogullari M, Cakmak S, Mutlu S, Guler O. Comparison of screw fixation with elastic fixation methods in the treatment of syndesmosis injuries in ankle fractures. Injury. 2015 Jul;46(Suppl 2):S19-23. Epub 2015 Jun 24.
3. Stiene A, Renner CE, Chen T, Liu J, Ebraheim NA. Distal tibiofibular syndesmosis dysfunction: a systematic literature review of dynamic versus static fixation over the last 10 years. J Foot Ankle Surg. 2019 Mar;58(2):320-7. Epub 2019 Jan 3.
4. Andersen MR, Frihagen F, Hellund JC, Madsen JE, Figved W. Randomized trial comparing suture button with single syndesmotic screw for syndesmosis injury. J Bone Joint Surg Am. 2018 Jan 3;100(1):2-12.
5. Ræder BW, Figved W, Madsen JE, Frihagen F, Jacobsen SB, Andersen MR. Better outcome for suture button compared with single syndesmotic screw for syndesmosis injury: five-year results of a randomized controlled trial. Bone Joint J. 2020 Feb;102-B(2):212-9.
6. Wolff J. Das gesetz der transformation der knochen. Berlin: Hirschwald; 1892.
7. Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab. 2000;18(6):305-16.
8. Norman D, Metcalfe AJ, Barlow T, Hutchinson CE, Thompson PJ, Spalding TJ, Williams MA. Cortical bony thickening of the lateral intercondylar wall: the functional attachment of the anterior cruciate ligament. Am J Sports Med. 2017 Feb;45(2):394-402. Epub 2016 Oct 1.
9. Nozaki T, Nimura A, Fujishiro H, Mochizuki T, Yamaguchi K, Kato R, Sugaya H, Akita K. The anatomic relationship between the morphology of the greater tubercle of the humerus and the insertion of the infraspinatus tendon. J Shoulder Elbow Surg. 2015 Apr;24(4):555-60. Epub 2014 Dec 3.
10. Sato T, Nimura A, Yamaguchi R, Fujita K, Okawa A, Akita K. Intramuscular tendon of the adductor pollicis and underlying capsule of the metacarpophalangeal joint: an anatomical study with possible implications for the Stener lesion. J Hand Surg Am. 2018 Jul;43(7):682.e1-8. Epub 2018 Feb 1.
11. Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ. BoneJ: free and extensible bone image analysis in ImageJ. Bone. 2010 Dec;47(6):1076-9. Epub 2010 Sep 15.
12. Horiuchi S, Nimura A, Tsutsumi M, Suzuki S, Fujita K, Nozaki T, Akita K. Anatomical relationship between the morphology of the styloid process of the ulna and the attachment of the radioulnar ligaments. J Anat. 2020 Dec;237(6):1032-9. Epub 2020 Jul 12.
13. Standring S, editor. Gray’s anatomy: the anatomical basis of clinical practice. 40th ed. Philadelphia: Churchill Livingstone Elsevier; 2008.
14. Fojtík P, Kostlivý K, Bartoníček J, Naňka O. The fibular notch: an anatomical study. Surg Radiol Anat. 2020 Oct;42(10):1161-6. Epub 2020 Apr 25.
15. Hermans JJ, Beumer A, de Jong TA, Kleinrensink GJ. Anatomy of the distal tibiofibular syndesmosis in adults: a pictorial essay with a multimodality approach. J Anat. 2010 Dec;217(6):633-45.
16. Kelikian AS. Sarrafian’s anatomy of the foot and ankle: descriptive, topographic, functional. Philadelphia: Wolters Kluwer Health; 2012.
17. Kelikian H, Kelikian AS. Disorders of the ankle. Philadelphia: WB Saunders; 1952.
18. Bartonícek J. Anatomy of the tibiofibular syndesmosis and its clinical relevance. Surg Radiol Anat. 2003 Nov-Dec;25(5-6):379-86. Epub 2003 Sep 19.
19. Williams BT, Ahrberg AB, Goldsmith MT, Campbell KJ, Shirley L, Wijdicks CA, LaPrade RF, Clanton TO. Ankle syndesmosis: a qualitative and quantitative anatomic analysis. Am J Sports Med. 2015 Jan;43(1):88-97. Epub 2014 Oct 31.
20. Huber JF. The arterial network supplying the dorsum of the foot. Anat Rec. 1941;80(3):373-91.
21. McKeon KE, Wright RW, Johnson JE, McCormick JJ, Klein SE. Vascular anatomy of the tibiofibular syndesmosis. J Bone Joint Surg Am. 2012 May 16;94(10):931-8.
22. Müller ME, Allgöwer M, Schneider R, Willenegger H. Manual of internal fixation: techniques recommended by the AO-ASIF Group. 3rd ed. Berlin: Springer; 1991.
23. Whittle AP. Fractures of the lower extremity. In: Canale ST, editor. Campbell’s operative orthopaedics. 39th ed. St. Louis, MO: Mosby, Elsevier; 1998. p 2046-8.
24. McBryde A, Chiasson B, Wilhelm A, Donovan F, Ray T, Bacilla P. Syndesmotic screw placement: a biomechanical analysis. Foot Ankle Int. 1997 May;18(5):262-6.
25. Verim O, Er MS, Altinel L, Tasgetiren S. Biomechanical evaluation of syndesmotic screw position: a finite-element analysis. J Orthop Trauma. 2014 Apr;28(4):210-5.
