- Email: [email protected]
Ultrasound melted polymer sleeve for improved screw anchorage in trabecular bone—A novel screw augmentation technique
Clinical Biomechanics 33 (2016) 79–83
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Ultrasound melted polymer sleeve for improved screw anchorage in trabecular bone—A novel screw augmentation technique W. Schmoelz a,⁎, R. Mayr a, F. Schlottig b, N. Ivanovic a, R. Hörmann c, J. Goldhahn d a
Department of Trauma Surgery, Medical University of Innsbruck, Innsbruck, Austria Thommen Medical, Neckarsulmstrasse 28, Grenchen 2540, Switzerland Division of Clinical and Functional Anatomy, Department of Anatomy, Medical University of Innsbruck, Innsbruck, Austria d Institute for Biomechanics, ETH Zurich, Switzerland b c
a r t i c l e
i n f o
Article history: Received 2 November 2015 Accepted 15 February 2016 Keywords: Bone amelioration Screw anchorage Augmentation Trabecular bone Insertion torque Primary stability
a b s t r a c t Background: Screw anchorage in osteoporotic bone is still limited and makes treatment of osteoporotic fractures challenging for surgeons. Conventional screws fail in poor bone quality due to loosening at the screw–bone interface. A new technology should help to improve this interface. In a novel constant amelioration process technique, a polymer sleeve is melted by ultrasound in the predrilled screw hole prior to screw insertion. The purpose of this study was to investigate in vitro the effect of the constant amelioration process platform technology on primary screw anchorage. Methods: Fresh frozen femoral heads (n = 6) and vertebrae (n = 6) were used to measure the maximum screw insertion torque of reference and constant amelioration process augmented screws. Specimens were cut in cranio-caudal direction, and the screws (reference and constant amelioration process) were implanted in predrilled holes in the trabecular structure on both sides of the cross section. This allowed the pairwise comparison of insertion torque for constant amelioration process and reference screws (femoral heads n = 18, vertebrae n = 12). Prior to screw insertion, a micro-CT scan was made to ensure comparable bone quality at the screw placement location. Findings: The mean insertion torque for the constant amelioration process augmented screws in both, the femoral heads (44.2 Ncm, SD 14.7) and the vertebral bodies (13.5 Ncm, SD 6.3) was significantly higher than for the reference screws of the femoral heads (31.7 Ncm, SD 9.6, p b 0.001) and the vertebral bodies (7.1 Ncm, SD 4.5, p b 0.001). Interpretation: The interconnection of the melted polymer sleeve with the surrounding trabecular bone in the constant amelioration process technique resulted in a higher screw insertion torque and can improve screw anchorage in osteoporotic trabecular bone. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction Due to demographic changes, the proportion of geriatric trauma patients and osteoporotic fractures is continuously increasing (Bleibler et al., 2013; Burge et al., 2007). Over the last decade, research and implant development focused on novel implant designs for the treatment of osteoporotic fractures. However, screw anchorage in trabecular bone of reduced bone quality is still limited. Insufficient screw anchorage
⁎ Corresponding author at: Department of Trauma Surgery, Medical University of Innsbruck, Innsbruck, Austria. E-mail addresses: [email protected] (W. Schmoelz), [email protected] (R. Mayr), [email protected] (F. Schlottig), [email protected] (N. Ivanovic), [email protected] (R. Hörmann), [email protected] (J. Goldhahn).
http://dx.doi.org/10.1016/j.clinbiomech.2016.02.010 0268-0033/© 2016 Elsevier Ltd. All rights reserved.
causes reduced load bearing capability of the screw increasing the risk of osteosynthesis failure. Screw anchorage in trabecular bone, such as pedicle screws, can be reinforced by cement injection into the adjacent bone around the screw. Biomechanical studies showed increased load bearing capability of screws with cement augmentation in comparison with non-augmented screws (Bostelmann et al., 2014; Bullmann et al., 2010). Cement augmentation of screws is already performed in clinical practice and investigated in experimental studies for several anatomic regions, e.g., spine (Bostelmann et al., 2014; Bullmann et al., 2010), proximal humerus (Roderer et al., 2013; Unger et al., 2012), hip (Erhart et al., 2011; Sermon et al., 2012), distal femur (Wahnert et al., 2013), and proximal tibia (Goetzen et al., 2014). However, this technique has potential disadvantages such as the additional surgical time caused by cement preparation, the excessive heating during curing of polymethylmethacrylat (PMMA) cement leading to bone necrosis, and the risk of cement leakage out of the bone into the
80
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
Fig. 1. The application of the CAP technique to improve screw anchorage includes the following steps: predrilling with 4.3 mm (b), insertion of polymer sleeve (c), attachment of the ultrasound applicator with core guidance into sleeve (d), melting of polymer sleeve by ultrasound (e + f), extraction of ultrasound applicator and re-drilling of borehole with melted sleeve (g), reinforced borehole for screw (h), and screw insertion (i).
