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Three-dimensional osseous micro-architecture of the distal humerus: Implications for internal fixation of osteoporotic fracture
J Shoulder Elbow Surg (2010) 19, 244-250
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Three-dimensional osseous micro-architecture of the distal humerus: Implications for internal fixation of osteoporotic fracture So Hyun Park, MDa, Sung Jung Kim, MDb, Byun Chul Park, MDb, Kyung Jin Suh, MDc, Jee Young Lee, MDd, Chun Woo Park, MDe, Im Hee Shin, PhDe, In-Ho Jeon, MDb,* a
Department of Physical Therapy, Daegu University, Daegu, Korea Department of Orthopaedic Surgery, School of Medicine, Kyungpook National University, Daegu, Korea c Musculoskeletal Imaging Service, Department of Radiology, Dongguk University Hospital, Gyungju, Korea d Department of Radiology, Dankook University, Hospital, Chunan, Korea e Department of Medical Statistics, Catholic University, Daegu, Korea b
Background: The purpose of this study is to analyze 3-dimensional structural parameters of cortical and trabecular bone in the distal humerus using quantitative CT and to find regional variations and differences according to age. Methods: We collected 14 cadaveric distal humeri with an average age of 58.4 years. The specimens were examined at 3 different levels: 1) distal trans-epicondylar section, 2) mid trans-olecranon fossa section, and 3) proximal supra-olecranon fossa section. Results: In the distal section, bone volume was the greatest in the anterior part of the lateral condyle and the least in the posterior part of the lateral condyle. Cortical thickness in the distal section was the thickest in the posterior medial and the thinnest in the anterior aspect followed by lateral aspect. The changes in cortical thickness with aging were obvious in the posterior side and trabecular bone on the medial condyle. Conclusion: This study evaluated the differences in cortical and trabecular bone parameters in each different region of the distal humerus. We found a potential weakness of plate fixation in the posterolateral aspect of the distal condyle because of relative insufficient osseous micro-architecture, which may affect the treatment of osteoporotic distal humerus fractures especially in elderly patients. Level of evidence: Basic Science Study, Anatomic Cadaver Study. Ó 2010 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Cortical bone; Trabecular bone; Bone volume; Cortical thickness
IRB (University Hospital) has been approved but no number was issued because this was a cadaveric study. Redeemed. *Reprint requests: In-Ho Jeon, MD, Department of Orthopaedic Surgery, Kyungpook National University Hospital, 50 Samduk, Chung-Gu, Daegu, Korea 700-721. E-mail address: [email protected] (I.-H. Jeon).
Fractures of the distal humerus in elderly patients are challenging for surgeons. Diminished bone mineral quality and increased joint destruction from trauma may make stable joint reconstruction more difficult in this age group.8, 14 There is, nevertheless, a debate on the optimal treatment of these fractures, especially for elderly patients with osteoporosis.7,14
1058-2746/2010/$36.00 - see front matter Ó 2010 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2009.08.005
3-Dimensional osseous micro-architecture of the distal humerus In the elderly patient, one of the most important failure factors in internal fixation is loosening of the implant following open reduction and internal fixation (Figure 1). Despite the high clinical relevance of bone mass and bone quality of the distal humerus,15 the anatomic microarchitecture of the various structural parameters of distal humerus has not been thoroughly investigated. When assessing bone mass, dual energy x-ray absorptiometry (DEXA) is widely used; but this is a 2-dimensional (2-D) technique that has limitations in assessing the spatial distribution of bone mass or discriminating trabecular from cortical bone. An improved analysis using 3-dimensional (3-D) volumetric CT scan, enables a separate determination of cortical and trabecular bone volume in all regions of interest. The purpose of this study is to analyze the 3-D structural parameters of cortical and trabecular bone in the distal humerus using volumetric quantitative computed tomogram (CT) scan and to find regional variations and differences with respect to age. A better understanding of the micro-architecture of the distal humerus has significant clinical ramifications for the internal fixation of distal humeral fractures, especially in the elderly with osteoporosis.
Material and methods We retrieved 14 unpaired distal humeri from cadavers, harvested at 15 cm from the joint line. Specimens having previous fractures, tumors, or surgical interventions were excluded. Specimens were dissected free of all soft tissue and plain radiographs were taken to detect any bone abnormalities. The distal humeri were separated from the ulnae. All specimens (14) were from males with a mean age of 58.4 years. These specimens were divided into 2 groups: younger than 60 years old and older than 60 years. Eight humeri were included in the younger group (mean age, 52 years) and 6 in the older group (mean age, 67 years).
Volumetric CT scan We used a 64-row multi-detector CT scanner, LightSpeed VCT (GE Healthcare, Milwaukee, WI) to investigate the 3-D architecture of the distal humerus. Analysis of the image was performed using Centricity AW Suite (GE Healthcare) achieving images from Advantage Workstation 4.3 and internal DICOM network. The long axis was fixed with a minimum of 0.3 mm, and a 5-mm cubic region of interest (ROI) was placed in the center of each cross-sectional area. The following variables were measured using the automated computed program: 1) trabecular bone volume in cubic ROI (Bone volume/Trabecular volume, Bv/Tv); 2) trabecular thickness; 3) number of nodes (N Nd); 4) inter-nodal distance, and 5) cortical thickness (Ct Th). Each distal humerus was examined at 3 different levels (Figure 2): 1) distal section: trans-epicondylar line which transverses the center of the epicondyles at saggital view; 2) mid section: trans-olecranon fossa line which transverses the centre of olecranon fossa at saggital view; and 3) proximal section:
245 supra-olecranon fossa line which transverses the upper edge of the olecranon fossa at saggital view. Each measurement was repeated 3 times and the average value was chosen for analysis.
