Overview Fukada and Yasuda (5.1) first demonstrated that dry bone is piezoelectric in the classic sense, i.e.

mechanical stress results in electric polarization, the indirect effect; and an applied electric field causes strain, the converse effect. he piezoelectric properties of bone are of interest in vie! of their hypothesized role in bone remodellin" (#.$.1). %et colla"en (the protein in bone, tendon and li"ament), ho!ever, does not e&hibit piezoelectric response. 'tudies of the dielectric and piezoelectric properties of fully hydrated bone raise some doubt as to !hether !et bone is piezoelectric at all at physiolo"ical fre(uencies (5.$). )iezoelectric effects occur in the kilohertz ran"e, !ell above the ran"e of physiolo"ically si"nificant fre(uencies (5.$). *oth the dielectric properties (5.+) and the piezoelectric properties of bone (5.#) depend stron"ly upon fre(uency. he ma"nitude of the piezoelectric sensitivity coefficients of bone depends on fre(uency, on direction of load, and on relative humidity. ,alues up to -.. p/01 have been observed (5.#), to be compared !ith -.. and $.+ p/01 for different directions in (uartz, and 2-- p/01 in some piezoelectric ceramics. 3t is, ho!ever, uncertain !hether bone is piezoelectric in the classic sense at the relatively lo! fre(uencies !hich dominate in the normal loadin" of bone. he streamin" potentials e&amined ori"inally by 4nderson and 5riksson (5.5,5.2) can result in stress "enerated potentials at relatively lo! fre(uencies even in the presence of dielectric rela&ation or electrical conductivity but this process is as yet poorly understood. *ecker and co6!orkers (5.1765.$$) have also e&plored tissue electrical properties in connection !ith "ro!th, repair and re"eneration. For e&ample, (5.$$, 5.$+) partial limb re"eneration in rats !as stimulated by application of !eak electrical si"nals. 5lectrical si"nals in amphibians (5.$#), !hich can naturally re"enerate lost limbs, differ from those in mammals, !hich ordinarily do not re"enerate lost limbs. /artila"e (5.$) e&hibits electrical response to applied force. Piezoelectricity equations )iezoelectricity is a coupled field effect as is thermoelasticity (!hich "overns thermal e&pansion). 3n piezoelectric materials stress and strain are coupled to electrical field and polarization. 1ot all materials are piezoelectric; only those materials lackin" a center of symmetry on the atomic scale can be piezoelectric. 5&amples of piezoelectric materials include (uartz, 8ochelle salt, barium titanate, and lead titanate zirconate ceramics. )iezoelectric materials are used as vibratin" elements for time keepin", as emitters of sound (speakers) or ultrasound, and as microphones. For a piezoelectric material, in the linear domain, the constitutive e(uations are (9.+.1): ;i <=di>k? >k@=Ai>?, 5> @ =pi? i>< ='i>kl ?5, kl@=dki>? 5k @ =i>?5 (9.1-.1) (9.1-.$)

Bere ; is the electric displacement vector, d is the piezoelectric modulus tensor at constant temperature , A is the dielectric tensor at constant stress and temperature , 5 is the electric field vector, p is the pyroelectric coefficient at constant stress, is the strain, ' is the elastic compliance tensor at constant electric field,and is the thermal

e&pansion tensor. he usual 5instein summation convention over repeated subscripts is used. 3n a material described by these e(uations, the isothermal compliance measured at constant electric displacement ='i>kl?; differs =9.+.1? from the compliance measured at constant field ='i>kl?5: ='i>kl?; 6='i>kl?5 < 6dmi>dnkl=Amn?61. (9.1-.+)

)iezoelectric rela&ation refers to dependence of the piezoelectric coefficients on time or fre(uency. 'uch rela&ation has been observed in many materials, includin" ceramics =9.1-.$?,composites =9.1-.+?, and bone =9.1-.#?. 'uch rela&ation can be represented !ith comple& piezoelectric coefficients or by a piezoelectric loss tan"ent =9.1-.$?, =9.1-.5?. Cechanical rela&ation also occurs in piezoelectric materials and is important in applications: lar"e dampin" is considered desirable in materials used to "enerate short acoustic pulses for fla! detection =9.1-.2?; small dampin" (hi"h mechanical D) is desirable in stable resonators and hi"h po!er transducers. For materials !hich do rela&, the coefficients in 5(. 9.1-.1 and 5(. 9.1-.$ are comple&. he si"n is ne"ative since these are compliances. dEi>k< dFi>k 6 idGi>k AEi>< AFi> 6 iAGi> 'Ei>kl< 'Fi>kl 6 i'Gi>kl.

(9.1-.#)

Bone electricity: wet and dry )otentials observed in bent bone differ from predictions based on the results of e&periments performed in compression (5..). he piezoelectric polarization may conse(uently depend on the strain "radient (5..) as !ell as on the strain. his piezoelectric theory has been criticized as ad hoc by some authors, ho!ever, the idea has some appeal in vie! of FrostFs modelin" (#.1.+, #.1.#) and /urreyFs su""estion (#) that strain "radients may be si"nificant in this re"ard. he "radient theory is not ad hoc but can be obtained theoretically from "eneral nonlocality considerations (5.9). Coreover, "radient effects are kno!n in ferroelectric ceramics as ori"inally reported in the 8ussian literature and recently referred to as Gfle&o electricG. he physical mechanism for such effects is hypothesized to lie in the fibrous architecture of bone ($.1-..,$.1-.1-, $.1-.11). heoretical analyses of bone piezoelectricity (5.765.1$) maybe relevant to the issue of bone remodelin". 8ecent, thorou"h, studies have e&plored electromechanical effects in !et and dry bone. hey su""est that t!o different mechanisms are responsible for these effects: classical piezoelectricity due to the molecular asymmetry of colla"en in dry bone, and fluid flo! effects, possibly streamin" potentials in !et bone (5.1+). *one e&hibits additional electrical properties !hich are of interest. For e&ample, the dielectric behavior (e.". the dynamic comple& permittivity) "overns the relationship bet!een the applied electric field and the resultin" electric polarization and current. ;ielectric permittivity of bone has been found to increase dramatically !ith increasin" humidity and decreasin" fre(uency (5.$,5.+). For bone under partial hydration conditions, the dielectric permittivity(!hich determines the capacitance) can e&ceed 1,--- and the

dielectric loss tan"ent (!hich determines the ratio of conductivity to capacitance) can e&ceed unity. *oth the permittivity and the loss are "reater if the electric field is ali"ned parallel to the bone a&is. *one under conditions of full hydration in saline behaves differently: the behavior of bovine femoral bone is essentially resistive, !ith very little rela&ation (5.1#). he resistivity is about #56#9 ohm6m for the lon"itudinal direction, and three to four times "reater in the radial direction. hese values are to be compared !ith a resistivity of -..$ ohm6m for physiolo"ical saline alone. 'ince the resistivity of fully hydrated bone is about 1-- times "reater than that of bone under 79H relative humidity, it is su""ested that at 79H humidity the lar"er pores are not fully filled !ith fluid (5.1#). /ompact bone also e&hibits a permanent electric polarization as !ell as pyroelectricity, !hich is a chan"e of polarization !ith temperature (5.15,5.12). hese phenomena are attributed to the polar structure of the colla"en molecule; these molecules are oriented in bone. he orientation of permanent polarization has been mapped in various bones and has been correlated !ith developmental events. Regeneration 5lectrical properties of bone are relevant not only as a hypothesized feedback mechanism for bone remodellin", but also in the conte&t of e&ternal electrical stimulation of bone to aid its healin" and repair (5.1., 5.19, 5.17, 5.17a). 4&ial electric si"nals have been considered in li"ht of the ability of salamanders to re"enerate limbs (5.$-). *iolo"ical effects of electrical si"nals (5.$1) have been used to stimulate the re"ro!th of portions of amputated limbs in rats (5.$$) !hich usually do not re"enerate (5.$+, 5.$#). Core recently, electrical stimulation and trainin" has been used to reverse paralysis from spinal cord in>ury in rats (7). References 1. Banco&, 1.C., *iolo"y of *one, /ambrid"e Iniversity )ress, 17.$. $. 5vans, F.J., he mechanical properties of bone, homas, 'prin"field, 3ll, 17.+. +. Jordon, K. 5. 'tructures, )en"uin (179+) #. /urrey, K., he mechanical adaptations of bones, )rinceton Iniversity )ress, 179#. 5. 8eilly, ;. . and *urstein, 4. B., he mechanical properties of cortical bone, K. *one Knt. 'ur"., 524, 1--161-$$, 17.#. 2. /urrey, K.;., he mechanical properties of bone, /lin. Lrthop. 8el. 8es., .+, $1-6$+1, 17.-. .. )hillips, 8. %., 'cience of dental materials, %. *. 'aunders, 17.+. 5.1 Fukada, 5. and Yasuda, 3. Ln the piezoelectric effect of bone, K. )hys. 'oc. Kapan,1$, 11596112$ , 175.. 5.$. 8einish, J., 4. '. 1o!ick, )iezoelectric properties of bone as functions of moisture content, 1ature, $5+, 2$262$., 17.5. 5.+. Makes, 8. '. and Aatz, K. M., ;ielectric rela&ation in cortical bone, K. 4ppl. )hys.,#9, 9-96911, 17... 5.#.*ur, 4., Ceasurements of the dynamic piezoelectric properties of bone as a function of temperature and humidity, K. *iomech. 1, #7565-., 17.2. 5.5.4nderson, K. /. and 5riksson, /., 5lectrical properties of !et colla"en, 1ature, $19, 12.6127, 1729.

