Vascularization and biocompatibility of scaffolds consisting of different calcium phosphate compounds
Corresponding Author
Martin Rücker
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, GermanySearch for more papers by this authorMatthias W. Laschke
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorDominic Junker
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorCarlos Carvalho
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, Germany
Search for more papers by this authorFrank Tavassol
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Search for more papers by this authorRolf Mülhaupt
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, Germany
Search for more papers by this authorNils-Claudius Gellrich
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Search for more papers by this authorMichael D. Menger
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorCorresponding Author
Martin Rücker
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, GermanySearch for more papers by this authorMatthias W. Laschke
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorDominic Junker
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorCarlos Carvalho
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, Germany
Search for more papers by this authorFrank Tavassol
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Search for more papers by this authorRolf Mülhaupt
Freiburg Materials Research Center and Institute for Macromolecular Chemistry, Albert-Ludwigs University, 79104 Freiburg, Germany
Search for more papers by this authorNils-Claudius Gellrich
Department of Oral and Maxillofacial Surgery, Hannover Medical School, 30625 Hannover, Germany
Search for more papers by this authorMichael D. Menger
Institute for Clinical and Experimental Surgery, University of Saarland, 66421 Homburg/Saar, Germany
Search for more papers by this authorAbstract
Scaffolds for tissue engineering of bone should mimic bone matrix and promote vascular ingrowth. Whether synthetic hydroxyapatite and acellular dentin, both materials composed from calcium phosphate, fulfill these material properties has not been studied yet. Therefore, we herein studied in vivo the host angiogenic and inflammatory response to these biomaterials. Porous scaffolds of hydroxyapatite and isogeneic acellular dentin were implanted into the dorsal skinfold chamber of balb/c mice. Additional animals received perforated implants of isogeneic calvarial bone displaying pores similar in size and structure to those of both scaffolds. Chambers of animals without implants served as controls. Angiogenesis and neovascularization as well as inflammatory leukocyte-endothelial cell interaction and microvascular leakage were analyzed over a 14-day time period using intravital fluorescence microscopy. Implantation of both hydroxyapatite and dentin scaffolds showed a slight increase in leukocyte recruitment compared with controls. This was associated with an elevation of microvascular permeability, which was comparable to that observed in response to isogeneic bone. In addition, hydroxyapatite as well as dentin scaffolds induced a marked angiogenic response, which resulted in complete vascularization of the implants until day 14. Of interest, in hydroxyapatite scaffolds, the newly formed capillaries were not as densely meshed as in dentin scaffolds, in which the functional capillary density was comparable to that measured in bone implants. Hydroxyapatite and, in particular, dentin scaffolds promote vascularization and exhibit a biocompatibility comparable to that of isogeneic bone. This may guarantee the rapid incorporation of these materials into the host tissue. © 2007 Wiley Periodicals, Inc. J Biomed Mater Res, 2008
References
- 1 Ahsan T,Nerem RM. Bioengineered tissues: The science, the technology, and the industry. Orthod Craniofac Res 2005; 8: 134–140.
- 2 Karageorgiou V,Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005; 26: 5474–5491.
- 3 Quelch KJ,Melick RA,Bingham PJ,Mercuri SM. Chemical composition of human bone. Arch Oral Biol 1983; 28: 665–674.
- 4
Maria del Pilar Gutiérrez-Salazar,Jorge Reyes-Gasga.
Microhardness and chemical composition of human tooth.
Mat Res
2003;
6:
367–373.
10.1590/S1516-14392003000300011 Google Scholar
- 5 Hellsing E,Alatli-Kut I,Hammarstrom L. Experimentally induced dentoalveolar ankylosis in rats. Int Endod J 1993; 26: 93–98.
- 6 Yarlagadda PK,Chandrasekharan M,Shyan JY. Recent advances and current developments in tissue scaffolding. Biomed Mater Eng 2005; 15: 159–177.
- 7 Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000; 6: 389–395.
- 8 Laschke MW,Harder Y,Amon M,Martin I,Farhadi J,Ring A,Torio-Padron N,Schramm R,Rücker M,Junker D,Ha JM,Carvalho C,Heberer M,Germann G,Vollmar B,Menger MD. Angiogenesis in tissue engineering: Breathing life into constructed tissue substitutes. Tissue Eng 2006; 12: 2093–2104.
- 9 Druecke D,Langer S,Lamme E,Pieper J,Ugarkovic M,Steinau HU,Homann HH. Neovascularization of poly(ether ester) block-copolymer scaffolds in vivo: Long-term investigations using intravital fluorescent microscopy. J Biomed Mater Res 2004; 68: 10–18.
- 10 Landers R,Hübner U,Schmelzeisen R,Mülhaupt R. Rapid prototyping of scaffolds derived from thermoreversible hydrogels and tailored for applications in tissue engineering. Biomaterials 2002; 23: 4437–4447.
- 11 Sung HJ,Meredith C,Johnson C,Galis ZS. The effect of scaffold degradation rate on three-dimensional cell growth and angiogenesis. Biomaterials 2004; 25: 5735–5742.
- 12 Laschke MW,Häufel JM,Thorlacius H,Menger MD. New experimental approach to study host tissue response to surgical mesh materials in vivo. J Biomed Mater Res A 2005; 74: 696–704.
- 13 Lehr HA,Leunig M,Menger MD,Nolte D,Messmer K. Dorsal skinfold chamber technique for intravital microscopy in nude mice. Am J Pathol 1993; 143: 1055–1062.
- 14 Carvalho C,Landers R,Hübner U,Schmelzeisen R,Mülhaupt R. Fabrication of soft and hard biocompatible scaffolds using 3D-Bioplotting™. In: PJ Bártolo, et al., editors. Virtual Modelling and Rapid Manufacturing—Advanced Research in Virtual and Rapid Prototyping. London: Taylor & Francis Group; 2005. p 97–102. ISBN 0415390621.
- 15 Rücker M,Schäfer T,Roesken F,Spitzer WJ,Bauer M,Menger MD. Reduction of inflammatory response in composite flap transfer by local stress conditioning-induced heat-shock protein 32. Surgery 2001; 129: 292–301.
- 16 Menger MD,Pelikan S,Steiner D,Messmer K. Microvascular ischemia-reperfusion injury in striated muscle: Significance of “reflow paradox”. Am J Physiol 1992; 263: H1901–H1906.
- 17 Baker M,Wayland H. On-line volume flow rate and velocity profile measurement for blood in microvessels. Microvasc Res 1974; 7: 131–143.
- 18 Menger MD,Steiner D,Messmer K Microvascular ischemia-reperfusion injury in striated muscle: significance of “no reflow”. Am J Physiol 1992; 263: H1892–H1900.
- 19 Ribatti D,Nico B,Vacca A,Roncali L,Burri PH,Djonov V. Chorioallantoic membrane capillary bed: A useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat Rec 2001; 264: 317–324.
- 20 Menger MD,Walter P,Hammersen F,Messmer K. Quantitative analysis of neovascularization of different PTFE-implants. Eur J Cardiothorac Surg 1990; 4: 191–196.
- 21 Menger MD,Hammersen F,Walter P,Messmer K. Neovascularization of prosthetic vascular grafts. Quantitative analysis of angiogenesis and microhemodynamics by means of intravital microscopy. Thorac Cardiovasc Surg 1990; 38: 139–145.
- 22 Menger MD,Hammersen F,Messmer K. In vivo assessment of neovascularization and incorporation of prosthetic vascular biografts. Thorac Cardiovasc Surg 1992; 40: 19–25.
- 23 Kaneko H,Hashimoto S,Enokiya Y,Ogiuchi H,Shimono M. Cell proliferation and death of Hertwig's epithelial root sheath in the rat. Cell Tissue Res 1999; 298: 95–103.
- 24 Pasteris JD,Wopenka B,Freeman JJ,Rogers K,Valsami-Jones E,van der Houwen JA,Silva MJ. Lack of OH in nanocrystalline apatite as a function of degree of atomic order: Implications for bone and biomaterials. Biomaterials 2004; 25: 229–238.
- 25 Butler WT,Ritchie HH,Bronckers AL. Extracellular matrix proteins of dentine. Ciba Found Symp 1997; 205: 107–115.
- 26 Ike M,Urist MR. Recycled dentin root matrix for a carrier of recombinant human bone morphogenetic protein. J Oral Implantol 1998; 24: 124–132.
- 27 About I,Bottero MJ,de Denato P,Camps J,Franquin JC,Mitsiadis TA. Human dentin production in vitro. Exp Cell Res 2000; 258: 33–41.
- 28 Nam YS,Yoon JJ,Park TG. A novel fabrication method of macroporous biodegradable polymer scaffolds using gas foaming salt as a porogen additive. J Biomed Mater Res 2000; 53: 1–7.
