0
Research Papers

The Size of Simulated Lytic Metastases Affects the Strain Distribution on the Anterior Surface of the Vertebra

[+] Author and Article Information
Marco Palanca

Department of Industrial Engineering,
School of Engineering and Architecture,
Alma Mater Studiorum—Università di Bologna,
Via Terracini 24-28,
Bologna 40131, Italy
e-mail: marco.palanca2@unibo.it

Giovanni Barbanti-Bròdano

Department of Oncologic and
Degenerative Spine Surgery,
Rizzoli Orthopaedic Institute,
Via G.C. Pupilli 1,
Bologna 40136, Italy
e-mail: giovanni.barbantibrodano@ior.it

Luca Cristofolini

Department of Industrial Engineering,
School of Engineering and Architecture,
Alma Mater Studiorum—Università di Bologna,
Via Terracini 24-28,
Bologna 40131, Italy
e-mail: luca.cristofolini@unibo.it

1Corresponding author.

Manuscript received February 6, 2018; final manuscript received June 4, 2018; published online August 20, 2018. Assoc. Editor: Anna Pandolfi.

J Biomech Eng 140(11), 111005 (Aug 20, 2018) (9 pages) Paper No: BIO-18-1069; doi: 10.1115/1.4040587 History: Received February 06, 2018; Revised June 04, 2018

Metastatic lesions of the vertebra are associated with risk of fracture, which can be disabling and life-threatening. In the literature, attempts are found to identify the parameters that reduce the strength of a metastatic vertebra leading to spine instability. However, a number of controversial issues remain. Our aim was to quantify how the strain distribution in the vertebral body is affected by the presence and by the size of a simulated metastatic defect. Five cadaveric thoracic spine segments were subjected to non-destructive presso-flexion while intact, and after simulation of metastases of increasing size. For the largest defect, the specimens were eventually tested to failure. The full-field strain distribution in the elastic range was measured with digital image correlation (DIC) on the anterior surface of the vertebral body. The mean strain in the vertebra remained similar to the intact when the defects were smaller than 30% of the vertebral volume. The mean strains became significantly larger than in the intact for larger defects. The map of strain and its statistical distribution indicated a rather uniform condition in the intact vertebra and with defects smaller than 30%. Conversely, the strain distribution became significantly different from the intact for defects larger than 30%. A strain peak appeared in the region of the simulated metastasis, where fracture initiated during the final destructive test. This is a first step in understanding how the features of metastasis influence the vertebral strain and for the construction of a mechanistic model to predicted fracture.

FIGURES IN THIS ARTICLE
<>
Copyright © 2018 by ASME
Your Session has timed out. Please sign back in to continue.