Trabecular bone volume, trabecular thickness, number of nodes, internodal distance, and width of trabeculae For trabecular bone-volume measurement, 1) the distal section was divided into 5 areas: lateral condyle anterior (LA), lateral condyle posterior (LP), medial condyle anterior (MA), medial condyle posterior (MP), and central (C); 2) the mid section was divided into lateral column (L) and medial column (M); and 3) the proximal section was further divided into lateral (L) representing lateral column, medial (M) representing medial column, and central area (C).
Cortical thickness As thresholds significantly affect the results of the cortical BMD, we used 1,200 mg/ml for accurate determination of cortical thickness following the guidelines of Ward et al.20 Cortical thickness was measured at all 3 sections. At each axial image, cortical thickness was measured at 8 different areas and the mean values analyzed: 12:00 (A ¼ anterior), 1:30 (MA ¼ medial anterior), 3:00 (M ¼ medial), 4:30 (MP ¼ medial posterior), 6:00 (P ¼ post), 7:30 (LP ¼ lateral posterior), 9:00 (L ¼ lateral), and 10:30 (LA ¼ lateral anterior area) based on the clock plate.
Statistical analysis All demographical characteristics were summarized as means and standard deviations for continuous data, frequency, and percentage for discrete data. Repeated measures 1 factor analysis was used to determine the regional differences in the proximal, middle, and distal section. For the comparison of 2 groups, Wilcoxon rank-sum test was used (younger and elder group). A cut-off P value of .05 was adopted for all statistical significance. All statistical analysis was performed using SPSS/PCþ for windows (version 14.0; SPSS Inc., Chicago, IL).
Results Trabecular parameters Trabecular bone volume Analysis of the trabecular bone volume (BV/TV) is demonstrated in Figure 3, A. In the most distal section (trans-epicondyle area), the mean trabecular bone volume was the greatest in the LA (mean SD ¼ 76.9 16.1), followed by the MP (62.8 222.3) and MA (58.6 21.5). It was measured the least in the LP (27.8 21.1). There were statistically significant differences (P < .05), as noted in Figure 3, A. In the mid section (trans-olecranon fossa area), trabecular bone volume in the medial column was greater than that of lateral (84.5 20.8 vs 69.0 21.6), which was statistically significant (P < .05). In the proximal section (supra-olecranon fossa area), trabecular bone volume in the lateral column was significantly greater followed by medial
246
Figure 1 fixation.
S.H. Park et al.
A 75-year-old lady presented with plate failure and screw pullout in the lateral condyle after open reduction and internal
Figure 2 Each distal humeri was examined at 3 different levels. A, Proximal section: supra-olecranon fossa line which transverses the upper edge of the olecranon fossa at saggital view. B, Mid section: trans-olecranon fossa line which transverses the center of olecranon fossa at saggital view. C, Distal section: trans-epicondylar line which transverses the center of the epicondyles at saggital view.
and central column. There were significant differences between the lateral and central columns (P < .05). Trabecular thickness Analysis of the trabecular thickness is shown in Figure 3, B. In the most distal section (trans-epicondyle area), trabecular thickness was the greatest in the LA, followed by the MP and MA, and the thinnest in the LP area (P < .05). In the mid (trans-olecranon fossa area) and proximal (supra-olecranon fossa area) sections, there was a thicker measurement in the lateral column than in the medial column, but there were no statistically significant differences (P > .05). Number of nodes Analysis of the number of nodes is presented in Figure 3, C. In the most distal section (trans-epicondyle area), the highest node number was noted in the MA area and the minimum in the LP area. There were significant differences
among the regions (P < .05). In the mid section (transolecranon fossa area), there were more nodes in the medial than the lateral column (P < .05), while it was similar in both columns in the proximal section (supra-olecranon fossa area) (P < .05) (Figure 3, C). Intertrabecular distance In the most distal section (trans-epicondyle area), distance between the trabeculae was at a minimum in the LA area and a maximum in the LP area (P < .05). In the mid (transolecranon fossa area) and proximal (supra-olecranon fossa area) sections, the measured distance was wider in the lateral column compared to the medial column (Figure 3, D). Internodal distance In the most distal section (trans-epicondyle area), the distance between the nodes was minimal in the MP area and maximal in the LP area. There were significant
3-Dimensional osseous micro-architecture of the distal humerus
247
Figure 3 Comparison of trabecular parameters for each region of interest in the distal humerus. A, Trabecular bone volume/tissue volume (Bv/Tv). B, Trabecular thickness. C, Node number. D, Intertrabecular distance. E, Internodal distance. Prox, proximal section (supraolecranon fossa area); Mid, mid section (trans-olecranon fossa section); Dist, distal section (trans-epicondylar section); M, medial; C, central; Lat, lateral; MA, medial/anterior; MP, medial/posterior; LA, lateral/anterior; LP, lateral/posterior. In the proximal and mid sections; ), signifies a difference among regions with respect to lateral as contrast group. In the distal section, ) signifies a difference among regions with respect to lateral/post as contrast group. All data reported as mean (standard deviation), results of repeated measures 1 factor analysis, )P < .05.
differences among the regions (P < .05). In the mid- (transolecranon fossa area) and proximal (supra-olecranon fossa area) sections, internodal distance was not significantly different among the regions (P > .05) (Figure 3, E).
was the greatest in the anterolateral aspect and thinnest in the anterior aspect. In the proximal section (supra-olecranon fossa area), it was thicker in the posterior medial aspect followed by the anterior lateral aspect, and thinnest in the lateral aspect (P < .05).
Cortical thickness Comparison of the 2 groups according to the age Analysis of the cortical thickness is demonstrated in Table I. In the most distal section (trans-epicondyle area), cortical thickness was thickest in the posterior medial side and the thinnest in the anterior aspect. Additionally, there were significant differences among the regions (P < .05). In the mid section (trans-olecranon fossa area), cortical thickness
There were several changes in terms of trabecular bone pattern between the 2 groups of specimens (Figure 4). In the younger group, the distal section indicated a greater value of Bv/Tv in the LA area, followed by the MP area with the minimum found in the LP area. In the elderly
248 Table I
S.H. Park et al. Comparison of cortical thickness for each region of the distal humerus
Cortical A thickness
MA
M
MP
P
LP
L
LA
F-value [p-value]
Proximal 2.02 (1.16)y,z 3.56 (0.65)y,z 3.69 (1.28)y 3.75 (0.92)y,z 3.64 (1.06)y 3.11 (0.77)y 1.14 (0.87)z 3.66 (0.76)y,z 22.05 [.00)] Mid 0.97 (0.58)z 3.09 (1.04)y 1.40 (0.89)z 2.57 (0.85)y 1.00 (0.58)z 3.01 (1.35)y 1.26 (1.04)z 3.57 (1.06)y 24.47 [.00)] Distal 1.97 (1.32)z 3.02 (1.40) 3.53 (1.56)y 3.76 (1.46)y 3.09 (1.03) 3.10 (1.02) 2.64 (1.12) 3.44 (1.30) y 4.20 [.00)] Parametric data reported as mean (standard deviation), results of repeated measures 1 factor analysis. ) Significant difference <.05 y Difference among position with respect to contrast group, lateral. z Difference among position with respect to contrast group, lateral post.
Figure 4 Comparison of trabecular parameters for each region in the distal humerus between two age groups. A, Trabecular bone volume/tissue volume (Bv/Tv). B, Trabecular thickness. C, Node number. D, Intertrabecular distance. E, Internodal distance. Prox, proximal section (supra-olecranon fossa area); Mid, mid section (trans-olecranon fossa section); Dist, distal section (trans-epicondylar section); M, medial; C, central; Lat, lateral; MA, medial/anterior; MP, medial/posterior; LA, lateral/anterior; LP, lateral/posterior. All data reported as mean (standard deviation), results of Wilcoxon rank sum test for comparison of 2 groups; age <60 and age 60, )P < .05.
group, it was the greatest in the LA area; however, there was a significant decrease of trabecular bone volume in the LP area. In the mid and proximal sections, Bv/Tv in the lateral column decreased significantly in the elderly group
(Figure 4, A). Overall, the trabecular thickness was greater in the younger group than in the elderly, especially at the MA, MP area (P < .05). In the proximal section, the decrease was more obvious in the lateral column compared
249
0.95 (0.97) 1.38 (0.72) 49.50 (0.17) 1.34 (1.24) 1.15 (0.80) 44.50 (0.95) 2.36 (1.09) 3.00 (1.13) 52.50 (0.33) 3.40 (0.65) 2.72 (0.79) 34.00 (0.15) 3.40 (1.50) 2.50 (1.03) 35.50 (0.22) 3.48 (0.96) 2.60 (0.93) 34.50 (0.17) 3.69 (1.08) 3.57 (1.14) 45.00 (1.00) 0.89 (0.65) 1.15 (0.48) 55.50 (0.56) 3.61 (0.67) 2.40 (1.05) 28.50 (0.03)) 4.13 (0.68) 3.25 (1.03) 34.50 (0.17) 2.74 (0.72) 2.35 (1.03) 37.50 (0.33) 4.09 (1.79) 3.33 (0.81) 36.00 (0.25) 1.65 (0.83) 2.52 (1.42) 52.50 (0.33) 0.94 (0.66) 1.02 (0.51) 43.00 (0.80) 2.10 (1.03) 2.50 (1.25) 34.50 (0.47) Distal
Mid
Younger group Elderly group Wilcoxon rank sum test Younger group Elderly group Wilcoxon rank sum test Younger group Elderly group Wilcoxon rank sum test
Mean (SD) Mean (SD) W (P value) Mean (SD) Mean (SD) W (P value) Mean (SD) Mean (SD) W (P value) Proximal
Parametric data reported as mean (standard deviation), results of Wilcoxon rank sum test ) Significant difference <.05
3.74 (1.12) 3.63 (1.59) 43.50 (0.85) 1.65 (1.04) 1.07 (0.57) 35.00 (0.20) 3.49 (1.46) 3.58 (1.84) 44.50 (0.95)
P MP M MA A Parameters
Comparison of cortical thickness for each region of the distal humerus between 2 groups Table II
