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Correlation between mineralization and mechanical strength of the subchondral bone plate of the humeral head
J Shoulder Elbow Surg (2012) 21, 887-893
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Correlation between mineralization and mechanical strength of the subchondral bone plate of the humeral head Valentin Zumstein, BMeda,*, Marko Kraljevic, BMeda, Dieter Wirz, MDb, €gli, MDc, Magdalena Mu €ller-Gerbl, MDa Rolf Hu a
Anatomical Institute, University of Basel, Basel, Switzerland Laboratory of Biomechanics and Biocalorimetry, University of Basel, Basel, Switzerland c Institute for Radiology and Nuclear Medicine, Bruderholz, Switzerland b
Background: One of the main problems in shoulder arthroplasty is the fixation of the prosthesis, where the subchondral bone plate plays an important role. Subchondral mineralization patterns represent the loading history of a joint and give information about the individual biomechanical situation. The objective of this study was to determine if a correlation between subchondral mineralization and mechanical strength in the humeral head exists. Materials and methods: Subchondral mineralization of 32 shoulder specimens was investigated by use of computed tomography (CT) osteoabsorptiometry. The previously dissected specimens were scanned axially in a CT scanner, and the obtained data sets were transferred into an image analyzing system. Maximum intensity projection was used to evaluate the density distribution of the subchondral bone plate. To get information about mechanical strength of the subchondral bone, each specimen was investigated at 29 predefined points by means of an indentation-testing machine. Results: The maximum strength was mostly detected in the center (monocentric pattern) or in anterior and posterior areas of the articular surface (bicentric pattern). The distribution of mineralization showed the same 2 reproducible patterns. The coefficient of correlation between mechanical strength and mineralization shown on CT was between 0.59 and 0.96. The obtained information was statistically significant (P < .01). Conclusion: Mechanical strength and subchondral mineralization in the humeral head are significantly associated (P < .01). As a consequence of these findings, CT osteoabsorptiometry can be indirectly used to give information about bone quality in vivo. Our findings could be useful for the development of new fixation methods in shoulder surgery (eg, humeral resurfacing arthroplasty). Level of evidence: Basic Science Study, Anatomic Study, Imaging. Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Mineralization; indentation; subchondral bone; humeral head; glenohumeral joint; shoulder arthroplasty
Investigational Review Board approval was not required for this basic science study.
*Reprint requests: Valentin Zumstein, BMed, Anatomical Institute, University of Basel, Pestalozzistrasse 20, 4056 Basel, Switzerland. E-mail address: [email protected] (V. Zumstein).
1058-2746/$ - see front matter Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2011.05.018
888 The subchondral bone plate plays an important role in the fixation of orthopedic implants. The loading history of a joint is represented by specific mineralization distribution patterns of the subchondral bone.18 Important factors of influence on the mineralization of the subchondral bone plate are age,19 geometry of the articular surface, and shape of a joint.3,29 Because long-term stress affects not only the subchondral bone but also the subarticular bone,14 we assume that the mineralization patterns of the subchondral bone plate continue in the underlying cancellous bone. A current study at our institute indicates a high correlation between the density values of the subchondral bone and the subarticular spongiosa. From the clinical point of view, knowing the subchondral bone density might be interesting for osteosynthesis, because this is the only solid bone where screws are to be put in case of open reduction and internal fixation. It is also necessary in case of resurfacing to get an optimal fixation of the prosthesis. Several authors have underlined the importance of subchondral bone for optimal screw positioning.6,12 Computed tomography osteoabsorptiometry (CT-OAM) can be used to gain information about subchondral bone mineralization patterns in vivo.18 In contrast to the usual methods of CT densitometry, which deal with the calculation of an absolute value for bone density, CT-OAM is a procedure for demonstrating differences in relative concentration within a joint surface.18 The correlation between the mineralization distribution patterns and mechanical strength of the subchondral bone plate is not yet sufficiently proven.17 If there were correlations at a high level between these parameters, predictions concerning bone quality could be made through CT-OAM in vivo. Several authors16,25,26 investigated the mechanical and architectural properties of the glenoid cavity and found interesting results. Schulz et al25,26 found a predominance of bicentric mineralization patterns and in rare cases a central maximum. Mimar et al16 showed that larger values of bone value fraction (BV/TV) are generally found in the posterior margins of the glenoid, whereas the anteroinferior edge was more porous. Because the subchondral mineralization and mechanical strength of the humeral head has not been investigated so far, to our knowledge, we focused our attention on the humeral head to provide information about mechanical properties that might be used for developing new fixation methods in shoulder surgery. Our hypotheses were that (1) we would find similar mineralization patterns in the humeral head as others have found in the glenoid (particularly bicentric and monocentric) and (2) a correlation exists between distribution patterns of mineral density and strength of the same anatomic specimen.
V. Zumstein et al. course at our university that were a mean age of 80.5 years (range, 59-95 years), and 11 additional specimens of unknown sex and age. All specimens were fixed in formalin. The specimens consisted of the scapula, the clavicula, the proximal humerus and the surrounding tissue. In a first step, specimens were dissected free of soft tissue, the joint capsule was opened, and the glenohumeral joint was disarticulated. All specimens were macroscopically examined, and shoulders with obvious signs of degeneration or traumatic findings were excluded.