surrounding structures (Breusch and Kuhn, 2003; Ciapetti et al., 2000; Jung et al., 2010; Stanczyk and van Rietbergen, 2004). A novel method for screw augmentation represents the constant amelioration process technique (CAP). A polymer sleeve consisting of poly-L-DL-lactide copolymers (PLLAA) gets melted within the borehole by ultrasound. The melted polymer penetrates the trabecular bone cavities, following a rapid solidification. A conventional screw can then be inserted into the reinforced borehole (Fig. 1). The melted polymer within the borehole increases the overall contact surface area between screw and bone. This method can considerably save operating time in comparison with cement screw augmentation due to the fast melting and resolidification of the polymer sleeve and no need of cement preparation. Stubinger et al. (2014) showed in an in vivo sheep model that the CAP technique significantly improved primary stability regarding insertion torque in sheep pelvic bone. However, the cancellous bone of the sheep has more densely packed bone trabeculae, lower porosity, and higher bone mass compared to human cancellous bone (Wang et al., 2010). It is still unknown if the beneficial effect on screw anchorage of the CAP screw augmentation technique is also present in human trabecular bone with reduced bone quality. The aim of the present study was to investigate the effect of an ultrasound melted polymer sleeve on the screw insertion torque in human trabecular bone. 2. Methods 2.1. Specimens In order to obtain trabecular bone densities of different anatomical regions six femoral heads (mean age 74.7 years, SD 9.1) and six vertebral bodies (mean age 79.3 years, SD 6.3) were used for testing. The bodies were donated by people who had given their informed consent for their use for scientific and educational purposes prior to death (McHanwell et al., 2008; Riederer et al., 2012). Specimens were stored at −20 °C and thawed at room temperature 12 h before testing. Specimens were cut in cranio-caudal direction in order to get comparable trabecular bone stock for a paired comparison of the augmented (CAP) and non-augmented reference (Ref) screw. Femoral heads were cut in the frontal plane through the axis of the femoral neck. Vertebrae were cut in the sagittal plane through the spinal process. Glass balls (2 mm
diameter) were glued to the corresponding sites of both cut cross sections serving as landmarks. The location of screw insertion in the cross section was determined by a template aligned to the landmarks. Screws were implanted in both sides of the cut cross sections at the corresponding positions in order to allow a paired comparison (Fig. 2) of CAP and reference screws. In the femoral heads, three screws were placed in each side of the cross sections while only two screws could be placed in each side of the cross section of the vertebrae. This resulted in a total number of 18 paired tests at the femoral head and 12 at the vertebral body with a total of 30 screws with (CAP) and without CAP (Ref) augmentation. 2.2. Screw implantation The same screws were implanted for both groups (SPI Element 5 mm diameter, 9 mm length, Thommen Medical AG, Switzerland). A borehole was drilled with a core diameter of 4.3 mm and a minimum depth of 9 mm prior to screw insertion. For the CAP technique, a polymer sleeve (outer diameter 4.3 mm, 0.3 mm thickness, 5 mm height) consisting of 70:30 PLA (70% L-lactide and 30% DL-lactide (Resomer LR708, Böhringer Ingelheim, Germany) was inserted in the borehole (Fig. 3). A commercially available ultrasound applicator was used (Branson E-150, Branson Ultrasonics SA, Carouge, Switzerland; 20 kHz, amplitude of max. 60 μm = 150 W, set at 50%) and attached to the polymere sleeve. The polymer sleeve was melted by ultrasound and disseminated in the trabecular cavities by pushing the outer casing of the ultrasound applicator into the borehole. The borehole was re-drilled with the 4.3 mm drill, and the screw was inserted in the reinforced borehole (Fig. 1). For the reference screw group, screws were inserted immediately after initial borehole drilling. During screw insertion, the torque was measured with a torque measurement device (Chiropro 980, Bien-Air, Switzerland), and maximum values were recorded. 2.3. Micro-computed tomography All specimens were scanned with a micro-CT (vivaCT 40, Scanco Medical) prior to testing. The following scan parameters were used: energy 70 kV, intensity 114 μA, image matrix of 1024 × 1024 pixels per slice, and integration time 200 ms. Total scanning time per sample
Fig. 2. Exemplary 3D reconstruction of micro-CT scans and the screw placement location in the femoral head (left) and in the vertebra (right).
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
81
was used to investigate the correlation between mechanical parameters and micro-CT measurements for both test groups. The level of significance was set to p b 0.05. 3. Results Fig. 3. Polymer sleeve, diameter 4.3 mm, 0.3 mm wall thickness, and 5 mm height and used screw (SPI Element 5 mm diameter, 9 mm length, Thommen Medical AG, Switzerland).
One screw location in the femoral head and two screw locations in the vertebra had to be excluded from data analysis due to technical difficulties in pilot hole drilling. This left for both, the reference and the CAP augmented group, 17 paired screws in the femoral heads and 10 paired screws in the vertebrae. The mean insertion torque for all CAP augmented screws in both, the femoral heads and the vertebral bodies (32.8 Ncm, SD 19.3) was significantly higher than for the reference screws (22.6 Ncm, SD 14.5; p b 0.001, Fig. 4). In general, the vertebral specimens showed a lower insertion torque and a reduced competence in the micro-CT parameters than the femoral heads (Table 1). Comparing the control with the CAP augmentation showed for the vertebral body screws a mean increase of insertion torque of 111% (SD 56%), while femoral head screws showed a mean increase of 45% (SD 43%). There was a significant negative correlation between the relative increase of insertion torque by the CAP augmentation and the BV/TV in both femoral heads and vertebral bodies (r = −0.51, p b 0.007). None of the structural parameters measured by the micro-CT showed significant differences in bone quality between at the paired locations for the CAP and reference screw. In both groups, the augmented group and the reference group, a significant correlation between the insertion torque and the BV/TV was found (CAP, r = 0.945, p b 0.001; Ref, r = 0.92, p b 0.001). (see Fig. 5.)
Fig. 4. Scatter plot showing the maximal insertion torque with CAP augmentation and without (ref) of all screw pairs. Note: points above the midline indicate that the CAP augmentation increased the insertion torque for the screw pair.
4. Discussion In the present study, the application of CAP polymer sleeve augmentation significantly improved primary stability of the screw in trabecular bone of human specimens. This beneficial effect for the CAP technique on the screw insertion torque was observed in regions of higher and lower trabecular bone density, such as the femoral head and the vertebral body. The results of this study are in concordance with the results of other authors. Stubinger et al. (2014). showed in an animal model that the CAP technique significantly increased the insertion torque in pelvic bone of the sheep. They reported a mean insertion torque of 41.9 Ncm (SD 19.5 Ncm) for screws with CAP augmentation and 23.3 Ncm (SD 13.6 Ncm) for screws without augmentation. Differences regarding trabecular structure and bone density between human and sheep bone made an investigation in human bone necessary. In the present study, the beneficial effect of CAP augmentation was higher in bone with lower trabecular bone density such as the vertebral bone in comparison with the femoral head. This provides promising results for the use of CAP augmentation in osteoporotic fractures. For the CAP technique, biodegradable PDLLA is used for augmentation. PDLLA 70:30 shows a high biocompatibility with an in vivo resorption time in bone of 1 to 3 years. PDLLA implants are routinely used in oral and maxillofacial surgery as also for orthopedic surgery such as interference screws for cruciate ligament reconstruction. Another technique using implants wholly manufactured of biodegradable PDLLA
was 69.5 min for femoral heads and 49.7 min for vertebras. One thousand fifty-four slices of vertebra and one thousand four hundred eighty-three femoral head slices were scanned where each slice was 38 μm thickness. After initial raw data reconstruction, additional 3D transformations and rotations (Scanco Micro-CT software) were carried out to align the specimen scans with the cutting planes and allow an accurate placement of the volumes of interest (VOIs) with the predefined drilling pattern of the screw insertion location. VOIs were selected and evaluated with the trabecular bone morphology evaluation script (Scanco MicroCT software). Drilling holes were represented as 3D cylinders of 164 × 164 × 262 px (approximately 6 × 6 × 10 mm) dimensions. A 3D segmentation of VOI cylinders was done with a Gauss Sigma value of 0.8, Gauss support value of 1, lower threshold value of 220, and upper threshold value of 1000. Results provided information on relative bone volume fraction (BV/TV), connectivity density, trabeculae, and anisotropy for each drilling site. 2.4. Statistical analysis For statistical comparison of the insertion torque of the reference and augmented group, a paired t-test was used. The Pearson correlation
Table 1 Measured maximal insertion torque and parameters on micro-CT scan given in means (SD). Significant differences (p b 0.05) between the CAP and Ref group are indicated with asterisks (*) Femoral heads
Vertebral bodies
All specimens
CAP
Ref
CAP
Ref
CAP
Ref
Insertion torque (Ncm) BV/TV
44.2* (14.7) 0.245 (0.080)
Mean TV (mgHA/ccm)
234.7 (69.4)
31.7 (9.6) 0.251 (0.069) 238.4 (57.9)
13.5* (6.3) 0.063 (0.023) 63.0 (32.7)
7.1 (4.5) 0.054 (0.023) 49.4 (38.8)
32.8* (19.3) 0.177 (0.111) 171.1 (102.4)
22.6 (14.5) 0.178 (0.111) 168.4 (106.0)
82
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
Fig. 5. A. Scatter plot showing the maximal insertion torque in relation to the BV/TV for screws with CAP augmentation (A) and without augmentation (B). R2—correlation lines indicate positive correlation between insertion torque and BV/TV for both groups.
