Mechano-electric~ properties of bone G.W. Hastings, MA ElMessiery and S. Rakowski B/o-Medical Engineering Unit, North Staffordshire Polytechnic/Sta ffordshire Area Heatm Authority, c/o Medical institute, Hartshill, Stoke on Trent, UK (Received 16 March 1981: revised 28 April 1981)

Bone has been shown to exhibit ferro~ee~ic properties. The mlatianship between applied electric field and pola~zation shows a hysteresis character typical of this type of msterial. This implies a domain st~c~re for the permanent dipoles present in bone. Attempts to demonstrate semiconductor properties were unsuccessful although a change of electrical resistance with applied tensile strain was demonstrated. No effect on conductivity of bone with change of pH of the fluid in which it was immersed was shown and hence no confirmation of streaming potential effects was obt8ined.

The causal relationship between bone modeiling or remodelling and the mechanical stresses placed upon it is sufficiently well understood for clinical use to be made of it in the correction of congenital disorders of the skeleton’-3. In orthodontics the ability to move teeth through bone in response to applied stress is well proven. However, the way in which the mechanical forces are mediated to the tissues at cellular level has not been understood. When bone was found to have electrical properties which were dependent upon mechanical loading it was suggested that the potentials might mediate the biological processes4.

If it was a correct assumption that these potentials do have an effect on bone growth, then it was not surprising that the effect of externally introduced voltages or currents should be studied. Bassett, Pawluk and Becker implanted electrodes into the femoral cortex of dogs, with penetration into the meduiia~ cavity. Weak direct currents passed through the electrodes were shown to produce bone growth5. The observation that the electric potential on the surface of long bones was changed on fracture, the diaphysis being positively charged with respect to the bone ends whereas the fracture site became electro-negative6, led Brighton eta/. to study the effect of direct currents on fracture healing7. It does seem certain that this technique can produce union in certain fractures which have failed to heal. Consideration of some of the problems in the use of implantable electrodes led other groups to consider non-invasive methods. Bassett, Pawluk and Pilla introduced the use of a pulsed electro- magnetic field using two air cored Helmholtz-aiding coils placed on either side of the fracture’. Their programme has been reviewed9 and their work with that of others has also been reviewed”.

Research has been developed along two main directions. On the one hand there has been the development of clinical methods to treat ununited fractures, together with an attempt to understand the mechanism by which invasive and non-invasive methods function and the establishment of objective methods for assessment of clinical results. This has been complemented by various studies on the effects of electrical fields on living systems

0142-9612/81/~0225~9 $02.00 0 1981 IPC Business Press

reiated to orthopaedic and general applications”-‘3. On the other hand there has been a continued study of the origins of mechano-electrical effects in bone, considering bone as a composite material per se rather than being concerned for the physiological consequences of these effects.

The work reported in this paper belongs to the second category and proposes that the strain-dependent potentials observed in bone are consequent on its ferroelectric character and derive from its osteonic structure. The implications of this for normal and stimulated bone growth or fracture treatment are discussed briefly and this will be followed in detail in a subsequent publication.

Electrical response of bone to mechanical strain The work of Bassett4 showed that when bone was deformed a negative charge developed on the concave side i.e. on the side under compression. Attempts to make quantitative measurements are affected by the impedance matching between the bone sample and the measuring equipment and the shape and amplitude of the recorded potential may be modified14* “. One of the present authors16 has studied the frequency dependence of strain-generated potentials and although, in accordance with other results” a super- ficial relationship was found, a careful analysis of the measuring circuit showed that the characteristics of the recorded potential could be attributed to the circuit elements”. Therefore, before any confidence can be placed on the interpretation of bone potential measure- ments more consideration should be given to measuring- circuit parameters. The mechano-electrical response of bone has been studied under a wide range of conditions and it is shown to be a feature of living, freshly excised and dry bone. It is a property of bone material perse and is unrelated to cellular or other in viva factors. It is shown that collagen alone can produce this response” and from experimental results and for reasons of crystal symmetry, bone mineral is discounted as the source.

The ability of bone material to transduce mechanical loads to electrical response was called piezo-electric by

Biomaterials 8981, Vof 2 October 225

Mechano-electrical properties of bone: G.W. Hastings et al.

