NANO LETTERS
Piezoelectric Effect in Human Bones Studied in Nanometer Scale
2004 Vol. 4, No. 7 1253-1256
C. Halperin,† S. Mutchnik,‡ A. Agronin,‡ M. Molotskii,‡ P. Urenski,‡ M. Salai,† and G. Rosenman*,‡ Department of Orthopedic Surgery, Beilinson Campus, Rabin Medical Center, Petah-Tiqwa, 49100, Israel, and Department of Electrical Engineering-Physical Electronics, School of Engineering, Tel AViV UniVersity, Ramat-AViV, 69978, Israel Received April 12, 2004; Revised Manuscript Received May 11, 2004
ABSTRACT The piezoelectric effect has been studied in wet and dry human bones using a piezoresponse force microscope (PFM). It allowed to measure piezoelectric response with nanometer scale resolution directly in a collagen matrix and to obtain a piezoresponse image near the Haversian channel. Dielectric response and dc conductivity have been measured. Theoretical calculations taking into account the inhomogeneity of the electric field under the PFM tip apex and its screening in highly conductive bone samples were performed for obtaining the piezoelectric coefficient in the bone collagen.
Ferroelectric phenomena have been observed in many biological materials. The origin of these fundamental physical properties is ascribed to high structural ordering of biological systems at any level that is a low symmetry configuration of elementary cells based of their helical or chiralic dissymmetry. Linear electrooptic effect has been found in nerve fibers.1 Dielectric spectroscopy studies of oriented purple membranes showed that bacteriorhodopsin, which is an integral membrane protein, possesses a significant electrical dipole moment and demonstrates a liquid crystal-like ferroelectric behavior.2 This experiment was a direct confirmation of the theoretical model of ion channels in a biological membrane3,4 acting as electric switches between ferroelectric (closed, insulating) and paraelectric (open, ion-conducting) states. Plants and animal and human tissues (protein amino acids, pineal gland of brain, bones, skin, tendon, etc.) reveal pronounced piezoelectric5,6 and pyroelectric properties.7-9 Reports on the observation of pyroelectric effect7-9 was a first evidence of the existence of macroscopic spontaneous electrical polarization in bones. Application of an ac electric field to the cortical human bone allowed to observe reversal of the spontaneous polarization by recording dielectric hysteresis loop.10 Both piezoelectric and pyroelectric phenomena were related to collagen, which is an organic crystalline matrix of the bone composed from strongly aligned polar organic protein molecules.11 It was proposed that the piezoelectric effect plays an important physiological role in bone growth, remodeling, and fracture healing.12 * Corresponding author. E-mail:
[email protected]. † Rabin Medical Center. ‡ Tel Aviv University. 10.1021/nl049453i CCC: $27.50 Published on Web 06/04/2004
© 2004 American Chemical Society
In this paper we report on studies of piezoelectric effect in moist and dry human bones by the use of a piezoresponse force microscope (PFM). It allowed both to measure piezoelectric response with nanometer scale resolution directly in a collagen matrix and to obtain a piezoresponse image near the Haversian channel. Theoretical calculations, taking into account the inhomogeneity of the electric field under the PFM tip apex and screening of the applied electric field, were performed for obtaining the piezoelectric coefficient in bone collagen. Human adult humerus and tibia diaphysial fragments were used for sample preparation. Bones were supplied by The Israeli National Bone Bank at the Chaim Sheba Medical Center. All the bones were obtained from young ( 100 kHz), which was used for calculation of piezoelectric coefficient, is ∼20. The obtained data are consistent with those published in the work of Khutorsky and Lang.15 DC Nano Lett., Vol. 4, No. 7, 2004
δ R
δ is the distance between the tip apex and the crystal surface, d ) R + δ. The second term in the brackets (eq 2) takes into account the contribution of the conical part of the tip where J is the following expression: J)
∫0∞
(
1
d + xx + d 2
2
1 d + L + xx2 + (d + L)2
)
dx
(4)
The integral J depends on the cone length and on its distance 1255
from the surface d; the parameter β is defined as β ) ln
cos θ (11 -+ cos θ)