CT-OAM analysis For the CT-OAM analysis,18 the shoulder joints were scanned in a GE Lightspeed 16 X-ray CT scanner (General Electric Healthcare Corp, Waukesha, WI, USA). The data sets were axially cut to a thickness of 0.6 mm and transferred into an ANALYZE 7.5.5. image analyzing system (Mayo Foundation, Rochester, MN, USA). In a first step, a 3-dimensional (3D) reconstruction of the humeral head was made and saved in such a way that a frontal view on the joint surface was achieved. Then, the subchondral bone plate of each slice was edited manually and reconstructed in 3D in the same way as the humeral head. The density distribution of the subchondral plate was evaluated by using a maximum intensity projection. For better visualization, steps of 100 Hounsfield units (HU) were assigned to false colors. High density values (>1200 HU) were typified black, followed by red, orange, yellow and green, with very low-density values (<200 HU) as blue. To get a finished densitogram, the reconstructed humeral heads were superimposed by the false color images (Fig. 1). To quantify the distribution pattern, a standardized template (21 21 units) was projected onto the humeral head; then, the coordinates of the mineralization maxima within the template were determined and noted in a summation chart.
Indentation testing For standardized and reproducible indentation testing, the position of the humeral head is of prime importance. Each humeral head was measured and divided into a standardized grid with 29 exactly defined measuring points. The distance between two points had to be between 7 and 10 mm (Fig. 2). Then, the humeral head was fixed into bone cement, rotated on a lockable ball joint, and visually adjusted so that the point to be measured was perpendicular to the needle of the test machine. A mechanical test machine (Synergie 100, MTS Systems, Eden Prairie, MN, USA) was used for all tests. For indentation testing, a steel needle, with a 1.3-mm diameter, created, with a vertical speed of 1 mm/sec, a standardized hole with a depth of 7 mm. On the basis of the work of Aitken et al,1 Saitoh et al,24 and Hofmann et al,13 we recorded all forces as well as the maximum force for every measuring point in Newtons (N). The force maximum was noted for every measuring point and recorded in a standardized grid system (21 21 units) with its corresponding coordinates.
Density-strength correlation
Materials and methods This study included 32 shoulder specimens from deceased donors, comprising 21 (8 men, 12 women, 1 unknown) from the dissecting
To find out if correlation between densitograms and indentation testing exists, we established for each indentation measuring point the corresponding density value in HU. Each measuring point was checked using the image analyzing system. To identify the exact
Humeral head mineralization and strength
889
Figure 1 The density distribution of the (A) humeral head subchondral plate was evaluated by using a (B) maximum intensity projection and visualized with different colors.
Figure 2 (A) The subchondral bone plate was indentated 29 times using a steel needle with 1.3 mm diameter and then evaluated using (B) maximum intensity projection measuring point, we used the same grid as for indentation testing and the surface measured was the same (5.5 mm2).
Statistical analysis Linear regression was used to evaluate statistical correlations. For all measured specimens, the Pearson product-moment correlation coefficient and the determination coefficient were applied. We used Steiger’s Z test to check if a significant correlation existed between the manifestations of the sample characteristics (n ¼ 29).
Results
maximum density of each specimen into a summary chart, two different distribution patterns occurred: 24 humeral heads had a bicentric pattern with anterior and posterior maxima and 8 showed a monocentric pattern with a large maximum in the center of the articular surface (Fig. 3 and Fig. 4). We did not find a statistically significant difference in the average age between monocentric and bicentric humeral heads: the mean age was 76 years for the bicentric humeral heads and 82 for the monocentric humeral heads. Of the 8 monocentric humeral heads, 4 were female, 2 were male, and 2 were unknown. The density maxima showed an interindividual range between 490 and 950 HU.
Subchondral mineralization
Strength distribution
The evaluation of the CT-OAM images showed areas of high density and areas of low density. After having filled in the
The results of the subchondral mineralization testing showed strength was not distributed homogenously. Indentation testing
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V. Zumstein et al.
Figure 3
Bicentric mineralization distribution by computed tomography osteoabsorptiometry is shown for 24 humeral heads.
Figure 4
Eight specimens were categorized as having monocentric mineralization patterns.
revealed the same 2 reproducible patterns as the CT-OAM did (Fig. 5). The maximum strength was mostly detected in the center (monocentric) or in anterior and posterior areas of the articular surface (bicentric). We recorded significant interindividual differences between absolute density values. The median force needed to indent the hole was 175 N, but there was great interindividual range of 10 to 930 N (25%-75% interquartile range, 137-236 N).
Density-strength correlation Avisual comparison of mineralization and strength distribution confirmed correlation in all articular surfaces (Fig. 6). We showed a linear dependence exists between density and strength values. The coefficient of correlation was between 0.59 and 0.96, and the coefficient of determination (R2) was
between 0.35 and 0.93 (Table I). For a 99% confidence interval, the obtained information was statistically relevant (Fig. 7).
