Variation in bone response to the placement of percutaneous osseointegrated endoprostheses: A 24-month follow-up in sheep

Autoři: Sujee Jeyapalina aff001;  James Peter Beck aff001;  Alex Drew aff004;  Roy D. Bloebaum aff003;  Kent N. Bachus aff001
Působiště autorů: Research, Department of Veterans Affairs Medical Center, Salt Lake City, Utah, United States of America aff001;  Division of Plastic Surgery, Department of Surgery, University of Utah School of Medicine, The University of Utah, Salt Lake City, Utah, United States of America aff002;  Department of Orthopaedics, University of Utah Orthopaedic Center, University of Utah School of Medicine, Salt Lake City, Utah, United States of America aff003;  Department of Bioengineering, University of Utah College of Engineering, The University of Utah, Salt Lake City, Utah, United States of America aff004;  Orthopaedic Research Laboratories, Department of Orthopaedics, University of Utah School of Medicine, Salt Lake City, Utah, United States of America aff005;  Bone and Joint Research Laboratory, Department of Veterans Affairs Medical Center, Salt Lake City, Utah, United States of America aff006
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Percutaneous osseointegrated (OI) devices for amputees are metallic endoprostheses, that are surgically implanted into the residual stump bone and protrude through the skin, allowing attachment of an exoprosthetic limb. In contrast to standard socket suspension systems, these percutaneous OI devices provide superior attachment platforms for artificial limbs. However, bone adaptation, which includes atrophy and/or hypertrophy along the extent of the host bone-endoprosthetic interface, is seen clinically and depends upon where along the bone the device ultimately transfers loading forces to the skeletal system. The goal of this study was to determine if a percutaneous OI device, designed with a porous coated distal region and an end-loading collar, could promote and maintain stable bone attachment. A total of eight, 18 to 24-month old, mixed-breed sheep were surgically implanted with a percutaneous OI device. For 24-months, the animals were allowed to bear weight as tolerated and were monitored for signs of bone remodelling. At necropsy, the endoprosthesis and the surrounding tissues were harvested, radiographically imaged, and histomorphometrically analyzed to determine the periprosthetic bone adaptation in five animals. Bone growth into the porous coating was achieved in all five animals. Serial radiographic data showed stress-shielding related bone adaptation occurs based on the placement of the endoprosthetic stem. When collar placement and achieved end-bearing against the transected bone, distal bone conservation/hypertrophy was observed. The results supported the use of a distally loading and distally porous coated percutaneous OI device to achieve distal host bone maintenance.

Klíčová slova:

Bone imaging – Bone remodeling – Coatings – Medical devices and equipment – Prosthetics – Sheep – Bone resorption – osteogenesis imperfecta


1. Al Muderis M, Khemka A, Lord SJ, Van de Meent H, Frolke JP. Safety of Osseointegrated Implants for Transfemoral Amputees: A Two-Center Prospective Cohort Study. J Bone Joint Surg Am. 2016;98(11):900–9. doi: 10.2106/JBJS.15.00808 27252434.

2. Branemark R, Berlin O, Hagberg K, Bergh P, Gunterberg B, Rydevik B. A novel osseointegrated percutaneous prosthetic system for the treatment of patients with transfemoral amputation: A prospective study of 51 patients. Bone Joint J. 2014;96-B(1):106–13. doi: 10.1302/0301-620X.96B1.31905 24395320.

3. Hagberg K, Branemark R. One hundred patients treated with osseointegrated transfemoral amputation prostheses—rehabilitation perspective. J Rehabil Res Dev. 2009;46(3):331–44. Epub 2009/08/14. 19675986.

4. Juhnke DL, Beck JP, Jeyapalina S, Aschoff HH. Fifteen years of experience with Integral-Leg-Prosthesis: Cohort study of artificial limb attachment system. J Rehabil Res Dev. 2015;52(4):407–20. Epub 2015/09/09. doi: 10.1682/JRRD.2014.11.0280 26348827.

5. Van de Meent H, Hopman MT, Frolke JP. Walking ability and quality of life in subjects with transfemoral amputation: a comparison of osseointegration with socket prostheses. Arch Phys Med Rehabil. 2013;94(11):2174–8. doi: 10.1016/j.apmr.2013.05.020 23774380.

6. Muderis MA, Tetsworth K, Khemka A, Wilmot S, Bosley B, Lord SJ, et al. The Osseointegration Group of Australia Accelerated Protocol (OGAAP-1) for two-stage osseointegrated reconstruction of amputated limbs. Bone Joint J. 2016;98-B(7):952–60. Epub 2016/07/02. doi: 10.1302/0301-620X.98B7.37547 27365474.

7. Branemark RP, Hagberg K, Kulbacka-Ortiz K, Berlin O, Rydevik B. Osseointegrated Percutaneous Prosthetic System for the Treatment of Patients With Transfemoral Amputation: A Prospective Five-year Follow-up of Patient-reported Outcomes and Complications. J Am Acad Orthop Surg. 2018. Epub 2018/12/15. doi: 10.5435/JAAOS-D-17-00621 30550396.