with ultrasound melting of the anchorage pins (BoneWelding® technology) was investigated in several histological studies on terms of polymer distribution and bone healing. The ultrasonic vibrations causes liquefaction of the thermoplastic polymer, which can then be successfully pressed into the cavities of the adjacent bone (Ferguson et al., 2006; Langhoff et al., 2009). In histological animal studies, ultrasonic fusion did not impair bone remodeling, and no signs of inflammatory reaction were noted (Heidenreich et al., 2011; Langhoff et al., 2009; Mai et al., 2007; Pilling et al., 2007). During the liquefaction of the polymer local temperature increases by 6 °C to 11 °C and temperature did not reach the threshold of 47° for bone tissue injury (Augustin et al., 2012; Heidenreich et al., 2011; Langhoff et al., 2009; Mai et al., 2007; Pilling et al., 2007). For the CAP technique used in the present study, the amount of implanted and ultrasound melted PLA material is reduced compared to the BoneWelding technology; therefore, it can be assumed that the temperature during the polymer melting process is not higher. In contrast to the BoneWelding technology, which uses a complete implant system made of PLA, in the CAP technology, only a PLA sleeve is used while implants and screws of any conventional implant system can be used. As the augmentation material for both systems is biodegradable, it is ideally used for temporary fixation (e.g., fractures). Its suitability for long-term fixation still needs further validation. The CAP augmentation technique seems to be a promising tool for improvement of screw anchorage in osteoporotic bone and represents an implant-independent augmentation system. After the borehole is augmented with melted polymer, the conventional screws can be inserted. Additional time for single screw placement (b1 min) required for polymer sleeve insertion, polymer ultrasonification, and second drilling regarding the clinical protocol seems to be acceptably in clinical practice. Some limitations of the present study should be mentioned. First, primary screw fixation strength was only assessed by measuring the insertion torque. The insertion torque has been reported to correlate with the primary screw fixation strength and is widely used in clinical practice allowing for fixation strength estimation (Ryken et al., 1995; Zdeblick et al., 1993). Differences in insertion torque can be attributed to the use of the CAP sleeve augmentation since group comparison was performed in the same bone specimens with no differences in trabecular BMD assessed by micro-CT scan. However, in clinical practice, screws will be subjected to dynamic loading perpendicular and along the screw axis causing screw loosening and pullout. Experiments applying a cyclic loading protocol for the screw with polymer sleeve augmentation for spinal instrumentations and fracture stabilization at various locations with physiological load vectors and magnitudes are planned. Second, the effect of the CAP polymer sleeve augmentation was reported for a relatively short screw size only. Further studies are needed to assess the effect of the technique with the use of longer drill holes and screws. Third, as in every cadaveric study the present study assessed
solely mechanical aspects of the screw augmentation technique and does not include any biological factors such as bone healing and incorporation of the screw. 5. Conclusion The CAP augmentation technique represents a promising method for screw augmentation, which can improve primary screw stability in osteoporotic trabecular bone. The fast melting process of the augmentation material and the compatibility with different screw implant systems make the CAP augmentation technique attractive for implementation into osteoporotic fracture treatment. 6. Conflict of interest Laboratory costs were supported by Thommen Medical AG, Switzerland Acknowledgements The authors wish to thank individuals who donated their bodies and tissues for the advancement of education and research. References Augustin, G., Zigman, T., Davila, S., Udilljak, T., Staroveski, T., Brezak, D., Babic, S., 2012. Cortical bone drilling and thermal osteonecrosis. Clin. Biomech. 27, 313–325. http:// dx.doi.org/10.1016/j.clinbiomech.2011.10.010. Bleibler, F., Konnopka, A., Benzinger, P., Rapp, K., Konig, H.H., 2013. The health burden and costs of incident fractures attributable to osteoporosis from 2010 to 2050 in Germany—a demographic simulation model. Osteoporos. Int. 24, 835–847. http:// dx.doi.org/10.1007/s00198-012-2020-z. R. KA. Bostelmann, Steiger, J.H., Cornelius, J., Schmoelz, W. (2014) Effect of augmentation techniques on the failure of pedicle screws under cranio-caudal cyclic loading. submitted to Eur Spine J Breusch, S.J., Kuhn, K.D., 2003. Bone cements based on polymethylmethacrylate. Der. Orthopade 32, 41–50. http://dx.doi.org/10.1007/s00132-002-0411-0. Bullmann, V., Schmoelz, W., Richter, M., Grathwohl, C., Schulte, T.L., 2010. Revision of cannulated and perforated cement-augmented pedicle screws: a biomechanical study in human cadavers. Spine 35, E932–E939. http://dx.doi.org/10.1097/BRS. 0b013e3181c6ec60. Burge, R., Dawson-Hughes, B., Solomon, D.H., Wong, J.B., King, A., Tosteson, A., 2007. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J. Bone Miner. Res. Off. J. Am. Soc. Bone Miner. Res. 22, 465–475. http:// dx.doi.org/10.1359/jbmr.061113. Ciapetti, G., Granchi, D., Cenni, E., Savarino, L., Cavedagna, D., Pizzoferrato, A., 2000. Cytotoxic effect of bone cements in HL-60 cells: distinction between apoptosis and necrosis. J. Biomed. Mater. Res. 52, 338–345. Erhart, S., Schmoelz, W., Blauth, M., Lenich, A., 2011. Biomechanical effect of bone cement augmentation on rotational stability and pull-out strength of the Proximal Femur Nail Antirotation. Injury 42, 1322–1327. http://dx.doi.org/10.1016/j.injury.2011.04.010. Ferguson, S.J., Weber, U., von Rechenberg, B., Mayer, J., 2006. Enhancing the mechanical integrity of the implant-bone interface with BoneWelding technology: determination