Fukada”. The spatial condition required for a crystal to be piezo-electric is that it should not have a centre of symmetry. The permanent electric dipoles already present in the unit cell will not therefore cancel eath other when the crystal is deformed but will produce a resultant dipole moment. Not all the crystal classes satisfy the condition for piezo-electric behaviour. A further condition is that there should be a linear stress-strain relationship. Viscoelasticity will complicate the relationship between applied stress and the polarization vector and the implication of this for bone will be discussed later.

The relationship between piezo-electric polarization P and mechanical stress u is expressed in terms of a series of twenty-seven constants of proportionality referred to as piezo-electric moduli d+“. When attempts were made to obtain experimental values for these moduli many dis- crepancies between results and the theoretical model were observed. Comparison of results is admittedly difficult since there is no standardization of sample preparation or of experimental conditions, and there may be no crystal class with a piezo-electric matrix corresponding exactly to that of bone. Particular problems in the application of classical theory are that the potential generated is dependent on strain gradientz2, and rotation of the bone sample by 180 degrees (end to end) does not change the sign of the potentia123. There is also an effect due to sample thickness. The potential was shown by 81ack17 to be directly related to strain rather than stress and this removes the argument from the commitment to the classical piezo-electric theory.

Consequently, various other models have been proposed to explain the phenomenon. Becker et al.24 claimed that bone should be treated as a semi-conductor. Hydroxyapatite crystals are classified as p-type semi- conductors and collagen crystallites as n-type. Results from photoconductive and photovoltaic studies were associated with p-n (apatite-collagen) semiconductor junctions. More recent confirmation appears to come from experiments in which application of infrared light leads to generation of photocurrent and ultra violet light appears to produce a permanent structural change.

Another proposal relates to the relationship between experiments carried out on dry bone samples in vitro and in vim A strain-related effect is certainly observed in viva

but since the water present may affect the symmetry considerations, other explanations have been sought for the origin of the potential. Cerquiglini26 proposed that streaming potentials could be invoked in explanation and this model is defended by others2’. This proposal suggests that it is the flow of bone tissue fluid resulting from external mechanical pressure that produces the electrical potential. This particular model is not necessarily contradictory of piezo-electricity but may be considered as a complementary process occurring in viva.

Bone as a ferroelectric material A subgroup of piezo-electric crystals is those that are pyroelectric. These produce electric charges on the surface during uniform heating and an additional structural require- ment is that the crystal should have a single polar axis and that a spontaneous electric polarization should exist in the absence of external electric fields. A further sub-group of pyroelectric crystals are called ferroelectric and are spon- taneously polarized dielectric materials. The crystal contains a number of domains and in each of these the polarization has a specific direction. The direction varies from one

domain to another and may be changed by the application of external electric fields.

The discovery that bone shows pyroelectric properties 2812g increased the credibility of the piezo- electric argument. It was decided, therefore, to investigate the ferroelectric properties of bone as further confirmation. The present authors have already published the preliminary results demonstrating that bone does indeed belong to this category of material. This paper gives a more detailed presentation of the ferroelectric studies and those directed to examination of the semiconductor and streaming potential propositions.

EXPERIMENTAL

All bone was taken from human tibiae following amputation and was obtained within twenty four hours. None of the patients had a known history of bone disease. The intact tibia was completely excised from the limb, cut into several pieces and after removal of marrow was defatted by immersion in trichloroethylene until no more fat was being extracted. The samples were then allowed to dry at room temperature for at least six weeks. The test pieces used in the different experiments were cut at the desired orientation and to the shape required using a diamond slitting wheel. This permitted very light loading of the sample during the cutting operation and by means of a low speed of rotation and water lubrication heating effects were avoided. Cylindrical samples were finished on a lathe. Although storage was usually at ambient conditions, test pieces were stored in vacua for two days prior to experimen- tation.

It did not prove possible to achieve uniform levels of decalcification throughout specimens to test the effect of this. Calcium levels were always lower on the surface than in the middle and this would invalidate any results obtained.

Electrodes were made using conductive silver paint (Acheson Colloid 21 Dag 915/50). The bone surface at the site of electrode attachment was polished with progressively finer grades of glass paper, washed with distilled water, acetone, water again and then dried. A thin layer of silver paint was applied and copper connecting leads were attached using the paint as adhesive. For experiments in which the bone was to be held between two metal electrodes, a layer of electrode jelly (Camjel, Cambridge Instruments) was interposed between sample and electrode.

