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Review

Bone remodeling and biological effects of mechanical stimulus

  • This review describes the physiology of normal bone tissue as an introduction to the subsequent discussion on bone remodeling and biomechanical stimulus. As a complex architecture with heterogeneous and anisotropic hierarchy, the skeletal bone has been anatomically analysed with different levelling principles, extending from nano- to the whole bone scale. With the interpretation of basic bone histomorphology, the main compositions in bone are summarized, including various organic proteins in the bone matrix and inorganic minerals as the reinforcement. The cell populations that actively participate in the bone remodeling—osteoclasts, osteoblasts and osteocytes—have also been discussed since they are the main operators in bone resorption and formation. A variety of factors affect the bone remodeling, such as hormones, cytokines, mechanical stimulus and electromagnetic stimulus. As a particularly potent stimulus for bone cells, mechanical forces play a crucial role in enhancing bone strength and preventing bone loss with aging. By combing all these aspects together, the information lays the groundwork for systematically understanding the link between bone physiology and orchestrated process of mechanically mediated bone homoestasis.

    Citation: Chao Hu, Qing-Hua Qin. Bone remodeling and biological effects of mechanical stimulus[J]. AIMS Bioengineering, 2020, 7(1): 12-28. doi: 10.3934/bioeng.2020002

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  • This review describes the physiology of normal bone tissue as an introduction to the subsequent discussion on bone remodeling and biomechanical stimulus. As a complex architecture with heterogeneous and anisotropic hierarchy, the skeletal bone has been anatomically analysed with different levelling principles, extending from nano- to the whole bone scale. With the interpretation of basic bone histomorphology, the main compositions in bone are summarized, including various organic proteins in the bone matrix and inorganic minerals as the reinforcement. The cell populations that actively participate in the bone remodeling—osteoclasts, osteoblasts and osteocytes—have also been discussed since they are the main operators in bone resorption and formation. A variety of factors affect the bone remodeling, such as hormones, cytokines, mechanical stimulus and electromagnetic stimulus. As a particularly potent stimulus for bone cells, mechanical forces play a crucial role in enhancing bone strength and preventing bone loss with aging. By combing all these aspects together, the information lays the groundwork for systematically understanding the link between bone physiology and orchestrated process of mechanically mediated bone homoestasis.


    For any two manifolds (M, g) and (N, h), a harmonic map ψ is the critical point of the energy functional defined as

    E(ψ)=12M|dψ|2dvg.

    The natural generalization of the harmonic maps was given by J. Eells and J. H. Sampson [1]. The established map ψ is called biharmonic if it is the critical point of energy functional

    E2(ψ)=12M|τ(ψ)|2dvg.

    with τ(ψ)=tr(dψ) as the vanishing tensor field for any harmonic map. For the above established E2, the first and second variation was studied by G. Y. Jiang [2]. For the same bi-harmonic functional, the associated Euler-Lagrange equation is τ2(ψ)=0, where τ2(ψ) is called bi-tension field and is defined as

    τ2(ψ)=Δτ(ψ)tr(RN(dψ,τ(ψ))dψ.

    In the above equation, Δ is the rough Laplacian acting on the sections of ψ1(TN) and RN is the curvature tensor for N. For any VΓ(ψ1(TN)) and X, Y Γ(TN), the definitions of Δ and RN are given by

    ΔV=tr(Δ2V),
    RN(X,Y)=[NX,NY]N[X,Y].

    A large number of studies have been done on biharmonic submanifolds [3,4,5,6,7,8]. It is a general fact that every harmonic map is biharmonic, but the vice-versa isn't true. The biharmonic maps, which are not harmonic, are called proper-biharmonic maps. If the harmonic map ψ is isometric immersion from the manifold (M,g) into (N,h), then the manifold M is called minimal submanifold of N. From the definition of proper biharmonic maps, it can be concluded that these are those submanifolds that aren't harmonic. Biharmonic submanifolds in different ambient spaces for different space forms have been extensively studied in the last few decades. Caddeo R. et al. [9] studied biharmonic submanifolds in spheres. Fetcu D. et al. [10,11,12] studied these submanifolds in complex, Sasakian and the product of sphere and real line space forms. J. Roth and A. Upadhyay [13,14] studied the biharmonic submanifolds on product spaces and generalized space forms. Chen B. Y. proved Chen's biharmonic conjecture stating that biharmonic surfaces do not exist in any Euclidean space with parallel normalized mean curvature vectors [15]. Yu F. et al. proved the same conjecture for hypersurfaces in R5 [16].