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5.$#. *ecker, 8. L., G he bioelectric factors in amphibian limb re"enerationG, Journal of Bone and Joint Surgery, #+64, 2#+6252, 1721. 5.$5. /. 4. M. *assett and 8. )a!luk, G5lectrical behavior of cartila"e durin" loadin"G, Science, 1.9, 79$679+, 17.$. For electronic access to early articles in Science and some other >ournals, see K' L8 archive or use the direct >ournal links provided. 9.+.1 1ye, K. F., Physical Properties of Crystals , L&ford Iniversity )ress, 17.2. 9.1-.1 Makes, 8. '., G'hape6dependent dampin" in piezoelectric solids,G 3555 rans. 'onics, Iltrasonics, 'I$., $-96$1+, (179-). 9.1-.$ Cartin, J. 5. G;ielectric, piezoelectric, and elastic losses in lon"itudinally polarized se"mented ceramic tubes,G I.'. 1avy K. Inder!ater 4coustics, 15,+$76++$, 4pr. 1725. 9.1-.+ Furuka!a, . and Fukada, 5. G)iezoelectric rela&ation in composite epo&y6)N system due to ionic conduction, Kap. K. 4ppl. )hys., 12, #5+6#59, Car. 17... 9.1-.# *ur, 4. K., GCeasurements of the dynamic piezoelectric properties of bone as a function of temperature and humidity,G K. *iomechanics, 7, #7565-., 17.2. 9.1-.5 Bolland, 8. G8epresentation of dielectric, elastic, and piezoelectric losses by comple& coefficients,G 3555 rans. 'onics Iltrason., 'I61#, 196$-, Kan. 172.. 9.1-.2 Kaffe, B. and *erlincourt, ;. 4., G)iezoelectric transducer materials,G )roc. 3555,5+, 1+.$61+92, 1725. 9.1-.. /ady, %. J., Piezoelectricity. 1e! York: ;over, 172#. 9.1-.9 Koffe,4. F., he Physics of Crystals. 1e! York: CcJra!6Bill, 17$9. 9.1-.7 G385 standards on piezoelectric crystals: Ceasurements of piezoelectric ceramics,G)roc. 385, #7, 112161127, Kuly 1721. 9.1-.1- 3555 'tandard on )iezoelectricity, 3555 1.2617.9; 3nst. 5lectrical, 5lectronics 5n"ineers, 1e! York, 17.9. 7. 8estorin" ,oluntary /ontrol of Mocomotion after )aralyzin" 'pinal /ord 3n>ury. 8ubia van den *rand, Kanine Beutschi, Duentin *arraud, Kack ;iJiovanna, Aay *artholdi, Cichele Buerlimann, Mucia Friedli, 3sabel ,ollen!eider, 5duardo Cartin Coraud, 'imone ;uis, 1adia ;ominici, 'ilvestro Cicera, )avel Cusienko, and Jre"oire /ourtine, Science 1 Kune $-1$: 119$61195.