Discussion Joint instability and glenoid loosening, which are among the most common postoperative complications15,27,30,32 in shoulder arthroplasty, are often caused by eccentric loading of the glenoid due to a malcentered humeral head.7,9,11,33 This underlines the importance of a preoperative identification of such malcentered cases to fix these problems already intraoperatively and prevent postoperative complications. Some authors have stated that posterior glenoid bone loss can cause posterior humeral head translation, which is important for preoperative planning of shoulder arthroplasty.2
Humeral head mineralization and strength
Figure 5
891
A bicentric strength distribution was shown for 24 humeral heads, and 8 specimens were categorized as monocentric.
Figure 6
(Left) Distribution of mineral density and (Right) distribution of strength are shown for the same specimen.
A method for preoperative identification could be the evaluation of the mineralization of the subchondral bone plate because it can be used as a marker for long-term stress distribution in diarthrodial joints.5,18 Some authors have mentioned the effect of poor bone quality on the results of shoulder arthroplasty and pointed out that bone quality is an important factor in glenoid loosening.23 Ding et al8 used micro CT to show that decreased mechanical properties of subchondral cancellous bone in osteoarthritis indicates poor bone quality. Many authors have described that the mineralization pattern of the subchondral bone plate, as well as the absolute degree of mineralization, depend on the shape, geometry, age, side, and the individual functional demand of a joint.3,10,19,22,29 Studies of patients with glenohumeral arthritis showed that pathologic conditions may alter subchondral bone mineralization. A cuff arthropathy, for example, leads to a fixed decentering of the glenohumeral position to superior, which can be seen in superiorly decentered mineralization patterns.32 A reproducible and highly sensitive method to determine subchondral bone mineralization is CT-OAM.18,21 In contrast to the usual methods of CT densitometry, which show an absolute value for the calculation for bone density, CT-OAM is able to demonstrate differences in relative concentration within a joint surface.18
Because we used formalin-fixed specimens, it is important to know whether fixing in formalin affects mineralization and strength. Previous studies pointed out that formalin-fixed specimens did not show any statistical differences in strength and bone mineral density compared with fresh specimens.4,31 We found two different distribution patterns: 24 of our 32 specimens were classified as bicentric, with an anterior and posterior maximum of subchondral mineralization. Several studies showed that these findings can be explained by the physiologic mismatch of the glenohumeral joint as a principle of physiologic stress distribution to prevent osteoarthritis.3,18,19,21,29 In this context, Soslowsky et al28 described the importance of the articular cartilage for glenohumeral congruity. A consecutive swelling of the articular cartilage after periods of high loading increases incongruity and serves as an important stimulus to keep cartilage healthy. Soslowsky et al demonstrated that the humeral head shows tendencies to a bigger radius of the ball than the socket, which underlines the concept of a physiologic mismatch for the glenohumeral joint. Eight densitograms showed a monocentric pattern with a centrally accentuated density distribution. According to several studies,19,20 these findings can be explained with a loss of incongruity with increasing age. Another explanation for these monocentric mineralization patterns could be the preponderance of several muscles (infraspinatus
892 Table I Spec 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
V. Zumstein et al. Clinical and statistical data of the specimens Age Sex Side Corr) Dety 86 86 76 76 95 95 75 75 84 84 59 59 74 74 92 87 87 88 88 70 . . . . . . . . . . . .
F F M M F F M M F F F F M M F M M F F F . . . . . . . . . . . .
Right Left Right Left Right Left Right Left Right Left Right Left Right Left Left Right Left Right Left Right Right Left Right Right Left Left Left Right Left Right Right Left
0.59 0.76 0.87 0.92 0.9 0.94 0.91 0.96 0.89 0.9 0.92 0.96 0.88 0.79 0.91 0.77 0.84 0.77 0.89 0.89 0.75 0.88 0.9 0.92 0.9 0.92 0.76 0.88 0.88 0.62 0.87 0.96
0.35 0.58 0.76 0.84 0.81 0.89 0.83 0.93 0.80 0.81 0.85 0.93 0.78 0.63 0.83 0.59 0.70 0.60 0.79 0.79 0.57 0.78 0.80 0.84 0.80 0.84 0.58 0.77 0.78 0.40 0.76 0.92
Spec, specimen. ) Pearson product-moment correlation coefficient. y Determination coefficient.
muscle and teres minor muscle) of the rotator cuff during internal rotation, as described by Schulz et al.26 This phenomenon leads to an anterior decentered humeral head, the posterior contact area no longer exists, and the anterior contact area shifts toward the center of the humeral head. This would explain the centrally accentuated density distribution we found. As expected, strength distribution was not homogenous as well. This became obvious as we filled in the obtained information in a summary chart and compared it with the results of the subchondral mineralization. The summary charts of strength maxima showed bicentric and monocentric distribution patterns that were similar to the mineralization summary charts. The force needed to penetrate areas of high density (red and yellow color in the densitograms) was significantly higher than in areas of lower density. Several authors demonstrated that long-term stress leads to specific patterns of mineralization in the subchondral bone plate.5,18 Our opinion is that long-term
Figure 7 Correlation between local strength and density on a single humeral head (n ¼ 29).