    The present study establishes the necessary and sufficient conditions for the submanifolds of Kaehler product manifolds to be biharmonic. Our future work then combines the work done in this paper with the techniques of singularity theory presented in [17,18,19,20]. We have derived the magnitude of scalar curvature for the hypersurfaces in a product of two spheres. We have also estimated the magnitude of the mean curvature vector for Lagrangian submanifolds in a product of two spheres. Finally, we proved the non-existence condition for totally complex Lagrangian submanifolds in a product of unit sphere and hyperbolic space.

    Let ˆMn and ˆMp be any Kehlerian manifolds of dimensions n (real dimension 2n) and p (real dimension 2p) respectively. Let us further assume Jn and Jp denote the almost complex structures of ˆMn and ˆMp, respectively. Suppose, ˆMn and ˆMp are complex space forms with constant holomorphic sectional curvatures c1 and c2, respectively. The Riemannian curvature tensor ˆRn of ˆMn(c1) is given by

    ˆRn(X,Y)Z = 14c1[gn(Y,Z)Xgn(X,Z)Y]

    + 14c1[gn(JnY,Z)JnXgn(JnX,Z)JnY+2gn(X,JnY)JnZ].

    Similarly, the Riemannian curvature tensor ˆRp of ˆMp(c2) is given by

    ˆRp(X,Y)Z = 14c2[gp(Y,Z)Xgp(X,Z)Y]

    + 14c2[gp(JpY,Z)JpXgp(JpX,Z)JpY+2gp(X,JpY)JpZ].

    For any generalized submanifold M of any complex space form N, the almost complex structure J induces the existence of four operators on M, namely

    j:TMTM,k:TMNM,l:NMTM,m:NMNM,

    defined for all X TM (tangent bundle) and ζNM (normal bundle) by

    JX=jX+kX,Jζ=lζ+mζ. (2.1)

    Since J is the almost complex structure, it satisfies J2 = Id. For any X, Y tangent to N, we also have g(JX,Y)=g(X,JY). Using the above properties of J, the relations for the operators, j, k, l and m are given as

    j2X+lkX+X=0, (2.2)
    m2ζ+klζ+ζ=0, (2.3)
    jlζ+lmζ=0, (2.4)
    kjX+mkX=0, (2.5)
    g(kX,ζ)+g(X,lζ)=0. (2.6)

    for all X Γ(TM) and ζΓ(NM). Also, j and m are skew-symmetric.

    Now, let us consider the Kaehler product manifold ˆMn(c1)׈Mp(c2) denoted by ˆM. If P and Q denote projection operators of the tangent spaces of ˆMn(c1) and ˆMp(c2), then we always have P2=P, Q2=Q and PQ=QP. If we put F=PQ, the properties of P and Q establish F2=I. This F is almost product structure of ˆMn(c1)׈Mp(c2). Moreover, we define a Riemannian metric g on ˆM as

    g(X, Y) = gn(PX,PY) + gp(QX,QY).

    Where X and Y are vector fields on ˆM. It further follows, g(FX,Y)=g(X,FY). If we put JX=JnPX+JpQX, we get JnP=PJ, JpQ=QJ, FJ=JF, g(JX,JY)=g(X,Y), ˆJ = 0. Thus J is the Kaehlerian structure on ˆM. The Riemannian curvature tensor ˆR of the product manifold ˆM is given as [21]