Loosening of implants and screw pullout can lead to serious complications after surgical reconstruction of distal humeral fractures, especially in the elderly, with more osteoporotic bone. Despite the clinical significance of bone quality in relation to fracture treatment outcome,6, 15 few studies have investigated the histomorphometric parameters of the distal humerus. Previous studies have quantified the morphological and mechanical property of cancellous bone at various sites with a primary focus on the hip12, 19 and spine,2, 5 while some studies have analyzed the histomorphometry of the proximal humerus for better understanding of fracture fixation and rotator cuff repair.9, 16, 17 To our knowledge, this is the first investigation of 3-D regional variations of histomorphometric parameters in the distal humerus. Unlike DXA, a major advantage of QCT over other techniques is its ability to isolate and measure trabecular bone separately from cortical bone.4 High-resolution multislice CT and micro-CT are useful tools for the assessment of bone micro-architecture.2,3 Trabecular bone volume in the distal condyle was at its greatest in the anterior half of the lateral condyle and was lowest in the posterior half of the lateral condyle. This observation has clinical implications for surgical treatment of distal humerus fracture, as placing screws or plates in this region may give a higher risk of implant loosening resulting in fracture re-displacement. Previous studies of the proximal humerus showed that trabecular BMD using 3-D pQCT has a greater impact on pullout strength of the screw or suture anchor than cortical BMD.17,18 Bone loss is one of the most important factors of fractures and treatment among the elderly. The strength of a bone is closely associated with the bone mass and architectural structure. We divided the specimens into 2 groups based on the fact that hip fracture risk rises 100- to 1000-fold after 60 years of age.11 Age-related change in cortical thickness was significant in the posterior aspect of the distal section. Studies on the femoral neck also demonstrated age-related microscopic structural and mineral changes around the femoral neck cortex, indicating the location of osteopenic differences in the elderly.1 A decrease in cortical thickness with aging was less obvious in the anterior and medial side than the posterior side in this
LP
Discussion
3.69 (0.60) 3.38 (0.72) 38.50 (0.40) 3.13 (1.12) 3.03 (1.03) 45.00 (1.00) 3.24 (1.41) 2.73 (1.47) 41.00 (0.60)
L
LA
to the medial column (P < .05) (Figure 4, B). With aging, the number of nodes decreased in all areas; the MP, LA of the distal section (Figure 4, C). When both groups were compared, the intertrabecular and internodal distances were wider in the elderly group (P < .05) (Figure 4, D, E). Differences in the cortical thickness in both groups showed that in the distal section, the posterior aspect became thinner (P < .05); however, no statistically significant decrease was noted in other areas (Table II).
3.78 (0.81) 3.50 (0.72) 39.00 (0.44) 3.65 (1.12) 3.47 (1.06) 42.50 (0.75) 3.46 (1.39) 3.42 (1.30) 59.50 (0.95)
3-Dimensional osseous micro-architecture of the distal humerus
250 study. The LP area of the distal section showed the least number of nodes, the thinnest trabecular thickness, and the widest intertrabecular distance when compared to other areas. According to finite element modeling, reductions in trabecular number have a 2- to 5-fold greater impact on bone strength compared with reductions in trabecular thickness despite similar decreases in bone volume.13 The limitation of this study is the small number of specimens and no comparative biomechanical analysis. Furthermore, large population-based studies using other imaging techniques to assess bone microstructure, such as MRI,10 should be done to independently test the findings from the 3-D pQCT technology.
Conclusion This study evaluated the differences in cortical and trabecular bone parameters in each region of the distal humerus. With aging, the cortices became thinner especially in the posterior and posterolateral side of the distal condyle. These findings suggest micro-architecture of the bone in the posterolateral area of the lateral condyle is weaker, especially in the elderly, which may lead to mechanical failure, loosening of the screws, or fracture re-displacement; therefore, positioning the plates on both ridges of the distal humerus could have an advantage compared to posterolateral plating. However, to delineate the mechanism of healing and failure in this anatomic area, further biomechanical and clinical studies are required.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
References 1. Boyce TM, Bloebaum RD. Cortical aging differences and fracture implications for the human femoral neck. Bone 1993;14:769-78. 2. Chen H, Shoumura S, Emura S, Bunai Y. Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos Int 2008;19:1473-83.13.