References

Smith, B. D. , Smith, G. L. , Hurria, A. , Hortobagyi, G. N. , and Buchholz, T. A. , 2009, “Future of Cancer Incidence in the United States: Burdens Upon an Aging, Changing Nation,” J. Clin. Oncol., 27(17), pp. 2758–2765. [CrossRef] [PubMed]
Siegel, R. L. , Miller, K, D. , and Jemal, A. , 2017, “Cancer Statistics,” CA Cancer J Clin., 67(1), pp. 7–30.
Mirels, H. , 1989, “Metastatic Disease in Long Bones. A Proposed Scoring System for Diagnosing Impending Pathologic Fractures,” Clin. Orthop. Relat. Res., 249, pp. 256–264.
Laufer, I. , Rubin, D. G. , Lis, E. , Cox, B. W. , Stubblefield, M. D. , Yamada, Y. , and Bilsky, M. H. , 2013, “The NOMS Framework: Approach to the Treatment of Spinal Metastatic Tumors,” Oncologist, 18(6), pp. 744–751. [CrossRef] [PubMed]
Jacobs, W. B. , and Perrin, R. G. , 2001, “Evaluation and Treatment of Spinal Metastases: An Overview,” Neurosurg. Focus, 11(6), pp. 1–11. [CrossRef]
Wong, D. A. , Fornasier, V. L. , and MacNab, I. , 1990, “Spinal Metastases: The Obvious, the Occult, and the Impostors,” Spine (Phila. Pa. 1976), 15(1), pp. 1–4. [CrossRef] [PubMed]
Klimo , P., Jr. , and Schmidt, M. H. , 2004, “Surgical Management of Spinal Metastases,” Oncologist, 9(2), pp. 188–196. [CrossRef] [PubMed]
Tomita, K. , Kawahara, N. , Kobayashi, T. , Yoshida, A. , Murakami, H. , and Akamaru, T. , 2001, “Surgical Strategy for Spinal Metastases,” Spine (Phila. Pa. 1976), 26(3), pp. 298–306. [CrossRef] [PubMed]
White, A. A. , Southwick, W. , and Panjabi, M. M. , 1976, “Clinical Instability in the Lower Cervical Spine a Review of past and Current Concepts,” Spine (Phila. Pa. 1976), 1(1), pp. 15–27. [CrossRef]
Whyne, C. M. , Hu, S. S. , Workman, K. L. , and Lotz, J. C. , 2000, “Biphasic Material Properties of Lytic Bone Metastases,” Ann. Biomed. Eng., 28(9), pp. 1154–1158. [CrossRef] [PubMed]
Kaneko, T. S. , Bell, J. S. , Pejcic, M. R. , Tehranzadeh, J. , and Keyak, J. H. , 2004, “Mechanical Properties, Density and Quantitative CT Scan Data of Trabecular Bone With and Without Metastases,” J. Biomech., 37(4), pp. 523–530. [CrossRef] [PubMed]
Szendrői, M. , Antal, I. , Szendrői, A. , Lazáry, Á. , and Varga, P. P. , 2017, “Diagnostic Algorithm, Prognostic Factors and Surgical Treatment of Metastatic Cancer Diseases of the Long Bones and Spine,” EFORT Open Rev., 2(9), pp. 372–381. [CrossRef] [PubMed]
Ibrahim, A. , Crockard, A. , Antonietti, P. , Boriani, S. , Bünger, C. , Gasbarrini, A. , Grejs, A. , Harms, J. , Kawahara, N. , Mazel, C. , Melcher, R. , and Tomita, K. , 2008, “Does Spinal Surgery Improve the Quality of Life for Those With Extradural (Spinal) Osseous Metastases? An International Multicenter Prospective Observational Study of 223 Patients,” J. Neurosurg. Spine, 8(3), pp. 271–278. [CrossRef] [PubMed]
Choi, D. , Crockard, A. , Bunger, C. , Harms, J. , Kawahara, N. , Mazel, C. , Melcher, R. , and Tomita, K. , 2010, “Review of Metastatic Spine Tumour Classification and Indications for Surgery: The Consensus Statement of the Global Spine Tumour Study Group,” Eur. Spine J., 19(2), pp. 215–222. [CrossRef] [PubMed]