stress on the humeral head leads not only to characteristic subchondral mineralization patterns but also to an increased amount of absolute density in these areas. Because the long-term stress affects not only the subchondral bone but also the subarticular cancellous bone,14 we assume that the mineralization patterns of the subchondral bone plate are continuing in cancellous bone. An ongoing study at our institute indicates a high correlation between the density values of the subchondral bone and the subarticular spongiosa. From the clinical view point, knowing subchondral bone density might be interesting for osteosynthesis because this is the only solid bone where screws are placed during open reduction and internal fixation. It is also necessary in case of resurfacing to achieve an optimal fixation of the prosthesis. Several authors underlined the importance of subchondral bone for optimal screw positioning.6,12 If further studies can show that differences in mineralization are clinically reflective of regions that perform better or worse for anchor placement, our findings might also be useful for rotator cuff tendon repair. An interesting starting point for further studies could be how anchor systems for tendon repair should be placed to hit these regions of great mechanical strength without injuring the articular surface.
Conclusions Our findings show that CT-OAM can indirectly be used to give information about bone quality in vivo. This allows the noninvasive measurement of the mechanical quality of implant basis. Our results showed that the best bone quality in the humeral head is generally found in the anterior and posterior parts; in some rare cases, the central part displays a large maximum. We showed that mineralization and mechanical strength in the humeral head correlate on a high level (P < .01). These findings might be useful for the development of new fixation
Humeral head mineralization and strength methods in shoulder surgery, such as humeral resurfacing arthroplasty.
893
15. 16.
Disclaimer
17.
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.
18. 19.
20.
References 1. Aitken GK, Bourne RB, Finlay JB, Rorabeck CH, Andreae PR. Indentation stiffness of the cancellous bone in the distal human tibia. Clin Orthop Relat Res 1985:264-70. 2. Bryce CD, Davison AC, Okita N, Lewis GS, Sharkey NA, Armstrong AD. A biomechanical study of posterior glenoid bone loss and humeral head translation. J Shoulder Elbow Surg 2010;19:9941002. doi:10.1016/j.jse.2010.04.010 3. Bullough PG. The geometry of diarthrodial joints, its physiologic maintenance, and the possible significance of age-related changes in geometry-to-load distribution and the development of osteoarthritis. Clin Orthop Relat Res 1981:61-6. 4. Burkhart KJ, Nowak TE, Blum J, Kuhn S, Welker M, Sternstein W, et al. Influence of formalin fixation on the biomechanical properties of human diaphyseal bone. Biomed Tech (Berl) 2010;55:361-5. doi:10. 1515/BMT.2010.043 5. Carter DR, Fyhrie DP, Whalen RT. Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy. J Biomech 1987;20:785-94. 6. Chapman JR, Harrington RM, Lee KM, Anderson PA, Tencer AF, Kowalski D. Factors affecting the pullout strength of cancellous bone screws. J Biomech Eng 1996;118:391-8. 7. Collins D, Tencer A, Sidles J, Matsen F 3rd. Edge displacement and deformation of glenoid components in response to eccentric loading. The effect of preparation of the glenoid bone. J Bone Joint Surg Am 1992;74:501-7. 8. Ding M, Odgaard A, Hvid I. Changes in the three-dimensional microstructure of human tibial cancellous bone in early osteoarthritis. J Bone Joint Surg Br 2003;85:906-12. doi:10.1302/0301-620X.85B6.12595 9. Franklin JL, Barrett WP, Jackins SE, Matsen FA 3rd. Glenoid loosening in total shoulder arthroplasty. Association with rotator cuff deficiency. J Arthroplasty 1988;3:39-46. 10. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff’s law: the remodeling problem. Anat Rec 1990;226:414-22. 11. Gerber C, Costouros JG, Sukthankar A, Fucentese SF. Static posterior humeral head subluxation and total shoulder arthroplasty. J Shoulder Elbow Surg 2009;18:505-10. doi:10.1016/j.jse.2009.03.003 12. Gordon KD, Duck TR, King GJ, Johnson JA. Mechanical properties of subchondral cancellous bone of the radial head. J Orthop Trauma 2003;17:285-9. 13. Hofmann AA, Hammon DJ, Daniels AU. Compressive strength mapping of femoral head trabecular bone. J Rehabil Res Dev 1991;28:25-32. 14. Lim D, Seliktar R, Farrell E, Tom J, Nunes L, Sun W, et al. Loading conditions and bone formation in the GH region of the shoulder. Conf
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Proc IEEE Eng Med Biol Soc 2004;7:5092-5. doi:10.1109/IEMBS. 