- Email: [email protected]
Topographical Anatomy of the Distal Ulna Attachment of the Radioulnar Ligament
EDITOR’S CHOICE
Topographical Anatomy of the Distal Ulna Attachment of the Radioulnar Ligament Won-Jeong Shin, MS,* Jong-Pil Kim, MD,* Hun-Mu Yang, PhD,† Eun-Young Lee, MD,‡ Jai-Hyang Go, MD,§ Kang Heo, MD*
Purpose The deep component of the distal radioulnar ligament provides translational stability and rotational guidance to the forearm. However, controversy exists regarding the importance of this structure as well as the nature of its attachment to the distal ulna. We aimed to evaluate the topographic anatomy of the distal ulna attachment of both the superficial and the deep components of the radioulnar ligament and to assess the relationship between its internal and its external morphometry. Methods Thirteen human distal ulnae attached by ulnar part of the distal radioulnar ligament were scanned using microecomputed tomography and reconstructed in 3 dimensions. In addition, the distal radioulnar ligaments were examined under polarized light microscopy to determine the histological characteristics of collagen contained within the ligaments. Results The deep limbs have broad marginal insertions at the fovea, whereas the superficial limbs have a circular and condensed insertion to the ulnar styloid. The center of the deep limb was separated from the base of the ulnar styloid by a mean of 2.0 0.76 mm, and this distance was positively correlated with the width of the ulnar styloid. The mean distance between the center of the ulnar head and the center of the fovea was 2.4 0.58 mm. The proportion of collagen type I was lower in the deep limb than in the superficial limb. Conclusions This new observation of the footprint of the radioulnar ligament in the distal ulna indicates that the deep limb may serve as an internal capsular ligament of the distal radioulnar joint, whereas the superficial limb as the external ligament. Clinical relevance Knowledge of the topographic anatomy of the radioulnar ligament’s attachment to the distal ulna may provide a better understanding of distal radioulnar ligamenterelated pathologies. (J Hand Surg Am. 2017;-(-):1.e1-e8. Copyright Ó 2017 by the American Society for Surgery of the Hand. All rights reserved.) Key words Micro-CT, triangular fibrocartilage complex, distal radioulnar ligament, footprint, fovea.
T
ligaments, which are the primary stabilizers of the distal radioulnar joint (DRUJ), converge from their origins at the sigmoid notch of the radius, into both HE DORSAL AND PALMAR RADIOULNAR
the ulnar styloid (superficial limb) and the ulnar styloid base or fovea of the ulnar head (deep limb), blending with the fibrocartilage structure to form the triangular fibrocartilage complex (TFCC).1,2
From the *Department of Orthopedic Surgery, College of Medicine; Department of Kinesiology and Medical Science, Graduate School, Dankook University; the †Department of Anatomy, Yonsei University College of Medicine, Seoul; the §Department of Pathology, Dankook University College of Medicine, Cheonan; and the ‡Department of Anatomy, Chungbuk National University College of Medicine, Cheungju, Korea.
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
Received for publication June 9, 2016; accepted in revised form March 22, 2017.
0363-5023/17/---0001$36.00/0 http://dx.doi.org/10.1016/j.jhsa.2017.03.031
Corresponding author: Jong-Pil Kim, MD, Department of Orthopedic Surgery, Dankook University College of Medicine, 119 Dandaero, Dongnam-gu, Cheonan 31116, Korea; e-mail: [email protected].
Ó 2017 ASSH
r
Published by Elsevier, Inc. All rights reserved.
r
1.e1
1.e2
ANATOMY OF THE DISTAL ULNA
Avulsion fractures involving the ulnar styloid base or fovea, where the distal radioulnar ligaments insert, have the potential risk to destabilize the DRUJ, but this remains controversial.3,4 In fact, several studies have reported neither the fracture size nor the degree of displacement of the ulnar styloid affects objective or subjective clinical outcomes or is a predictor of DRUJ instability.5e7 Furthermore, it has also been suggested that ulnar styloid fixation may not be necessary if the distal radius is treated with rigid internal fixation. However, few studies have described the detailed topographic anatomy of the distal ulna and its ligamentous attachments, knowledge of which may provide a better understanding of the biomechanical role of the distal radioulnar ligaments and their relationship to DRUJ stability. Studies utilizing micro-imaging techniques, such as microecomputed tomography (CT), have demonstrated detailed bone morphology and microarchitecture.8e12 Microimaging can provide the detailed anatomy of the distal radioulnar ligament footprints on the distal ulna head and styloid. The purpose of this study was to evaluate the topographic anatomy of the distal ulna and the insertions of both the superficial and the deep components of the distal radioulnar ligaments and to assess the relationships between their internal and their external morphometry using micro-CT scans of cadaveric ulnar heads. We also investigated the ratios of type I/III collagen at different locations of the distal radioulnar ligament in order to study the histological characteristics of the ligament.
carefully dissected from nonligamentous soft tissue (Fig. 1A). The exact origin, insertion, and course of the ligamentous complex were examined under a dissecting microscope (HSZ-600; HUVITZ Inc., Seoul, Korea). Both the superficial and the deep components of the ligament were cut near their insertions to identify the footprint. The 2 components of the ligament were easily separated by loose connective tissue from the more distal fibers (Fig. 1B).13 The ligament remnants were marked and painted with Telebrix (Meglumine ioxithalamate; Gubebet, Aulnay-sous-Bois, France) contrast media solution, which is commonly used for enhanced CT.
MATERIALS AND METHODS Specimen preparation A sample of convenience comprising 13 human cadaver wrists (7 right and 6 left wrists from 8 males and 5 females; mean age at death, 65 years [range, 54e75 years]) were inspected. All wrists were radiographically imaged and demonstrated normal osseous anatomy. Exclusion criteria were a degenerative or traumatic tear of the TFCC, a known history of previous trauma, infection, or surgical trauma affecting the wrist. However, specimens with evidence of an age-related change on the TFCC were included if both of the superficial and deep components of the distal radioulnar ligaments were intact. The entire distal ulna was harvested from the wrist, leaving the ulnar part of the TFCC and DRUJ capsule intact through meticulous dissection of all periarticular skin and musculature. Each component of the distal radioulnar ligament complex was
Topographic parameters After reconstructing the 3-dimensional image of the distal ulna, the footprints of the 2 components were separated from the cortical surface of the distal ulna and reconstructed using an appropriate threshold, which isolates tissue dyed with the contrast media solution from bone in the software (Fig. 2A). The footprint sizes, including the maximal width and height and an area of each limb to their insertions, were measured using a reverse-engineering software system (Rapidfom 2006; Inus Technology, Seoul, Korea). The accuracy of the measurements was 0.01 mm or mm2 or less. Circularity was measured from the data by calculating the ratio of the area of the shape to the area of a perfect circle which has the same perimeter.14 A perfect circle would have a circularity ratio equal to 1; a value less than 1 indicates a deviation from the outline of a circle. In addition, the center of the ulnar head contour was
J Hand Surg Am.