    R(X,Y)Z=c1+c216[g(Y,Z)Xg(X,Z)Y+g(JY,Z)JXg(JX,Z)JY+2g(X,JY)JZ+g(FY,Z)FXg(FX,Z)FY+g(FJY,Z)FJXg(FJX,Z)FJY+g(FZ,JY)FJZ]+c1c216[g(FY,Z)Xg(FX,Z)Y+g(Y,Z)FXg(X,Z)FY+g(FJY,Z)JXg(FJX,Z)JY+g(JY,Z)FJXg(JX,Z)FJY+2g(FX,JY)JZ+2g(X,JY)JFZ]. (2.7)

    The product structure F induces the existence of four operators:

    f:TMTM,h:TMNM,s:NMTMandt:NMNM,

    defined for all X TM (tangent bundle) and ζNM (normal bundle) by

    FX=fX+hX,Fζ=sζ+tζ. (2.8)

    These four operators follow the following relations

    f2X+shX=X, (2.9)
    t2ζ+hsζ=ζ, (2.10)
    fsζ+stζ=0, (2.11)
    hfX+thX=0, (2.12)
    g(hX,ζ)=g(X,sζ). (2.13)

    for all X Γ(TM) and ζΓ(NM). Also, f and t are symmetric.

    The first theorem gives necessary and sufficient condition for the manifold to be biharmonic.

    Theorem 3.1. Let M be a u-dimensional submanifold of the Kaehler product manifold ˆM = ˆMn(c1)׈Mp(c2) with A, B and H, respectively denoting the shape operator, second fundamental form and mean curvature vector. Then, this submanifold is biharmonic if and only if the following equations are satisfied:

    H+tr(B(.,AH.))+c1+c216[uH+3klH+hsHtr(f)tH+2(hjflH+tkflH+hjsmH+tksmH)tr(fj+sk)(hlH+tmH)]+c1c216[tr(f)HutH+3(kflH+ksmH)tr(fj+sk)(mH)+3(hjlH+tklH)]=0. (3.1)
    u2grad|H|2+2tr(AH(.))+c1+c28[3jlH+fsHtr(f)sH+2(fjflH+skflH+fjsmH+sksmH)tr(fj+sk)(flH+smH)]+c1c28[sHusH+3(jflH+jsmH)tr(fj+sk)(lH)+3(fjlH+sklH)]=0. (3.2)

    Proof. The equations of biharmonicity have been already established in [12,22,23]. Projection of the equation τ(ψ)=0 on both tangential and normal bundles establishes the following equations

    H+tr(B(.,AH.))+tr(ˉR(.,H.)=0,u2grad|H|2+2tr(AH(.))+2tr(ˉR(.,H.)=0. (3.3)

    Suppose that {Xi}ui=1 is a local orthonormal frame for TM, then by using the Eq 2.7 of curvarture tensor ˉR, we have

    tr(ˉR(.,H.)=ui=1ˉR(Xi,H)Xi, (3.4)

    tr(ˉR(.,H.) = ui=1{c1+c216[g(H,Xi)Xig(Xi,Xi)H+g(JH,Xi)JXi

    g(JXi,Xi)JH+2g(Xi,JH)JXi+g(FH,Xi)FXig(FXi,Xi)FH

    +g(FJH,Xi)FJXig(FJXi,Xi)FJH+g(FXi,JH)FJXi]

    +c1c216[g(FH,Xi)Xig(FXi,Xi)H+g(H,Xi)FXig(Xi,Xi)FH

    +g(FJH,Xi)JXig(FJXi,Xi)JH+g(JH,Xi)FJXig(JXi,Xi)FJH

    +2g(FXi,JH)JXi+2g(Xi,JH)JFXi]},

    Introducing the established sets of four operators, j, k, l and m and f, h, s and t for J and F respectively, we get the simplified equation as

    tr(ˉR(.,H.) = c1+c216[uH+ui=1g(lH,Xi)JXi+ui=12g(Xi,lH)JXi

    +F(FH)tr(f)FH+FJ(FJH)tr(fj+sk)FJH+FJ(FJH)]

    +c1c216[(FH)tr(f)HuFH+J(FJH)tr(fj+sk)JH

    +ui=1g(lH,Xi)FJXi+2J(FJH)+ui=12g(Xi,lH)JFXi],

    or tr(ˉR(.,H.) = c1+c216[uH+3JlH+fsH+hsHtr(f)sHtr(f)tH

    +2FJ(flH+smH)tr(fj+sk)FJH]

    +c1c216[sHtr(f)HuFH+J(flH+smH)tr(fj+sk)JH+

    3FJlH+2J(flH+smH)],

    tr(ˉR(.,H.) = c1+c216[uH+3jlH+3klH+fsH+hsHtr(f)sHtr(f)tH

    + 2(fjflH+hjflH+skflH+tkflH+fjsmH+hjsmH+sksmH+tksmH)

    tr(fj+sk)(flH+hlH+smH+tmH)]

    + c1c216[sHtr(f)HushutH+3(jflH+kflH+jsmH+ksmH)

    tr(fj+sk)(lH+mH)+3(fjlH+hjlH+sklH+tklH)].

    By identification of tangential and normal parts, we get the required equations.

    Corollary 3.2. If M is a u-dimensional totally real submanifold of the Kaehler product manifold ˆM = ˆMn(c1)׈Mp(c2). Then, this submanifold is biharmonic if and only if the following equations are satisfied

    H+tr(B(.,AH.))+c1+c216[uH+3klH+hsHtr(f)tH+2(tkflH+tksmH)tr(sk)(hlH+tmH)]+c1c216[tr(f)HutH+3(kflH+ksmH)tr(sk)(mH)+3(tklH)]=0. (3.5)
    u2grad|H|2+2tr(AH(.))+c1+c28[fsHtr(f)sH+2(skflH+sksmH)tr(sk)(flH+smH)]+c1c28[sHusHtr(sk)(lH)+3(sklH)]=0. (3.6)

    Proof. If M is a totally real submanifold, then we know that for any XΓ(TM), we have

    JX=kX,

    In other words, jX=0. Using this fact in Theorem 3.1, we get the required equations.

    Corollary 3.3. a): If M is any hypersurface of the Kaehler product manifold

    ˆM=ˆMp(c1)׈Mnp(c2).

    Then, M is biharmonic if and only if the following equations are satisfied

    H+tr(B(.,AH.))+c1+c216[(n2)H+hsHtr(f)tH+2(hjflH+tkflH)tr(fj+sk)(hlH)]+c1c216[tr(f)H(n1)tH+3(kflH)+3(tklH)]=0. (3.7)
    n12grad|H|2+2tr(AH(.))+c1+c28[fsHtr(f)sH+2(fjflH+skflH)tr(fj+sk)(flH)]+c1c28[sH(n1)sH+3(jflH)tr(fj+sk)(lH)3sH]=0. (3.8)

    b): If M is any totally real hypersurface of the Kaehler product manifold

    ˆM=ˆMp(c1)׈Mnp(c2).

    Then, M is biharmonic if and only if the following equations are satisfied:

    H+tr(B(.,AH.))+c1+c216[(n2)H+hsHtr(f)tH+2(tkflH)tr(sk)(hlH)]+c1c216[tr(f)H(n1)tH+3(kflH)+3(tklH)]=0. (3.9)
    n12grad|H|2+2tr(AH(.))+c1+c28[fsHtr(f)sH+2(skflH)tr(sk)(flH)]+c1c28[sH(n1)sHtr(sk)(lH)3sH]=0. (3.10)

    Proof. a): For any hypersurface M,J maps normal vectors to tangent vectors as such m=0. Using this fact with the Eqs 2.3 and 2.4 for H, we get the required equations from Theorem 3.1.

    b): For any totally real hypersurface M, we have j=0 and m=0.

    Corollary 3.4. If M is a u-dimensional Lagrangian manifold of the Kaehler product manifold

    ˆM=ˆMn(c1)׈Mp(c2).

    Then, M is biharmonic if and only if the following equations are satisfied

    H+tr(B(.,AH.))+c1+c216[(u+3)H+hsHtr(f)tH+2(tkflH)tr(sk)(hlH)]+c1c216[tr(f)HutH+3(kflH)+3(tklH)]=0. (3.11)
    u2grad|H|2+2tr(AH(.))+c1+c28[fsHtr(f)sH+2(skflH)tr(sk)(flH)]+c1c28[sHusHtr(sk)(lH)3(sH)]=0. (3.12)

    Proof. If M is a Lagrangian manifold, then j=0 and m=0. Using this fact with Eq 2.3, we get the required equations from Theorem 3.1.

    From now on, the authors will consider the ambient space to be product of two 2-spheres of same radius (for simplicity radius equals 1 unit). The reason for taking 2-sphere follows from[24] as it is the only sphere which accepts Kaehler structure. In the following equations, we will have

    c1+c216=c18=18andc1c28=b=0.

    To estimate the magnitude of mean curvature vector and scalar curvature, the authors will further assume the cases where F will map the whole of tangent bundle or normal vectors to respective bundles only. The reason being the equations involve the product of almost complex structure J and product structure F. As such it isn't possible to get simpler equations involving dimensions of submanifolds and mean curvature vector only.

    Proposition 3.5. Let M be any hypersurface of S2×S2 with non-zero constant mean curvature such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM). Then M is biharmonic if we have

    |B|2=18[1+1|H|2tr(sk)FJH,H]. (3.13)

    Proof. By the established hypothesis on F, we have f=0 and t=0. Using these equations along with Eqs 2.9 and 2.10 in Eq 3.7, we get

    H+tr(B(.,AH.))18[H+tr(sk)(hlH)]=0, (3.14)

    Since M is a hypersurface, the above equation becomes,

    tr(B(.,AH.))18[H+tr(sk)(hlH)]=0, (3.15)

    Since tr(B(.,AH.)) = |B|2H, on further simplifying, we get,

    |B|2H2=18[H2+tr(sk)hlH,H], (3.16)

    or

    |B|2=18[1+1|H|2tr(sk)FJH,H]. (3.17)

    Remark 3.6. It can be easily concluded from above proposition that there doesn't exist any hypersurface of S2×S2 when FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM) for

    tr(sk)FJH,H+|H|20.

    The above proposition can be used to derive the value of scalar curvature for biharmonic hypersurface M when FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM).

    Proposition 3.7. Let M be any proper-biharmonic hypersurface of S2×S2 with non-zero constant mean curvature such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM). Then the scalar curvature τ of M is given by

    τM=18[5+tr(sk)21|H|2tr(sk)FJH,H]+3|H|2.

    Proof. By the equation of Gauss, we have,

    τM=n1i,j=1ˉR(Xi,Xj)Xj,Xi|B|2+(n1)|H|2,

    The curvature tensor ˆR for S2×S2 is given by Eq 2.7 with

    c1+c216=c18=18andc1c28=0.

    And,

    ˆR(Xi,Xj)Xj,Xi=18[1+FXj,XjFXi,XiFXi,Xj2+FJXj,XjFXi,Xi], (3.18)

    Since FXiΓ(TM) and f=0. We have

    n1i,j=1ˆR(Xi,Xj)Xj,Xi=18[6+tr(sk)2]. (3.19)

    Using the value of |B|2 gives the required equation.

    Proposition 3.8. Let M be any totally complex-hypersurface of S2×S2 with non-zero constant mean curvature such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM). Then for trivially biharmonic M, we have

    |B|2=18. (3.20)

    Proof. By the established hypothesis on F, we have f=0 and t=0. Using these equations along with Eqs 2.9 and 2.10 in Theorem 3.1, we get

    H+tr(B(.,AH.))18H=0, (3.21)

    Since M is a hypersurface, the above equation becomes

    tr(B(.,AH.))18H=0. (3.22)

    Since tr(B(.,AH.)) = |B|2H. On further simplifying, we get the required equation.

    Proposition 3.9. Let M be any proper-biharmonic totally complex-hypersurface of S2×S2 with non-zero constant mean curvature such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM). Then the scalar curvature τ of M is given as

    τM=18[5+tr(sk)2]+3|H|2. (3.23)

    Proof. By the equation of Gauss, we have

    τM=n1i,j=1ˆR(Xi,Xj)Xj,Xi|B|2+(n1)|H|2,

    The curvature tensor ˆR for S2×S2 is given by Eq 2.7 with

    c1+c216=c18=18andc1c28=0.