where θ is the half angle of the cone. To evaluate the actual deformation, the dielectric permittivity along (c) and perpendicular to (a) the diaphysial bone axis of the tip-sample system should be considered. Measured dielectric permittivity values at high frequency f∼1 MHz for all samples were very close c∼a∼20. The permittivity c of the studied moist and dry bones is characterized by a dispersion at low frequencies; it drops from ∼120 at 100 kHz for wet tibia to about 20 at 1 MHz at room temperature (Figure 3). The origin of the dielectric dispersion in bones at room temperature is ascribed to the orientational mobility of water molecules.15 The high density of Volkmann’s and Haversian canals, which are normal and parallel to the diaphysial bone axis, provides quasi-isotropic behavior of the dielectric permittivity of moist bone samples. In the experiments carried out here, the PFM tip electric field decreases sharply as a function of the distance from the surface so that the influence of water molecule orientational mobility in the bulk can be neglected. This means that the high frequency permittivity value has to be used for the piezoelectric coefficient calculation of bone samples. The tip radius was R ) 50 nm, the distance between the tip apex and the surface δ ) 0.5 nm, tip angle opening θ ) 12°, tip cone length L ) 10 µm. The integral J ∼ 5.3. Using eqs 1-3 and the experimental data (Figure 2), the piezoelectric coefficients were evaluated for points 1-4 as follows: 8.48 pC/N, 7.80 pC/N, 8.72 pC/N, 7.66 pC/N. Bone represents a microporous structure consisting of two different principal crystalline matrixes. They are mineral hydroxylapatite and the protein collagen. Hydroxylapatite has a centrosymmetrical crystallographic point group18 of 6/m and therefore cannot be a source of piezoelectric effect. Collagen is a family of proteins with very high tensile strength. It is the major fibrous component of skin, bone, tendon, cartilage, blood vessels, and teeth. Collagen molecules have a structural point group 3 which is asymmetric and demonstrates pyroelectric7,8,15 and piezoelectric5,10-12 properties. It was proposed11 that the macroscopic electrical dipole moment results from strongly oriented protein molecules composing the collagen matrix. In the collagen, peptide groups forming the intramolecular hydrogen bonds
1256
have a permanent electric dipole moment, which may primarily contribute to the piezoelectric polarization. We found dozens of papers on measurements of piezoelectric coefficients in animal and human bones as well in collagen. The results were widely discussed in some review papers showing a great inconsistency in the published data on bone symmetry, basic physics of generated strain-induced potentials, and values of the measured piezoelectric coefficients, which differed by 3 orders of magnitude.5,9,10,12 Our data are close to those obtained from bovine tendon, which consists of collagen fibers with highly oriented and crystallized collagen molecules.19,20 It may be assumed that the point-like PFM tip electrode allows to measure the piezoelectric coefficient directly in the collagen matrix. Close values of piezoelectric coefficients obtained in transverse cuts of moist and dry tibia and humerus bones and quasihomogeneous piezoresponse nanometer scale imaging of the studied bone samples (Figure 4b,c) are evidence that piezoelectric properties are uniform for the bones of a specific human individual. We believe that the proposed influence of piezoelectric effect on physiological properties of human bones12 will apply to the development of a nanometer resolution PFM method for the investigation of human aging problems concerned with reduction of the ability of bone to grow, remodeling, and fracture healing. References (1) Tasaki, I.; Byrne, P. M. Jpn. J. Physiol. 1993, 43, S67. (2) Ermolina, I.; Strinkovski, A.; Lewis, A.; Feldman, Y. J. Phys. Chem. B 2001, 105, 2673. (3) Bystrov, V. Ferroelectrics Lett. 1997, 23, 87. (4) Leuchtag, H. R.; Bystrov, V. S. Ferroelectrics 1999, 220, 157. (5) Fukada, E.; Yasuda, I. J. Phys. Soc. Jpn. 1957, 12, 1158. (6) Lemanov, V. Ferroelectrics 2000, 238, 211. (7) Lang, S. Nature 1966, 212, 704. (8) Lang, S. Ferroelectrics 1981, 34, 3. (9) Lang, S. IEEE Trans. Dielectr. Electr. Insul. 2000, 7, 466. (10) Hastings, G.; el Messiery, M. A.; Rakowski, S. Biomaterials 1981, 2, 225. (11) Athenstaedt, H. Ann. N. Y. Acad. Sci. 1974, 238, 68. (12) Hastings, G.; Mahmud, F. J. Biomed. Eng. 1988, 10, 515. (13) Urenski, P.; Gorbatov, N.; Rosenman, G. J. Appl. Phys. 2001, 89, 1850. (14) Agronin, A.; Molotskii, M.; Rosenwaks, Y.; Strassburg, E.; Boag, A.; Mutchnik, S.; Rosenman, G. J. Appl. Phys., submitted 2004. (15) Khutorsky, V.; Lang, S. Ferroelectrics Lett. 1993, 15, 153. (16) Saint Jean, M.; Hudlet, S.; Guthmann, C.; Berger, J. J. Appl. Phys. 1999, 86, 5245. (17) Molotskii, M. J. Appl. Phys. 2003, 93, 6234. (18) Kay, M.; Young, R.; Posner, A. Nature 1964, 204, 1050. (19) Fukada, E.; Yasuda, I. Jpn. J. Appl. Phys. 1964, 3, 117. (20) Marino, A.; Becker, R. Nature 1975, 253, 627.
NL049453I
Nano Lett., Vol. 4, No. 7, 2004