Micro-CT imaging Three-dimensional micro-CT renderings of the distal ulna were used to examine external and internal bony architecture. A scan was performed on all specimens using a micro-CT scanner (1076; SkyScan, Antwerp, Belgium). This system comprised an x-ray microscope with a high-definition x-ray microfocus tube, focal spot diameter of 10 mm; a 1.0-mm-thick aluminum filter to remove noise during x-ray scanning; a precision-controlled specimen holder; a 2-dimensional x-ray charge coupled device camera connected to a frame grabber; and a workstation running tomography reconstruction software (NRecon, ver. 1.6.3.3; SkyScan). A 3-dimensional structural image of the distal ulna with voxels 35 35 35 mm in size was reconstructed from 2-dimensional cross-sectional images in bitmap format with a 35-mm slice thickness (pixel, 35 35 mm).
r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e3
FIGURE 1: Radial view of the distal radioulnar ligaments inserting onto the distal ulna, with their origin detached from the sigmoid notch. A The dorsal and volar fibers of the deep limb converge on the fovea. B The ligaments were transected near insertion revealing that the deep limb has a marginal insertion just behind the pole of the distal ulna, whereas the superficial limb has a more circular condensing insertion on the styloid process. Asterisk indicates loose connective tissue between the 2 limbs of the ligaments.
FIGURE 2: Measurements of distal radioulnar ligament footprint size and intercenter distance between the centers of the fovea and the ulnar head on a 3-dimensional reconstructed model of the left distal ulna with each of the limbs separated from the distal ulna using the appropriate threshold in the software. A The footprint size of both limbs was measured using a reverse engineering software system (Rapidform 2006; Inus Technology, Seoul, Korea). W, width; L, length. B The center of the ulnar head was identified on the axial plane using the circle approximation technique, and the center of the fovea was subjectively determined where the point was in the centroid of the fovea. Then, the intercenter distance was measured.
identified on the axial plane using the circle approximation technique (Fig. 2B). The center of the deep limb footprint on the same axial plane was also determined, and then the distance between the centers of the ulnar head contour and deep limb footprint, defined as intercenter distance, was measured. To analyze the topography of the footprint of the distal radioulnar ligament, coronal and 30 dorsal and volar semicoronal section images based on the center of the ulnar styloid were reconstructed using CT Analyzer software (DataViewer; Skyscan) (Fig. 3). The distal ulnar head width (mm) measured at the level of the ulnar styloid base, width and length of the ulnar styloid (mm), and distances from the deep limb center to the ulnar styloid base (mm) were measured in each plane. The relationship between the ulnar styloid and the distal ulnar head was determined by J Hand Surg Am.
calculating the ratio of the width of the ulnar styloid compared with the distal ulnar head width. Internal trabecular bone morphometric analysis To quantitatively compare the internal bone microarchitecture in the distal ulna, a cylindrical volume of interest (VOI) containing only trabecular bone (length, 2 mm; diameter, 2 mm) was isolated from 4 locations in the distal ulna and trabecular bone morphometry was calculated for the pole and fovea of the ulnar head and the base and process of the ulnar styloid (Fig. 4). We determined the following morphometric parameters within the cylindrical trabecular VOI: trabecular bone volume fraction (BV/ TV [%]); trabecular thickness (Tb.Th [mm]); trabecular number, (Tb.N [mme1]); trabecular separation (Tb.Sp [mm]); and the structural model index (SMI).9 r
Vol. -, - 2017
1.e4
ANATOMY OF THE DISTAL ULNA
FIGURE 3: Analysis of distal ulna topography on coronal reconstructed images. Ulnar head width—which is based on the level of the ulnar styloid base, size of the ulnar styloid, and distance from the deep limb center to the ulnar styloid base—was measured in each of three coronal CT images: central coronal A, 30 dorsal B, and volar semicoronal C. L, length; W, width; v, distance from the deep limb center to the ulnar styloid base (mm).
Histological characteristics of the ligaments To compare the characteristics of collagen types in the superficial and deep components of the distal radioulnar ligaments inserting onto the distal ulna, an illumination method under polarized light microscopy after picrosirius red staining was applied to 9 TFCC specimens (4 specimens in which accurate transverse sections failed to be obtained were excluded) at the midportion of the volar and dorsal radioulnar ligaments and the superficial and deep limbs of the ligaments attaching to the distal ulna (Fig. 5).15e17 The specimens were fixed in 10% neutral buffered formaldehyde solution and embedded in paraffin. The specimens were stained by 0.1% picrosirius red solutions (Sirius Red F3B; Sigma-Aldrich Co., St. Louis, MO) after sectioning along with the longitudinal direction of the fibers at 5 mm, similar to the methods used by previous investigators.15,17 The sections were then examined under bright field and polarizing microscopy and photographed at 200 magnification. Collagen fibers display uniformly as red or yellow color in type I and as a greenish color in type III under polarized light. The distributions of type I/III collagen were obtained by discriminating the Hue value of each pixel in the images of Hue-Saturation-Brightness color model using i-solution software (IMT i-Solution Inc., Vancouver, BC, Canada). Each of the Hue values of collagen type I and III was measured in 3 rectangular areas (6,400 mm2), which were randomly selected, and collagen I/III ratios were calculated (Fig. 6). Five sequential sections of each specimen were examined to reduce sampling error. J Hand Surg Am.
FIGURE 4: Locations of the trabecular region of interest in the central coronal section. Cylindrical volume of interest in trabecular bone (2 mm diameter, 2 mm length) extracted from 4 lesions in the distal ulna: the pole and fovea of the ulnar head and the base and process of the ulnar styloid, which were highlighted in yellow, red, green, and blue, respectively.
Statistical analysis Results are expressed as mean SD. Nonparametric tests were used because of the small number of samples. The Wilcoxon signed rank test was used to compare the morphometry of the footprint between the deep and the superficial components. The Friedman test was performed to compare topographical parameters in the 3 coronal planes and the internal bone morphometric parameters in 4 locations of the distal ulna as well as collagen I/III ratios in 4 sites of the distal radioulnar ligament. Spearman correlation r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e5
all specimens. The distances from the center of the footprint of the deep limb to the ulnar styloid base, measured in the 3 coronal planes, averaged 2.0 0.76 mm, which corresponded to an average of 50% 5.7% of the width of the distal ulnar head from the most medial cortex. The intercenter distance between the fovea center and ulnar head center averaged 2.4 0.58 mm. Internal trabecular bone morphometry of the distal ulna A 3-dimensional morphometric analysis of the cylindrical trabecular VOI revealed that the base of the ulnar styloid had decreased BV/TV(%) and Tb.N (mme1), and increased Tb.Sp and SMI, compared with the ulnar head and deep and superficial limb insertions. Among them, the differences were significant for Tb.N, Tb.Sp, and SMI (all comparisons, P < .05).
FIGURE 5: The schematic illustration of the 4 anatomical sites of the distal radioulnar ligament for quantitative analysis of histological characteristics of collagen. DL, deep limb of the distal radioulnar ligament inserting to the ulna; DM, midportion of the dorsal radioulnar ligament; SL, superficial limb of the distal radioulnar ligament inserting onto the ulna; VM, midportion of the volar radioulnar ligament.