    Then,

    ˆR(Xi,Xj)Xj,Xi=18[1+FXj,XjFXi,XiFXi,Xj2+FJXj,XjFXi,Xi]. (3.24)

    Since FXiΓ(TM) and f=0. We have

    n1i,j=1ˆR(Xi,Xj)Xj,Xi=18[6+tr(sk)2]. (3.25)

    Using the value of |B|2 gives the required equation.

    Corollary 3.10. Let M be u-dimensional Lagrangian submanifold of S2×S2 with non-zero constant mean curvature such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM). Let us further assume [tr(sk)FJH,H]0 Then we have

    a): If M is a proper-biharmonic, then 0<|H|2u+28u.

    b): If |H|2=u+28u, then M is biharmonic if and only if it is pseudo-umbilical manifold, H=0 and tr(sk) = 0.

    Proof. By the given hypothesis for F, we have f=0 and t=0.

    Implementing the above conditions along with Eq 2.9 in Corollary 3.4 a), we get,

    ΔH+tr(B(.,AH.))18[(u+2)Htr(sk)(hlH)]=0. (3.26)

    By taking the inner product with H, we get

    ΔH,H+|AH|218[(u+2)|H|2+tr(sk)FJH,H)]=0, (3.27)

    where AH is the shape operator associated with mean curvature vector H.

    Using Bochner formula, we get

    18(u+2)|H|2=|AH|2+|H|2+18tr(sk)FJH,H). (3.28)

    By the Cauchy-Schwarz inequality, we have |AH|2u|H|4. Using this fact, we have

    18(u+2)|H|2u|H|4+|H|2+18tr(sk)FJH,H)u|H|4+18tr(sk)FJH,H)u|H|4. (3.29)

    Since H is a non-zero constant, we have

    0<|H|2u+28u.

    If |H|2u+28u and M is proper-biharmonic, all of the above inequalities become equalities. Thus, we have H|2=0 and tr(sk)=0 as FJ is an isometry. Since the Cuachy-Schwarz inequality becomes equality, we have M as pseudo-umbilical.

    Remark 3.11. The cases for which FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM) establish the results comparable to those established in this paper. The proofs of all those results follow a similar procedure; thus, they haven't been discussed here.

    Finally, we discuss a non-existence case for the product of a unit sphere and a hyperbolic space. Out of all the discussed cases, the non-existence result can be found only for totally-complex Lagrangian submanifolds. Same has been discussed here:

    Proposition 3.12. There doesn't exist any proper biharmonic totally complex Lagrangian submanifold (dimension 2) with parallel mean curvature in S2×Hn2 such that FXΓ(TM) and FNΓ(TM) for any XΓ(TM) and NΓ(TM).

    Proof. Since mean curvature H is parallel and not identically zero. Therefore, FH isn't zero identically.

    M is trivially biharmonic, according to Theorem 3.1, we have

    u2grad|H|2+2tr(AH(.))+c1+c28[fsHtr(f)sH]+c1c28[sHusH3(sH)]=0. (3.30)

    For the above equation, we have c1+c2=0 and c1c2=2,

    or

    u2grad|H|2+2tr(AH(.))+14[(u+2)sH]=0. (3.31)

    Using the hypothesis, we have sH=0 or FH=0, which isn't possible.

    We established the necessary and sufficient conditions for the submanifolds of Kaehler product manifolds to be biharmonic. And we derived the magnitude of scalar curvature for the hypersurfaces in a product of two unit spheres. Also, for the same product, the magnitude of the mean curvature vector for Lagrangian submanifolds has been estimated. Finally, we proved the non-existence condition for totally complex Lagrangian submanifolds in a product of unit sphere and a hyperbolic space.

    The authors declare no conflict of interest.


    Acknowledgments



    The authors would like to acknowledge the financial support from Australian Research Council (Grant No. DP160102491).

    Conflict of interest



    The authors declare no conflict of interests.

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