Fisher, C. G. , Dipaola, C. P. , Ryken, T. C. , Bilsky, M. H. , Shaffrey, C. I. , Berven, S. H. , Harrop, J. S. , Fehlings, M. G. , Boriani, S. , Chou, D. , Schmidt, M. H. , Polly, D. W. , Biagini, R. , Burch, S. , Dekutoski, M. B. , Ganju, A. , Gerszten, P. C. , Gokaslan, Z. L. , Groff, M. W. , Liebsch, N. J. , Mendel, E. , Okuno, S. H. , Patel, S. , Rhines, L. D. , Rose, P. S. , Sciubba, D. M. , Sundaresan, N. , Tomita, K. , Varga, P. P. , Vialle, L. R. , Vrionis, F. D. , Yamada, Y. , and Fourney, D. R. , 2010, “A Novel Classification System for Spinal Instability in Neoplastic Disease,” Spine (Phila. Pa. 1976), 35(22), pp. 1221–1229. [CrossRef]
Fourney, D. R. , Frangou, E. M. , Ryken, T. C. , DiPaola, C. P. , Shaffrey, C. I. , Berven, S. H. , Bilsky, M. H. , Harrop, J. S. , Fehlings, M. G. , Boriani, S. , Chou, D. , Schmidt, M. H. , Polly, D. W. , Biagini, R. , Burch, S. , Dekutoski, M. B. , Ganju, A. , Gerszten, P. C. , Gokaslan, Z. L. , Groff, M. W. , Liebsch, N. J. , Mendel, E. , Okuno, S. H. , Patel, S. , Rhines, L. D. , Rose, P. S. , Sciubba, D. M. , Sundaresan, N. , Tomita, K. , Varga, P. P. , Vialle, L. R. , Vrionis, F. D. , Yamada, Y. , and Fisher, C. G. , 2011, “Spinal Instability Neoplastic Score: An Analysis of Reliability and Validity From the Spine Oncology Study Group,” J. Clin. Oncol., 29(22), pp. 3072–3077. [CrossRef] [PubMed]
Benca, E. , Patsch, J. M. , Mayr, W. , Pahr, D. H. , and Windhager, R. , 2016, “The Insufficiencies of Risk Analysis of Impending Pathological Fractures in Patients With Femoral Metastases: A Literature Review,” Bone Rep., 5, pp. 51–56. [CrossRef] [PubMed]
Hipp, J. A. , Mcbroom, R. J. , Cheal, E. J. , and Hayes, W. C. , 1989, “Structural Consequences of Endosteal Metastatic Lesions in Long Bones,” J. Orthop. Res., 7(6), pp. 828–837. [CrossRef] [PubMed]
Hipp, J. A. , Edgerton, B. C. , An, K. N. , and Hayes, W. C. , 1990, “Structural Consequences of Transcortical Holes in Long Bones Loaded in Torsion,” J. Biomech., 23(12), pp. 1261–1268. [CrossRef] [PubMed]
Fidler, M. , 1981, “Incidence of Fracture Through Metastases in Long Bones,” Acta Orthop., 52(6), pp. 623–627. [CrossRef]
Menck, H. , Schulze, S. , and Larsen, E. , 1988, “Metastasis Size in Pathologic Femoral Fractures,” Acta Orthop., 59(2), pp. 151–154. [CrossRef]
Van der Linden, Y. M. , Dijkstra, P. D. , Kroon, H. M. , Lok, J. J. , Noordijk, E. M. , Leer, J. W. , and Marijnen, C. A. , 2004, “Comparative Analysis of Risk Factors for Pathological Fracture With Femoral Metastases,” J. Bone Jt. Surg. Br., 86(4), pp. 566–573. [CrossRef]
Whyne, C. M. , Hu, S. S. , and Lotz, J. C. , 2001, “Parametric Finite Element Analysis of Vertebral Bodies Affected by Tumors,” J. Biomech., 34(10), pp. 1317–1324. [CrossRef] [PubMed]
Whyne, C. M. , Hu, S. S. , and Lotz, J. C. , 2003, “Burst Fracture in the Metastatically Involved Spine: Development, Validation, and Parametric Analysis of a Three-Dimensional Poroelastic Finite-Element Model,” Spine (Phila. Pa. 1976), 28(7), pp. 652–660. [PubMed]
Tschirhart, C. E. , Nagpurkar, A. , and Whyne, C. M. , 2004, “Effects of Tumor Location, Shape and Surface Serration on Burst Fracture Risk in the Metastatic Spine,” J. Biomech., 37(5), pp. 653–660. [CrossRef] [PubMed]
Tschirhart, C. E. , Finkelstein, J. A. , and Whyne, C. M. , 2007, “Biomechanics of Vertebral Level, Geometry, and Transcortical Tumors in the Metastatic Spine,” J. Biomech., 40(1), pp. 46–54. [CrossRef] [PubMed]
Snyder, B. D. , Cordio, M. A. , Nazarian, A. , Kwak, S. D. , Chang, D. J. , Entezari, V. , Zurakowski, D. , and Parker, L. M. , 2009, “Noninvasive Prediction of Fracture Risk in Patients With Metastatic Cancer to the Spine,” Clin. Cancer Res., 15(24), pp. 7676–7683. [CrossRef] [PubMed]
Alkalay, R. N. , and Harrigan, T. P. , 2016, “Mechanical Assessment of the Effects of Metastatic Lytic Defect on the Structural Response of Human Thoracolumbar Spine,” J. Orthop. Res., 34(10), pp. 1808–1819. [CrossRef] [PubMed]
Alkalay, R. N. , 2015, “Effect of the Metastatic Defect on the Structural Response and Failure Process of Human Vertebrae: An Experimental Study,” Clin. Biomech., 30(2), pp. 121–128. [CrossRef]
Silva, M. J. , Hipp, J. A. , Gowan, D. P. M. , Hayes, W. C. , McGowan, D. P. , Takeuchi, T. , and Hayes, W. C. , 1993, “Strength Reductions of Thoracic Vertebrae in the Presence of Transcortical Osseous Defects: Effects of Defect Location, Pedicle Disruption, and Defect Size,” Eur. Spine J., 2(3), pp. 118–125. [CrossRef] [PubMed]
Windhagen, H. J. , Hipp, J. A. , Silva, M. J. , Lipson, S. J. , and Hayes, W. C. , 1997, “Predicting Failure of Thoracic Vertebrae With Simulated and Actual MEtastatic Defects,” Clin. Orthop. Relat. Res., 344, pp. 313–319. [CrossRef]
Palanca, M. , Marco, M. , Ruspi, M. L. , and Cristofolini, L. , 2018, “Full-Field Strain Distribution in Multi-Vertebra Spine Segments: An In-Vitro Application of DIC,” Med. Eng. Phys., 52, pp. 76–83. [CrossRef] [PubMed]
Danesi, V. , Zani, L. , Scheele, A. , Berra, F. , and Cristofolini, L. , 2014, “Reproducible Reference Frame for In Vivo Testing of the Human Vertebrae,” J. Biomech., 47(1), pp. 313–318. [CrossRef] [PubMed]
Lionello, G. , Sirieix, C. , and Baleani, M. , 2014, “An Effective Procedure to Create a Speckle Pattern on Biological Soft Tissue for Digital Image Correlation Measurements,” J. Mech. Behav. Biomed. Mater., 39, pp. 1–8. [CrossRef] [PubMed]
Palanca, M. , Tozzi, G. , and Cristofolini, L. , 2016, “The Use of Digital Image Correlation in the Biomechanical Area: A Review,” Int. Biomech., 3(1), pp. 1–21. [CrossRef]
Lionello, G. , and Cristofolini, L. , 2014, “A Practical Approach to Optimizing the Preparation of Speckle Patterns for Digital-Image Correlation,” Meas. Sci. Technol., 25(10), p. 107001. [CrossRef]
Taneichi, H. , Kaneda, K. , Takeda, N. , Abumi, K. , and Satoh, S. , 1997, “Risk Factors and Probability of Vertebral Body Collapse in Metastases of the Thoracic and Lumbar Spine,” Spine (Phila. Pa. 1976), 22(3), pp. 239–245. [CrossRef] [PubMed]
Sutton, M. A. , Orteu, J. J. , and Schreier, H. W. , 2009, Image Correlation for Shape, Motion and Deformation Measurements, Springer, New York.
Palanca, M. , Brugo, T. M. M. , and Cristofolini, L. , 2015, “Use of Digital Image Correlation to Understand the Biomechanics of the Vertebra,” J. Mech. Med. Biol., 15(02), p. 1540004. [CrossRef]
Cristofolini, L. , Brandolini, N. , Danesi, V. , Juszczyk, M. M. , Erani, P. , and Viceconti, M. , 2013, “Strain Distribution in the Lumbar Vertebrae Under Different Loading Configurations,” Spine J., 13(10), pp. 1281–1292. [CrossRef] [PubMed]
Panjabi, M. M. , 2007, “Hybrid Multidirectional Test Method to Evaluate Spinal Adjacent-Level Effects,” Clin. Biomech. (Bristol, Avon), 22(3), pp. 257–265. [CrossRef] [PubMed]
Dall'Ara, E. , Schmidt, R. , Pahr, D. , Varga, P. , Chevalier, Y. , Patsch, J. , Kainberger, F. , and Zysset, P. , 2010, “A Nonlinear Finite Element Model Validation Study Based on a Novel Experimental Technique for Inducing Anterior Wedge-Shape Fractures in Human Vertebral Bodies In Vivo,” J. Biomech., 43(12), pp. 2374–2380. [CrossRef] [PubMed]
Wilke, H.-J. , Wenger, K. , and Claes, L. , 1998, “Testing Criteria for Spinal Implants: Recommentations for the Standardardization of In Vivo Stability Testing of Spinal Implants,” Eur. Spine J., 7(2), pp. 148–154. [CrossRef] [PubMed]
Cristofolini, L. , Conti, G. , Juszczyk, M. , Cremonini, S. , Van Sint Jan, S. , and Viceconti, M. , 2010, “Structural Behaviour and Strain Distribution of the Long Bones of the Human Lower Limbs,” J. Biomech., 43(5), pp. 826–835. [CrossRef] [PubMed]
Aamodt, A. , Lund-Larsen, J. , Eine, J. , Andersen, E. , Benum, P. , and Husby, O. S. , 1997, “In Vivo Measuments Show Tensile Axial Strain in the Proximal Lateral Aspect of the Human Femur,” J. Orthop. Res., 15(6), pp. 927–931. [CrossRef] [PubMed]
Bayraktar, H. H. , Morgan, E. F. , Niebur, G. L. , Morris, G. E. , Wong, E. K. , and Keaveny, T. M. , 2004, “Comparison of the Elastic and Yield Properties of Human Femoral Trabecular and Cortical Bone Tissue,” J. Biomech., 37(1), pp. 27–35. [CrossRef] [PubMed]
Cristofolini, L. , 2015, “In Vitro Evidence of the Structural Optimization of the Human Skeletal Bones,” J. Biomech., 48(5), pp. 787–796. [CrossRef] [PubMed]
Danesi, V. , Erani, P. , Brandolini, N. , Juszczyk, M. , and Cristofolini, L. , 2016, “Effect of the In Vivo Boundary Conditions on the Surface Strain Experienced by the Vertebral Body in the Elastic Regime,” ASME J. Biomech. Eng., 138(10), p. 104503. [CrossRef]
Benca, E. , Reisinger, A. , Patsch, J. M. , Hirtler, L. , Synek, A. , Stenicka, S. , Windhager, R. , Mayr, W. , and Pahr, D. H. , 2017, “Effect of Simulated Metastatic Lesions on the Biomechanical Behavior of the Proximal Femur,” J. Orthop. Res., 35(11), pp. 2407–2414. [CrossRef] [PubMed]
Burke, M. , Atkins, A. , Kiss, A. , Akens, M. , Yee, A. , and Whyne, C. , 2017, “The Impact of Metastasis on the Mineral Phase of Vertebral Bone Tissue,” J. Mech. Behav. Biomed. Mater., 69, pp. 75–84. [CrossRef] [PubMed]
Nazarian, A. , Von Stechow, D. , Zurakowski, D. , Müller, R. , and Snyder, B. D. , 2008, “Bone Volume Fraction Explains the Variation in Strength and Stiffness of Cancellous Bone Affected by Metastatic Cancer and Osteoporosis,” Calcif. Tissue Int., 83(6), pp. 368–379. [CrossRef] [PubMed]
Palanca, M. , Cristofolini, L. , Dall'Ara, E. , Curto, M. , Innocente, F. , Danesi, V. , and Tozzi, G. , 2016, “Digital Volume Correlation Can Be Used to Estimate Local Strains in Natural and Augmented Vertebrae: An Organ-Level Study,” J. Biomech., 49(16), pp. 3882–3890. [CrossRef] [PubMed]
Tozzi, G. , Danesi, V. , Palanca, M. , and Cristofolini, L. , 2016, “Elastic Full-Field Strain Analysis and Microdamage Progression in the Vertebral Body From Digital Volume Correlation,” Strain, 52(5), pp. 446–455. [CrossRef]
Costa, M. C. , Tozzi, G. , Cristofolini, L. , Danesi, V. , Viceconti, M. , and Dall'Ara, E. , 2017, “Micro Finite Element Models of the Vertebral Body: Validation of Local Displacement Predictions,” PLoS One, 12(7), p. e0180151. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