S.H. Park et al. 3. Damilakis J, Maris TG, Karantanas AH. An update on the assessment of osteoporosis using radiologic techniques. Eur Radiol 2007;17:1591602. 4. Dougherty G. Quantitative CT in the measurement of bone quantity and bone quality for assessing osteoporosis. Med Eng Phys 1996;18: 557-68. 5. Gordon CL, Lang TF, Augat P, Genant HK. Image-based assessment of spinal trabecular bone structure from high-resolution CT images. Osteoporos Int 1998;8:317-25. 6. Homminga J, McCreadie BR, Ciarelli TE, Weinans H, Goldstein SA, Huiskes R. Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level. Bone 2002;30:759-64. 7. Huang TL, Chiu FY, Chuang TY, Chen TH. The results of open reduction and internal fixation in elderly patients with severe fractures of the distal humerus: a critical analysis of the results. J Trauma 2005; 58:62-9. 8. Kamineni S, Morrey BF. Distal humeral fractures treated with noncustom total elbow replacement. Surgical technique. J Bone Joint Surg Am 2005;87:41-50. 9. Lehtinen JT, Tingart MJ, Apreleva M, Ticker JB, Warner JJ. Variations in glenoid rim anatomy: implications regarding anchor insertion. Arthroscopy 2004;20:175-8. 10. Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, et al. Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res 1997;12:111-8. 11. Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, et al. Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 2005;366:129-35. 12. Perilli E, Baleani M, Ohman C, Baruffaldi F, Viceconti M. Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age. Bone 2007;41: 760-8. 13. Silva MJ, Gibson LJ. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone 1997;21:191-9. 14. Srinivasan K, Agarwal M, Matthews SJ, Giannoudis PV. Fractures of the distal humerus in the elderly: is internal fixation the treatment of choice? Clin Orthop Relat Res 2005;434:222-30. 15. Thiele OC, Eckhardt C, Linke B, Schneider E, Lill CA. Factors affecting the stability of screws in human cortical osteoporotic bone: a cadaver study. J Bone Joint Surg Br 2007;89:701-5. 16. Tingart MJ, Apreleva M, Zurakowski D, Warner JJ. Pullout strength of suture anchors used in rotator cuff repair. J Bone Joint Surg Am 2003; 85:2190-8. 17. Tingart MJ, Bouxsein ML, Zurakowski D, Warner JP, Apreleva M. Three-dimensional distribution of bone density in the proximal humerus. Calcif Tissue Int 2003;73:531-6. 18. Tingart MJ, Lehtinen J, Zurakowski D, Warner JJ, Apreleva M. Proximal humeral fractures: regional differences in bone mineral density of the humeral head affect the fixation strength of cancellous screws. J Shoulder Elbow Surg 2006;15:620-4. 19. Uitewaal PJ, Lips P, Netelenbos JC. An analysis of bone structure in patients with hip fracture. Bone Miner 1987;3:63-73. 20. Ward KA, Adams JE, Hangartner TN. Recommendations for thresholds for cortical bone geometry and density measurement by peripheral quantitative computed tomography. Calcif Tissue Int 2005;77: 275-80.
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Three-dimensional osseous micro-architecture of the distal humerus: Implications for internal fixation of osteoporotic fracture So Hyun Park, MDa, Sung Jung Kim, MDb, Byun Chul Park, MDb, Kyung Jin Suh, MDc, Jee Young Lee, MDd, Chun Woo Park, MDe, Im Hee Shin, PhDe, In-Ho Jeon, MDb,* a
Department of Physical Therapy, Daegu University, Daegu, Korea Department of Orthopaedic Surgery, School of Medicine, Kyungpook National University, Daegu, Korea c Musculoskeletal Imaging Service, Department of Radiology, Dongguk University Hospital, Gyungju, Korea d Department of Radiology, Dankook University, Hospital, Chunan, Korea e Department of Medical Statistics, Catholic University, Daegu, Korea b
Background: The purpose of this study is to analyze 3-dimensional structural parameters of cortical and trabecular bone in the distal humerus using quantitative CT and to find regional variations and differences according to age. Methods: We collected 14 cadaveric distal humeri with an average age of 58.4 years. The specimens were examined at 3 different levels: 1) distal trans-epicondylar section, 2) mid trans-olecranon fossa section, and 3) proximal supra-olecranon fossa section. Results: In the distal section, bone volume was the greatest in the anterior part of the lateral condyle and the least in the posterior part of the lateral condyle. Cortical thickness in the distal section was the thickest in the posterior medial and the thinnest in the anterior aspect followed by lateral aspect. The changes in cortical thickness with aging were obvious in the posterior side and trabecular bone on the medial condyle. Conclusion: This study evaluated the differences in cortical and trabecular bone parameters in each different region of the distal humerus. We found a potential weakness of plate fixation in the posterolateral aspect of the distal condyle because of relative insufficient osseous micro-architecture, which may affect the treatment of osteoporotic distal humerus fractures especially in elderly patients. Level of evidence: Basic Science Study, Anatomic Cadaver Study. Ó 2010 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Cortical bone; Trabecular bone; Bone volume; Cortical thickness
IRB (University Hospital) has been approved but no number was issued because this was a cadaveric study. Redeemed. *Reprint requests: In-Ho Jeon, MD, Department of Orthopaedic Surgery, Kyungpook National University Hospital, 50 Samduk, Chung-Gu, Daegu, Korea 700-721. E-mail address: [email protected] (I.-H. Jeon).
Fractures of the distal humerus in elderly patients are challenging for surgeons. Diminished bone mineral quality and increased joint destruction from trauma may make stable joint reconstruction more difficult in this age group.8, 14 There is, nevertheless, a debate on the optimal treatment of these fractures, especially for elderly patients with osteoporosis.7,14
1058-2746/2010/$36.00 - see front matter Ó 2010 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2009.08.005
3-Dimensional osseous micro-architecture of the distal humerus In the elderly patient, one of the most important failure factors in internal fixation is loosening of the implant following open reduction and internal fixation (Figure 1). Despite the high clinical relevance of bone mass and bone quality of the distal humerus,15 the anatomic microarchitecture of the various structural parameters of distal humerus has not been thoroughly investigated. When assessing bone mass, dual energy x-ray absorptiometry (DEXA) is widely used; but this is a 2-dimensional (2-D) technique that has limitations in assessing the spatial distribution of bone mass or discriminating trabecular from cortical bone. An improved analysis using 3-dimensional (3-D) volumetric CT scan, enables a separate determination of cortical and trabecular bone volume in all regions of interest. The purpose of this study is to analyze the 3-D structural parameters of cortical and trabecular bone in the distal humerus using volumetric quantitative computed tomogram (CT) scan and to find regional variations and differences with respect to age. A better understanding of the micro-architecture of the distal humerus has significant clinical ramifications for the internal fixation of distal humeral fractures, especially in the elderly with osteoporosis.
