Carbon Fiber-Reinforced Carbon as a Potential Implant Material D. ADAMS and D. F. WILLIAMS, Departments of Operative Dental Surgery and Dental Sciences, University of Liverpool, England, and J. HILL, Atomic Weapons Research Establishment, Aldermaston, Berkshire, England
Summary A carbon fiber-reinforced carbon is being evaluated as a promising implant material. I n a unidirectional composite, high strengths (1200 MN/m2 longitudinal flexural strength) and high modulus (140 GN/m2 flexural modulus) may be obtained with an interlaminar shear strength of 18 MN/m2. Alternatively, layers of fibers may be laid in two directions to give more isotopic properties. The compatibility of the material with bone has been studied by implanting specimens in holes drilled fn rat femora. For a period of up t o 8 weeks, a thin layer of fibrous tissue bridged the gap between bone and implant; but this tissue mineralizes and by 10 weeks, bone can be observed adjacent t o the implant, giving firm fixation. Potential applications include endosseous dental implants where a greater strength in the neck than that provided by unreinforced carbon would be advantageous.
INTRODUCTION During recent years, there has been a growing interest in the use of carbon as an implant material. The intuitive assumption that carbon must possess good biocompatibility has been substantiated by a number of experiments, and various forms of carbon are now in use, either experimentally or, in some cases, routinely in human patients.' Elemental carbon may exist in a number of forms of varying degrees of crystallinity and correspondingly varying properties. The two forms of greatest interest for implantation have been pyrolytic graphite and vitreous carbon. Vitreous carbon may be prepared by the thermal degradation of some organic polymers, as described by Journal of Biomedical Materials Research, Vol. 12,35-42 (1978) 0 1978 by John Wiley & Sons, Inc. 0021-9304/78/0012-0035$01.00
36
ADAMS, WILLIAMS, AND HILL
Cowlard and Lewis.2 The material is essentially ajlass, with crystallinity confined t o the presence of many small (50 A X 15 A) crystallites of random orientation. Because of this structure, vitreous carbon has a low impact strength and claims of high tensile strengths must be viewed with caution because of the low toughness and high notch sensitivity. A further disadvantage of the material3 is the relative difficulty of fabrication since it is prepared from a preformed polymer precursor by pyrolysis in the region of 1800°C and cannot be easily machined afterwards. Pyrolytic graphite (or pyrolytic carbon) is prepared by a chemical vapor-deposition process in which carbon is deposited from a hydrocarbon-containing gaseous environment onto a suitable ~ u b s t r a t e . ~ The operating conditions will control the structure of the coating, particular interest being displayed in the LTI carbon (low-temperature isotropic) , where a n isotropic layer of reasonably good meehanical properties is produced. There has also been some interest in alloy-pyrolytic carbon deposits, especially those containing small amounts of silicon, which can be easily mixed in the fluidizing gas. Both these types of carbon have been used clinically. Grenoble et aL5 and Markle et aL6 have reported on the use of vitreous carbon as endosseous dental implants in baboons, and Hulbert et al.7 have described work with silicon-alloyed pyrolytic graphite in similar applications. The mechanical behavior of these LTI carbon dental implants have been described by Shim.8 Bjorkg has incorporated a n LTI carbon occluder in the Bjork-Shiley tilting disk heart valve, reporting encouraging experimental and clinical data. Similarly, the DeBakey-Sugitool aortic and Beall-Surgitool mitral prosthetic valves have been made with silicon-alloyed LTI carbon ball cages and seats, giving good thromboresistance. The apparently good biocompatibility shown by these materials has led t o their use in percutaneous devices; Kadefors and Reswick’” have described the construction and use of carbon percutaneous electrodes, and Stanitski and hilooneyl1 have reported the use of skeletally fixed limb prostheses. While there seems to be general satisfaction with the biocompatibility of these carbons, the mechanical properties, especially of the vitreous carbon, are not very good. KaaeI2 has compared their properties, showing that, for a typical vitreous carbon in three-point bending, the fracture stress is 225 MN/m2, the elastic modulus 23-28
CARBON FIBER-REINFORCED CARBON
37
GN/m2, the strain energy t o fracture 10 MN/m2, and the strain t o fracture 0.01. The strain and strain energy to fracture are particularly low. This conclusion was substantiated by Stanitski and Mooney,ll who found that vitreous carbon is too brittle t o withstand functional loading in skeletal prostheses but admitted that their design was less than optimum. The mechanical properties of LTI carbon are dependent on density, values a t 1.9 g/m3 being fracture stress 520 MN/m2, elastic modulus 28 GN/m2, strain energy to fracture 56 MN/m2, and strain t o fracture 0.019. Also, some of the material used clinically is an alloy of pyrolytic carbon with silicon, a typical composition of 10 wt yo silicon having a fracture stress of 575 MN/m2, as described by Kaae and G ~ 1 d e n . I ~These figures indicate considerable improvement over vitreous carbon, but there is clearly room for even better properties. It is for this reason that reinforced carbons have been considered and preliminary data concerning a carbon fiber-reinforced carbon composite is presented in this paper.