Correlations between the footprint and distal ulnar topography The area of the superficial limb was positively correlated with the length and width of the ulnar styloid (r ¼ 0.69, P < .05; r ¼ 0.76, P < .05). No correlation was found between the area of deep limb footprint and the distal ulna topographic data. The distance from the deep limb center to the ulnar styloid base was correlated with the width of the ulnar styloid (r ¼ 0.56, P < .05). The intercenter distances were correlated with the distance from the center of the deep limb footprint to the ulnar styloid base (r ¼ 0.51, P < .05).
coefficient analysis was used to correlate the topographical and internal bone morphometry data of the distal ulna. P less than .05 was considered significant for all results. RESULTS Morphometry of the footprint of the distal radioulnar ligament The deep limbs have a long marginal insertion between the pole of the ulnar head and the ulnar styloid base, but the width of the footprint was larger at the fovea than at the peripheral site (Figs. 1B and 2). The superficial limbs inserted at the radial surface of the ulnar styloid process and were condensed and circular in shape, with an approximate circularity ratio of 1. The measured areas of the deep limb were larger than those of the superficial limb (P < .05) (Table 1).
Characteristics of collagen types in the distal radioulnar ligament The results of the collagen I/III ratios for 4 different sites of the distal radioulnar ligament are shown in Figure 7. The mean collagen I/III ratio of the distal radioulnar ligament was 1.27 0.56. The collagen I/III ratio for the deep limb was significantly lower than those of the midportion of the volar radioulnar ligament and superficial limb sections (all comparisons, P < .05). DISCUSSION The fovea has been considered the primary attachment site for the deep fibers of the distal radioulnar ligaments and is critical for providing rotational guidance because the pronation-supination axis of the forearm runs through it.18e21 This also provides primary DRUJ stability because the deep fibers act as a check to prevent further translation of the distal ulna.2,22e24 Therefore, avulsion fractures involving the ulnar
Topographic analysis of the distal ulna The sizes of the distal ulnar head and the widths and length of the ulnar styloid in the coronal plane averaged 16.7 1.58 mm, 6.3 0.89 mm, and 5.3 0.01 mm, respectively, which were similar to those of the other seminal coronal planes (P > .05) (Table 2). The deep limb footprints were located radially, apart from the base of the ulnar styloid in J Hand Surg Am.
r
Vol. -, - 2017
1.e6
ANATOMY OF THE DISTAL ULNA
FIGURE 6: The histological images of the distal radioulnar ligament under polarized light with picrosirius red staining (magnification 200). Greenish birefringence (type III collagen) was observed more in the deep limb section A, whereas red-yellow birefringence (type I collagen) was more predominant in the superficial limb B.
TABLE 1.
Morphometry of the Footprints of the Distal Radioulnar Ligament Superficial Limb
Deep Limb
P Value
Maximal width (mm)
4.11 0.85
12.68 1.93
< .01
Maximal height (mm)
5.25 1.15
3.10 0.34
< .01
Area (mm2)
18.36 6.07
29.67 5.74
< .01
Perimeter (mm)
14.69 2.84
27.44 5.63
< .01
Circularity ratio
1.06 0.11
2.86 0.67
< .01
TABLE 2. Topographical Parameters of the Distal Ulna in the Central Coronal, and 30 Volar, and 30 Dorsal Semicoronal Planes Parameter
30 Volar Plane
Central Plane
30 Dorsal Plane
P Value
15.64 1.72
16.51 1.69
15.52 1.62
.44
Width of the ulnar styloid (mm)
5.69 1.09
6.15 0.87
6.15 1.04
.55
Length of the ulnar styloid (mm)
3.30 0.68
3.15 0.76
3.52 1.07
.79
Distance from the deep limb center to the ulnar styloid base (mm)
2.15 0.71
1.72 0.62
2.12 0.81
.38
Distal ulnar head length (mm)
styloid base or fovea, where the deep limb inserts, increase the potential risk for DRUJ instability.3,4 The fovea of the distal ulna is a central, roughened bony depression on the distal pole of the ulna that lies between the hyaline cartilage of the ulnar pole and the ulnar styloid.1,25,26 The base of the ulnar styloid, which is different from the fovea, is a shallow, concave recess, devoid of cartilage or ligament but with abundant with vascular foramina.24 We found that the fovea was radially apart from the base of the ulnar styloid, and that the average distance from the center of the deep limb attachment to ulnar styloid base was 2.0 mm in all coronal planes. The microarchitectural morphometric analysis of the distal ulna in the present study revealed that bone density and J Hand Surg Am.
trabecular thickness were the lowest at the ulnar styloid base, predisposing this area to fracture. These findings may explain why neither size nor displacement of an ulnar styloid fragment predicts DRUJ instability.6,7,27,28 An injury of the deep component of the distal radioulnar ligament is more likely when a fracture involving the ulnar styloid is more proximal or radial from the ulnar styloid base. One study recorded the maximum size of the fovea as an average of 4.7 mm.29 However, the deep limb had a long marginal insertion just behind the pole of the distal ulna, and maximum width and length averaged 3.1 mm and 12.6 mm, respectively. The width of the deep limb footprint was maximized on the fovea. In contrast, the footprint shape of the r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e7
FIGURE 7: Comparison of the collagen I/III ratio between the 4 lesions of the distal radioulnar ligament (RUL). Note that the collagen I/ III ratio at the deep limb was significantly lower than those of the volar RUL and superficial limb sections. The error bars represent SD. * indicates P < .05.
superficial limb was close to circular and condensed in shape. Based on the morphometric findings of the ligament footprint, we speculate that the deep limb is an internal ligament that forms the DRUJ capsule and also serves as a rotational and translational joint stabilizer, whereas the superficial limb acts as an external ligament of the joint, like the medial collateral ligament of the knee. These findings support previous biomechanical observations that the palmar part of the deep limb is taut with forearm supination as the ulna translates palmarly, whereas the dorsal part is taut with the forearm pronated as the ulna translates dorsally.22,23,30 The center of the ulnar head is known to be near the fovea of the distal ulna, indicating that the DRUJ axis of rotation runs through the center of the ulnar head.18,19,31 In fact, several studies have suggested various CT methods to assess DRUJ instability according to how much the center of the ulnar head is translated either anteriorly or posteriorly during forearm rotation.32e34 However, our data demonstrate that the center of the ulnar head was not congruent with the anatomical center of the fovea because the anatomical center of the fovea was located more ulnarly and farther from the center of the ulnar head. This finding agrees with the data reported by Kataoka et al21 showing a greater discrepancy between the center of the ulnar head and the pronosupination axis of the forearm. It is well established that collagen type is related to the mechanical properties of ligaments and an J Hand Surg Am.
increasing percentage of type III collagen has been found to result in decreasing mechanical properties.15,35 From the histological data in the present study, it is speculated that each limb of the radioulnar ligament inserting into the distal ulna has different mechanical properties, and this also supports our previous assumption that the deep limb serves as an internal ligament that forms the joint capsule whereas the superficial limb as an external ligament in the DRUJ. This study was limited by the small number of specimens. However, the consistency of this distinct footprint pattern of the footprint of the 2 components in all specimens indicates that our sample might be adequate. This study was also limited by less clear visualization of the footprints caused by painting them with contrast media because of the small area on the small distal ulna. Quantification of the proportion of collagen types might be biased by examination of a limited portion of each component of the TFCC. Finally, the measurement of the distribution of collagen type I/III ratio was dependent upon observer factors, such as how much the Hue value of each pixel was discriminated in the images. ACKNOWLEDGMENTS The authors thank Chae-Eun Lee, radiological technologist, for her support. The authors also gratefully thank the individuals who donated their bodies to the Department of Anatomy, Dankook University r
Vol. -, - 2017
1.e8
ANATOMY OF THE DISTAL ULNA
College of Medicine. This article would not have been possible without their selfless gift.