Material and methods We retrieved 14 unpaired distal humeri from cadavers, harvested at 15 cm from the joint line. Specimens having previous fractures, tumors, or surgical interventions were excluded. Specimens were dissected free of all soft tissue and plain radiographs were taken to detect any bone abnormalities. The distal humeri were separated from the ulnae. All specimens (14) were from males with a mean age of 58.4 years. These specimens were divided into 2 groups: younger than 60 years old and older than 60 years. Eight humeri were included in the younger group (mean age, 52 years) and 6 in the older group (mean age, 67 years).
Volumetric CT scan We used a 64-row multi-detector CT scanner, LightSpeed VCT (GE Healthcare, Milwaukee, WI) to investigate the 3-D architecture of the distal humerus. Analysis of the image was performed using Centricity AW Suite (GE Healthcare) achieving images from Advantage Workstation 4.3 and internal DICOM network. The long axis was fixed with a minimum of 0.3 mm, and a 5-mm cubic region of interest (ROI) was placed in the center of each cross-sectional area. The following variables were measured using the automated computed program: 1) trabecular bone volume in cubic ROI (Bone volume/Trabecular volume, Bv/Tv); 2) trabecular thickness; 3) number of nodes (N Nd); 4) inter-nodal distance, and 5) cortical thickness (Ct Th). Each distal humerus was examined at 3 different levels (Figure 2): 1) distal section: trans-epicondylar line which transverses the center of the epicondyles at saggital view; 2) mid section: trans-olecranon fossa line which transverses the centre of olecranon fossa at saggital view; and 3) proximal section:
245 supra-olecranon fossa line which transverses the upper edge of the olecranon fossa at saggital view. Each measurement was repeated 3 times and the average value was chosen for analysis.
Trabecular bone volume, trabecular thickness, number of nodes, internodal distance, and width of trabeculae For trabecular bone-volume measurement, 1) the distal section was divided into 5 areas: lateral condyle anterior (LA), lateral condyle posterior (LP), medial condyle anterior (MA), medial condyle posterior (MP), and central (C); 2) the mid section was divided into lateral column (L) and medial column (M); and 3) the proximal section was further divided into lateral (L) representing lateral column, medial (M) representing medial column, and central area (C).
Cortical thickness As thresholds significantly affect the results of the cortical BMD, we used 1,200 mg/ml for accurate determination of cortical thickness following the guidelines of Ward et al.20 Cortical thickness was measured at all 3 sections. At each axial image, cortical thickness was measured at 8 different areas and the mean values analyzed: 12:00 (A ¼ anterior), 1:30 (MA ¼ medial anterior), 3:00 (M ¼ medial), 4:30 (MP ¼ medial posterior), 6:00 (P ¼ post), 7:30 (LP ¼ lateral posterior), 9:00 (L ¼ lateral), and 10:30 (LA ¼ lateral anterior area) based on the clock plate.
Statistical analysis All demographical characteristics were summarized as means and standard deviations for continuous data, frequency, and percentage for discrete data. Repeated measures 1 factor analysis was used to determine the regional differences in the proximal, middle, and distal section. For the comparison of 2 groups, Wilcoxon rank-sum test was used (younger and elder group). A cut-off P value of .05 was adopted for all statistical significance. All statistical analysis was performed using SPSS/PCþ for windows (version 14.0; SPSS Inc., Chicago, IL).
Results Trabecular parameters Trabecular bone volume Analysis of the trabecular bone volume (BV/TV) is demonstrated in Figure 3, A. In the most distal section (trans-epicondyle area), the mean trabecular bone volume was the greatest in the LA (mean SD ¼ 76.9 16.1), followed by the MP (62.8 222.3) and MA (58.6 21.5). It was measured the least in the LP (27.8 21.1). There were statistically significant differences (P < .05), as noted in Figure 3, A. In the mid section (trans-olecranon fossa area), trabecular bone volume in the medial column was greater than that of lateral (84.5 20.8 vs 69.0 21.6), which was statistically significant (P < .05). In the proximal section (supra-olecranon fossa area), trabecular bone volume in the lateral column was significantly greater followed by medial
246
Figure 1 fixation.
S.H. Park et al.
A 75-year-old lady presented with plate failure and screw pullout in the lateral condyle after open reduction and internal
Figure 2 Each distal humeri was examined at 3 different levels. A, Proximal section: supra-olecranon fossa line which transverses the upper edge of the olecranon fossa at saggital view. B, Mid section: trans-olecranon fossa line which transverses the center of olecranon fossa at saggital view. C, Distal section: trans-epicondylar line which transverses the center of the epicondyles at saggital view.
and central column. There were significant differences between the lateral and central columns (P < .05). Trabecular thickness Analysis of the trabecular thickness is shown in Figure 3, B. In the most distal section (trans-epicondyle area), trabecular thickness was the greatest in the LA, followed by the MP and MA, and the thinnest in the LP area (P < .05). In the mid (trans-olecranon fossa area) and proximal (supra-olecranon fossa area) sections, there was a thicker measurement in the lateral column than in the medial column, but there were no statistically significant differences (P > .05). Number of nodes Analysis of the number of nodes is presented in Figure 3, C. In the most distal section (trans-epicondyle area), the highest node number was noted in the MA area and the minimum in the LP area. There were significant differences
among the regions (P < .05). In the mid section (transolecranon fossa area), there were more nodes in the medial than the lateral column (P < .05), while it was similar in both columns in the proximal section (supra-olecranon fossa area) (P < .05) (Figure 3, C). Intertrabecular distance In the most distal section (trans-epicondyle area), distance between the trabeculae was at a minimum in the LA area and a maximum in the LP area (P < .05). In the mid (transolecranon fossa area) and proximal (supra-olecranon fossa area) sections, the measured distance was wider in the lateral column compared to the medial column (Figure 3, D). Internodal distance In the most distal section (trans-epicondyle area), the distance between the nodes was minimal in the MP area and maximal in the LP area. There were significant
3-Dimensional osseous micro-architecture of the distal humerus
247
Figure 3 Comparison of trabecular parameters for each region of interest in the distal humerus. A, Trabecular bone volume/tissue volume (Bv/Tv). B, Trabecular thickness. C, Node number. D, Intertrabecular distance. E, Internodal distance. Prox, proximal section (supraolecranon fossa area); Mid, mid section (trans-olecranon fossa section); Dist, distal section (trans-epicondylar section); M, medial; C, central; Lat, lateral; MA, medial/anterior; MP, medial/posterior; LA, lateral/anterior; LP, lateral/posterior. In the proximal and mid sections; ), signifies a difference among regions with respect to lateral as contrast group. In the distal section, ) signifies a difference among regions with respect to lateral/post as contrast group. All data reported as mean (standard deviation), results of repeated measures 1 factor analysis, )P < .05.
differences among the regions (P < .05). In the mid- (transolecranon fossa area) and proximal (supra-olecranon fossa area) sections, internodal distance was not significantly different among the regions (P > .05) (Figure 3, E).
was the greatest in the anterolateral aspect and thinnest in the anterior aspect. In the proximal section (supra-olecranon fossa area), it was thicker in the posterior medial aspect followed by the anterior lateral aspect, and thinnest in the lateral aspect (P < .05).
Cortical thickness Comparison of the 2 groups according to the age Analysis of the cortical thickness is demonstrated in Table I. In the most distal section (trans-epicondyle area), cortical thickness was thickest in the posterior medial side and the thinnest in the anterior aspect. Additionally, there were significant differences among the regions (P < .05). In the mid section (trans-olecranon fossa area), cortical thickness
There were several changes in terms of trabecular bone pattern between the 2 groups of specimens (Figure 4). In the younger group, the distal section indicated a greater value of Bv/Tv in the LA area, followed by the MP area with the minimum found in the LP area. In the elderly
248 Table I
S.H. Park et al. Comparison of cortical thickness for each region of the distal humerus
Cortical A thickness
MA
M
MP
P
LP
L
LA
F-value [p-value]
Proximal 2.02 (1.16)y,z 3.56 (0.65)y,z 3.69 (1.28)y 3.75 (0.92)y,z 3.64 (1.06)y 3.11 (0.77)y 1.14 (0.87)z 3.66 (0.76)y,z 22.05 [.00)] Mid 0.97 (0.58)z 3.09 (1.04)y 1.40 (0.89)z 2.57 (0.85)y 1.00 (0.58)z 3.01 (1.35)y 1.26 (1.04)z 3.57 (1.06)y 24.47 [.00)] Distal 1.97 (1.32)z 3.02 (1.40) 3.53 (1.56)y 3.76 (1.46)y 3.09 (1.03) 3.10 (1.02) 2.64 (1.12) 3.44 (1.30) y 4.20 [.00)] Parametric data reported as mean (standard deviation), results of repeated measures 1 factor analysis. ) Significant difference <.05 y Difference among position with respect to contrast group, lateral. z Difference among position with respect to contrast group, lateral post.
Figure 4 Comparison of trabecular parameters for each region in the distal humerus between two age groups. A, Trabecular bone volume/tissue volume (Bv/Tv). B, Trabecular thickness. C, Node number. D, Intertrabecular distance. E, Internodal distance. Prox, proximal section (supra-olecranon fossa area); Mid, mid section (trans-olecranon fossa section); Dist, distal section (trans-epicondylar section); M, medial; C, central; Lat, lateral; MA, medial/anterior; MP, medial/posterior; LA, lateral/anterior; LP, lateral/posterior. All data reported as mean (standard deviation), results of Wilcoxon rank sum test for comparison of 2 groups; age <60 and age 60, )P < .05.