2004.1404407 Matsen FAr, Lippitt SB, Sidles JA, Harryman DTn. Practical evaluation and management of the shoulder. Philadelphia: Saunders W; 1994. Mimar R, Limb D, Hall RM. Evaluation of the mechanical and architectural properties of glenoid bone. J Shoulder Elbow Surg 2008; 17:336-41. doi:10.1016/j.jse.2007.07.024 Muhlhofer H, Ercan Y, Drews S, Matsuura M, Meissner J, Linsenmaier U, et al. Mineralisation and mechanical strength of the subchondral bone plate of the inferior tibial facies. Surg Radiol Anat 2009;31:237-43. doi:10.1007/s00276-008-0430-6 Muller-Gerbl M. The subchondral bone plate. Adv Anat Embryol Cell Biol 1998;141:III-XI. 1-134. Muller-Gerbl M, Putz R, Kenn R. [Distribution pattern of subchondral mineralization in the glenoid cavity in normal subjects, athletes and patients]. Z Orthop Ihre Grenzgeb 1993;131:10-3. Muller-Gerbl M, Putz R, Hodapp N, Schulte E, Wimmer B. [Demonstration of subchondral density pattern using CTosteoabsorptiometry (CT-OAM) for the assessment of individual joint stress in live patients]. Z Orthop Ihre Grenzgeb 1990;128:128-33. Muller-Gerbl M, Putz R, Hodapp N, Schulte E, Wimmer B. Computed tomography-osteoabsorptiometry for assessing the density distribution of subchondral bone as a measure of long-term mechanical adaptation in individual joints. Skeletal Radiol 1989;18:507-12. Oberlander W. [The stress of the human hip joint. V. The distribution of bone density in the human acetabulum (author’s transl)]. Z Anat Entwicklungsgesch 1973;140:367-84. Raiss P, Pape G, Kleinschmidt K, Jager S, Sowa B, Jakubowitz E, et al. Bone cement penetration pattern and primary stability testing in keeled and pegged glenoid components. J Shoulder Elbow Surg 2011; 20:723-31. doi:10.1016/j.jse.2010.09.006 Saitoh S, Nakaksuchi Y, Latta L, Milne E. Distribution of bone mineral density and bone strength of the proximal humerus. J Shoulder Elbow Surg 1994;3:234-42. Schulz CU, Anetzberger H, Pfahler M, Refior HJ, Muller-Gerbl M. Anterior shoulder instability modifies glenoid subchondral bone density. Clin Orthop Relat Res 2004:259-63. doi:10.1097/01.blo. 0000127117.90506.ac Schulz CU, Pfahler M, Anetzberger HM, Becker CR, Muller-Gerbl M, Refior HJ. The mineralization patterns at the subchondral bone plate of the glenoid cavity in healthy shoulders. J Shoulder Elbow Surg 2002; 11:174-81. doi:10.1067/mse.2002.121635 Skirving AP. Total shoulder arthroplasty e current problems and possible solutions. J Orthop Sci 1999;4:42-53. Soslowsky LJ, Flatow EL, Bigliani LU, Mow VC. Articular geometry of the glenohumeral joint. Clin Orthop Relat Res 1992:181-90. Tillmann B. [The stress of the human elbow joint. I. Functional morphology of the articular surfaces]. Z Anat Entwicklungsgesch 1971;134:328-42. Torchia ME, Cofield RH, Settergren CR. Total shoulder arthroplasty with the Neer prosthesis: long-term results. J Shoulder Elbow Surg 1997;6:495-505. van Haaren EH, van der Zwaard BC, van der Veen AJ, Heyligers IC, Wuisman PI, Smit TH. Effect of long-term preservation on the mechanical properties of cortical bone in goats. Acta Orthop 2008;79: 708-16. doi:10.1080/17453670810016759 von Eisenhart-Rothe R, Muller-Gerbl M, Wiedemann E, Englmeier KH, Graichen H. Functional malcentering of the humeral head and asymmetric long-term stress on the glenoid: potential reasons for glenoid loosening in total shoulder arthroplasty. J Shoulder Elbow Surg 2008;17:695-702. doi:10.1016/j.jse.2008.02.008 Walch G, Boulahia A, Boileau P, Kempf JF. Primary glenohumeral osteoarthritis: clinical and radiographic classification. The Aequalis Group. Acta Orthop Belg 1998;64(suppl 2):46-52.
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Correlation between mineralization and mechanical strength of the subchondral bone plate of the humeral head Valentin Zumstein, BMeda,*, Marko Kraljevic, BMeda, Dieter Wirz, MDb, €gli, MDc, Magdalena Mu €ller-Gerbl, MDa Rolf Hu a
Anatomical Institute, University of Basel, Basel, Switzerland Laboratory of Biomechanics and Biocalorimetry, University of Basel, Basel, Switzerland c Institute for Radiology and Nuclear Medicine, Bruderholz, Switzerland b
Background: One of the main problems in shoulder arthroplasty is the fixation of the prosthesis, where the subchondral bone plate plays an important role. Subchondral mineralization patterns represent the loading history of a joint and give information about the individual biomechanical situation. The objective of this study was to determine if a correlation between subchondral mineralization and mechanical strength in the humeral head exists. Materials and methods: Subchondral mineralization of 32 shoulder specimens was investigated by use of computed tomography (CT) osteoabsorptiometry. The previously dissected specimens were scanned axially in a CT scanner, and the obtained data sets were transferred into an image analyzing system. Maximum intensity projection was used to evaluate the density distribution of the subchondral bone plate. To get information about mechanical strength of the subchondral bone, each specimen was investigated at 29 predefined points by means of an indentation-testing machine. Results: The maximum strength was mostly detected in the center (monocentric pattern) or in anterior and posterior areas of the articular surface (bicentric pattern). The distribution of mineralization showed the same 2 reproducible patterns. The coefficient of correlation between mechanical strength and mineralization shown on CT was between 0.59 and 0.96. The obtained information was statistically significant (P < .01). Conclusion: Mechanical strength and subchondral mineralization in the humeral head are significantly associated (P < .01). As a consequence of these findings, CT osteoabsorptiometry can be indirectly used to give information about bone quality in vivo. Our findings could be useful for the development of new fixation methods in shoulder surgery (eg, humeral resurfacing arthroplasty). Level of evidence: Basic Science Study, Anatomic Study, Imaging. Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Mineralization; indentation; subchondral bone; humeral head; glenohumeral joint; shoulder arthroplasty
Investigational Review Board approval was not required for this basic science study.