METHOD OF PREPARATION The method used to prepare the carbon fiber-reinforced carbon in this work involved coating polyacrylonitrile-based carbon fibers with a solution of a thermosetting resin and then heating t o remove the solvent and increase the molecular weight of the resin. The coated fibers were placed in a mold in the desired alignment, pressed and heated. The resulting carbon fiber-reinforced resin was further heated in a n inert atmosphere to 1250°K a t 5"K/hr. During this carbonization process, the resin was converted t o carbon which was cracked due to the increase in density in changing from resin t o carbon and t o the gases which were evolved during the chemical reaction. The composites were densified by infiltrating the pores and cracks with a hydrocarbon gas a t a temperature sufficiently high to cause it t o form carbon on the walls of the pores. Normally, methane gas is used at a temperature of 1300"IC The properties of unidirectional carbon fiber-reinforced composites, when tested a t an angle t o the principal fiber axis, fall off rapidly when the angle exceeds a value of about 5", but it is possible t o maintain adequate mechanical properties in the longitudinal direction with improved transverse properties by using angled ply lay-ups in
ADAMS, WILLIAMS, AND HILL
38
which the fibers are aligned a t a n angle to the principal axis of the composite. By using a balanced construction where alternate layers are aligned a t angles of +O and -0 to the principal composite axis, the fall-off in longitudinal properties is somewhat less rapid, and the composite is more resistant t o splitting. An alternative method of improving the composite strength perpendicular to the fiber direction is to fabricate a sandwich construction where a core of unidirectional carbon fibers is contained within skins of square woven low-modulus rayon-based carbon cloth. By using this lay-up, the strength and modulus in the principal axis are reduced but the strength perpendicular t o this axis is increased. All three of these composites have been tested in vivo. However, in this paper only cloth-sandwich experiments are discussed.
MECHANICAL PROPERTIES The longitudinal and transverse flexural properties and the interlaminar shear strength were measurcd by simple three-point bend tests using appropriate span t o depth ratios. The results are listed in Table I. The material has a density range of 1.4-1.45 g-cm3 with a porosity of 35-38%.
MATERIALS AND METHOD The preliminary in vivo testing consisted of implanting rods of the material into holes drilled transversely through the femora of anesthetized black and white rats. Controls were provided in this TABLE I Mechanical Properties of Carbon Fiber-Reinforced Carbon -
Property
'..
1 .
Unidirectional
0-90" Cross Ply
Cloth/Fiber Sandwich
Flexural Modulus Longitudinal GN/m2 Transverse GN/m2
140 7
60 60
60 8
Flexural Strength Longitudinal MN/m2 Transverse MN/m2
1200 15
500 500
650 70
18
18
20
Interlaminar shear strength MN/m2
CARBON FIBER-REINFORCED CARBON
39
experiment by drilling holes of the same dimensions as those for the rods and letting them heal without any foreign material present. All animals recovered uneventfully from the anesthetic and immediately led normal active lives with the operated limbs functioning normally. The animals were sacrificed a t intervals from 2 to 14 weeks postoperatively and the femora removed and fixed in formal saline. Half the sppimens were decalcified with formic acid and the implant then carefully removed after which the decalcified bone was blocked in paraffin wax, sectioned, stained with haemotoxylin and eosin, and viewed by transmitted light. The remaining specimens were embedded in poly(methy1 methacrylate), sectioned, and stained with Azure A. These too were viewed by transmitted light. Control material was similarly processed.