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83 of quasi-static interfacial strength and fatigue resistance. J. Biomed. Mater. Res. B Appl. Biomater. 77, 13–20. http://dx.doi.org/10.1002/jbm.b.30427. Goetzen, M., Nicolino, T., Hofmann-Fliri, L., Blauth, M., Windolf, M., 2014. Metaphyseal screw augmentation of the LISS-PLT plate with polymethylmethacrylate improves angular stability in osteoporotic proximal third tibial fractures: a biomechanical study in human cadaveric tibiae. J. Orthop. Trauma 28, 294–299. http://dx.doi.org/ 10.1097/BOT.0000000000000004. Heidenreich, D., Langhoff, J.D., Nuss, K., Kluge, K., Kampf, K., Zlinsky, K., Hilbe, M., Mayer, J., von Rechenberg, B., 2011. The use of BoneWelding(R) technology in spinal surgery: an experimental study in sheep. Eur. Spine J. 20, 1821–1836. http://dx.doi.org/10. 1007/s00586-011-1799-1. Jung, M.Y., Shin, D.A., Hahn, I.B., Kim, T.G., Huh, R., Chung, S.S., 2010. Serious complication of cement augmentation for damaged pilot hole. Yonsei Med. J. 51, 466–468. http:// dx.doi.org/10.3349/ymj.2010.51.3.466. Langhoff, J.D., Kuemmerle, J.M., Mayer, J., Weber, U., Berra, M., Mueller, J.M., Kaestner, S.B., Zlinszky, K., Auer, J.A., von Rechenberg, B., 2009. An ultrasound assisted anchoring technique (BoneWelding technology) for fixation of implants to bone—a histological pilot study in sheep. Open Orthop. J. 3, 40–47. http://dx. doi.org/10.2174/1874325000903010040. Mai, R., Lauer, G., Pilling, E., Jung, R., Leonhardt, H., Proff, P., Stadlinger, B., Pradel, W., Eckelt, U., Fanghanel, J., Gedrange, T., 2007. Bone welding—a histological evaluation in the jaw. Anm. Anat. 189, 350–355. http://dx.doi.org/10.1016/j.aanat.2007.02.023. McHanwell, S., Brenner, E., Chirculescu, A.R.M., J vMH, Drukker, Mazzotti, G., Pais, D., Paulsen, F., Plaisant, O., MM, Caillaud, Laforet, E., BM, Riedere, J.R., Sanudo, JL, Bueno-Lopez, Donate-Oliver, F., Sprumont, P., Teofilovski-Parapid, G., BJ, Moxham, 2008. The legal and ethical framework governing body donation in Europe—a review of current practice and recommendations for good practice. Eur. J. Anat. 12, 1–24. Pilling, E., Mai, R., Theissig, F., Stadlinger, B., Loukota, R., Eckelt, U., 2007. An experimental in vivo analysis of the resorption to ultrasound activated pins (Sonic weld) and standard biodegradable screws (ResorbX) in sheep. Br. J. Oral Maxillofac. Surg. 45, 447–450. http://dx.doi.org/10.1016/j.bjoms.2006.12.002. Riederer, B.M.B.S., Brenner, E., Bueno-Lopez, J.L., Circulescu, A.R.M., Davies, D.C., DeCaro, R., Gerrits, P.O., McHanwell, S., Pais, D., Paulsen, F., Sendemir, E., Stabile, I., Moxham, B.J., 2012. The legal and ethical framework governing Body Donation in Europe—1st update on current practice. Eur. J. Anat. 16, 1–21.
83
Roderer, G., Scola, A., Schmolz, W., Gebhard, F., Windolf, M., Hofmann-Fliri, L., 2013. Biomechanical in vitro assessment of screw augmentation in locked plating of proximal humerus fractures. Injury 44, 1327–1332. http://dx.doi.org/10.1016/j.injury.2013.05. 008. Ryken, T.C., Clausen, J.D., Traynelis, V.C., Goel, V.K., 1995. Biomechanical analysis of bone mineral density, insertion technique, screw torque, and holding strength of anterior cervical plate screws. J. Neurosurg. 83, 325–329. Sermon, A., Boner, V., Boger, A., Schwieger, K., Boonen, S., Broos, P.L., Richards, R.G., Windolf, M., 2012. Potential of polymethylmethacrylate cement-augmented helical proximal femoral nail antirotation blades to improve implant stability—a biomechanical investigation in human cadaveric femoral heads. J. Trauma Acute Care Surg. 72, E54–E59. Stanczyk, M., van Rietbergen, B., 2004. Thermal analysis of bone cement polymerisation at the cement–bone interface. J. Biomech. 37, 1803–1810. http://dx.doi.org/10.1016/j. jbiomech.2004.03.002. Stubinger, S., Waser, J., Hefti, T., Drechsler, A., Sidler, M., Klein, K., von Rechenberg, B., Schlottig, F., 2014. Evaluation of local cancellous bone amelioration by poly-L-DLlactide copolymers to improve primary stability of dental implants: a biomechanical study in sheep. Clin. Oral Implants Res. http://dx.doi.org/10.1111/clr.12445. Unger, S., Erhart, S., Kralinger, F., Blauth, M., Schmoelz, W., 2012. The effect of in situ augmentation on implant anchorage in proximal humeral head fractures. Injury 43, 1759–1763. http://dx.doi.org/10.1016/j.injury.2012.07.003. Wahnert, D., Lange, J.H., Schulze, M., Gehweiler, D., Kosters, C., Raschke, M.J., 2013. A laboratory investigation to assess the influence of cement augmentation of screw and plate fixation in a simulation of distal femoral fracture of osteoporotic and nonosteoporotic bone. Bone Joint J. 95-B, 1406–1409. http://dx.doi.org/10.1302/0301620X.95B10.31220. Wang, Y., Liu, G., Li, T., Xiao, Y., Han, Q., Xu, R., Li, Y., 2010. Morphometric comparison of the lumbar cancellous bone of sheep, deer, and humans. Commun. Med. 60, 374–379. Zdeblick, T.A., Kunz, D.N., Cooke, M.E., McCabe, R., 1993. Pedicle screw pullout strength. Correlation with insertional torque. Spine 18, 1673–1676.