*Reprint requests: Valentin Zumstein, BMed, Anatomical Institute, University of Basel, Pestalozzistrasse 20, 4056 Basel, Switzerland. E-mail address: [email protected] (V. Zumstein).
1058-2746/$ - see front matter Ó 2012 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2011.05.018
888 The subchondral bone plate plays an important role in the fixation of orthopedic implants. The loading history of a joint is represented by specific mineralization distribution patterns of the subchondral bone.18 Important factors of influence on the mineralization of the subchondral bone plate are age,19 geometry of the articular surface, and shape of a joint.3,29 Because long-term stress affects not only the subchondral bone but also the subarticular bone,14 we assume that the mineralization patterns of the subchondral bone plate continue in the underlying cancellous bone. A current study at our institute indicates a high correlation between the density values of the subchondral bone and the subarticular spongiosa. From the clinical point of view, knowing the subchondral bone density might be interesting for osteosynthesis, because this is the only solid bone where screws are to be put in case of open reduction and internal fixation. It is also necessary in case of resurfacing to get an optimal fixation of the prosthesis. Several authors have underlined the importance of subchondral bone for optimal screw positioning.6,12 Computed tomography osteoabsorptiometry (CT-OAM) can be used to gain information about subchondral bone mineralization patterns in vivo.18 In contrast to the usual methods of CT densitometry, which deal with the calculation of an absolute value for bone density, CT-OAM is a procedure for demonstrating differences in relative concentration within a joint surface.18 The correlation between the mineralization distribution patterns and mechanical strength of the subchondral bone plate is not yet sufficiently proven.17 If there were correlations at a high level between these parameters, predictions concerning bone quality could be made through CT-OAM in vivo. Several authors16,25,26 investigated the mechanical and architectural properties of the glenoid cavity and found interesting results. Schulz et al25,26 found a predominance of bicentric mineralization patterns and in rare cases a central maximum. Mimar et al16 showed that larger values of bone value fraction (BV/TV) are generally found in the posterior margins of the glenoid, whereas the anteroinferior edge was more porous. Because the subchondral mineralization and mechanical strength of the humeral head has not been investigated so far, to our knowledge, we focused our attention on the humeral head to provide information about mechanical properties that might be used for developing new fixation methods in shoulder surgery. Our hypotheses were that (1) we would find similar mineralization patterns in the humeral head as others have found in the glenoid (particularly bicentric and monocentric) and (2) a correlation exists between distribution patterns of mineral density and strength of the same anatomic specimen.
V. Zumstein et al. course at our university that were a mean age of 80.5 years (range, 59-95 years), and 11 additional specimens of unknown sex and age. All specimens were fixed in formalin. The specimens consisted of the scapula, the clavicula, the proximal humerus and the surrounding tissue. In a first step, specimens were dissected free of soft tissue, the joint capsule was opened, and the glenohumeral joint was disarticulated. All specimens were macroscopically examined, and shoulders with obvious signs of degeneration or traumatic findings were excluded.
CT-OAM analysis For the CT-OAM analysis,18 the shoulder joints were scanned in a GE Lightspeed 16 X-ray CT scanner (General Electric Healthcare Corp, Waukesha, WI, USA). The data sets were axially cut to a thickness of 0.6 mm and transferred into an ANALYZE 7.5.5. image analyzing system (Mayo Foundation, Rochester, MN, USA). In a first step, a 3-dimensional (3D) reconstruction of the humeral head was made and saved in such a way that a frontal view on the joint surface was achieved. Then, the subchondral bone plate of each slice was edited manually and reconstructed in 3D in the same way as the humeral head. The density distribution of the subchondral plate was evaluated by using a maximum intensity projection. For better visualization, steps of 100 Hounsfield units (HU) were assigned to false colors. High density values (>1200 HU) were typified black, followed by red, orange, yellow and green, with very low-density values (<200 HU) as blue. To get a finished densitogram, the reconstructed humeral heads were superimposed by the false color images (Fig. 1). To quantify the distribution pattern, a standardized template (21 21 units) was projected onto the humeral head; then, the coordinates of the mineralization maxima within the template were determined and noted in a summation chart.
