Biomaterials for reconstruction of cranial defects
Tao SONG1,Zhi-Ye QIU2,3,Fu-Zhai CUI2,*()
1. Department of Neurosurgery, Shandong Provincial Hospital, Jinan 250021, China 2. School of Materials Science and Engineering, Tsinghua University, Beijing 100084, China 3. Beijing Allgens Medical Science and Technology Co., Ltd., No. 1 Disheng East Road, Yizhuang Economic and Technological Development Zone, Beijing 100176, China
Reconstruction of cranial defect is commonly performed in neurosurgical operations. Many materials have been employed for repairing cranial defects. In this paper, materials used for cranioplasty, including autografts, allografts, and synthetic biomaterials are comprehensively reviewed. This paper also gives future perspective of the materials and development trend of manufacturing process for cranioplasty implants.
good biomechanical properties, radiolucent, heat resistant
high cost, lack of osteointegration, infection, inflammation
Mineralized collagen
biomimetic chemical compositions and microstructure, good biocompatibility, osteoconductivity, bioresorbable, radiolucent
low mechanical strength
Tab.1
Fig.1
1
Wilson D B. Embryonic development of the head and neck: Part 5, the brain and cranium. Head & Neck Surgery, 1980, 2(4): 312–320
2
Hayashi S, Kim J H, Hwang S E, . Interface between intramembranous and endochondral ossification in human foetuses. Folia Morphologica, 2014, 73(2): 199–205
3
Govindarajan V, Overbeek P A. FGF9 can induce endochondral ossification in cranial mesenchyme. BMC Developmental Biology, 2006, 6(1): 7
4
Opperman L A. Cranial sutures as intramembranous bone growth sites. Developmental Dynamics, 2000, 219(4): 472–485
5
Gagan J R, Tholpady S S, Ogle R C. Cellular dynamics and tissue interactions of the dura mater during head development. Birth Defects Research Part C: Embryo Today: Reviews, 2007, 81(4): 297–304
6
Santaolalla-Montoya F, Martinez-Ibargüen A, Sánchez-Fernández J M, . Principles of cranial base ossification in humans and rats. Acta Oto-Laryngologica, 2012, 132(4): 349–354
7
Sanan A, Haines S J. Repairing holes in the head: a history of cranioplasty. Neurosurgery, 1997, 40(3): 588–603
8
Andrushko V A, Verano J W. Prehistoric trepanation in the Cuzco region of Peru: a view into an ancient Andean practice. American Journal of Physical Anthropology, 2008, 137(1): 4–13
9
Eftekhar B, Dadmehr M, Ghodsi M, . Cranial trephination in ancient Iran. Case illustration. Journal of Neurosurgery, 2007, 106(1 Suppl): 70
10
Ghannaee A M, Fakharian E, Sarbandi F. Ancient legacy of cranial surgery. Archives of Trauma Research, 2012, 1(2): 72–74
11
Erdal Y S, Erdal Ö D. A review of trepanations in Anatolia with new cases. International Journal of Osteoarchaeology, 2011, 21(5): 505–534
12
Aciduman A, Belen D. The earliest document regarding the history of cranioplasty from the Ottoman era. Surgical Neurology, 2007, 68(3): 349–352
13
Missios S. Hippocrates, Galen, and the uses of trepanation in the ancient classical world. Neurosurgical Focus, 2007, 23(1): 1–9
14
Shah A M, Jung H, Skirboll S. Materials used in cranioplasty: a history and analysis. Neurosurgical Focus, 2014, 36(4): E19
15
Spetzger U, Vougioukas V, Schipper J. Materials and techniques for osseous skull reconstruction. Minimally Invasive Therapy & Allied Technologies, 2010, 19(2): 110–121
16
Aydin S, Kucukyuruk B, Abuzayed B, . Cranioplasty: Review of materials and techniques. Journal of Neurosciences in Rural Practice, 2011, 2(2): 162–167
17
Prolo D J, Burres K P, McLaughlin W T, . Autogenous skull cranioplasty: fresh and preserved (frozen), with consideration of the cellular response. Neurosurgery, 1979, 4(1): 18–29
18
Viterbo F, Palhares A, Modenese E. Cranioplasty: the autograft option. The Journal of Craniofacial Surgery, 1995, 6(1): 80–82
19
Worm P V, Ferreira N P, Faria M B, . Comparative study between cortical bone graft versus bone dust for reconstruction of cranial burr holes. Surgical Neurology International, 2010, 1(1): 91
20
Greene A K, Mulliken J B, Proctor M R, . Pediatric cranioplasty using particulate calvarial bone graft. Plastic and Reconstructive Surgery, 2008, 122(2): 563–571
21
Matsumoto K, Kohmura E, Kato A, . Restoration of small bone defects at craniotomy using autologous bone dust and fibrin glue. Surgical Neurology, 1998, 50(4): 344–346
22
Cokluk C, Senel A, Iyigün O, . Reconstruction of burr hole by using autologous button-shaped graft harvested from inner table of craniotomy flap: technique and clinical result. Minimally Invasive Neurosurgery, 2003, 46(6): 372–373
23
Boström S, Kourtopoulos H, Nilsson I. Reconstruction of craniotomy burr-holes with autologous bone blugs made by a new hole-saw. Acta Neurochirurgica, 1990, 105(3−4): 132–134
24
Beekmans S J, Don Griot J P, Mulder J W. Split rib cranioplasty for aplasia cutis congenita and traumatic skull defects: more than 30 years of follow-up. The Journal of Craniofacial Surgery, 2007, 18(3): 594–597
25
Taggard D A, Menezes A H. Successful use of rib grafts for cranioplasty in children. Pediatric Neurosurgery, 2001, 34(3): 149–155
26
Munro I R, Guyuron B. Split-rib cranioplasty. Annals of Plastic Surgery, 1981, 7(5): 341–346
27
Rosenthal A H, Buchman S R. Volume maintenance of inlay bone grafts in the craniofacial skeleton. Plastic and Reconstructive Surgery, 2003, 112(3): 802–811
28
Lee J C, Kleiber G M, Pelletier A T, . Autologous immediate cranioplasty with vascularized bone in high-risk composite cranial defects. Plastic and Reconstructive Surgery, 2013, 132(4): 967–975
29
Tubbs R S, Loukas M, Shoja M M, . Use of autologous scapula for cranioplasty: cadaveric feasibility study. Child’s Nervous System, 2008, 24(8): 955–959
30
Woodroffe H L W. The reparation of cranial defects by means of cartilaginous grafts. British Journal of Surgery, 1917, 5(17): 42–52
31
Munroe A R. The operation of cartilage-cranioplasty. Canadian Medical Association Journal, 1924, 14(1): 47–49
32
Feroze A H, Walmsley G G, Choudhri O, . Evolution of cranioplasty techniques in neurosurgery: historical review, pediatric considerations, and current trends. Journal of Neurosurgery, 2015 (in press)
33
Grant F C, Norcross N C. Repair of cranial defects by cranioplasty. Annals of Surgery, 1939, 110(4): 488–512
34
Prolo D J, Gutierrez R V, DeVine J S, . Clinical utility of allogeneic skull discs in human craniotomy. Neurosurgery, 1984, 14(2): 183–186
35
Cornioly C E. A propos de cranioplastie. Revue Medicale de la Suisse Romande, 1929, 49: 677–693
36
Woodhall B, Spurling R G. Tantalum cranioplasty for war wounds of the skull. Annals of Surgery, 1945, 121(5): 649–668
37
Bonfield C M, Kumar A R, Gerszten P C. The history of military cranioplasty. Neurosurgical Focus, 2014, 36(4): E18
38
Flanigan P, Kshettry V R, Benzel E C. World War II, tantalum, and the evolution of modern cranioplasty technique. Neurosurgical Focus, 2014, 36(4): E22
39
Murtagh F, Scott M, Wycis H T. Stainless steel cranioplasty. American Journal of Surgery, 1956, 92(3): 393–402
40
Boldrey E. Stainless steel wire-mesh in the repair of small cranial defects. Annals of Surgery, 1945, 121(6): 821–825
41
Simpson D. Titanium in cranioplasty. Journal of Neurosurgery, 1965, 22(3): 292–293
42
Gordon D S, Blair G A. Titanium cranioplasty. British Medical Journal, 1974, 2(5917): 478–481
43
Cabraja M, Klein M, Lehmann T N. Long-term results following titanium cranioplasty of large skull defects. Neurosurgical Focus, 2009, 26(6): E10
44
Marbacher S, Andres R H, Fathi A R, . Primary reconstruction of open depressed skull fractures with titanium mesh. The Journal of Craniofacial Surgery, 2008, 19(2): 490–495
45
Wind J J, Ohaegbulam C, Iwamoto F M, . Immediate titanium mesh cranioplasty for treatment of postcraniotomy infections. World Neurosurgery, 2013, 79(1): 207.e11–207.e13
46
Sunderland I R, Edwards G, Mainprize J, . A technique for intraoperative creation of patient-specific titanium mesh implants. Plast Surg (Oakv), 2015, 23(2): 95–99
47
Lau D, McDermott M W. A method for combining thin and thick malleable titanium mesh in the repair of cranial defects. Cureus, 2015, 7(5): e267
48
Hill C S, Luoma A M V, Wilson S R, . Titanium cranioplasty and the prediction of complications. British Journal of Neurosurgery, 2012, 26(6): 832–837
49
Mukherjee S, Thakur B, Haq I, . Complications of titanium cranioplasty — a retrospective analysis of 174 patients. Acta Neurochirurgica, 2014, 156(5): 989–998
50
Williams L R, Fan K F, Bentley R P. Custom-made titanium cranioplasty: early and late complications of 151 cranioplasties and review of the literature. International Journal of Oral and Maxillofacial Surgery, 2015, 44(5): 599–608
51
Black S P. Reconstruction of the supraorbital ridge using aluminum. Surgical Neurology, 1978, 9(2): 121–128
52
Black S P W, Kam C C M, Sights W P. Aluminum cranioplasty. Journal of Neurosurgery, 1968, 29(5): 562–564
53
Gage E L. Vitallium cranioplasty. The West Virginia Medical Journal, 1971, 67(11): 325–335
54
Kobayashi S, Hara H, Okudera H, . Usefulness of ceramic implants in neurosurgery. Neurosurgery, 1987, 21(5): 751–755
55
Shirai T, Tsuchiya H, Terauchi R, . Treatment of a simple bone cyst using a cannulated hydroxyapatite pin. Medicine, 2015, 94(25): e1027
56
Yoshikawa H, Tamai N, Murase T, . Interconnected porous hydroxyapatite ceramics for bone tissue engineering. Journal of the Royal Society Interface, 2009, 6(Suppl 3): S341–S348
57
Guo W G, Qiu Z Y, Cui H, . Strength and fatigue properties of three-step sintered dense nanocrystal hydroxyapatite bioceramics. Frontiers of Materials Science, 2013, 7(2): 190–195
58
Pompili A, Caroli F, Carpanese L, . Cranioplasty performed with a new osteoconductive osteoinducing hydroxyapatite-derived material. Journal of Neurosurgery, 1998, 89(2): 236–242
59
Zide M F, Kent J N, Machado L. Hydroxylapatite cranioplasty directly over dura. Journal of Oral and Maxillofacial Surgery, 1987, 45(6): 481–486
60
Waite P D, Morawetz R B, Zeiger H E, . Reconstruction of cranial defects with porous hydroxylapatite blocks. Neurosurgery, 1989, 25(2): 214–217
61
Yamashima T. Cranioplasty with hydroxylapatite ceramic plates that can easily be trimmed during surgery. Acta Neurochirurgica, 1989, 96(3−4): 149–153
62
Staffa G, Nataloni A, Compagnone C, . Custom made cranioplasty prostheses in porous hydroxyapatite using 3D design techniques: 7 years experience in 25 patients. Acta Neurochirurgica, 2007, 149(2): 161–170
63
Staffa G, Barbanera A, Faiola A, . Custom made bioceramic implants in complex and large cranial reconstruction: a two-year follow-up. Journal of Cranio-Maxillo-Facial Surgery, 2012, 40(3): e65–e70
64
Stefini R, Zanotti B, Nataloni A, . The efficacy of custom-made porous hydroxyapatite prostheses for cranioplasty: evaluation of postmarketing data on 2697 patients. Journal of Applied Biomaterials & Functional Materials, 2015, 13(2): e136–e144
65
Yamashima T. Modern cranioplasty with hydroxylapatite ceramic granules, buttons, and plates. Neurosurgery, 1993, 33(5): 939–940
66
Marbacher S, Andereggen L, Erhardt S, . Intraoperative template-molded bone flap reconstruction for patient-specific cranioplasty. Neurosurgical Review, 2012, 35(4): 527–535
67
Fischer C M, Burkhardt J K, Sarnthein J, . Aesthetic outcome in patients after polymethyl-methacrylate (PMMA) cranioplasty − a questionnaire-based single-centre study. Neurological Research, 2012, 34(3): 281–285
68
Ronderos J F, Wiles D A, Ragan F A, . Cranioplasty using gentamicin-loaded acrylic cement: a test of neurotoxicity. Surgical Neurology, 1992, 37(5): 356–360
69
Pochon J P, Klöti J. Cranioplasty for acquired skull defects in children — a comparison between autologous material and methylmethacrylate 1974−1990. European Journal of Pediatric Surgery, 1991, 1(4): 199–201
70
Caro-Osorio E, Garza-Ramos R D, Martínez-Sánchez S R, . Cranioplasty with polymethylmethacrylate prostheses fabricated by hand using original bone flaps: Technical note and surgical outcomes. Surgical Neurology International, 2013, 4(1): 136
71
Gladstone H B, McDermott M W, Cooke D D. Implants for cranioplasty. Otolaryngologic Clinics of North America, 1995, 28(2): 381–400
72
Lara W C, Schweitzer J, Lewis R P, . Technical considerations in the use of polymethylmethacrylate in cranioplasty. Journal of Long-Term Effects of Medical Implants, 1998, 8(1): 43–53
73
Huang G J, Zhong S, Susarla S M, . Craniofacial reconstruction with poly(methyl methacrylate) customized cranial implants. The Journal of Craniofacial Surgery, 2015, 26(1): 64–70
74
Rotaru H, Stan H, Florian I S, . Cranioplasty with custom-made implants: analyzing the cases of 10 patients. Journal of Oral and Maxillofacial Surgery, 2012, 70(2): e169–e176
75
Fathi A R, Marbacher S, Lukes A. Cost-effective patient-specific intraoperative molded cranioplasty. The Journal of Craniofacial Surgery, 2008, 19(3): 777–781
76
Jaberi J, Gambrell K, Tiwana P, . Long-term clinical outcome analysis of poly-methyl-methacrylate cranioplasty for large skull defects. Journal of Oral and Maxillofacial Surgery, 2013, 71(2): e81–e88
77
Moreira-Gonzalez A, Jackson I T, Miyawaki T, . Clinical outcome in cranioplasty: critical review in long-term follow-up. The Journal of Craniofacial Surgery, 2003, 14(2): 144–153
78
Al-Tamimi Y Z, Sinha P, Trivedi M, . Comparison of acrylic and titanium cranioplasty. British Journal of Neurosurgery, 2012, 26(4): 510–513
79
Pikis S, Goldstein J, Spektor S. Potential neurotoxic effects of polymethylmethacrylate during cranioplasty. Journal of Clinical Neuroscience, 2015, 22(1): 139–143
80
Wu J, Xu S, Qiu Z, . Comparison of human mesenchymal stem cells proliferation and differentiation on poly(methyl methacrylate) bone cements with and without mineralized collagen incorporation. Journal of Biomaterials Applications, 2015,
https://doi.org/doi: 10.1177/0885328215582112
81
Jiang H J, Xu J, Qiu Z Y, . Mechanical properties and cytocompatibility improvement of vertebroplasty PMMA bone cements by incorporating mineralized collagen. Materials, 2015, 8(5): 2616–2634
82
Kuemmerle J M, Oberle A, Oechslin C, . Assessment of the suitability of a new brushite calcium phosphate cement for cranioplasty − an experimental study in sheep. Journal of Cranio-Maxillo-Facial Surgery, 2005, 33(1): 37–44
83
Pang D, Tse H H, Zwienenberg-Lee M, . The combined use of hydroxyapatite and bioresorbable plates to repair cranial defects in children. Journal of Neurosurgery, 2005, 102(1 Suppl): 36–43
84
Matic D B, Manson P N. Biomechanical analysis of hydroxyapatite cement cranioplasty. Journal of Craniofacial Surgery, 2004, 15(3): 415–422
85
Zins J E, Langevin C J, Nasir S. Controversies in skull reconstruction. The Journal of Craniofacial Surgery, 2010, 21(6): 1755–1760
86
Afifi A M, Gordon C R, Pryor L S, . Calcium phosphate cements in skull reconstruction: a meta-analysis. Plastic and Reconstructive Surgery, 2010, 126(4): 1300–1309
87
Busch E, Bing J, Hansen E H. Gelatine and polythene film as dura substitutes and polythene plates as bone substitute in skull defects. Acta Chirurgica Scandinavica, 1949, 97(5): 410–416
88
Liu J K, Gottfried O N, Cole C D, . Porous polyethylene implant for cranioplasty and skull base reconstruction. Neurosurgical Focus, 2004, 16(3): 1
89