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Ultrasound melted polymer sleeve for improved screw anchorage in trabecular bone—A novel screw augmentation technique W. Schmoelz a,⁎, R. Mayr a, F. Schlottig b, N. Ivanovic a, R. Hörmann c, J. Goldhahn d a
Department of Trauma Surgery, Medical University of Innsbruck, Innsbruck, Austria Thommen Medical, Neckarsulmstrasse 28, Grenchen 2540, Switzerland Division of Clinical and Functional Anatomy, Department of Anatomy, Medical University of Innsbruck, Innsbruck, Austria d Institute for Biomechanics, ETH Zurich, Switzerland b c
a r t i c l e
i n f o
Article history: Received 2 November 2015 Accepted 15 February 2016 Keywords: Bone amelioration Screw anchorage Augmentation Trabecular bone Insertion torque Primary stability
a b s t r a c t Background: Screw anchorage in osteoporotic bone is still limited and makes treatment of osteoporotic fractures challenging for surgeons. Conventional screws fail in poor bone quality due to loosening at the screw–bone interface. A new technology should help to improve this interface. In a novel constant amelioration process technique, a polymer sleeve is melted by ultrasound in the predrilled screw hole prior to screw insertion. The purpose of this study was to investigate in vitro the effect of the constant amelioration process platform technology on primary screw anchorage. Methods: Fresh frozen femoral heads (n = 6) and vertebrae (n = 6) were used to measure the maximum screw insertion torque of reference and constant amelioration process augmented screws. Specimens were cut in cranio-caudal direction, and the screws (reference and constant amelioration process) were implanted in predrilled holes in the trabecular structure on both sides of the cross section. This allowed the pairwise comparison of insertion torque for constant amelioration process and reference screws (femoral heads n = 18, vertebrae n = 12). Prior to screw insertion, a micro-CT scan was made to ensure comparable bone quality at the screw placement location. Findings: The mean insertion torque for the constant amelioration process augmented screws in both, the femoral heads (44.2 Ncm, SD 14.7) and the vertebral bodies (13.5 Ncm, SD 6.3) was significantly higher than for the reference screws of the femoral heads (31.7 Ncm, SD 9.6, p b 0.001) and the vertebral bodies (7.1 Ncm, SD 4.5, p b 0.001). Interpretation: The interconnection of the melted polymer sleeve with the surrounding trabecular bone in the constant amelioration process technique resulted in a higher screw insertion torque and can improve screw anchorage in osteoporotic trabecular bone. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction Due to demographic changes, the proportion of geriatric trauma patients and osteoporotic fractures is continuously increasing (Bleibler et al., 2013; Burge et al., 2007). Over the last decade, research and implant development focused on novel implant designs for the treatment of osteoporotic fractures. However, screw anchorage in trabecular bone of reduced bone quality is still limited. Insufficient screw anchorage
⁎ Corresponding author at: Department of Trauma Surgery, Medical University of Innsbruck, Innsbruck, Austria. E-mail addresses: [email protected] (W. Schmoelz), [email protected] (R. Mayr), [email protected] (F. Schlottig), [email protected] (N. Ivanovic), [email protected] (R. Hörmann), [email protected] (J. Goldhahn).
http://dx.doi.org/10.1016/j.clinbiomech.2016.02.010 0268-0033/© 2016 Elsevier Ltd. All rights reserved.
causes reduced load bearing capability of the screw increasing the risk of osteosynthesis failure. Screw anchorage in trabecular bone, such as pedicle screws, can be reinforced by cement injection into the adjacent bone around the screw. Biomechanical studies showed increased load bearing capability of screws with cement augmentation in comparison with non-augmented screws (Bostelmann et al., 2014; Bullmann et al., 2010). Cement augmentation of screws is already performed in clinical practice and investigated in experimental studies for several anatomic regions, e.g., spine (Bostelmann et al., 2014; Bullmann et al., 2010), proximal humerus (Roderer et al., 2013; Unger et al., 2012), hip (Erhart et al., 2011; Sermon et al., 2012), distal femur (Wahnert et al., 2013), and proximal tibia (Goetzen et al., 2014). However, this technique has potential disadvantages such as the additional surgical time caused by cement preparation, the excessive heating during curing of polymethylmethacrylat (PMMA) cement leading to bone necrosis, and the risk of cement leakage out of the bone into the
80
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
Fig. 1. The application of the CAP technique to improve screw anchorage includes the following steps: predrilling with 4.3 mm (b), insertion of polymer sleeve (c), attachment of the ultrasound applicator with core guidance into sleeve (d), melting of polymer sleeve by ultrasound (e + f), extraction of ultrasound applicator and re-drilling of borehole with melted sleeve (g), reinforced borehole for screw (h), and screw insertion (i).
surrounding structures (Breusch and Kuhn, 2003; Ciapetti et al., 2000; Jung et al., 2010; Stanczyk and van Rietbergen, 2004). A novel method for screw augmentation represents the constant amelioration process technique (CAP). A polymer sleeve consisting of poly-L-DL-lactide copolymers (PLLAA) gets melted within the borehole by ultrasound. The melted polymer penetrates the trabecular bone cavities, following a rapid solidification. A conventional screw can then be inserted into the reinforced borehole (Fig. 1). The melted polymer within the borehole increases the overall contact surface area between screw and bone. This method can considerably save operating time in comparison with cement screw augmentation due to the fast melting and resolidification of the polymer sleeve and no need of cement preparation. Stubinger et al. (2014) showed in an in vivo sheep model that the CAP technique significantly improved primary stability regarding insertion torque in sheep pelvic bone. However, the cancellous bone of the sheep has more densely packed bone trabeculae, lower porosity, and higher bone mass compared to human cancellous bone (Wang et al., 2010). It is still unknown if the beneficial effect on screw anchorage of the CAP screw augmentation technique is also present in human trabecular bone with reduced bone quality. The aim of the present study was to investigate the effect of an ultrasound melted polymer sleeve on the screw insertion torque in human trabecular bone. 2. Methods 2.1. Specimens In order to obtain trabecular bone densities of different anatomical regions six femoral heads (mean age 74.7 years, SD 9.1) and six vertebral bodies (mean age 79.3 years, SD 6.3) were used for testing. The bodies were donated by people who had given their informed consent for their use for scientific and educational purposes prior to death (McHanwell et al., 2008; Riederer et al., 2012). Specimens were stored at −20 °C and thawed at room temperature 12 h before testing. Specimens were cut in cranio-caudal direction in order to get comparable trabecular bone stock for a paired comparison of the augmented (CAP) and non-augmented reference (Ref) screw. Femoral heads were cut in the frontal plane through the axis of the femoral neck. Vertebrae were cut in the sagittal plane through the spinal process. Glass balls (2 mm
diameter) were glued to the corresponding sites of both cut cross sections serving as landmarks. The location of screw insertion in the cross section was determined by a template aligned to the landmarks. Screws were implanted in both sides of the cut cross sections at the corresponding positions in order to allow a paired comparison (Fig. 2) of CAP and reference screws. In the femoral heads, three screws were placed in each side of the cross sections while only two screws could be placed in each side of the cross section of the vertebrae. This resulted in a total number of 18 paired tests at the femoral head and 12 at the vertebral body with a total of 30 screws with (CAP) and without CAP (Ref) augmentation. 2.2. Screw implantation The same screws were implanted for both groups (SPI Element 5 mm diameter, 9 mm length, Thommen Medical AG, Switzerland). A borehole was drilled with a core diameter of 4.3 mm and a minimum depth of 9 mm prior to screw insertion. For the CAP technique, a polymer sleeve (outer diameter 4.3 mm, 0.3 mm thickness, 5 mm height) consisting of 70:30 PLA (70% L-lactide and 30% DL-lactide (Resomer LR708, Böhringer Ingelheim, Germany) was inserted in the borehole (Fig. 3). A commercially available ultrasound applicator was used (Branson E-150, Branson Ultrasonics SA, Carouge, Switzerland; 20 kHz, amplitude of max. 60 μm = 150 W, set at 50%) and attached to the polymere sleeve. The polymer sleeve was melted by ultrasound and disseminated in the trabecular cavities by pushing the outer casing of the ultrasound applicator into the borehole. The borehole was re-drilled with the 4.3 mm drill, and the screw was inserted in the reinforced borehole (Fig. 1). For the reference screw group, screws were inserted immediately after initial borehole drilling. During screw insertion, the torque was measured with a torque measurement device (Chiropro 980, Bien-Air, Switzerland), and maximum values were recorded. 2.3. Micro-computed tomography All specimens were scanned with a micro-CT (vivaCT 40, Scanco Medical) prior to testing. The following scan parameters were used: energy 70 kV, intensity 114 μA, image matrix of 1024 × 1024 pixels per slice, and integration time 200 ms. Total scanning time per sample
Fig. 2. Exemplary 3D reconstruction of micro-CT scans and the screw placement location in the femoral head (left) and in the vertebra (right).
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
81
was used to investigate the correlation between mechanical parameters and micro-CT measurements for both test groups. The level of significance was set to p b 0.05. 3. Results Fig. 3. Polymer sleeve, diameter 4.3 mm, 0.3 mm wall thickness, and 5 mm height and used screw (SPI Element 5 mm diameter, 9 mm length, Thommen Medical AG, Switzerland).
One screw location in the femoral head and two screw locations in the vertebra had to be excluded from data analysis due to technical difficulties in pilot hole drilling. This left for both, the reference and the CAP augmented group, 17 paired screws in the femoral heads and 10 paired screws in the vertebrae. The mean insertion torque for all CAP augmented screws in both, the femoral heads and the vertebral bodies (32.8 Ncm, SD 19.3) was significantly higher than for the reference screws (22.6 Ncm, SD 14.5; p b 0.001, Fig. 4). In general, the vertebral specimens showed a lower insertion torque and a reduced competence in the micro-CT parameters than the femoral heads (Table 1). Comparing the control with the CAP augmentation showed for the vertebral body screws a mean increase of insertion torque of 111% (SD 56%), while femoral head screws showed a mean increase of 45% (SD 43%). There was a significant negative correlation between the relative increase of insertion torque by the CAP augmentation and the BV/TV in both femoral heads and vertebral bodies (r = −0.51, p b 0.007). None of the structural parameters measured by the micro-CT showed significant differences in bone quality between at the paired locations for the CAP and reference screw. In both groups, the augmented group and the reference group, a significant correlation between the insertion torque and the BV/TV was found (CAP, r = 0.945, p b 0.001; Ref, r = 0.92, p b 0.001). (see Fig. 5.)
Fig. 4. Scatter plot showing the maximal insertion torque with CAP augmentation and without (ref) of all screw pairs. Note: points above the midline indicate that the CAP augmentation increased the insertion torque for the screw pair.
4. Discussion In the present study, the application of CAP polymer sleeve augmentation significantly improved primary stability of the screw in trabecular bone of human specimens. This beneficial effect for the CAP technique on the screw insertion torque was observed in regions of higher and lower trabecular bone density, such as the femoral head and the vertebral body. The results of this study are in concordance with the results of other authors. Stubinger et al. (2014). showed in an animal model that the CAP technique significantly increased the insertion torque in pelvic bone of the sheep. They reported a mean insertion torque of 41.9 Ncm (SD 19.5 Ncm) for screws with CAP augmentation and 23.3 Ncm (SD 13.6 Ncm) for screws without augmentation. Differences regarding trabecular structure and bone density between human and sheep bone made an investigation in human bone necessary. In the present study, the beneficial effect of CAP augmentation was higher in bone with lower trabecular bone density such as the vertebral bone in comparison with the femoral head. This provides promising results for the use of CAP augmentation in osteoporotic fractures. For the CAP technique, biodegradable PDLLA is used for augmentation. PDLLA 70:30 shows a high biocompatibility with an in vivo resorption time in bone of 1 to 3 years. PDLLA implants are routinely used in oral and maxillofacial surgery as also for orthopedic surgery such as interference screws for cruciate ligament reconstruction. Another technique using implants wholly manufactured of biodegradable PDLLA
was 69.5 min for femoral heads and 49.7 min for vertebras. One thousand fifty-four slices of vertebra and one thousand four hundred eighty-three femoral head slices were scanned where each slice was 38 μm thickness. After initial raw data reconstruction, additional 3D transformations and rotations (Scanco Micro-CT software) were carried out to align the specimen scans with the cutting planes and allow an accurate placement of the volumes of interest (VOIs) with the predefined drilling pattern of the screw insertion location. VOIs were selected and evaluated with the trabecular bone morphology evaluation script (Scanco MicroCT software). Drilling holes were represented as 3D cylinders of 164 × 164 × 262 px (approximately 6 × 6 × 10 mm) dimensions. A 3D segmentation of VOI cylinders was done with a Gauss Sigma value of 0.8, Gauss support value of 1, lower threshold value of 220, and upper threshold value of 1000. Results provided information on relative bone volume fraction (BV/TV), connectivity density, trabeculae, and anisotropy for each drilling site. 2.4. Statistical analysis For statistical comparison of the insertion torque of the reference and augmented group, a paired t-test was used. The Pearson correlation
Table 1 Measured maximal insertion torque and parameters on micro-CT scan given in means (SD). Significant differences (p b 0.05) between the CAP and Ref group are indicated with asterisks (*) Femoral heads
Vertebral bodies
All specimens
CAP
Ref
CAP
Ref
CAP
Ref
Insertion torque (Ncm) BV/TV
44.2* (14.7) 0.245 (0.080)
Mean TV (mgHA/ccm)
234.7 (69.4)
31.7 (9.6) 0.251 (0.069) 238.4 (57.9)
13.5* (6.3) 0.063 (0.023) 63.0 (32.7)
7.1 (4.5) 0.054 (0.023) 49.4 (38.8)
32.8* (19.3) 0.177 (0.111) 171.1 (102.4)
22.6 (14.5) 0.178 (0.111) 168.4 (106.0)
82
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83
Fig. 5. A. Scatter plot showing the maximal insertion torque in relation to the BV/TV for screws with CAP augmentation (A) and without augmentation (B). R2—correlation lines indicate positive correlation between insertion torque and BV/TV for both groups.