Indentation testing For standardized and reproducible indentation testing, the position of the humeral head is of prime importance. Each humeral head was measured and divided into a standardized grid with 29 exactly defined measuring points. The distance between two points had to be between 7 and 10 mm (Fig. 2). Then, the humeral head was fixed into bone cement, rotated on a lockable ball joint, and visually adjusted so that the point to be measured was perpendicular to the needle of the test machine. A mechanical test machine (Synergie 100, MTS Systems, Eden Prairie, MN, USA) was used for all tests. For indentation testing, a steel needle, with a 1.3-mm diameter, created, with a vertical speed of 1 mm/sec, a standardized hole with a depth of 7 mm. On the basis of the work of Aitken et al,1 Saitoh et al,24 and Hofmann et al,13 we recorded all forces as well as the maximum force for every measuring point in Newtons (N). The force maximum was noted for every measuring point and recorded in a standardized grid system (21 21 units) with its corresponding coordinates.
Density-strength correlation
Materials and methods This study included 32 shoulder specimens from deceased donors, comprising 21 (8 men, 12 women, 1 unknown) from the dissecting
To find out if correlation between densitograms and indentation testing exists, we established for each indentation measuring point the corresponding density value in HU. Each measuring point was checked using the image analyzing system. To identify the exact
Humeral head mineralization and strength
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Figure 1 The density distribution of the (A) humeral head subchondral plate was evaluated by using a (B) maximum intensity projection and visualized with different colors.
Figure 2 (A) The subchondral bone plate was indentated 29 times using a steel needle with 1.3 mm diameter and then evaluated using (B) maximum intensity projection measuring point, we used the same grid as for indentation testing and the surface measured was the same (5.5 mm2).
Statistical analysis Linear regression was used to evaluate statistical correlations. For all measured specimens, the Pearson product-moment correlation coefficient and the determination coefficient were applied. We used Steiger’s Z test to check if a significant correlation existed between the manifestations of the sample characteristics (n ¼ 29).
Results
maximum density of each specimen into a summary chart, two different distribution patterns occurred: 24 humeral heads had a bicentric pattern with anterior and posterior maxima and 8 showed a monocentric pattern with a large maximum in the center of the articular surface (Fig. 3 and Fig. 4). We did not find a statistically significant difference in the average age between monocentric and bicentric humeral heads: the mean age was 76 years for the bicentric humeral heads and 82 for the monocentric humeral heads. Of the 8 monocentric humeral heads, 4 were female, 2 were male, and 2 were unknown. The density maxima showed an interindividual range between 490 and 950 HU.
Subchondral mineralization
Strength distribution
The evaluation of the CT-OAM images showed areas of high density and areas of low density. After having filled in the
The results of the subchondral mineralization testing showed strength was not distributed homogenously. Indentation testing
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V. Zumstein et al.
Figure 3
Bicentric mineralization distribution by computed tomography osteoabsorptiometry is shown for 24 humeral heads.
Figure 4
Eight specimens were categorized as having monocentric mineralization patterns.
revealed the same 2 reproducible patterns as the CT-OAM did (Fig. 5). The maximum strength was mostly detected in the center (monocentric) or in anterior and posterior areas of the articular surface (bicentric). We recorded significant interindividual differences between absolute density values. The median force needed to indent the hole was 175 N, but there was great interindividual range of 10 to 930 N (25%-75% interquartile range, 137-236 N).
Density-strength correlation Avisual comparison of mineralization and strength distribution confirmed correlation in all articular surfaces (Fig. 6). We showed a linear dependence exists between density and strength values. The coefficient of correlation was between 0.59 and 0.96, and the coefficient of determination (R2) was
between 0.35 and 0.93 (Table I). For a 99% confidence interval, the obtained information was statistically relevant (Fig. 7).
Discussion Joint instability and glenoid loosening, which are among the most common postoperative complications15,27,30,32 in shoulder arthroplasty, are often caused by eccentric loading of the glenoid due to a malcentered humeral head.7,9,11,33 This underlines the importance of a preoperative identification of such malcentered cases to fix these problems already intraoperatively and prevent postoperative complications. Some authors have stated that posterior glenoid bone loss can cause posterior humeral head translation, which is important for preoperative planning of shoulder arthroplasty.2
Humeral head mineralization and strength
Figure 5
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A bicentric strength distribution was shown for 24 humeral heads, and 8 specimens were categorized as monocentric.
Figure 6
(Left) Distribution of mineral density and (Right) distribution of strength are shown for the same specimen.