18. Youm Y, Dryer RF, Thambyrajah K, Flatt AE, Sprague BL. Biomechanical analyses of forearm pronation-supination and elbow flexion-extension. J Biomech. 1979;12(4):245e255. 19. Kapandji A. Biomechanics of pronation and supination of the forearm. Hand Clin. 2001;17(1):111e122, vii. 20. Hollister AM, Gellman H, Waters RL. The relationship of the interosseous membrane to the axis of rotation of the forearm. Clin Orthop Relat Res. 1994;298:272e276. 21. Kataoka T, Moritomo H, Omokawa S, Iida A, Murase T, Sugamoto K. Ulnar variance: its relationship to ulnar foveal morphology and forearm kinematics. J Hand Surg Am. 2012;37(4): 729e735. 22. Kihara H, Short WH, Werner FW, Fortino MD, Palmer AK. The stabilizing mechanism of the distal radioulnar joint during pronation and supination. J Hand Surg Am. 1995;20(6):930e936. 23. Ward LD, Ambrose CG, Masson MV, Levaro F. The role of the distal radioulnar ligaments, interosseous membrane, and joint capsule in distal radioulnar joint stability. J Hand Surg Am. 2000;25(2): 341e351. 24. Huang JI, Hanel DP. Anatomy and biomechanics of the distal radioulnar joint. Hand Clin. 2012;28(2):157e163. 25. Ishii S, Palmer AK, Werner FW, Short WH, Fortino MD. An anatomic study of the ligamentous structure of the triangular fibrocartilage complex. J Hand Surg. 1998;23(6):977e985. 26. Kleinman WB. Stability of the distal radioulna joint: biomechanics, pathophysiology, physical diagnosis, and restoration of function what we have learned in 25 years. J Hand Surg Am. 2007;32(7): 1086e1106. 27. Arealis G, Galanopoulos I, Nikolaou VS, Lacon A, Ashwood N, Kitsis C. Does the CT improve inter- and intra-observer agreement for the AO, Fernandez and Universal classification systems for distal radius fractures? Injury. 2014;45(10):1579e1584. 28. Kim JK, Yun YH, Kim DJ, Yun GU. Comparison of united and nonunited fractures of the ulnar styloid following volar-plate fixation of distal radius fractures. Injury. 2011;42(4):371e375. 29. Sharma A, Kumar A, Singh P. Anatomical study of the distal end of cadaveric human ulnae: a clinical consideration for the management of distal radioulnar joint injuries. Singapore Med J. 2011;52(9): 673e676. 30. Schuind F, An KN, Berglund L, et al. The distal radioulnar ligaments: a biomechanical study. J Hand Surg Am. 1991;16(6): 1106e1114. 31. af Ekenstam F, Hagert CG. Anatomical studies on the geometry and stability of the distal radio ulnar joint. Scand J Plast Reconstr Surg. 1985;19(1):17e25. 32. Wechsler RJ, Wehbe MA, Rifkin MD, Edeiken J, Branch HM. Computed tomography diagnosis of distal radioulnar subluxation. Skeletal Radiol. 1987;16(1):1e5. 33. Lo IK, MacDermid JC, Bennett JD, Bogoch E, King GJ. The radioulnar ratio: a new method of quantifying distal radioulnar joint subluxation. J Hand Surg Am. 2001;26(2):236e243. 34. Kim JP, Park MJ. Assessment of distal radioulnar joint instability after distal radius fracture: comparison of computed tomography and clinical examination results. J Hand Surg. 2008;33(9):1486e1492. 35. Woo SL, Abramowitch SD, Kilger R, Liang R. Biomechanics of knee ligaments: injury, healing, and repair. J Biomech. 2006;39(1): 1e20.
REFERENCES 1. Stuart PR, Berger RA, Linscheid RL, An KN. The dorsopalmar stability of the distal radioulnar joint. J Hand Surg Am. 2000;25(4):689e699. 2. Haugstvedt JR, Berger RA, Nakamura T, Neale P, Berglund L, An KN. Relative contributions of the ulnar attachments of the triangular fibrocartilage complex to the dynamic stability of the distal radioulnar joint. J Hand Surg Am. 2006;31(3):445e451. 3. Sammer DM, Chung KC. Management of the distal radioulnar joint and ulnar styloid fracture. Hand Clin. 2012;28(2):199e206. 4. May MM, Lawton JN, Blazar PE. Ulnar styloid fractures associated with distal radius fractures: incidence and implications for distal radioulnar joint instability. J Hand Surg Am. 2002;27(6):965e971. 5. Souer JS, Ring D, Matschke S, et al. Effect of an unrepaired fracture of the ulnar styloid base on outcome after plate-and-screw fixation of a distal radial fracture. J Bone Joint Surg Am. 2009;91(4):830e838. 6. Sammer DM, Shah HM, Shauver MJ, Chung KC. The effect of ulnar styloid fractures on patient-rated outcomes after volar locking plating of distal radius fractures. J Hand Surg Am. 2009;34(9):1595e1602. 7. Kim JK, Koh YD, Do NH. Should an ulnar styloid fracture be fixed following volar plate fixation of a distal radial fracture? J Bone Joint Surg Am. 2010;92(1):1e6. 8. Rozental TD, Deschamps LN, Taylor A, et al. Premenopausal women with a distal radial fracture have deteriorated trabecular bone density and morphology compared with controls without a fracture. J Bone Joint Surg Am. 2013;95(7):633e642. 9. Jenkins PJ, Ramaesh R, Pankaj P, et al. A micro-architectural evaluation of osteoporotic human femoral heads to guide implant placement in proximal femoral fractures. Acta Orthop. 2013;84(5):453e459. 10. Hsu JT, Wang SP, Huang HL, Chen YJ, Wu J, Tsai MT. The assessment of trabecular bone parameters and cortical bone strength: a comparison of micro-CT and dental cone-beam CT. J Biomech. 2013;46(15):2611e2618. 11. Hsu JT, Chen YJ, Ho JT, et al. A comparison of micro-CT and dental CT in assessing cortical bone morphology and trabecular bone microarchitecture. PloS One. 2014;9(9):e107545. 12. Norman DG, Getgood A, Thornby J, et al. Quantitative topographic anatomy of the femoral ACL footprint: a micro-CT analysis. Med Biol Engi Comput. 2014;52(11):985e995. 13. Chidgey LK, Dell PC, Bittar ES, Spanier SS. Histologic anatomy of the triangular fibrocartilage. J Hand Surg Am. 1991;16(6):1084e1100. 14. Wang Y, Zhao C, Passe SM, et al. Transverse ultrasound assessment of median nerve deformation and displacement in the human carpal tunnel during wrist movements. Ultrasound Med Biol. 2014;40(1):53e61. 15. Wan C, Hao Z, Wen S. A quantitative comparison of morphological and histological characteristics of collagen in the rabbit medial collateral ligament. Ann Anat. 2013;195(6):562e569. 16. Cohen DB, Kawamura S, Ehteshami JR, Rodeo SA. Indomethacin and celecoxib impair rotator cuff tendon-to-bone healing. Am J Sports Med. 2006;34(3):362e369. 17. Junqueira LC, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J. 1979;11(4):447e455.