8. Aschoff HH, Kennon RE, Keggi JM, Rubin LE. Transcutaneous, distal femoral, intramedullary attachment for above-the-knee prostheses: an endo-exo device. J Bone Joint Surg Am. 2010;92(Suppl 2):180–6. Epub 2010/12/09. doi: 92/Supplement_2/180 [pii] doi: 10.2106/JBJS.J.00806 21123601.

9. Hoffmeister T, Schwarze F, Aschoff HH. [The endo-exo prosthesis treatment concept: Improvement in quality of life after limb amputation]. Unfallchirurg. 2017;120(5):371–7. Epub 2017/05/05. doi: 10.1007/s00113-017-0350-1 28470463.

10. Nebergall A, Bragdon C, Antonellis A, Karrholm J, Branemark R, Malchau H. Stable fixation of an osseointegated implant system for above-the-knee amputees: Titel RSA and radiographic evaluation of migration and bone remodeling in 55 cases. Acta Orthopaedica. 2012;83(2):121–8. Epub 2012/04/12. doi: 10.3109/17453674.2012.678799 22489885; PubMed Central PMCID: PMC3339524.

11. Aschoff HH. The endo-exo-femoral prosthesis. Traumatology and Orthopaedic Surgery of Russia. 2011;1(59):101–5.

12. Shelton TJ, Beck JP, Bloebaum RD, Bachus KN. Percutaneous osseointegrated prostheses for amputees: Limb compensation in a 12-month ovine model. J Biomech. 2011;44(15):2601–6. Epub 2011/09/17. doi: S0021-9290(11)00580-X [pii] doi: 10.1016/j.jbiomech.2011.08.020 21920525.

13. Jeyapalina S, Beck JP, Bachus KN, Bloebaum RD. Cortical bone response to the presence of load-bearing percutaneous osseointegrated prostheses. Anatomical Record. 2012;295(9):1437–45. Epub 2012/07/19. doi: 10.1002/ar.22533 22807281.

14. Jeyapalina S, Beck JP, Bachus KN, Williams DL, Bloebaum RD. Efficacy of a porous-structured titanium subdermal barrier for preventing infection in percutaneous osseointegrated prostheses. J Orthop Res. 2012;30(8):1304–11. Epub 2012/02/02. doi: 10.1002/jor.22081 22294380.

15. Jeyapalina S, Beck JP, Bloebaum RD, Bachus KN. Progression of bone ingrowth and attachment strength for stability of percutaneous osseointegrated prostheses. Clin Orthop Relat Res. 2014;472(10):2957–65. Epub 2013/11/22. doi: 10.1007/s11999-013-3381-0 24258685; PubMed Central PMCID: PMC4160472.

16. Jeyapalina S, Beck JP, Bachus KN, Chalayon O, Bloebaum RD. Radiographic evaluation of bone adaptation adjacent to percutaneous osseointegrated prostheses in a sheep model. Clin Orthop Relat Res. 2014;472(10):2966–77. Epub 2014/02/22. doi: 10.1007/s11999-014-3523-z 24557934; PubMed Central PMCID: PMC4160482.

17. Willie BM, Bloebaum RD, Bireley WR, Bachus KN, Hofmann AA. Determining relevance of a weight-bearing ovine model for bone ingrowth assessment. J Biomed Mater Res A. 2004;69A(3):567–76. Epub 2004/05/06. doi: 10.1002/jbm.a.30038 15127404.

18. Duda GN, Eckert-Hubner K, Sokiranski R, Kreutner A, Miller R, Claes L. Analysis of inter-fragmentary movement as a function of musculoskeletal loading conditions in sheep. J Biomech. 1998;31(3):201–10. doi: 10.1016/s0021-9290(97)00127-9 9645534.

19. Jeyapalina S, Beck JP, Agarwal J, Bachus KN. A 24-month evaluation of a percutaneous osseointegrated limb-skin interface in an ovine amputation model. J Mater Sci Mater Med. 2017;28(11):179. Epub 2017/10/06. doi: 10.1007/s10856-017-5980-x 28980174.

20. Holt BM, Bachus KN, Beck JP, Bloebaum RD, Jeyapalina S. Immediate post-implantation skin immobilization decreases skin regression around percutaneous osseointegrated prosthetic implant systems. J Biomed Mater Res A. 2013;101(7):2075–82. Epub 2013/01/03. doi: 10.1002/jbm.a.34510 23281016.

21. Jeyapalina S, Beck JP, Bachus KN, Williams DL, Bloebaum RD. Efficacy of a porous-structured titanium subdermal barrier for preventing infection in percutaneous osseointegrated prostheses. J Orthop Res. 2012;30(8):1304–11. Epub 2012/02/02. doi: 10.1002/jor.22081 22294380.

22. Emmanual J, Hornbeck C, Bloebaum RD. A polymethyl methacrylate method for large specimens of mineralized bone with implants. Stain Technology. 1987;62(6):401–10. Epub 1987/11/01. doi: 10.3109/10520298709108030 3433310.

23. Tsikandylakis G, Berlin O, Branemark R. Implant survival, adverse events, and bone remodeling of osseointegrated percutaneous implants for transhumeral amputees. Clin Orthop Relat Res. 2014;472(10):2947–56. doi: 10.1007/s11999-014-3695-6 24879569; PubMed Central PMCID: PMC4160502.