A method for preoperative identification could be the evaluation of the mineralization of the subchondral bone plate because it can be used as a marker for long-term stress distribution in diarthrodial joints.5,18 Some authors have mentioned the effect of poor bone quality on the results of shoulder arthroplasty and pointed out that bone quality is an important factor in glenoid loosening.23 Ding et al8 used micro CT to show that decreased mechanical properties of subchondral cancellous bone in osteoarthritis indicates poor bone quality. Many authors have described that the mineralization pattern of the subchondral bone plate, as well as the absolute degree of mineralization, depend on the shape, geometry, age, side, and the individual functional demand of a joint.3,10,19,22,29 Studies of patients with glenohumeral arthritis showed that pathologic conditions may alter subchondral bone mineralization. A cuff arthropathy, for example, leads to a fixed decentering of the glenohumeral position to superior, which can be seen in superiorly decentered mineralization patterns.32 A reproducible and highly sensitive method to determine subchondral bone mineralization is CT-OAM.18,21 In contrast to the usual methods of CT densitometry, which show an absolute value for the calculation for bone density, CT-OAM is able to demonstrate differences in relative concentration within a joint surface.18
Because we used formalin-fixed specimens, it is important to know whether fixing in formalin affects mineralization and strength. Previous studies pointed out that formalin-fixed specimens did not show any statistical differences in strength and bone mineral density compared with fresh specimens.4,31 We found two different distribution patterns: 24 of our 32 specimens were classified as bicentric, with an anterior and posterior maximum of subchondral mineralization. Several studies showed that these findings can be explained by the physiologic mismatch of the glenohumeral joint as a principle of physiologic stress distribution to prevent osteoarthritis.3,18,19,21,29 In this context, Soslowsky et al28 described the importance of the articular cartilage for glenohumeral congruity. A consecutive swelling of the articular cartilage after periods of high loading increases incongruity and serves as an important stimulus to keep cartilage healthy. Soslowsky et al demonstrated that the humeral head shows tendencies to a bigger radius of the ball than the socket, which underlines the concept of a physiologic mismatch for the glenohumeral joint. Eight densitograms showed a monocentric pattern with a centrally accentuated density distribution. According to several studies,19,20 these findings can be explained with a loss of incongruity with increasing age. Another explanation for these monocentric mineralization patterns could be the preponderance of several muscles (infraspinatus
892 Table I Spec 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
V. Zumstein et al. Clinical and statistical data of the specimens Age Sex Side Corr) Dety 86 86 76 76 95 95 75 75 84 84 59 59 74 74 92 87 87 88 88 70 . . . . . . . . . . . .
F F M M F F M M F F F F M M F M M F F F . . . . . . . . . . . .
Right Left Right Left Right Left Right Left Right Left Right Left Right Left Left Right Left Right Left Right Right Left Right Right Left Left Left Right Left Right Right Left
0.59 0.76 0.87 0.92 0.9 0.94 0.91 0.96 0.89 0.9 0.92 0.96 0.88 0.79 0.91 0.77 0.84 0.77 0.89 0.89 0.75 0.88 0.9 0.92 0.9 0.92 0.76 0.88 0.88 0.62 0.87 0.96
0.35 0.58 0.76 0.84 0.81 0.89 0.83 0.93 0.80 0.81 0.85 0.93 0.78 0.63 0.83 0.59 0.70 0.60 0.79 0.79 0.57 0.78 0.80 0.84 0.80 0.84 0.58 0.77 0.78 0.40 0.76 0.92
Spec, specimen. ) Pearson product-moment correlation coefficient. y Determination coefficient.
muscle and teres minor muscle) of the rotator cuff during internal rotation, as described by Schulz et al.26 This phenomenon leads to an anterior decentered humeral head, the posterior contact area no longer exists, and the anterior contact area shifts toward the center of the humeral head. This would explain the centrally accentuated density distribution we found. As expected, strength distribution was not homogenous as well. This became obvious as we filled in the obtained information in a summary chart and compared it with the results of the subchondral mineralization. The summary charts of strength maxima showed bicentric and monocentric distribution patterns that were similar to the mineralization summary charts. The force needed to penetrate areas of high density (red and yellow color in the densitograms) was significantly higher than in areas of lower density. Several authors demonstrated that long-term stress leads to specific patterns of mineralization in the subchondral bone plate.5,18 Our opinion is that long-term
Figure 7 Correlation between local strength and density on a single humeral head (n ¼ 29).
stress on the humeral head leads not only to characteristic subchondral mineralization patterns but also to an increased amount of absolute density in these areas. Because the long-term stress affects not only the subchondral bone but also the subarticular cancellous bone,14 we assume that the mineralization patterns of the subchondral bone plate are continuing in cancellous bone. An ongoing study at our institute indicates a high correlation between the density values of the subchondral bone and the subarticular spongiosa. From the clinical view point, knowing subchondral bone density might be interesting for osteosynthesis because this is the only solid bone where screws are placed during open reduction and internal fixation. It is also necessary in case of resurfacing to achieve an optimal fixation of the prosthesis. Several authors underlined the importance of subchondral bone for optimal screw positioning.6,12 If further studies can show that differences in mineralization are clinically reflective of regions that perform better or worse for anchor placement, our findings might also be useful for rotator cuff tendon repair. An interesting starting point for further studies could be how anchor systems for tendon repair should be placed to hit these regions of great mechanical strength without injuring the articular surface.
Conclusions Our findings show that CT-OAM can indirectly be used to give information about bone quality in vivo. This allows the noninvasive measurement of the mechanical quality of implant basis. Our results showed that the best bone quality in the humeral head is generally found in the anterior and posterior parts; in some rare cases, the central part displays a large maximum. We showed that mineralization and mechanical strength in the humeral head correlate on a high level (P < .01). These findings might be useful for the development of new fixation
Humeral head mineralization and strength methods in shoulder surgery, such as humeral resurfacing arthroplasty.
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15. 16.
Disclaimer
17.
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.
18. 19.
20.
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