with ultrasound melting of the anchorage pins (BoneWelding® technology) was investigated in several histological studies on terms of polymer distribution and bone healing. The ultrasonic vibrations causes liquefaction of the thermoplastic polymer, which can then be successfully pressed into the cavities of the adjacent bone (Ferguson et al., 2006; Langhoff et al., 2009). In histological animal studies, ultrasonic fusion did not impair bone remodeling, and no signs of inflammatory reaction were noted (Heidenreich et al., 2011; Langhoff et al., 2009; Mai et al., 2007; Pilling et al., 2007). During the liquefaction of the polymer local temperature increases by 6 °C to 11 °C and temperature did not reach the threshold of 47° for bone tissue injury (Augustin et al., 2012; Heidenreich et al., 2011; Langhoff et al., 2009; Mai et al., 2007; Pilling et al., 2007). For the CAP technique used in the present study, the amount of implanted and ultrasound melted PLA material is reduced compared to the BoneWelding technology; therefore, it can be assumed that the temperature during the polymer melting process is not higher. In contrast to the BoneWelding technology, which uses a complete implant system made of PLA, in the CAP technology, only a PLA sleeve is used while implants and screws of any conventional implant system can be used. As the augmentation material for both systems is biodegradable, it is ideally used for temporary fixation (e.g., fractures). Its suitability for long-term fixation still needs further validation. The CAP augmentation technique seems to be a promising tool for improvement of screw anchorage in osteoporotic bone and represents an implant-independent augmentation system. After the borehole is augmented with melted polymer, the conventional screws can be inserted. Additional time for single screw placement (b1 min) required for polymer sleeve insertion, polymer ultrasonification, and second drilling regarding the clinical protocol seems to be acceptably in clinical practice. Some limitations of the present study should be mentioned. First, primary screw fixation strength was only assessed by measuring the insertion torque. The insertion torque has been reported to correlate with the primary screw fixation strength and is widely used in clinical practice allowing for fixation strength estimation (Ryken et al., 1995; Zdeblick et al., 1993). Differences in insertion torque can be attributed to the use of the CAP sleeve augmentation since group comparison was performed in the same bone specimens with no differences in trabecular BMD assessed by micro-CT scan. However, in clinical practice, screws will be subjected to dynamic loading perpendicular and along the screw axis causing screw loosening and pullout. Experiments applying a cyclic loading protocol for the screw with polymer sleeve augmentation for spinal instrumentations and fracture stabilization at various locations with physiological load vectors and magnitudes are planned. Second, the effect of the CAP polymer sleeve augmentation was reported for a relatively short screw size only. Further studies are needed to assess the effect of the technique with the use of longer drill holes and screws. Third, as in every cadaveric study the present study assessed
solely mechanical aspects of the screw augmentation technique and does not include any biological factors such as bone healing and incorporation of the screw. 5. Conclusion The CAP augmentation technique represents a promising method for screw augmentation, which can improve primary screw stability in osteoporotic trabecular bone. The fast melting process of the augmentation material and the compatibility with different screw implant systems make the CAP augmentation technique attractive for implementation into osteoporotic fracture treatment. 6. Conflict of interest Laboratory costs were supported by Thommen Medical AG, Switzerland Acknowledgements The authors wish to thank individuals who donated their bodies and tissues for the advancement of education and research. References Augustin, G., Zigman, T., Davila, S., Udilljak, T., Staroveski, T., Brezak, D., Babic, S., 2012. Cortical bone drilling and thermal osteonecrosis. Clin. Biomech. 27, 313–325. http:// dx.doi.org/10.1016/j.clinbiomech.2011.10.010. Bleibler, F., Konnopka, A., Benzinger, P., Rapp, K., Konig, H.H., 2013. The health burden and costs of incident fractures attributable to osteoporosis from 2010 to 2050 in Germany—a demographic simulation model. Osteoporos. Int. 24, 835–847. http:// dx.doi.org/10.1007/s00198-012-2020-z. R. KA. Bostelmann, Steiger, J.H., Cornelius, J., Schmoelz, W. (2014) Effect of augmentation techniques on the failure of pedicle screws under cranio-caudal cyclic loading. submitted to Eur Spine J Breusch, S.J., Kuhn, K.D., 2003. Bone cements based on polymethylmethacrylate. Der. Orthopade 32, 41–50. http://dx.doi.org/10.1007/s00132-002-0411-0. Bullmann, V., Schmoelz, W., Richter, M., Grathwohl, C., Schulte, T.L., 2010. Revision of cannulated and perforated cement-augmented pedicle screws: a biomechanical study in human cadavers. Spine 35, E932–E939. http://dx.doi.org/10.1097/BRS. 0b013e3181c6ec60. Burge, R., Dawson-Hughes, B., Solomon, D.H., Wong, J.B., King, A., Tosteson, A., 2007. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J. Bone Miner. Res. Off. J. Am. Soc. Bone Miner. Res. 22, 465–475. http:// dx.doi.org/10.1359/jbmr.061113. Ciapetti, G., Granchi, D., Cenni, E., Savarino, L., Cavedagna, D., Pizzoferrato, A., 2000. Cytotoxic effect of bone cements in HL-60 cells: distinction between apoptosis and necrosis. J. Biomed. Mater. Res. 52, 338–345. Erhart, S., Schmoelz, W., Blauth, M., Lenich, A., 2011. Biomechanical effect of bone cement augmentation on rotational stability and pull-out strength of the Proximal Femur Nail Antirotation. Injury 42, 1322–1327. http://dx.doi.org/10.1016/j.injury.2011.04.010. Ferguson, S.J., Weber, U., von Rechenberg, B., Mayer, J., 2006. Enhancing the mechanical integrity of the implant-bone interface with BoneWelding technology: determination
W. Schmoelz et al. / Clinical Biomechanics 33 (2016) 79–83 of quasi-static interfacial strength and fatigue resistance. J. Biomed. Mater. Res. B Appl. Biomater. 77, 13–20. http://dx.doi.org/10.1002/jbm.b.30427. Goetzen, M., Nicolino, T., Hofmann-Fliri, L., Blauth, M., Windolf, M., 2014. Metaphyseal screw augmentation of the LISS-PLT plate with polymethylmethacrylate improves angular stability in osteoporotic proximal third tibial fractures: a biomechanical study in human cadaveric tibiae. J. Orthop. Trauma 28, 294–299. http://dx.doi.org/ 10.1097/BOT.0000000000000004. Heidenreich, D., Langhoff, J.D., Nuss, K., Kluge, K., Kampf, K., Zlinsky, K., Hilbe, M., Mayer, J., von Rechenberg, B., 2011. The use of BoneWelding(R) technology in spinal surgery: an experimental study in sheep. Eur. Spine J. 20, 1821–1836. http://dx.doi.org/10. 1007/s00586-011-1799-1. Jung, M.Y., Shin, D.A., Hahn, I.B., Kim, T.G., Huh, R., Chung, S.S., 2010. Serious complication of cement augmentation for damaged pilot hole. Yonsei Med. J. 51, 466–468. http:// dx.doi.org/10.3349/ymj.2010.51.3.466. Langhoff, J.D., Kuemmerle, J.M., Mayer, J., Weber, U., Berra, M., Mueller, J.M., Kaestner, S.B., Zlinszky, K., Auer, J.A., von Rechenberg, B., 2009. An ultrasound assisted anchoring technique (BoneWelding technology) for fixation of implants to bone—a histological pilot study in sheep. Open Orthop. J. 3, 40–47. http://dx. doi.org/10.2174/1874325000903010040. Mai, R., Lauer, G., Pilling, E., Jung, R., Leonhardt, H., Proff, P., Stadlinger, B., Pradel, W., Eckelt, U., Fanghanel, J., Gedrange, T., 2007. Bone welding—a histological evaluation in the jaw. Anm. Anat. 189, 350–355. http://dx.doi.org/10.1016/j.aanat.2007.02.023. McHanwell, S., Brenner, E., Chirculescu, A.R.M., J vMH, Drukker, Mazzotti, G., Pais, D., Paulsen, F., Plaisant, O., MM, Caillaud, Laforet, E., BM, Riedere, J.R., Sanudo, JL, Bueno-Lopez, Donate-Oliver, F., Sprumont, P., Teofilovski-Parapid, G., BJ, Moxham, 2008. The legal and ethical framework governing body donation in Europe—a review of current practice and recommendations for good practice. Eur. J. Anat. 12, 1–24. Pilling, E., Mai, R., Theissig, F., Stadlinger, B., Loukota, R., Eckelt, U., 2007. An experimental in vivo analysis of the resorption to ultrasound activated pins (Sonic weld) and standard biodegradable screws (ResorbX) in sheep. Br. J. Oral Maxillofac. Surg. 45, 447–450. http://dx.doi.org/10.1016/j.bjoms.2006.12.002. Riederer, B.M.B.S., Brenner, E., Bueno-Lopez, J.L., Circulescu, A.R.M., Davies, D.C., DeCaro, R., Gerrits, P.O., McHanwell, S., Pais, D., Paulsen, F., Sendemir, E., Stabile, I., Moxham, B.J., 2012. The legal and ethical framework governing Body Donation in Europe—1st update on current practice. Eur. J. Anat. 16, 1–21.
83
Roderer, G., Scola, A., Schmolz, W., Gebhard, F., Windolf, M., Hofmann-Fliri, L., 2013. Biomechanical in vitro assessment of screw augmentation in locked plating of proximal humerus fractures. Injury 44, 1327–1332. http://dx.doi.org/10.1016/j.injury.2013.05. 008. Ryken, T.C., Clausen, J.D., Traynelis, V.C., Goel, V.K., 1995. Biomechanical analysis of bone mineral density, insertion technique, screw torque, and holding strength of anterior cervical plate screws. J. Neurosurg. 83, 325–329. Sermon, A., Boner, V., Boger, A., Schwieger, K., Boonen, S., Broos, P.L., Richards, R.G., Windolf, M., 2012. Potential of polymethylmethacrylate cement-augmented helical proximal femoral nail antirotation blades to improve implant stability—a biomechanical investigation in human cadaveric femoral heads. J. Trauma Acute Care Surg. 72, E54–E59. Stanczyk, M., van Rietbergen, B., 2004. Thermal analysis of bone cement polymerisation at the cement–bone interface. J. Biomech. 37, 1803–1810. http://dx.doi.org/10.1016/j. jbiomech.2004.03.002. Stubinger, S., Waser, J., Hefti, T., Drechsler, A., Sidler, M., Klein, K., von Rechenberg, B., Schlottig, F., 2014. Evaluation of local cancellous bone amelioration by poly-L-DLlactide copolymers to improve primary stability of dental implants: a biomechanical study in sheep. Clin. Oral Implants Res. http://dx.doi.org/10.1111/clr.12445. Unger, S., Erhart, S., Kralinger, F., Blauth, M., Schmoelz, W., 2012. The effect of in situ augmentation on implant anchorage in proximal humeral head fractures. Injury 43, 1759–1763. http://dx.doi.org/10.1016/j.injury.2012.07.003. Wahnert, D., Lange, J.H., Schulze, M., Gehweiler, D., Kosters, C., Raschke, M.J., 2013. A laboratory investigation to assess the influence of cement augmentation of screw and plate fixation in a simulation of distal femoral fracture of osteoporotic and nonosteoporotic bone. Bone Joint J. 95-B, 1406–1409. http://dx.doi.org/10.1302/0301620X.95B10.31220. Wang, Y., Liu, G., Li, T., Xiao, Y., Han, Q., Xu, R., Li, Y., 2010. Morphometric comparison of the lumbar cancellous bone of sheep, deer, and humans. Commun. Med. 60, 374–379. Zdeblick, T.A., Kunz, D.N., Cooke, M.E., McCabe, R., 1993. Pedicle screw pullout strength. Correlation with insertional torque. Spine 18, 1673–1676.