Strain gauges were supplied by Kenyogo Ltd., Tokyo (gauge resistance 120 kO.3 ohm, gauge length 6 mm and gauge factor 2.14). A standard procedure was used to attach gauges to bone with Kenyogo P2 adhesive. A quarter bridge technique was used for the measurements. When wet bone samples were to be studied, the gauges were attached first to dry bone which was then rehydrated by immersing in deionized water for one week. Gauge resistance was not in general found to be changed.

For the measurements of ferroelectricity vacuum dried samples were prepared in rectangular form of thickness between 0.5 and 8 mm and electrodes and leads were attached to the two opposite parallel faces. Thickness and area of each sample was measured and the value of the capacitance determined.

The basic circuit for this study was first proposed by Sawyer3’ Figure 7). In this an a.c. high voltage from the transformer secondary is applied to the sample prepared as

226 Biomaterials 198 1, Vol2 October

Mechanoelectricalproperties of bone: G. W. Hastings et al.

a rectangular parallel plate capacitor. The applied electric field E, produces a displacement current D in the sample and this is made up of two components. One of these is due to the linear part of the dielectric constant of the sample f, the other to a non-linear polarization vector Pferr corres- ponding to the ferroelectric domains such that D = erE + 4?rPf,,. The mathematical relationship between V, and Vv (Figure 7) is shown to be the same as that between D and E. The D-E relationship for ferroelectric materials shows a hysteresis loop. Figure 2 shows the increase of polarization occurring when domains are rotated, (OA), saturation being attained at 6. As the external field E is reduced a polarization P, remains when E is zero. This is the remnant polarization and to remove it E must be reduced to a value E,, called the coercive field.

For poor ferroelectric materials it is necessary to eliminate a phase shift between V, and V,, arising from dissipative and real components in the dielectric constants expressive of charge leakage from one plate surface to the next. Furthermore, the linear capacitor effect must also be eliminated to ensure that horizontal saturation limits are obtained at the ends of the hysteresis loop, since at this point Pfem does not change but the slope is still proportional to E,.

A bridge technique was considered for the measure- ment but was not found satisfactory for bone and a phase shift technique modified from that proposed by Roetschi3’ was found to be satisfactory3’.

The phase shift between V, and V, was compensated for by using a 3-phase supply to produce a voltage with a phase difference of 90’ across RI and R2 (Figure 3). Impedance buffering was achieved using two 305 operational amplifiers as source followers, the output being fed into a 741 differential amplifier.

When the bone sample in rectangular form, prepared as discussed above, was under examination, a low voltage (20 VI was first applied to it and the elliptical display

H.T

t

Oscilloscope

1

<

_

i-t 1

1

Figure 1 Basic circuit proposed for measurement of ferroelectricity (Reference 301

Figure 2 Type of hysteresis loop for ferroelectric materials.

showing relationship between externally applied field E and internal polarization P

“$.‘~~~~‘:r _

Figure 3 Circuit used in this study to compensate for phase shifts

shown on the oscilloscope was reduced to linear form using the phase compensation unit. Applied voltage was progressively increased and displayed values of V, and V,, were recorded from which E and D were calculated. Voltage increase continued until the oscilloscope trace showed a linear relationship between Vv and Vx, implying saturation. This was usually in the region of E = 5.8 kV/cm (breakdown potential - 11 kV/cm). The field was applied in a direction normal to the bone shaft axis.

The apparatus in Figure 4 was used to study the effect of pressure on the D-E relationship, the force applied being measured with a B & K 8200 force transducer.

The thesis that bone components behave as a pressure sensitive semi-conductor junction was examined by applying stress to vacuum stored rectangular- bone samples (7.0 x 1 .l x 0.2 cm) by means of a Hounsfield tensometer. Strain was measured with strain gauges bonded to opposite faces of the sample and bone resistance by electrodes embedded into the sample and secured with silver conductive paint. Constant direct voltage was applied and the current measured with a Keithly 4145 picoammeter. Tensile and compressive stresses were applied by appropriate modifications of the test rig (Figure 5a) and for shear tests the sample was modified (Figure 5b). Electrical resistance was measured in both x and y directions respectively using end electrodes painted at the ends of the shear zone and edge electrodes painted along the edge of the shear zone in the y axis.