group, it was the greatest in the LA area; however, there was a significant decrease of trabecular bone volume in the LP area. In the mid and proximal sections, Bv/Tv in the lateral column decreased significantly in the elderly group
(Figure 4, A). Overall, the trabecular thickness was greater in the younger group than in the elderly, especially at the MA, MP area (P < .05). In the proximal section, the decrease was more obvious in the lateral column compared
249
0.95 (0.97) 1.38 (0.72) 49.50 (0.17) 1.34 (1.24) 1.15 (0.80) 44.50 (0.95) 2.36 (1.09) 3.00 (1.13) 52.50 (0.33) 3.40 (0.65) 2.72 (0.79) 34.00 (0.15) 3.40 (1.50) 2.50 (1.03) 35.50 (0.22) 3.48 (0.96) 2.60 (0.93) 34.50 (0.17) 3.69 (1.08) 3.57 (1.14) 45.00 (1.00) 0.89 (0.65) 1.15 (0.48) 55.50 (0.56) 3.61 (0.67) 2.40 (1.05) 28.50 (0.03)) 4.13 (0.68) 3.25 (1.03) 34.50 (0.17) 2.74 (0.72) 2.35 (1.03) 37.50 (0.33) 4.09 (1.79) 3.33 (0.81) 36.00 (0.25) 1.65 (0.83) 2.52 (1.42) 52.50 (0.33) 0.94 (0.66) 1.02 (0.51) 43.00 (0.80) 2.10 (1.03) 2.50 (1.25) 34.50 (0.47) Distal
Mid
Younger group Elderly group Wilcoxon rank sum test Younger group Elderly group Wilcoxon rank sum test Younger group Elderly group Wilcoxon rank sum test
Mean (SD) Mean (SD) W (P value) Mean (SD) Mean (SD) W (P value) Mean (SD) Mean (SD) W (P value) Proximal
Parametric data reported as mean (standard deviation), results of Wilcoxon rank sum test ) Significant difference <.05
3.74 (1.12) 3.63 (1.59) 43.50 (0.85) 1.65 (1.04) 1.07 (0.57) 35.00 (0.20) 3.49 (1.46) 3.58 (1.84) 44.50 (0.95)
P MP M MA A Parameters
Comparison of cortical thickness for each region of the distal humerus between 2 groups Table II
Loosening of implants and screw pullout can lead to serious complications after surgical reconstruction of distal humeral fractures, especially in the elderly, with more osteoporotic bone. Despite the clinical significance of bone quality in relation to fracture treatment outcome,6, 15 few studies have investigated the histomorphometric parameters of the distal humerus. Previous studies have quantified the morphological and mechanical property of cancellous bone at various sites with a primary focus on the hip12, 19 and spine,2, 5 while some studies have analyzed the histomorphometry of the proximal humerus for better understanding of fracture fixation and rotator cuff repair.9, 16, 17 To our knowledge, this is the first investigation of 3-D regional variations of histomorphometric parameters in the distal humerus. Unlike DXA, a major advantage of QCT over other techniques is its ability to isolate and measure trabecular bone separately from cortical bone.4 High-resolution multislice CT and micro-CT are useful tools for the assessment of bone micro-architecture.2,3 Trabecular bone volume in the distal condyle was at its greatest in the anterior half of the lateral condyle and was lowest in the posterior half of the lateral condyle. This observation has clinical implications for surgical treatment of distal humerus fracture, as placing screws or plates in this region may give a higher risk of implant loosening resulting in fracture re-displacement. Previous studies of the proximal humerus showed that trabecular BMD using 3-D pQCT has a greater impact on pullout strength of the screw or suture anchor than cortical BMD.17,18 Bone loss is one of the most important factors of fractures and treatment among the elderly. The strength of a bone is closely associated with the bone mass and architectural structure. We divided the specimens into 2 groups based on the fact that hip fracture risk rises 100- to 1000-fold after 60 years of age.11 Age-related change in cortical thickness was significant in the posterior aspect of the distal section. Studies on the femoral neck also demonstrated age-related microscopic structural and mineral changes around the femoral neck cortex, indicating the location of osteopenic differences in the elderly.1 A decrease in cortical thickness with aging was less obvious in the anterior and medial side than the posterior side in this
LP
Discussion
3.69 (0.60) 3.38 (0.72) 38.50 (0.40) 3.13 (1.12) 3.03 (1.03) 45.00 (1.00) 3.24 (1.41) 2.73 (1.47) 41.00 (0.60)
L
LA
to the medial column (P < .05) (Figure 4, B). With aging, the number of nodes decreased in all areas; the MP, LA of the distal section (Figure 4, C). When both groups were compared, the intertrabecular and internodal distances were wider in the elderly group (P < .05) (Figure 4, D, E). Differences in the cortical thickness in both groups showed that in the distal section, the posterior aspect became thinner (P < .05); however, no statistically significant decrease was noted in other areas (Table II).
3.78 (0.81) 3.50 (0.72) 39.00 (0.44) 3.65 (1.12) 3.47 (1.06) 42.50 (0.75) 3.46 (1.39) 3.42 (1.30) 59.50 (0.95)
3-Dimensional osseous micro-architecture of the distal humerus
250 study. The LP area of the distal section showed the least number of nodes, the thinnest trabecular thickness, and the widest intertrabecular distance when compared to other areas. According to finite element modeling, reductions in trabecular number have a 2- to 5-fold greater impact on bone strength compared with reductions in trabecular thickness despite similar decreases in bone volume.13 The limitation of this study is the small number of specimens and no comparative biomechanical analysis. Furthermore, large population-based studies using other imaging techniques to assess bone microstructure, such as MRI,10 should be done to independently test the findings from the 3-D pQCT technology.
Conclusion This study evaluated the differences in cortical and trabecular bone parameters in each region of the distal humerus. With aging, the cortices became thinner especially in the posterior and posterolateral side of the distal condyle. These findings suggest micro-architecture of the bone in the posterolateral area of the lateral condyle is weaker, especially in the elderly, which may lead to mechanical failure, loosening of the screws, or fracture re-displacement; therefore, positioning the plates on both ridges of the distal humerus could have an advantage compared to posterolateral plating. However, to delineate the mechanism of healing and failure in this anatomic area, further biomechanical and clinical studies are required.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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