RESULTS Healing around the implants was histologically uneventful with no more than an initial traumatic inflammatory response followed by new bone formation up to the implant surface. Figure 1 shows the appearance a t 2 weeks with a wide band of granulation tissue separating the implant from some new immature bone. The junction
Fig. 1. Appearance around bone/implant interface at 2 weeks.
(H & E, 12OX.)
40
ADAMS, WILLIAMS, AND HILL
between mature and immature bone is clearly seen in the upper right portion of the photomicrograph. Figure 2 shows the appearance at 6 weeks in which the bone is separated from the implant by a very thin epithelial-like layer. There is, in addition to this, evidence in this section of the bone lipping over the exterior surface of the implant. By 12 weeks there is no evidence of any tissue separating the bone from the implant surface, as shown in Figure 3. Healing in the control specimens progressed at a similar rate to that seen with the implant specimens, although because of the greater volume of new bone required to fill the defect, complete repair took somewhat longer. While some materials in bulk are felt to be biologically compatible, concern is expressed about the same material in a particulate phase. It was found in one section from around an implant which had been in place for 8 weeks that some carbon particles had become detached from the implant presumably during insertion, but these had been completely engulfed by new bone with no observable inflammatory reaction. This section is shown in Figure 4.
Fig. 2.
Appearance around bone/implant interface at 6 weeks.
(H & E, 120 X .)
CARBON FIBER-REINFORCED CARBON
Fig. 3. Appearance around bone/implant interface at 12 weeks. 120 x .)
Fig. 4. A “nest” of carbon particles surrounded by bone a t 8 weeks. 120 x .)
41
(Azure A,
(H & E,
42
ADAMS, WILLIAMS, AND HILL
CONCLUSION These results seem to confirm the biocompatibility of carboncarbon composites. It is intended that these materials be used in the oral cnvironment, which is potentially far more hostile than that found in these experiments. The presence of the carbon implant matcrial both in bulk and particulate phase had no observable effect on the healing process, and further work is now being undertaken with this material in an oral environment.
References 1. J. C. Bokros, R. J. Atkins, H. S. Shim, A. D. Haubold, and N. K. Agarwal,
2. 3.
4. 5.
6. 7.
8. 9. 10. 11.
12. 13.
in Petroleum Deriued Carbons (American Chemical Society Symposium Series N o . 21), M. L. Deviney and T. M. O’Grady, Eds., ACS, Washington, D.C., 1975, p. 237. F. C. Cowlard and J. C. Lewis, b. Muter. Sci., 2, 507 (1967). J. A. von Fraunhofer, P. R. L’Estrange, and A. 0. Mack, Biomed. Eng., 6, 114 (1971). J. C. Bokros and R. E . Akins, in Proceedings of the Fourth Buhl Conference on Materials, Carnegie Press, Pittsburgh, 1971, p. 243. D. E. Grenoble, R. J. Melrose, and I). H. Markle, Biomuter. Med. Dev. Artif. Organs, 3, 245 (1975). D. H. Markle, D. E. Grenoble, and R. J. Melrose, Biomater. Med. Dev. Artif. Organs, 3, 97 (1975). S. F. Hulbert, J. N. Kent, J. C. Bokros, H. 9. Shim, and 0. M. Reed, Oral Implant., 6, 79 (1975). H. S. Shim, Biomater. Med. Dev. Artif. Organs, 4, 181 (1976). V. 0. Bjork, Scand. J. ‘I’hor. Cardiovasc. Surg., 6, 109 (1972). R. Kadefors and J. B. Reswick, Med. Bio2. Eng., 8, 129 (1970). C. C. Stanitski and V. Mooney, J . Biomed. Muter. Res. S y m p . No. 4, 97 (1973). J. L. Kaae, J. Biomed. Muter. Res., 6,279 (1972). J. L. Kaae and T. D. Gulden, J . Am. Cerum. SOC.,54, 605 (1971).
Received March 14, 1977 Revised May 16, 1977
Summary A carbon fiber-reinforced carbon is being evaluated as a promising implant material. I n a unidirectional composite, high strengths (1200 MN/m2 longitudinal flexural strength) and high modulus (140 GN/m2 flexural modulus) may be obtained with an interlaminar shear strength of 18 MN/m2. Alternatively, layers of fibers may be laid in two directions to give more isotopic properties. The compatibility of the material with bone has been studied by implanting specimens in holes drilled fn rat femora. For a period of up t o 8 weeks, a thin layer of fibrous tissue bridged the gap between bone and implant; but this tissue mineralizes and by 10 weeks, bone can be observed adjacent t o the implant, giving firm fixation. Potential applications include endosseous dental implants where a greater strength in the neck than that provided by unreinforced carbon would be advantageous.
INTRODUCTION During recent years, there has been a growing interest in the use of carbon as an implant material. The intuitive assumption that carbon must possess good biocompatibility has been substantiated by a number of experiments, and various forms of carbon are now in use, either experimentally or, in some cases, routinely in human patients.' Elemental carbon may exist in a number of forms of varying degrees of crystallinity and correspondingly varying properties. The two forms of greatest interest for implantation have been pyrolytic graphite and vitreous carbon. Vitreous carbon may be prepared by the thermal degradation of some organic polymers, as described by Journal of Biomedical Materials Research, Vol. 12,35-42 (1978) 0 1978 by John Wiley & Sons, Inc. 0021-9304/78/0012-0035$01.00
36
ADAMS, WILLIAMS, AND HILL
Cowlard and Lewis.2 The material is essentially ajlass, with crystallinity confined t o the presence of many small (50 A X 15 A) crystallites of random orientation. Because of this structure, vitreous carbon has a low impact strength and claims of high tensile strengths must be viewed with caution because of the low toughness and high notch sensitivity. A further disadvantage of the material3 is the relative difficulty of fabrication since it is prepared from a preformed polymer precursor by pyrolysis in the region of 1800°C and cannot be easily machined afterwards. Pyrolytic graphite (or pyrolytic carbon) is prepared by a chemical vapor-deposition process in which carbon is deposited from a hydrocarbon-containing gaseous environment onto a suitable ~ u b s t r a t e . ~ The operating conditions will control the structure of the coating, particular interest being displayed in the LTI carbon (low-temperature isotropic) , where a n isotropic layer of reasonably good meehanical properties is produced. There has also been some interest in alloy-pyrolytic carbon deposits, especially those containing small amounts of silicon, which can be easily mixed in the fluidizing gas. Both these types of carbon have been used clinically. Grenoble et aL5 and Markle et aL6 have reported on the use of vitreous carbon as endosseous dental implants in baboons, and Hulbert et al.7 have described work with silicon-alloyed pyrolytic graphite in similar applications. The mechanical behavior of these LTI carbon dental implants have been described by Shim.8 Bjorkg has incorporated a n LTI carbon occluder in the Bjork-Shiley tilting disk heart valve, reporting encouraging experimental and clinical data. Similarly, the DeBakey-Sugitool aortic and Beall-Surgitool mitral prosthetic valves have been made with silicon-alloyed LTI carbon ball cages and seats, giving good thromboresistance. The apparently good biocompatibility shown by these materials has led t o their use in percutaneous devices; Kadefors and Reswick’” have described the construction and use of carbon percutaneous electrodes, and Stanitski and hilooneyl1 have reported the use of skeletally fixed limb prostheses. While there seems to be general satisfaction with the biocompatibility of these carbons, the mechanical properties, especially of the vitreous carbon, are not very good. KaaeI2 has compared their properties, showing that, for a typical vitreous carbon in three-point bending, the fracture stress is 225 MN/m2, the elastic modulus 23-28
CARBON FIBER-REINFORCED CARBON
37
GN/m2, the strain energy t o fracture 10 MN/m2, and the strain t o fracture 0.01. The strain and strain energy to fracture are particularly low. This conclusion was substantiated by Stanitski and Mooney,ll who found that vitreous carbon is too brittle t o withstand functional loading in skeletal prostheses but admitted that their design was less than optimum. The mechanical properties of LTI carbon are dependent on density, values a t 1.9 g/m3 being fracture stress 520 MN/m2, elastic modulus 28 GN/m2, strain energy to fracture 56 MN/m2, and strain t o fracture 0.019. Also, some of the material used clinically is an alloy of pyrolytic carbon with silicon, a typical composition of 10 wt yo silicon having a fracture stress of 575 MN/m2, as described by Kaae and G ~ 1 d e n . I ~These figures indicate considerable improvement over vitreous carbon, but there is clearly room for even better properties. It is for this reason that reinforced carbons have been considered and preliminary data concerning a carbon fiber-reinforced carbon composite is presented in this paper.
METHOD OF PREPARATION The method used to prepare the carbon fiber-reinforced carbon in this work involved coating polyacrylonitrile-based carbon fibers with a solution of a thermosetting resin and then heating t o remove the solvent and increase the molecular weight of the resin. The coated fibers were placed in a mold in the desired alignment, pressed and heated. The resulting carbon fiber-reinforced resin was further heated in a n inert atmosphere to 1250°K a t 5"K/hr. During this carbonization process, the resin was converted t o carbon which was cracked due to the increase in density in changing from resin t o carbon and t o the gases which were evolved during the chemical reaction. The composites were densified by infiltrating the pores and cracks with a hydrocarbon gas a t a temperature sufficiently high to cause it t o form carbon on the walls of the pores. Normally, methane gas is used at a temperature of 1300"IC The properties of unidirectional carbon fiber-reinforced composites, when tested a t an angle t o the principal fiber axis, fall off rapidly when the angle exceeds a value of about 5", but it is possible t o maintain adequate mechanical properties in the longitudinal direction with improved transverse properties by using angled ply lay-ups in
ADAMS, WILLIAMS, AND HILL
38
which the fibers are aligned a t a n angle to the principal axis of the composite. By using a balanced construction where alternate layers are aligned a t angles of +O and -0 to the principal composite axis, the fall-off in longitudinal properties is somewhat less rapid, and the composite is more resistant t o splitting. An alternative method of improving the composite strength perpendicular to the fiber direction is to fabricate a sandwich construction where a core of unidirectional carbon fibers is contained within skins of square woven low-modulus rayon-based carbon cloth. By using this lay-up, the strength and modulus in the principal axis are reduced but the strength perpendicular t o this axis is increased. All three of these composites have been tested in vivo. However, in this paper only cloth-sandwich experiments are discussed.
MECHANICAL PROPERTIES The longitudinal and transverse flexural properties and the interlaminar shear strength were measurcd by simple three-point bend tests using appropriate span t o depth ratios. The results are listed in Table I. The material has a density range of 1.4-1.45 g-cm3 with a porosity of 35-38%.
MATERIALS AND METHOD The preliminary in vivo testing consisted of implanting rods of the material into holes drilled transversely through the femora of anesthetized black and white rats. Controls were provided in this TABLE I Mechanical Properties of Carbon Fiber-Reinforced Carbon -
Property
'..
1 .
Unidirectional
0-90" Cross Ply
Cloth/Fiber Sandwich
Flexural Modulus Longitudinal GN/m2 Transverse GN/m2
140 7
60 60
60 8
Flexural Strength Longitudinal MN/m2 Transverse MN/m2
1200 15
500 500
650 70
18
18
20
Interlaminar shear strength MN/m2
CARBON FIBER-REINFORCED CARBON
39
experiment by drilling holes of the same dimensions as those for the rods and letting them heal without any foreign material present. All animals recovered uneventfully from the anesthetic and immediately led normal active lives with the operated limbs functioning normally. The animals were sacrificed a t intervals from 2 to 14 weeks postoperatively and the femora removed and fixed in formal saline. Half the sppimens were decalcified with formic acid and the implant then carefully removed after which the decalcified bone was blocked in paraffin wax, sectioned, stained with haemotoxylin and eosin, and viewed by transmitted light. The remaining specimens were embedded in poly(methy1 methacrylate), sectioned, and stained with Azure A. These too were viewed by transmitted light. Control material was similarly processed.
RESULTS Healing around the implants was histologically uneventful with no more than an initial traumatic inflammatory response followed by new bone formation up to the implant surface. Figure 1 shows the appearance a t 2 weeks with a wide band of granulation tissue separating the implant from some new immature bone. The junction
Fig. 1. Appearance around bone/implant interface at 2 weeks.
(H & E, 12OX.)
40
ADAMS, WILLIAMS, AND HILL
between mature and immature bone is clearly seen in the upper right portion of the photomicrograph. Figure 2 shows the appearance at 6 weeks in which the bone is separated from the implant by a very thin epithelial-like layer. There is, in addition to this, evidence in this section of the bone lipping over the exterior surface of the implant. By 12 weeks there is no evidence of any tissue separating the bone from the implant surface, as shown in Figure 3. Healing in the control specimens progressed at a similar rate to that seen with the implant specimens, although because of the greater volume of new bone required to fill the defect, complete repair took somewhat longer. While some materials in bulk are felt to be biologically compatible, concern is expressed about the same material in a particulate phase. It was found in one section from around an implant which had been in place for 8 weeks that some carbon particles had become detached from the implant presumably during insertion, but these had been completely engulfed by new bone with no observable inflammatory reaction. This section is shown in Figure 4.
Fig. 2.
Appearance around bone/implant interface at 6 weeks.
(H & E, 120 X .)
CARBON FIBER-REINFORCED CARBON
Fig. 3. Appearance around bone/implant interface at 12 weeks. 120 x .)
Fig. 4. A “nest” of carbon particles surrounded by bone a t 8 weeks. 120 x .)
41
(Azure A,
(H & E,
42
ADAMS, WILLIAMS, AND HILL
CONCLUSION These results seem to confirm the biocompatibility of carboncarbon composites. It is intended that these materials be used in the oral cnvironment, which is potentially far more hostile than that found in these experiments. The presence of the carbon implant matcrial both in bulk and particulate phase had no observable effect on the healing process, and further work is now being undertaken with this material in an oral environment.
References 1. J. C. Bokros, R. J. Atkins, H. S. Shim, A. D. Haubold, and N. K. Agarwal,
2. 3.
4. 5.
6. 7.
8. 9. 10. 11.
12. 13.
in Petroleum Deriued Carbons (American Chemical Society Symposium Series N o . 21), M. L. Deviney and T. M. O’Grady, Eds., ACS, Washington, D.C., 1975, p. 237. F. C. Cowlard and J. C. Lewis, b. Muter. Sci., 2, 507 (1967). J. A. von Fraunhofer, P. R. L’Estrange, and A. 0. Mack, Biomed. Eng., 6, 114 (1971). J. C. Bokros and R. E . Akins, in Proceedings of the Fourth Buhl Conference on Materials, Carnegie Press, Pittsburgh, 1971, p. 243. D. E. Grenoble, R. J. Melrose, and I). H. Markle, Biomuter. Med. Dev. Artif. Organs, 3, 245 (1975). D. H. Markle, D. E. Grenoble, and R. J. Melrose, Biomater. Med. Dev. Artif. Organs, 3, 97 (1975). S. F. Hulbert, J. N. Kent, J. C. Bokros, H. 9. Shim, and 0. M. Reed, Oral Implant., 6, 79 (1975). H. S. Shim, Biomater. Med. Dev. Artif. Organs, 4, 181 (1976). V. 0. Bjork, Scand. J. ‘I’hor. Cardiovasc. Surg., 6, 109 (1972). R. Kadefors and J. B. Reswick, Med. Bio2. Eng., 8, 129 (1970). C. C. Stanitski and V. Mooney, J . Biomed. Muter. Res. S y m p . No. 4, 97 (1973). J. L. Kaae, J. Biomed. Muter. Res., 6,279 (1972). J. L. Kaae and T. D. Gulden, J . Am. Cerum. SOC.,54, 605 (1971).
Received March 14, 1977 Revised May 16, 1977