Lin A Y, Kinsella C R, Rottgers S A, . Custom porous polyethylene implants for large-scale pediatric skull reconstruction: early outcomes. The Journal of Craniofacial Surgery, 2012, 23(1): 67–70
90
Wang J C, Wei L, Xu J, . Clinical outcome of cranioplasty with high-density porous polyethylene. The Journal of Craniofacial Surgery, 2012, 23(5): 1404–1406
91
Wang J C, Wang S Y, Gui L, . Porous polyethylene combined with split calvarial bone graft to cover complex calvarial defect. The Journal of Craniofacial Surgery, 2012, 23(6): 1802–1804
92
Hanasono M M, Goel N, DeMonte F. Calvarial reconstruction with polyetheretherketone implants. Annals of Plastic Surgery, 2009, 62(6): 653–655
93
Rosenthal G, Ng I, Moscovici S, . Polyetheretherketone implants for the repair of large cranial defects: a 3-center experience. Neurosurgery, 2014, 75(5): 523–529
94
Rammos C K, Cayci C, Castro-Garcia J A, . Patient-specific polyetheretherketone implants for repair of craniofacial defects. The Journal of Craniofacial Surgery, 2015, 26(3): 631–633
95
Lethaus B, Safi Y, ter Laak-Poort M, . Cranioplasty with customized titanium and PEEK implants in a mechanical stress model. Journal of Neurotrauma, 2012, 29(6): 1077–1083
96
Alonso-Rodriguez E, Cebrián J L, Nieto M J, . Polyetheretherketone custom-made implants for craniofacial defects: Report of 14 cases and review of the literature. Journal of Cranio-Maxillo-Facial Surgery, 2015, 43(7): 1232–1238
97
Thien A, King N K, Ang B T, . Comparison of polyetheretherketone and titanium cranioplasty after decompressive craniectomy. World Neurosurgery, 2015, 83(2): 176–180
98
Cui F Z, Li Y, Ge J. Self-assembly of mineralized collagen composites. Materials Science and Engineering R: Reports, 2007, 57(1−6): 1–27
99
Weiner S, Traub W. Bone structure: from angstroms to microns. FASEB Journal, 1992, 6(3): 879–885
100
Olszta M J, Cheng X, Jee S S, . Bone structure and formation: A new perspective. Materials Science and Engineering R: Reports, 2007, 58(3−5): 77–116
101
Landis W J, Silver F H. Mineral deposition in the extracellular matrices of vertebrate tissues: identification of possible apatite nucleation sites on type I collagen. Cells, Tissues, Organs, 2009, 189(1−4): 20–24
102
Zhang W, Liao S S, Cui F Z. Hierarchical self-assembly of nano-fibrils in mineralized collagen. Chemistry of Materials, 2003, 15(16): 3221–3226
103
Wang R Z, Cui F Z, Lu H B, . Synthesis of nanophase hydroxyapatite/collagen composite. Journal of Materials Science Letters, 1995, 14(7): 490–492
104
Du C, Cui F Z, Zhang W, . Formation of calcium phosphate/collagen composites through mineralization of collagen matrix. Journal of Biomedical Materials Research, 2000, 50(4): 518–527
105
Kikuchi M, Itoh S, Ichinose S, . Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials, 2001, 22(13): 1705–1711
106
Constantz B R, Gunasekaran S. Mineralized collagen. US Patent, 5 231 169, 1993–07–27
107
Bradt J H, Mertig M, Teresiak A, . Biomimetic mineralization of collagen by combined fibril assembly and calcium phosphate formation. Chemistry of Materials, 1999, 11(10): 2694–2701
108
Qiu Z Y, Tao C S, Cui H, . High-strength mineralized collagen artificial bone. Frontiers of Materials Science, 2014, 8(1): 53–62
109
Kou J M, Fu T Y, Jia X J, . Clinical observations on repair of non-infected bone nonunion by using mineralized collagen graft. Journal of Biomaterials and Tissue Engineering, 2014, 4(12): 1107–1112
110
Lian K, Lu H, Guo X, . The mineralized collagen for the reconstruction of intra-articular calcaneal fractures with trabecular defects. Biomatter, 2013, 3(4): e27250
111
Yu X, Xu L, Cui F Z, . Clinical evaluation of mineralized collagen as a bone graft substitute for anterior cervical intersomatic fusion. Journal of Biomaterials and Tissue Engineering, 2012, 2(2): 170–176
112
Hvistendahl M. China’s push in tissue engineering. Science, 2012, 338(6109): 900–902