J Hand Surg Am.
r
Vol. -, - 2017
Topographical Anatomy of the Distal Ulna Attachment of the Radioulnar Ligament Won-Jeong Shin, MS,* Jong-Pil Kim, MD,* Hun-Mu Yang, PhD,† Eun-Young Lee, MD,‡ Jai-Hyang Go, MD,§ Kang Heo, MD*
Purpose The deep component of the distal radioulnar ligament provides translational stability and rotational guidance to the forearm. However, controversy exists regarding the importance of this structure as well as the nature of its attachment to the distal ulna. We aimed to evaluate the topographic anatomy of the distal ulna attachment of both the superficial and the deep components of the radioulnar ligament and to assess the relationship between its internal and its external morphometry. Methods Thirteen human distal ulnae attached by ulnar part of the distal radioulnar ligament were scanned using microecomputed tomography and reconstructed in 3 dimensions. In addition, the distal radioulnar ligaments were examined under polarized light microscopy to determine the histological characteristics of collagen contained within the ligaments. Results The deep limbs have broad marginal insertions at the fovea, whereas the superficial limbs have a circular and condensed insertion to the ulnar styloid. The center of the deep limb was separated from the base of the ulnar styloid by a mean of 2.0 0.76 mm, and this distance was positively correlated with the width of the ulnar styloid. The mean distance between the center of the ulnar head and the center of the fovea was 2.4 0.58 mm. The proportion of collagen type I was lower in the deep limb than in the superficial limb. Conclusions This new observation of the footprint of the radioulnar ligament in the distal ulna indicates that the deep limb may serve as an internal capsular ligament of the distal radioulnar joint, whereas the superficial limb as the external ligament. Clinical relevance Knowledge of the topographic anatomy of the radioulnar ligament’s attachment to the distal ulna may provide a better understanding of distal radioulnar ligamenterelated pathologies. (J Hand Surg Am. 2017;-(-):1.e1-e8. Copyright Ó 2017 by the American Society for Surgery of the Hand. All rights reserved.) Key words Micro-CT, triangular fibrocartilage complex, distal radioulnar ligament, footprint, fovea.
T
ligaments, which are the primary stabilizers of the distal radioulnar joint (DRUJ), converge from their origins at the sigmoid notch of the radius, into both HE DORSAL AND PALMAR RADIOULNAR
the ulnar styloid (superficial limb) and the ulnar styloid base or fovea of the ulnar head (deep limb), blending with the fibrocartilage structure to form the triangular fibrocartilage complex (TFCC).1,2
From the *Department of Orthopedic Surgery, College of Medicine; Department of Kinesiology and Medical Science, Graduate School, Dankook University; the †Department of Anatomy, Yonsei University College of Medicine, Seoul; the §Department of Pathology, Dankook University College of Medicine, Cheonan; and the ‡Department of Anatomy, Chungbuk National University College of Medicine, Cheungju, Korea.
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
Received for publication June 9, 2016; accepted in revised form March 22, 2017.
0363-5023/17/---0001$36.00/0 http://dx.doi.org/10.1016/j.jhsa.2017.03.031
Corresponding author: Jong-Pil Kim, MD, Department of Orthopedic Surgery, Dankook University College of Medicine, 119 Dandaero, Dongnam-gu, Cheonan 31116, Korea; e-mail: [email protected].
Ó 2017 ASSH
r
Published by Elsevier, Inc. All rights reserved.
r
1.e1
1.e2
ANATOMY OF THE DISTAL ULNA
Avulsion fractures involving the ulnar styloid base or fovea, where the distal radioulnar ligaments insert, have the potential risk to destabilize the DRUJ, but this remains controversial.3,4 In fact, several studies have reported neither the fracture size nor the degree of displacement of the ulnar styloid affects objective or subjective clinical outcomes or is a predictor of DRUJ instability.5e7 Furthermore, it has also been suggested that ulnar styloid fixation may not be necessary if the distal radius is treated with rigid internal fixation. However, few studies have described the detailed topographic anatomy of the distal ulna and its ligamentous attachments, knowledge of which may provide a better understanding of the biomechanical role of the distal radioulnar ligaments and their relationship to DRUJ stability. Studies utilizing micro-imaging techniques, such as microecomputed tomography (CT), have demonstrated detailed bone morphology and microarchitecture.8e12 Microimaging can provide the detailed anatomy of the distal radioulnar ligament footprints on the distal ulna head and styloid. The purpose of this study was to evaluate the topographic anatomy of the distal ulna and the insertions of both the superficial and the deep components of the distal radioulnar ligaments and to assess the relationships between their internal and their external morphometry using micro-CT scans of cadaveric ulnar heads. We also investigated the ratios of type I/III collagen at different locations of the distal radioulnar ligament in order to study the histological characteristics of the ligament.
carefully dissected from nonligamentous soft tissue (Fig. 1A). The exact origin, insertion, and course of the ligamentous complex were examined under a dissecting microscope (HSZ-600; HUVITZ Inc., Seoul, Korea). Both the superficial and the deep components of the ligament were cut near their insertions to identify the footprint. The 2 components of the ligament were easily separated by loose connective tissue from the more distal fibers (Fig. 1B).13 The ligament remnants were marked and painted with Telebrix (Meglumine ioxithalamate; Gubebet, Aulnay-sous-Bois, France) contrast media solution, which is commonly used for enhanced CT.
MATERIALS AND METHODS Specimen preparation A sample of convenience comprising 13 human cadaver wrists (7 right and 6 left wrists from 8 males and 5 females; mean age at death, 65 years [range, 54e75 years]) were inspected. All wrists were radiographically imaged and demonstrated normal osseous anatomy. Exclusion criteria were a degenerative or traumatic tear of the TFCC, a known history of previous trauma, infection, or surgical trauma affecting the wrist. However, specimens with evidence of an age-related change on the TFCC were included if both of the superficial and deep components of the distal radioulnar ligaments were intact. The entire distal ulna was harvested from the wrist, leaving the ulnar part of the TFCC and DRUJ capsule intact through meticulous dissection of all periarticular skin and musculature. Each component of the distal radioulnar ligament complex was
Topographic parameters After reconstructing the 3-dimensional image of the distal ulna, the footprints of the 2 components were separated from the cortical surface of the distal ulna and reconstructed using an appropriate threshold, which isolates tissue dyed with the contrast media solution from bone in the software (Fig. 2A). The footprint sizes, including the maximal width and height and an area of each limb to their insertions, were measured using a reverse-engineering software system (Rapidfom 2006; Inus Technology, Seoul, Korea). The accuracy of the measurements was 0.01 mm or mm2 or less. Circularity was measured from the data by calculating the ratio of the area of the shape to the area of a perfect circle which has the same perimeter.14 A perfect circle would have a circularity ratio equal to 1; a value less than 1 indicates a deviation from the outline of a circle. In addition, the center of the ulnar head contour was
J Hand Surg Am.
Micro-CT imaging Three-dimensional micro-CT renderings of the distal ulna were used to examine external and internal bony architecture. A scan was performed on all specimens using a micro-CT scanner (1076; SkyScan, Antwerp, Belgium). This system comprised an x-ray microscope with a high-definition x-ray microfocus tube, focal spot diameter of 10 mm; a 1.0-mm-thick aluminum filter to remove noise during x-ray scanning; a precision-controlled specimen holder; a 2-dimensional x-ray charge coupled device camera connected to a frame grabber; and a workstation running tomography reconstruction software (NRecon, ver. 1.6.3.3; SkyScan). A 3-dimensional structural image of the distal ulna with voxels 35 35 35 mm in size was reconstructed from 2-dimensional cross-sectional images in bitmap format with a 35-mm slice thickness (pixel, 35 35 mm).
r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e3
FIGURE 1: Radial view of the distal radioulnar ligaments inserting onto the distal ulna, with their origin detached from the sigmoid notch. A The dorsal and volar fibers of the deep limb converge on the fovea. B The ligaments were transected near insertion revealing that the deep limb has a marginal insertion just behind the pole of the distal ulna, whereas the superficial limb has a more circular condensing insertion on the styloid process. Asterisk indicates loose connective tissue between the 2 limbs of the ligaments.
FIGURE 2: Measurements of distal radioulnar ligament footprint size and intercenter distance between the centers of the fovea and the ulnar head on a 3-dimensional reconstructed model of the left distal ulna with each of the limbs separated from the distal ulna using the appropriate threshold in the software. A The footprint size of both limbs was measured using a reverse engineering software system (Rapidform 2006; Inus Technology, Seoul, Korea). W, width; L, length. B The center of the ulnar head was identified on the axial plane using the circle approximation technique, and the center of the fovea was subjectively determined where the point was in the centroid of the fovea. Then, the intercenter distance was measured.
identified on the axial plane using the circle approximation technique (Fig. 2B). The center of the deep limb footprint on the same axial plane was also determined, and then the distance between the centers of the ulnar head contour and deep limb footprint, defined as intercenter distance, was measured. To analyze the topography of the footprint of the distal radioulnar ligament, coronal and 30 dorsal and volar semicoronal section images based on the center of the ulnar styloid were reconstructed using CT Analyzer software (DataViewer; Skyscan) (Fig. 3). The distal ulnar head width (mm) measured at the level of the ulnar styloid base, width and length of the ulnar styloid (mm), and distances from the deep limb center to the ulnar styloid base (mm) were measured in each plane. The relationship between the ulnar styloid and the distal ulnar head was determined by J Hand Surg Am.
calculating the ratio of the width of the ulnar styloid compared with the distal ulnar head width. Internal trabecular bone morphometric analysis To quantitatively compare the internal bone microarchitecture in the distal ulna, a cylindrical volume of interest (VOI) containing only trabecular bone (length, 2 mm; diameter, 2 mm) was isolated from 4 locations in the distal ulna and trabecular bone morphometry was calculated for the pole and fovea of the ulnar head and the base and process of the ulnar styloid (Fig. 4). We determined the following morphometric parameters within the cylindrical trabecular VOI: trabecular bone volume fraction (BV/ TV [%]); trabecular thickness (Tb.Th [mm]); trabecular number, (Tb.N [mme1]); trabecular separation (Tb.Sp [mm]); and the structural model index (SMI).9 r
Vol. -, - 2017
1.e4
ANATOMY OF THE DISTAL ULNA
FIGURE 3: Analysis of distal ulna topography on coronal reconstructed images. Ulnar head width—which is based on the level of the ulnar styloid base, size of the ulnar styloid, and distance from the deep limb center to the ulnar styloid base—was measured in each of three coronal CT images: central coronal A, 30 dorsal B, and volar semicoronal C. L, length; W, width; v, distance from the deep limb center to the ulnar styloid base (mm).
Histological characteristics of the ligaments To compare the characteristics of collagen types in the superficial and deep components of the distal radioulnar ligaments inserting onto the distal ulna, an illumination method under polarized light microscopy after picrosirius red staining was applied to 9 TFCC specimens (4 specimens in which accurate transverse sections failed to be obtained were excluded) at the midportion of the volar and dorsal radioulnar ligaments and the superficial and deep limbs of the ligaments attaching to the distal ulna (Fig. 5).15e17 The specimens were fixed in 10% neutral buffered formaldehyde solution and embedded in paraffin. The specimens were stained by 0.1% picrosirius red solutions (Sirius Red F3B; Sigma-Aldrich Co., St. Louis, MO) after sectioning along with the longitudinal direction of the fibers at 5 mm, similar to the methods used by previous investigators.15,17 The sections were then examined under bright field and polarizing microscopy and photographed at 200 magnification. Collagen fibers display uniformly as red or yellow color in type I and as a greenish color in type III under polarized light. The distributions of type I/III collagen were obtained by discriminating the Hue value of each pixel in the images of Hue-Saturation-Brightness color model using i-solution software (IMT i-Solution Inc., Vancouver, BC, Canada). Each of the Hue values of collagen type I and III was measured in 3 rectangular areas (6,400 mm2), which were randomly selected, and collagen I/III ratios were calculated (Fig. 6). Five sequential sections of each specimen were examined to reduce sampling error. J Hand Surg Am.
FIGURE 4: Locations of the trabecular region of interest in the central coronal section. Cylindrical volume of interest in trabecular bone (2 mm diameter, 2 mm length) extracted from 4 lesions in the distal ulna: the pole and fovea of the ulnar head and the base and process of the ulnar styloid, which were highlighted in yellow, red, green, and blue, respectively.
Statistical analysis Results are expressed as mean SD. Nonparametric tests were used because of the small number of samples. The Wilcoxon signed rank test was used to compare the morphometry of the footprint between the deep and the superficial components. The Friedman test was performed to compare topographical parameters in the 3 coronal planes and the internal bone morphometric parameters in 4 locations of the distal ulna as well as collagen I/III ratios in 4 sites of the distal radioulnar ligament. Spearman correlation r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e5
all specimens. The distances from the center of the footprint of the deep limb to the ulnar styloid base, measured in the 3 coronal planes, averaged 2.0 0.76 mm, which corresponded to an average of 50% 5.7% of the width of the distal ulnar head from the most medial cortex. The intercenter distance between the fovea center and ulnar head center averaged 2.4 0.58 mm. Internal trabecular bone morphometry of the distal ulna A 3-dimensional morphometric analysis of the cylindrical trabecular VOI revealed that the base of the ulnar styloid had decreased BV/TV(%) and Tb.N (mme1), and increased Tb.Sp and SMI, compared with the ulnar head and deep and superficial limb insertions. Among them, the differences were significant for Tb.N, Tb.Sp, and SMI (all comparisons, P < .05).
FIGURE 5: The schematic illustration of the 4 anatomical sites of the distal radioulnar ligament for quantitative analysis of histological characteristics of collagen. DL, deep limb of the distal radioulnar ligament inserting to the ulna; DM, midportion of the dorsal radioulnar ligament; SL, superficial limb of the distal radioulnar ligament inserting onto the ulna; VM, midportion of the volar radioulnar ligament.
Correlations between the footprint and distal ulnar topography The area of the superficial limb was positively correlated with the length and width of the ulnar styloid (r ¼ 0.69, P < .05; r ¼ 0.76, P < .05). No correlation was found between the area of deep limb footprint and the distal ulna topographic data. The distance from the deep limb center to the ulnar styloid base was correlated with the width of the ulnar styloid (r ¼ 0.56, P < .05). The intercenter distances were correlated with the distance from the center of the deep limb footprint to the ulnar styloid base (r ¼ 0.51, P < .05).
coefficient analysis was used to correlate the topographical and internal bone morphometry data of the distal ulna. P less than .05 was considered significant for all results. RESULTS Morphometry of the footprint of the distal radioulnar ligament The deep limbs have a long marginal insertion between the pole of the ulnar head and the ulnar styloid base, but the width of the footprint was larger at the fovea than at the peripheral site (Figs. 1B and 2). The superficial limbs inserted at the radial surface of the ulnar styloid process and were condensed and circular in shape, with an approximate circularity ratio of 1. The measured areas of the deep limb were larger than those of the superficial limb (P < .05) (Table 1).
Characteristics of collagen types in the distal radioulnar ligament The results of the collagen I/III ratios for 4 different sites of the distal radioulnar ligament are shown in Figure 7. The mean collagen I/III ratio of the distal radioulnar ligament was 1.27 0.56. The collagen I/III ratio for the deep limb was significantly lower than those of the midportion of the volar radioulnar ligament and superficial limb sections (all comparisons, P < .05). DISCUSSION The fovea has been considered the primary attachment site for the deep fibers of the distal radioulnar ligaments and is critical for providing rotational guidance because the pronation-supination axis of the forearm runs through it.18e21 This also provides primary DRUJ stability because the deep fibers act as a check to prevent further translation of the distal ulna.2,22e24 Therefore, avulsion fractures involving the ulnar
Topographic analysis of the distal ulna The sizes of the distal ulnar head and the widths and length of the ulnar styloid in the coronal plane averaged 16.7 1.58 mm, 6.3 0.89 mm, and 5.3 0.01 mm, respectively, which were similar to those of the other seminal coronal planes (P > .05) (Table 2). The deep limb footprints were located radially, apart from the base of the ulnar styloid in J Hand Surg Am.
r
Vol. -, - 2017
1.e6
ANATOMY OF THE DISTAL ULNA
FIGURE 6: The histological images of the distal radioulnar ligament under polarized light with picrosirius red staining (magnification 200). Greenish birefringence (type III collagen) was observed more in the deep limb section A, whereas red-yellow birefringence (type I collagen) was more predominant in the superficial limb B.
TABLE 1.
Morphometry of the Footprints of the Distal Radioulnar Ligament Superficial Limb
Deep Limb
P Value
Maximal width (mm)
4.11 0.85
12.68 1.93
< .01
Maximal height (mm)
5.25 1.15
3.10 0.34
< .01
Area (mm2)
18.36 6.07
29.67 5.74
< .01
Perimeter (mm)
14.69 2.84
27.44 5.63
< .01
Circularity ratio
1.06 0.11
2.86 0.67
< .01
TABLE 2. Topographical Parameters of the Distal Ulna in the Central Coronal, and 30 Volar, and 30 Dorsal Semicoronal Planes Parameter
30 Volar Plane
Central Plane
30 Dorsal Plane
P Value
15.64 1.72
16.51 1.69
15.52 1.62
.44
Width of the ulnar styloid (mm)
5.69 1.09
6.15 0.87
6.15 1.04
.55
Length of the ulnar styloid (mm)
3.30 0.68
3.15 0.76
3.52 1.07
.79
Distance from the deep limb center to the ulnar styloid base (mm)
2.15 0.71
1.72 0.62
2.12 0.81
.38
Distal ulnar head length (mm)
styloid base or fovea, where the deep limb inserts, increase the potential risk for DRUJ instability.3,4 The fovea of the distal ulna is a central, roughened bony depression on the distal pole of the ulna that lies between the hyaline cartilage of the ulnar pole and the ulnar styloid.1,25,26 The base of the ulnar styloid, which is different from the fovea, is a shallow, concave recess, devoid of cartilage or ligament but with abundant with vascular foramina.24 We found that the fovea was radially apart from the base of the ulnar styloid, and that the average distance from the center of the deep limb attachment to ulnar styloid base was 2.0 mm in all coronal planes. The microarchitectural morphometric analysis of the distal ulna in the present study revealed that bone density and J Hand Surg Am.
trabecular thickness were the lowest at the ulnar styloid base, predisposing this area to fracture. These findings may explain why neither size nor displacement of an ulnar styloid fragment predicts DRUJ instability.6,7,27,28 An injury of the deep component of the distal radioulnar ligament is more likely when a fracture involving the ulnar styloid is more proximal or radial from the ulnar styloid base. One study recorded the maximum size of the fovea as an average of 4.7 mm.29 However, the deep limb had a long marginal insertion just behind the pole of the distal ulna, and maximum width and length averaged 3.1 mm and 12.6 mm, respectively. The width of the deep limb footprint was maximized on the fovea. In contrast, the footprint shape of the r
Vol. -, - 2017
ANATOMY OF THE DISTAL ULNA
1.e7
FIGURE 7: Comparison of the collagen I/III ratio between the 4 lesions of the distal radioulnar ligament (RUL). Note that the collagen I/ III ratio at the deep limb was significantly lower than those of the volar RUL and superficial limb sections. The error bars represent SD. * indicates P < .05.
superficial limb was close to circular and condensed in shape. Based on the morphometric findings of the ligament footprint, we speculate that the deep limb is an internal ligament that forms the DRUJ capsule and also serves as a rotational and translational joint stabilizer, whereas the superficial limb acts as an external ligament of the joint, like the medial collateral ligament of the knee. These findings support previous biomechanical observations that the palmar part of the deep limb is taut with forearm supination as the ulna translates palmarly, whereas the dorsal part is taut with the forearm pronated as the ulna translates dorsally.22,23,30 The center of the ulnar head is known to be near the fovea of the distal ulna, indicating that the DRUJ axis of rotation runs through the center of the ulnar head.18,19,31 In fact, several studies have suggested various CT methods to assess DRUJ instability according to how much the center of the ulnar head is translated either anteriorly or posteriorly during forearm rotation.32e34 However, our data demonstrate that the center of the ulnar head was not congruent with the anatomical center of the fovea because the anatomical center of the fovea was located more ulnarly and farther from the center of the ulnar head. This finding agrees with the data reported by Kataoka et al21 showing a greater discrepancy between the center of the ulnar head and the pronosupination axis of the forearm. It is well established that collagen type is related to the mechanical properties of ligaments and an J Hand Surg Am.
increasing percentage of type III collagen has been found to result in decreasing mechanical properties.15,35 From the histological data in the present study, it is speculated that each limb of the radioulnar ligament inserting into the distal ulna has different mechanical properties, and this also supports our previous assumption that the deep limb serves as an internal ligament that forms the joint capsule whereas the superficial limb as an external ligament in the DRUJ. This study was limited by the small number of specimens. However, the consistency of this distinct footprint pattern of the footprint of the 2 components in all specimens indicates that our sample might be adequate. This study was also limited by less clear visualization of the footprints caused by painting them with contrast media because of the small area on the small distal ulna. Quantification of the proportion of collagen types might be biased by examination of a limited portion of each component of the TFCC. Finally, the measurement of the distribution of collagen type I/III ratio was dependent upon observer factors, such as how much the Hue value of each pixel was discriminated in the images. ACKNOWLEDGMENTS The authors thank Chae-Eun Lee, radiological technologist, for her support. The authors also gratefully thank the individuals who donated their bodies to the Department of Anatomy, Dankook University r
Vol. -, - 2017
1.e8
ANATOMY OF THE DISTAL ULNA
College of Medicine. This article would not have been possible without their selfless gift.
18. Youm Y, Dryer RF, Thambyrajah K, Flatt AE, Sprague BL. Biomechanical analyses of forearm pronation-supination and elbow flexion-extension. J Biomech. 1979;12(4):245e255. 19. Kapandji A. Biomechanics of pronation and supination of the forearm. Hand Clin. 2001;17(1):111e122, vii. 20. Hollister AM, Gellman H, Waters RL. The relationship of the interosseous membrane to the axis of rotation of the forearm. Clin Orthop Relat Res. 1994;298:272e276. 21. Kataoka T, Moritomo H, Omokawa S, Iida A, Murase T, Sugamoto K. Ulnar variance: its relationship to ulnar foveal morphology and forearm kinematics. J Hand Surg Am. 2012;37(4): 729e735. 22. Kihara H, Short WH, Werner FW, Fortino MD, Palmer AK. The stabilizing mechanism of the distal radioulnar joint during pronation and supination. J Hand Surg Am. 1995;20(6):930e936. 23. Ward LD, Ambrose CG, Masson MV, Levaro F. The role of the distal radioulnar ligaments, interosseous membrane, and joint capsule in distal radioulnar joint stability. J Hand Surg Am. 2000;25(2): 341e351. 24. Huang JI, Hanel DP. Anatomy and biomechanics of the distal radioulnar joint. Hand Clin. 2012;28(2):157e163. 25. Ishii S, Palmer AK, Werner FW, Short WH, Fortino MD. An anatomic study of the ligamentous structure of the triangular fibrocartilage complex. J Hand Surg. 1998;23(6):977e985. 26. Kleinman WB. Stability of the distal radioulna joint: biomechanics, pathophysiology, physical diagnosis, and restoration of function what we have learned in 25 years. J Hand Surg Am. 2007;32(7): 1086e1106. 27. Arealis G, Galanopoulos I, Nikolaou VS, Lacon A, Ashwood N, Kitsis C. Does the CT improve inter- and intra-observer agreement for the AO, Fernandez and Universal classification systems for distal radius fractures? Injury. 2014;45(10):1579e1584. 28. Kim JK, Yun YH, Kim DJ, Yun GU. Comparison of united and nonunited fractures of the ulnar styloid following volar-plate fixation of distal radius fractures. Injury. 2011;42(4):371e375. 29. Sharma A, Kumar A, Singh P. Anatomical study of the distal end of cadaveric human ulnae: a clinical consideration for the management of distal radioulnar joint injuries. Singapore Med J. 2011;52(9): 673e676. 30. Schuind F, An KN, Berglund L, et al. The distal radioulnar ligaments: a biomechanical study. J Hand Surg Am. 1991;16(6): 1106e1114. 31. af Ekenstam F, Hagert CG. Anatomical studies on the geometry and stability of the distal radio ulnar joint. Scand J Plast Reconstr Surg. 1985;19(1):17e25. 32. Wechsler RJ, Wehbe MA, Rifkin MD, Edeiken J, Branch HM. Computed tomography diagnosis of distal radioulnar subluxation. Skeletal Radiol. 1987;16(1):1e5. 33. Lo IK, MacDermid JC, Bennett JD, Bogoch E, King GJ. The radioulnar ratio: a new method of quantifying distal radioulnar joint subluxation. J Hand Surg Am. 2001;26(2):236e243. 34. Kim JP, Park MJ. Assessment of distal radioulnar joint instability after distal radius fracture: comparison of computed tomography and clinical examination results. J Hand Surg. 2008;33(9):1486e1492. 35. Woo SL, Abramowitch SD, Kilger R, Liang R. Biomechanics of knee ligaments: injury, healing, and repair. J Biomech. 2006;39(1): 1e20.
REFERENCES 1. Stuart PR, Berger RA, Linscheid RL, An KN. The dorsopalmar stability of the distal radioulnar joint. J Hand Surg Am. 2000;25(4):689e699. 2. Haugstvedt JR, Berger RA, Nakamura T, Neale P, Berglund L, An KN. Relative contributions of the ulnar attachments of the triangular fibrocartilage complex to the dynamic stability of the distal radioulnar joint. J Hand Surg Am. 2006;31(3):445e451. 3. Sammer DM, Chung KC. Management of the distal radioulnar joint and ulnar styloid fracture. Hand Clin. 2012;28(2):199e206. 4. May MM, Lawton JN, Blazar PE. Ulnar styloid fractures associated with distal radius fractures: incidence and implications for distal radioulnar joint instability. J Hand Surg Am. 2002;27(6):965e971. 5. Souer JS, Ring D, Matschke S, et al. Effect of an unrepaired fracture of the ulnar styloid base on outcome after plate-and-screw fixation of a distal radial fracture. J Bone Joint Surg Am. 2009;91(4):830e838. 6. Sammer DM, Shah HM, Shauver MJ, Chung KC. The effect of ulnar styloid fractures on patient-rated outcomes after volar locking plating of distal radius fractures. J Hand Surg Am. 2009;34(9):1595e1602. 7. Kim JK, Koh YD, Do NH. Should an ulnar styloid fracture be fixed following volar plate fixation of a distal radial fracture? J Bone Joint Surg Am. 2010;92(1):1e6. 8. Rozental TD, Deschamps LN, Taylor A, et al. Premenopausal women with a distal radial fracture have deteriorated trabecular bone density and morphology compared with controls without a fracture. J Bone Joint Surg Am. 2013;95(7):633e642. 9. Jenkins PJ, Ramaesh R, Pankaj P, et al. A micro-architectural evaluation of osteoporotic human femoral heads to guide implant placement in proximal femoral fractures. Acta Orthop. 2013;84(5):453e459. 10. Hsu JT, Wang SP, Huang HL, Chen YJ, Wu J, Tsai MT. The assessment of trabecular bone parameters and cortical bone strength: a comparison of micro-CT and dental cone-beam CT. J Biomech. 2013;46(15):2611e2618. 11. Hsu JT, Chen YJ, Ho JT, et al. A comparison of micro-CT and dental CT in assessing cortical bone morphology and trabecular bone microarchitecture. PloS One. 2014;9(9):e107545. 12. Norman DG, Getgood A, Thornby J, et al. Quantitative topographic anatomy of the femoral ACL footprint: a micro-CT analysis. Med Biol Engi Comput. 2014;52(11):985e995. 13. Chidgey LK, Dell PC, Bittar ES, Spanier SS. Histologic anatomy of the triangular fibrocartilage. J Hand Surg Am. 1991;16(6):1084e1100. 14. Wang Y, Zhao C, Passe SM, et al. Transverse ultrasound assessment of median nerve deformation and displacement in the human carpal tunnel during wrist movements. Ultrasound Med Biol. 2014;40(1):53e61. 15. Wan C, Hao Z, Wen S. A quantitative comparison of morphological and histological characteristics of collagen in the rabbit medial collateral ligament. Ann Anat. 2013;195(6):562e569. 16. Cohen DB, Kawamura S, Ehteshami JR, Rodeo SA. Indomethacin and celecoxib impair rotator cuff tendon-to-bone healing. Am J Sports Med. 2006;34(3):362e369. 17. Junqueira LC, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J. 1979;11(4):447e455.
J Hand Surg Am.
r
Vol. -, - 2017