Hall effect measurements in which an applied current is deflected to upper or lower surfaces of the sample were made by applying a magnetic field to rectangular samples

&materials 1981, Vol2 October 227

Mechanoelectrical properties of bone: G. W. Hastings et al.

Figure 4 Apparatus used to apply pressure to bone samples

to determine whether the bone had any nett charge carriers and if so, to measure the Hall coefficient.

The effect of ionic fluids was studied using cylindrical samples (0.5-l .5 cm length, 0.3-0.4 cm diameter). These were immersed in deionized water for two weeks to try to ensure absence of ions, then after drying in vacua silver electrodes were painted on the end faces. The electrodes were sealed from water ingress by coating with epoxy resin and then encapsulating with silicone rubber. Samples were conditiond by immersion in solutions of known conductivity buffered to known pH with standard buffers. Resistance was measured with a Wayne Kerr bridge (model 347M). Temperature was controlled to f 0.05”C.

RESULTS

Mechanical properties

Stress-strain measurements were made on rectangular shaped dry specimens using strain gauges on different faces. A strain rate of 5 x 10v4 mm/s was used and viscoelastic behaviour was not considered. Combined results are shown in Figures 6 and 7 and Tables 1 and 2.

Electrical measurements Dielectric constant for samples of dry tibia was measured at 1.5 Hz and found to be 6.2 +0.31 in good agreement with other published values. The measured value of the electric breakdown strength subjected to a 50 Hz sinusoidal field was 11.79 + 0.28 kV/cm.

Table 1 Young’s modulus of dry bone

Site Direction E 1010 N/m2 Reference

Tibia

Tibia

Longitudinal 2.04 % 0.03 1.97 * 0.021 This work 2.12 * 0.03 2.25 r 0.02

Longitudinal 1 .72 Lakes 81 Katz 197733

Bovine Femur Longitudinal 2.31 Bonfield 197734

Femur Longitudinal 1 .5 Sweeney 196535

Table 2 Ultimate tensile strength of dry bone

UTS Site Direction I 08 N/m2 Reference

Tibia

Femur

Femur

Longitudinal 1.65 + 0.08 This work

Longitudinal 1.51 f 0.18 Burstein 81 Currey 197236

Longitudinal 0.087 ;ec&t337& Hirsch

Electromechanical behaviour

The results of frequency dependence and of parameters of the measuring circuit have been reported elsewhere16, 18. Although interpretation is uncertain due to restraints imposed by circuit factors, the variation with collagen fibre orientation shown by others was confirmed but the frequency effect may be totally dependent upon circuit elements and impedance matching.

Bone as a semiconductor

Variation of resistance with temperature was measured between ambient temperature and approximately 6O”C, temperature being controlled to f 0.5’C. The slope of the straight line plots obtained gives the value for the energy gap in the expression:

p = Aexp(Eg/2kt)

2 Y

\ I Strain

1 ww \ \ / Bone shaft

032cm n \\ v -x \

\

082cm

\

a c 6cm \

\ Electrodes

Z

Il6cm

f

t 8cm

b I

Figure 5 Arrangement of bone samples to study effect of: (al tensile and compressive forces and lb) shear forces

228 Biomaterials 1981, Vol2 October

0 2 4 6 8 IO 12

stro1n (x10-T

Figure 6 Stress/strain relationship for dry bone samples. Strain rate 5 x lo-Amm/s; room temperature; Young’s modulus

12.115+0.03231x 10qoN/m2

6

5 I

I / I I

5 6 7

Strain (arbitrary mts)

Figure 7 Sample taken to break. Ultimate strength of dry cortical human bone (tibia), A = Ultimate strength (1.65.~ l@ N/mY

where A = constant; E, = energy gap; p = resistivity; t =

temperature Kelvin.

Values of 42.5 + 1.2.37.3 f. 0.5 and 41.8 + 0.6 x

1O-2o Joules were obtained for the three samples and were

consistent with results reported elsewhere.

The voltage-current characteristic curve is shown in

Figure 8. The values of current as voltage increases up to

240V are the same as those obtained for a decreasing

voltage, but as reported by Becker et a/.24 the slope changes

when polarity is reversed.

The measurement of possible variation in bone

resistance in response to applied mechanical stress was used

to determine whether electron or hole flow occurred as a

result of external forces. No dependence was found on

compression (correlation coefficient 0.1) or shear forces

(correlation 0.12 for measurement along bone axis, 0.1 for

direction normal to axis). A cantilever bend test showed no

correlation between strain and resistance (0.1 correlation).