- 29 Wake MC,Gupta PK,Mikos AG. Fabrication of pliable biodegradable polymer foams to engineer soft tissues. Cell Transplant 1996; 5: 465–473.
- 30 Mikos AG,Bao Y,Cima LG,Ingber DE,Vacanti JP,Langer R. Preparation of poly(glycolic acid) bonded fiber structures for cell attachment and transplantation. J Biomed Mater Res 1993; 27: 183–189.
- 31
Lo H,Kadiyala S,Guggino SE,Leong KW.
Poly(L-lactic acid) foams with cell seeding and controlled-release capacity.
JBiomed Mater Res
1996;
30:
475–484.
10.1002/(SICI)1097-4636(199604)30:4<475::AID-JBM5>3.0.CO;2-M CAS PubMed Web of Science® Google Scholar
- 32 Wake MC,Patrick CWJr,Mikos AG. Pore morphology effects on the fibrovascular tissue growth in porous polymer substrates. Cell Transplant 1994; 3: 339–343.
- 33 Rücker M,Laschke MW,Junker D,Carvalho C,Schramm A,Mülhaupt R,Gellrich NC,Menger MD. Angiogenic and inflammatory response to biodegradable scaffolds in dorsal skinfold chambers of mice. Biomaterials 2006; 27: 5027–5038.
- 34
Klosterhalfen B,Hermanns B,Rosch R,Junge K.
Biological response to mesh.
Eur Surg
2003;
35:
16–20.
10.1046/j.1563-2563.2003.03011.x Google Scholar
- 35 Tang L,Jennings TA,Eaton JW. Mast cells mediate acute inflammatory responses to implanted biomaterials. Proc Natl Acad Sci USA 1998; 95: 8841–8846.
- 36 Rosch R,Junge K,Schachtrupp A,Klinge U,Klosterhalfen B,Schumpelick V. Mesh implants in hernia repair—Inflammatory cell response in a rat model. Eur Surg Res 2003; 35: 161–166.
- 37
Van Luyn MJ,Khouw IM,van Wachem PB,Blaauw EH,Werkmeister JA.
Modulation of the tissue reaction to biomaterials. II. The function of T cells in the inflammatory reaction to crosslinked collagen implanted in T-cell-deficient rats.
JBiomed Mater Res
1998;
39:
398–406.
10.1002/(SICI)1097-4636(19980305)39:3<398::AID-JBM8>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 38 Munro JM. Endothelial-leukocyte adhesive interactions in inflammatory diseases. Eur Heart J 1993; 14( Suppl K): 72–77.
- 39 Croll SD,Ransohoff RM,Cai N,Zhang Q,Martin FJ,Wei T,Kasselman LJ,Kintner J,Murphy AJ,Yancopoulos GD,Wiegand SJ. VEGF-mediated inflammation precedes angiogenesis in adult brain. Exp Neurol 2004; 187: 388–402.
- 40 Fantone JC,Ward PA. Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am J Pathol 1982; 107: 395–418.
- 41 Siflinger-Birnboim A,Goligorsky MS,Del Vecchio PJ,Malik AB. Activation of protein kinase C contributes to hydrogen peroxide-induced increase in endothelial permeability. Lab Invest 1992; 67: 24–30.
- 42
Kraft CN,Hansis M,Arens S,Menger MD,Vollmar B.
Striated muscle microvascular response to silver implants: A comparative in vivo study with titanium and stainless steel.
JBiomed Mater Res
2000;
49:
192–199.
10.1002/(SICI)1097-4636(200002)49:2<192::AID-JBM6>3.0.CO;2-C CAS PubMed Web of Science® Google Scholar
- 43 Schliephake H. Bone growth factors in maxillofacial skeletal reconstruction. Int J Oral Maxillofac Surg 2002; 31: 469–484.
- 44 Möhle R,Green D,Moore MAS,Nachman RL,Rafii S. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryo-cytes and platelets. Proc Natl Acad Sci USA 1997; 94: 663–668.
- 45 Shaw JP,Chuang N,Yee H,Shamamian P. Polymorphonuclear neutrophils promote rFGF-2-induced angiogenesis in vivo. J Surg Res 2003; 109: 37–42.
- 46 Karayiannakis AJ,Zbar A,Polychronidis A,Simopoulos C. Serum and drainage fluid vascular endothelial growth factor levels in early surgical wounds. Eur Surg Res 2003; 35: 492–496.