Workflow of each specimen: it is tested intact in the elastic regime; then two defects of 6 mm of diameter were produced in the vertebral body through a bipedicular access and then retested. This procedure was repeated enlarging the defect diameters to 8, 10, and 12 mm. Finally, they were tested up to failure.

Grahic Jump Location
Fig. 2

Experimental test setup viewed from anterior. Left: overview showing the specimen (a) in the testing machine (b), the DIC cameras (c) and the system of lights (d). Right: detail of the test setup. The specimen (a) was loaded through the pots (e) at the two extremities. A ball joint (f) and two orthogonal linear bearings (under the ball joint and both covered by the towels) were used to avoid transmission of bending moments and horizontal forces.

Grahic Jump Location
Fig. 3

Strain fields (minimum principal strain εmin, maximum principal strain εmax, and max shear strain γmax) of a typical specimen under load at the selected load (Fspecimen) for the intact condition and for each simulated lytic defect group. For each defect group, the percentage of simulated lesion of this specific specimen is reported in brackets. The white spots in the strain field are no correlated regions due to light reflections and fluid leakages.

Grahic Jump Location
Fig. 4

Strains (mean on the anterior surface) for the different sizes of simulated defect (binned as in Table 1) at the full load (Fspecimen) expressed as a percentage of the strain in the intact (values greater than 100% indicate a strain increase with respect to the intact condition, in absolute value). Statistical significance is reported (Tukey HSD tests): *p < 0.05, **p < 0.01. The results of the Tukey's multiple comparisons test are reported in the Supplementary Materials which are available under “Supplemental Data” tab for this paper on the ASME Digital Collection.

Grahic Jump Location
Fig. 5

Histograms of the statistical distribution of the magnitudes of principal strain on the anterior surface of a generic specimen at selected load (Fspecimen) for intact and for each simulated lytic defect group. The significance of differences is also reported (two-sample, Kolmogorov-Smirnov, p < 0.05).

Grahic Jump Location
Fig. 6

Residual strains after unloading (mean on the anterior surface) for the different sizes of simulated defect (binned as in Table 1) in microstrain. The gray band indicates the order of magnitude of the errors associated with DIC strain measurement. Statistical significance is reported (Tukey HSD tests): *p < 0.05, **p < 0.01. The results of the Tukey's multiple comparisons test are reported in the Supplementary Materials which are available under “Supplemental Data” tab for this paper on the ASME Digital Collection.

Grahic Jump Location
Fig. 7

Destructive test: Typical force–displacement plot (left), and lateral view of a specimen (with the white pattern on the blue background) after failure, showing a typical matastatic vertebral fracture (right). The first dot on the plot represents the Fspecimen, while the second dot is the Fultimate. The arrows delineate the propagated crack.

Grahic Jump Location
Fig. 8

Development of the strain field during the destructive test: maximum and minimum principal strains and maximum shear strain in the elastic regime, prior to failure, and after failure

Grahic Jump Location
Fig. 9

Strain field (minimum principal strain εmin, maximum principal strain εmax and max shear strain γmax) of all specimens, with the largest defect, before the failure. The failure point (identified with the arrows) correspond in all specimens to a region with high shear strain gradients.

Tables

Errata

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In