Samples were examined during application of tensile

stress, measuring resistance along the direction of the bone

axis. A significant linear increase in In R with tensile

strain was found (0.999 correlation) (Figure 9). If

resistance due to strain is expressed as Rsrmin = const*exp(as)

where a depends on the slope and s is the strain, values

obtained for a were 4.84 f 0.26 x low4 and 5.09 f 0.2 x low4

(microstrain)-‘.

Mechano-electrical properties of bone: G.W. Hastings et al.

240

1

220

200

/

180

160 I

140

z

’ 120 L

1001

80-

I I I I I I

0 2 4 6 8 -10 I2 14

Current (x 10-eomp)

Figure 8 Relationship between voltage and current for dry human bone at room temperature. 0, Voltage increasing; u, Voltage decreasing; polarity reversed: x, voltage increasing: A, voltage decreasing

2oor

ILLYcL3 0 50 100 150 200

Mmostraln

Figure 9 Variation of bone electrical resistance with applied strain. An effect was found only for tensile strain. Sample II; dry

bone; room temperature 1293 KI; slope (5.09 t- 0.2) x 10-A

Completely negative results were obtained for Hall

effect measurements using germanium for comparison.

Streaming potential investigation

Conductivity of cylindrical samples of tibia1 bone hydrated

in distilled water were found as 2.619, 2.684 and

2.26 x 10v2 ohm-’ cm-’ for three samples at 18°C. By

carrying out the experiment in distilled water at different

temperatures a value for the activation energy of water

molecules in bone was determined as 18.49 kO.26 k Joule

mole-’ (4.417 * 0.06 kcal mole-‘). This compares with a

value of 4.16 kcal mole-’ for D20 in water. The relation-

ship between bound and unbound water in bone needs to

be determined. This method could be extended to study

ion diffusion generally in bone.

The pH of the solution in which samples were placed

was changed by using a series of mixed Na,HPO, (0.2 M)

and citric acid (0.1 M) buffer solutions. The increase of

conductivity of the solution with pH at 32’C is shown in

Figure 70~1. Cylindrical bone samples prepared as described

Bromatenals 198 1. Vol2 October 229

Mechanoelectrical properties of bone: G.W. Hastings et al.

!”

9-

0-

d 3-

2-

I-

a 0 I I I I I I I

0 I 2 3 4 5 6 7 8

PH

I-

!_

b

:: 0

x” 0

x

0

b , I I I I I I I 2 3 4 5 6 7

PH

Figure 10 (a) Increase in solution conductivity as a function ofpH. Temperature 32’C; solution is a mixture of 0.2M Na2HPO4 and 0. 1M citric acid. (61 Variation of bone conductivity with pH when immersed in the solutions of (al. Four samples given

earlier were preconditioned in the solutions of different pH at 32°C for periods of two weeks monitoring pH and conductivities of solution and bone frequently until the latter value became constant. The experiment was commenced at a low pH value and after the constant conductivity value was obtained Na2HP04 was added to increase pH and the next level of conductivity was measured when a constant value was obtained. This was repeated in steps up to pH7. Results are shown in Figure 706.

Ferroelectric behaviour of bone

Using the phase compensation technique a standard 4pf capacitor was first used as a sample and by adjustment of the compensation unit and of resistance values (Rl, R2) the elliptical shape of the Vv-Vx response (D-E) was reduced to a straight line which held for values of V, up to 2 kV. When this capacitor was replaced by a known ferroelectric material, TGS, a hysteresis loop was observed at low values of V, with saturation at E = 0.8 kV/cm (Figure II). The frequency of the applied field was 50 Hz. Values of D

(displacement current) and E (applied electric field) were calculated from the following equations:

E = VJd = /3V,fd

where V, = voltage applied to sample i.e. total HT voltage; /3 = constant potential divider; d = sample thickness; V, =

voltage fed to oscilloscope.

D = V/A = Co&/A

and further derivation shows that:

D = Co Vov/A

where V,, is the amplitude of the voltage fed to the oscilloscope; A is the cross section of the sample; Co see Figure 3.

I Ill

b

Figure 11 la) Tracing from oscilloscope of Vv-Vx response of known ferroelectric crystal, TGS. lb) D-E relationship derived from results

230 Biomaterials 1981, Vo12 October

Figure 72 shows a typical hysteresis loop obtained

with bone at 20°C and a D-E curve derived from it. The

area within the loop represents electrical energy stored in

the material per unit volume per cycle. Results typically

ranged between 5.2 and 7.74 pJ/cm3 cycle.

When the applied field is reduced, polarization also

decreases but when the applied field is zero there remains

a remnant polarization (P,). To remove this the applied field

is reversed to the opposite direction and the field required

to restore nett polarization to zero is referred to as the

coercive field EC. Values of P, and EC obtained are shown in Table 3

together with values for energy stored. There does not

seem to be any effect of orientation.

When pressure was applied to the samples, a

completely linear D-E relationship pertained and Vv values

decreased. No significant variation in P,, EC and stored

energy value were found when temperature was increased

between 20” and 32°C.

DISCUSSION

Despite variation in techniques it was repeatedly impossible

to obtain positive results for Hall effect measurements. Any

b

/ / 2 4

EC kv/cml

Figure 12 la) Typical hysteresis response for dry bone at 2@C. lb) Typical D-E relationship for dry bone sample. The error bars represent the variation in the value of D from one sample to another

Mechano-electrical properties of bone: G.W. Hastings et al.

Table 3 Values of remnant polarization Pr, coercive field Ec and

stored energy for dry tibia1 samples. Effect of angle at which field was applied relative to bone main axis is shown. Temperature 20°C

Angle Energy Stored 1 Degrees Pr (ncb cm-z) E,(kVcm-1) (p J cm-scycle-1)

90 0.41 0.64 5.2 90 0.52 0.9 6.2 90 0.55 0.82 7.7 90 0.62 1 .l 6.5 60 0.58 0.85 7.4 45 0.68 0.95 7.9 30 0.48 0.81 6.6 0 0.62 0.85 7.6

effect should be independent of the orientation of any

supposed junctions because charges of opposite sign should

in any case be produced on opposite faces of the sample.

No evidence for semiconductor properties was obtained from

piezoresistivity studies investigating effects of compression,

shear and bending conditions on resistance. Hence, if bone

is a semiconductor, these results show that it is not able as

such to respond to these mechanical forces. Tensile forces

did produce significant resistance increase, however,

calculation of the energy term in the resistance-pressure

relationship of piezoresistivity theory (R = const.exp (E/k&9)) when applied to the tensile strain case gives a low value of

1.23 x low5 eV/microstain. This compared with a typical

result of 0.75 eV for an applied pressure of 1.013 x IO5 N/m2.

It should be noted that tensile forces applied to bone act

primarily on the collagen whereas compressive forces act

on the apatite mineral. This is expressed in the different

ratios of Youngs modulus for the two cases and generally

in the anisotropy of bone with respect to orientation

effects38. It is probable that the resistance change is a

consequence of collagen matrix response to tension rather

than an indication of semiconductor behaviour. There are

indeed anomalies in the electrical behaviour of bone, for

example the change in voltage-current characteristics with

reversal of polarity. Behari and Andrabi25 also obtained a

linear V-l relationship for forward and reverse bias but only

when the electrodes contacted similar components in the

sample i.e. when collagen-collagen or apatite-apatite

contact was made by their electrodes. When care was taken

to ensure collagen-apatite contact, p-n junction diode

characteristics were shown. Their results were fitted to a

theoretical expression derived from consideration of a

banded structure model. Localization of particular

components of bone structure is important in determining

the actual electrical response of bone components. This will

be discussed subsequently but we made no attempt to

achieve this.

Turning now to the investigation of streaming potential

characteristics, the strict concept of the movement of ionic

fluids through a stationary capillary cannot apply to bone

in which the solid phase of collagen-mineral composite

surrounding the capillary structures is deformed by virtue

of being the load-bearing part of the structure. Cignitti3’

did however, compare results from ionic fluid flowing

through bone in the absence and presence of mechanical

force applied to the bone. Their results indicate an added

effect due to electromechanical causes.

The present work was based on the proposition4’* 41

that at certain values of pH the streaming potential becomes

zero. A relationship between conductivity and streaming

potential indicates that conductivity is inversely proportional

to the zeta potential of the capillary and the streaming

Biomaterials 1981, Vol2 October 231

Mechenoeiectricef properties of bone: G.W, Hastings et al.

potential and at pH 4.7 the resistance to the movement of ions produced by the streaming potential should be a minimum42. Hence, the conductivity should show a peak at this point. The present results do not vary as expected on the basis of the streaming potential theory.

It is probable that the conditioning treatments given to the bone have affected its structure so that it is no longer typical and collagen may have undergone irreversible damage.

Apart from the effect of fluids on mechanical properties, e.g. that dry bone has greater stiffness than wet due to changes in the organic matrix3*, the movement of ions is of prize importance in establishing communications within an organism, Wjlliams in his Liversidge Lecture43 points out that it is changes in rates of flow that are so significant in transmitting signals to cells and which lead to changes in cell structure. He stresses that it is dynamics which are important in biological control and in affecting the variety of energized states of biological macromolecules which we refer to as structures.

Ferroelectric studies showed that the D-E relationship of dry cortical bone was characterised by a hysteresis loop comparable to that of a weakly ferroelectric material. This was repeatable with different samples irrespective of age, or site and orientation in the tibia. It is concluded therefore that ferroelectricity is an intrinsic property of dry bone and that its piezoelectric character is thereby confirmed. No result was obtained from moist bone since the leakage current became too great to permit compensation. This does not mean that the results can not be applied to moist bone unless the structural impli~tions of ferroelectrici~ (discussed below) are invalidated by changes occurring on hydration.

The structural implications are that bone possesses a domain structure with respect to charge distributions. The charged dipoles are arranged in domains and the orientation of them within the domains can be changed by the application of an external electric field. Applied mechanical forces can also produce a ~rturbation and can lead to a non~quilibrium situation in which the distortion of the dipoles leads to a nett measurable electric charge being produced. Since it is the deformation of the domain structure which is likely to be of more importance than the magnitude of the force per se this emphasises the significance of strain rather than stress. It is observed that mechanical restraint inhibits the effect of the applied field and suppresses ferroelectric behaviour.

Confirmatory evidence for an internal arrangement of dipoles into a domain structure comes from observations that bone can behave as an electret? These authors stress the importance of persistent charge storage effects. Both electret and ferroelectric behaviour require a grouping of dipoles in domains which can be affected by applied electrical fields. The importance of domain structures at the micro-level upon biological organisation has been discussed by Williams43. A micro domain can be energised separately within an organised layer, for example, in a membrane so that local ‘circuits’ for the movement of small ions can be set up.

Hence, local domains may have a very important role in monitoring the constant mechanical strains to which the bones are subjected and in controlling or triggering the trans- port of calcium and other ions at cellular level. Once a transport mechanism has been triggered there are various in-built amplification systems which will increase the effectiveness of the process.

232 Biometerials 1981, Vol2 October

The question is unanswered experimentally as to whether ferroelectricity is also present in moist bone and in viva. The dimensions of the collagen matrix will change with extent of hydration but it is not necessarily the case that an intrinsic property related to basic structural elements will be destroyed by such changes. A dry matrix may however be irretrievably different from its hydrated nature and firm conclusions await more evidence.

It may also be asked whether the electrical phenom- enon is of primary importance in determining cell regulation and hence growth or heating characteristics. The charges measured may be only an indication of structural deform- ation (strain) i.e. of secondary importance in being descriptive of conformational changes that have occurred in response to other factors. The healing of bone, in vivo

and other biological processes in vitro can be influenced by externally applied electrical fields, but this does not necessarily mean that these operate in viva under normal conditions. Different mechanisms may well be involved.

Further consideration of bone structure and relation- ship to growth and healing will be developed in a subsequent paper.

CONCLUSIONS

The present work has not found any evidence to confirm that bone is a semiconductor or that streaming potentials are a major factor in electro-mechanical behaviour. Dry bone does show ferroelectric behaviour. This relates it directly to piezoelectric materials and implies that it possesses a structure in which the charged dipoles are arranged in domains. The orientation within the domain can be changed by external electrical fields or mechanical forces.

ACKNOWLEDGEMENTS

The Department of Medical Photography, North Stafford- shire Hospital Centre, is thanked for assistance in preparation of diagrams and photographs. The provision of a Research Assistantship for one of the authors (M.A. ElMessiery) by the North Staffordshire Polytechnic permitted this work to be carried out.

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