24. Tillander J, Hagberg K, Berlin O, Hagberg L, Branemark R. Osteomyelitis Risk in Patients With Transfemoral Amputations Treated With Osseointegration Prostheses. Clin Orthop Relat Res. 2017;475(12):3100–8. Epub 2017/09/25. doi: 10.1007/s11999-017-5507-2 28940152; PubMed Central PMCID: PMC5670076.

25. Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Sloof TJ. Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech. 1987;20(11/12):1135–50.

26. Wolff J. The Law of Bone Remodelling (Das Gesetz der Transformation der Knochen, Hirschwald). Berlin: Springer-Verlag; 1892. 3–100 p.

27. Wolff J. The classic: On the theory of fracture healing. 1873. Clin Orthop Relat Res. 2010;468(4):1052–5. Epub 2010/02/11. doi: 10.1007/s11999-010-1240-9 20146037; PubMed Central PMCID: PMC2835578.

28. Ruff C, Holt B, Trinkaus E. Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol. 2006;129(4):484–98. doi: 10.1002/ajpa.20371 16425178.

29. Mont MA, Hungerford DS. Proximally coated ingrowth prostheses. A review. Clin Orthop Relat Res. 1997;(344):139–49. Epub 1997/12/31. 9372766.

30. Cristofolini L. A critical analysis of stress shielding evaluation of hip prostheses. Crit Rev Biomed Eng. 1997;25(4–5):409–83. Epub 1997/01/01. 9505138.

31. Haket LM, Frolke JP, Verdonschot N, Tomaszewski PK, van de Meent H. Periprosthetic cortical bone remodeling in patients with an osseointegrated leg prosthesis. J Orthop Res. 2016. Epub 2016/07/29. doi: 10.1002/jor.23376 27467497.

32. Stenlund P, Murase K, Stalhandske C, Lausmaa J, Palmquist A. Understanding mechanisms and factors related to implant fixation; a model study of removal torque. J Mech Behav Biomed Mater. 2014;34:83–92. Epub 2014/02/26. doi: 10.1016/j.jmbbm.2014.02.006 24566379.

33. Spector M. Bone ingrowth into Porous Metals. In: Williams DF, editor. Biocompatibilty of Orthopedic Implants. 2. Boca Raton: CRC Press; 1982. p. 89–128.

34. Zippel H. Julius Wolff and the law of bone remodelling. In: Regling G, editor. Wolff's Law and Connective Tissue Regulation. Berlin: Walter de Gruyter; 1992. p. 1–12.

35. Frost HM. From Wolff's Law to the Utah paradigm: insights about bone physiology and its clinical applications. Anatomical Record. 2001;262(4):398–419. doi: 10.1002/ar.1049 11275971.

36. Chamay A, Tschantz P. Mechanical influences in bone remodeling. Experimental research on Wolff's Law. J Biomech. 1972;5:173–80. doi: 10.1016/0021-9290(72)90053-x 5020948

37. Werner CM, Jacob HA, Ramseier LE, Favre P, Exner GU. Uncemented short-length diaphyseal segmental replacement prosthesis fixation—finite element analysis and long-term results. J Orthop Res. 2005;23(5):1065–72. Epub 2005/05/14. doi: S0736-0266(05)00072-0 [pii] doi: 10.1016/j.orthres.2004.12.013 15890487.

38. Bini SA, Johnston JO, Martin DL. Compliant prestress fixation in tumor prostheses: interface retrieval data. Orthopedics. 2000;23(7):707–11; discussion 11–2. 10917246.

39. Avedian RS, Goldsby RE, Kramer MJ, O'Donnell RJ. Effect of chemotherapy on initial compressive osseointegration of tumor endoprostheses. Clin Orthop Relat Res. 2007;459:48–53. Epub 2007/06/05. doi: 10.1097/BLO.0b013e3180514c66 00003086-200706000-00009 [pii]. 17545758.

40. Pedtke AC, Wustrack RL, Fang AS, Grimer RJ, O'Donnell RJ. Aseptic failure: how does the Compress((R)) implant compare to cemented stems? Clinical orthopaedics and related research. 2012;470(3):735–42. Epub 2011/11/03. doi: 10.1007/s11999-011-2159-5 22045069; PubMed Central PMCID: PMC3270164.

41. Kramer MJ, Tanner BJ, Horvai AE, O'Donnell RJ. Compressive osseointegration promotes viable bone at the endoprosthetic interface: retrieval study of Compress implants. Int Orthop. 2008;32(5):567–71. Epub 2007/06/20. doi: 10.1007/s00264-007-0392-z 17576554; PubMed Central PMCID: PMC2551719.

42. Healey JH, Morris CD, Athanasian EA, Boland PJ. Compress knee arthroplasty has 80% 10-year survivorship and novel forms of bone failure. Clinical orthopaedics and related research. 2013;471(3):774–83. Epub 2012/10/12. doi: 10.1007/s11999-012-2635-6 23054526; PubMed Central PMCID: PMC3563794.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden