Abstract

The objective of this study was to investigate whether the two most common growth mechanics modeling frameworks, the constrained-mixture growth model and the kinematic growth model, could be reconciled mathematically. The purpose of this effort was to provide practical guidelines for potential users of these modeling frameworks. Results showed that the kinematic growth model is mathematically consistent with a special form of the constrained-mixture growth model, where only one generation of a growing solid exists at any given time, overturning its entire solid mass at each instant of growth in order to adopt the reference configuration dictated by the growth deformation. The thermodynamics of the kinematic growth model, along with the specialized constrained-mixture growth model, requires a cellular supply of chemical energy to allow deposition of solid mass under a stressed state. A back-of-the-envelope calculation shows that the amount of chemical energy required to sustain biological growth under these models is negligibly small, when compared to the amount of energy normally consumed daily by the human body. In conclusion, this study successfully reconciled the two most popular growth theories for biological growth and explained the special circumstances under which the constrained-mixture growth model reduces to the kinematic growth model.

References

1.
Cowin
,
S.
, and
Hegedus
,
D.
,
1976
, “
Bone Remodeling I: Theory of Adaptive Elasticity
,”
J. Elasticity
,
6
(
3
), pp.
313
326
.10.1007/BF00041724
2.
Skalak
,
R.
,
Dasgupta
,
G.
,
Moss
,
M.
,
Otten
,
E.
,
Dullemeijer
,
P.
, and
Vilmann
,
H.
,
1982
, “
Analytical Description of Growth
,”
J. Theor. Biol.
,
94
(
3
), pp.
555
577
.10.1016/0022-5193(82)90301-0
3.
Rodriguez
,
E. K.
,
Hoger
,
A.
, and
McCulloch
,
A. D.
,
1994
, “
Stress-Dependent Finite Growth in Soft Elastic Tissues
,”
J. Biomech.
,
27
(
4
), pp.
455
467
.10.1016/0021-9290(94)90021-3
4.
Taber
,
L. A.
,
1995
, “
Biomechanics of Growth, Remodeling, and Morphogenesis
,”
ASME Appl. Mech. Rev.
,
48
(
8
), pp.
487
545
.10.1115/1.3005109
5.
Humphrey
,
J. D.
,
2021
, “
Constrained Mixture Models of Soft Tissue Growth and remodeling - Twenty Years After
,”
J. Elasticity
,
145
(
1–2
), pp.
49
75
.10.1007/s10659-020-09809-1
6.
Menzel
,
A.
, and
Kuhl
,
E.
,
2012
, “
Frontiers in Growth and Remodeling
,”
Mech. Res. Commun.
,
42
, pp.
1
14
.10.1016/j.mechrescom.2012.02.007
7.
Coleman
,
B. D.
, and
Gurtin
,
M. E.
,
1967
, “
Thermodynamics With Internal State Variables
,”
J. Chem. Phys.
,
47
(
2
), pp.
597
613
.10.1063/1.1711937
8.
Humphrey
,
J.
, and
Rajagopal
,
K.
,
2002
, “
A Constrained Mixture Model for Growth and Remodeling of Soft Tissues
,”
Math. Models Methods Appl. Sci.
,
12
(
3
), pp.
407
430
.10.1142/S0218202502001714
9.
Nims
,
R. J.
,
Cigan
,
A. D.
,
Albro
,
M. B.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
2014
, “
Synthesis Rates and Binding Kinetics of Matrix Products in Engineered Cartilage Constructs Using Chondrocyte-Seeded Agarose Gels
,”
J. Biomech.
,
47
(
9
), pp.
2165
2172
.10.1016/j.jbiomech.2013.10.044
10.
Myers
,
K.
, and
Ateshian
,
G. A.
,
2014
, “
Interstitial Growth and Remodeling of Biological Tissues: Tissue Composition as State Variables
,”
J. Mech. Behav. Biomed.
,
29
, pp.
544
556
.10.1016/j.jmbbm.2013.03.003
11.
Nims
,
R. J.
,
Cigan
,
A. D.
,
Albro
,
M. B.
,
Vunjak-Novakovic
,
G.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
2015
, “
Matrix Production in Large Engineered Cartilage Constructs is Enhanced by Nutrient Channels and Excess Media Supply
,”
Tissue Eng.. Part C
,
21
(
7
), pp.
747
757
.10.1089/ten.tec.2014.0451
12.
Ateshian
,
G. A.
,
Morrison
,
B.
, III
,
Holmes
,
J. W.
, and
Hung
,
C. T.
,
2012
, “
Mechanics of Cell Growth
,”
Mech. Res. Commun.
,
42
, pp.
118
125
.10.1016/j.mechrescom.2012.01.010
13.
Azeloglu
,
E. U.
,
Albro
,
M. B.
,
Thimmappa
,
V. A.
,
Ateshian
,
G. A.
, and
Costa
,
K. D.
,
2008
, “
Heterogeneous Transmural Proteoglycan Distribution Provides a Mechanism for Regulating Residual Stresses in the Aorta
,”
Am. J. Physiol. Heart Circ. Physiol.
,
294
(
3
), pp.
H1197
H1205
.10.1152/ajpheart.01027.2007
14.
Nims
,
R. J.
, and
Ateshian
,
G. A.
,
2017
, “
Reactive Constrained Mixtures for Modeling the Solid Matrix of Biological Tissues
,”
J. Elasticity
,
129
(
1–2
), pp.
69
105
.10.1007/s10659-017-9630-9
15.
Ateshian
,
G. A.
, and
Ricken
,
T.
,
2010
, “
Multigenerational Interstitial Growth of Biological Tissues
,”
Biomech. Model. Mechanobiol.
,
9
(
6
), pp.
689
702
.10.1007/s10237-010-0205-y
16.
Hsu
,
F. H.
,
1968
, “
The Influences of Mechanical Loads on the Form of a Growing Elastic Body
,”
J. Biomech.
,
1
(
4
), pp.
303
311
.10.1016/0021-9290(68)90024-9
17.
Garikipati
,
K.
,
Arruda
,
E. M.
,
Grosh
,
K.
,
Narayanan
,
H.
, and
Calve
,
S.
,
2004
, “
A Continuum Treatment of Growth in Biological Tissue: The Coupling of Mass Transport and Mechanics
,”
J. Mech. Phys. Solids
,
52
(
7
), pp.
1595
1625
.10.1016/j.jmps.2004.01.004
18.
Ambrosi
,
D.
,
Preziosi
,
L.
, and
Vitale
,
G.
,
2010
, “
The Insight of Mixtures Theory for Growth and Remodeling
,”
Z. Angew. Math. Phys.
,
61
(
1
), pp.
177
191
.10.1007/s00033-009-0037-8
19.
Ateshian
,
G. A.
,
Hung
,
C. T.
,
Weiss
,
J. A.
, and
Zimmerman
,
B. K.
,
2023
, “
Modeling Inelastic Responses Using Constrained Reactive Mixtures
,”
Eur. J. Mech. A/Solids
,
100
, p.
105009
.10.1016/j.euromechsol.2023.105009
20.
Kröner
,
E.
,
1959
, “
General Continuum Theory of Dislocations and Proper Stresses
,”
Arch. Rat. Mech. Anal.
,
4
(
1
), pp.
273
334
.https://www.neo-classicalphysics.info/uploads/3/4/3/6/34363841/kroner_-_nonlinear_theory.pdf
21.
Lee
,
E. H.
,
1968
, “
Elastic-Plastic Deformation at Finite Strains
,”
Stanford University, Division of Engineering Mechanics
, Report No. AD 678433.
22.
Rajagopal
,
K.
, and
Srinivasa
,
A.
,
1998
, “
Mechanics of the Inelastic Behavior of Materials—Part 1, Theoretical Underpinnings
,”
Int. J. Plast.
,
14
(
10–11
), pp.
945
967
.10.1016/S0749-6419(98)00037-0
23.
Truesdell
,
C.
, and
Toupin
,
R.
,
1960
, “
The Classical Field Theories
,”
Encyclopedia of Physics
, Vol. III/1,
Springer-Verlag
,
Berlin
.
24.
Kelly
,
P. D.
,
1964
, “
A Reacting Continuum
,”
Int. J. Eng. Sci.
,
2
(
2
), pp.
129
153
.10.1016/0020-7225(64)90001-1
25.
Ateshian
,
G. A.
, and
Zimmerman
,
B. K.
,
2022
, “
Continuum Thermodynamics of Constrained Reactive Mixtures
,”
ASME J. Biomech. Eng.
,
144
(
4
), p.
041011
.10.1115/1.4053084
26.
Ateshian
,
G. A.
,
Petersen
,
C. A.
,
Maas
,
S. A.
, and
Weiss
,
J. A.
,
2023
, “
A Numerical Scheme for Anisotropic Reactive Nonlinear Viscoelasticity
,”
ASME J. Biomech. Eng.
,
145
(
1
), p.
011004
.10.1115/1.4054983
27.
Baek
,
S.
,
Rajagopal
,
K. R.
, and
Humphrey
,
J. D.
,
2006
, “
A Theoretical Model of Enlarging Intracranial Fusiform Aneurysms
,”
ASME J. Biomech. Eng.
,
128
(
1
), pp.
142
149
.10.1115/1.2132374
28.
Bowen
,
R. M.
, and
Wiese
,
J.
,
1969
, “
Diffusion in Mixtures of Elastic Materials
,”
Int. J. Eng. Sci.
,
7
(
7
), pp.
689
722
.10.1016/0020-7225(69)90048-2
29.
Nims
,
R. J.
,
Durney
,
K. M.
,
Cigan
,
A. D.
,
Dusséaux
,
A.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
2016
, “
Continuum Theory of Fibrous Tissue Damage Mechanics Using Bond Kinetics: Application to Cartilage Tissue Engineering
,”
Interface Focus
,
6
(
1
), p.
20150063
.10.1098/rsfs.2015.0063
30.
Ateshian
,
G. A.
,
2015
, “
Viscoelasticity Using Reactive Constrained Solid Mixtures
,”
J. Biomech.
,
48
(
6
), pp.
941
947
.10.1016/j.jbiomech.2015.02.019
31.
Fung
,
Y. C.
,
1991
, “
What Are the Residual Stresses Doing in Our Blood Vessels?
,”
Ann. Biomed. Eng.
,
19
(
3
), pp.
237
249
.10.1007/BF02584301
32.
Zimmerman
,
B. K.
,
Jiang
,
D.
,
Weiss
,
J. A.
,
Timmins
,
L. H.
, and
Ateshian
,
G. A.
,
2021
, “
On the Use of Constrained Reactive Mixtures of Solids to Model Finite Deformation Isothermal Elastoplasticity and Elastoplastic Damage Mechanics
,”
J. Mech. Phys. Solids
,
155
, p.
104534
.10.1016/j.jmps.2021.104534
33.
Johnson
,
B. E.
, and
Hoger
,
A.
,
1995
, “
The Use of a Virtual Configuration in Formulating Constitutive Equations for Residually Stressed Elastic Materials
,”
J. Elasticity
,
41
(
3
), pp.
177
215
.10.1007/BF00041874
34.
Maas
,
S. A.
,
Erdemir
,
A.
,
Halloran
,
J. P.
, and
Weiss
,
J. A.
,
2016
, “
A General Framework for Application of Prestrain to Computational Models of Biological Materials
,”
J. Mech. Behav. Biomed.
,
61
, pp.
499
510
.10.1016/j.jmbbm.2016.04.012
35.
Ateshian
,
G. A.
,
2007
, “
On the Theory of Reactive Mixtures for Modeling Biological Growth
,”
Biomech. Model. Mechanobiol.
,
6
(
6
), pp.
423
445
.10.1007/s10237-006-0070-x
36.
Shim
,
J. J.
, and
Ateshian
,
G. A.
,
2022
, “
A Hybrid Reactive Multiphasic Mixture With a Compressible Fluid Solvent
,”
ASME J. Biomech. Eng.
,
144
(
1
), p.
011013
.10.1115/1.4051926
37.
Lai
,
W.
,
Hou
,
J.
, and
Mow
,
V.
,
1991
, “
A Triphasic Theory for the Swelling and Deformation Behaviors of Articular Cartilage
,”
ASME J. Biomech. Eng.
,
113
(
3
), pp.
245
258
.10.1115/1.2894880
38.
Shim
,
J. J.
, and
Ateshian
,
G. A.
,
2022
, “
A Hybrid Biphasic Mixture Formulation for Modeling Dynamics in Porous Deformable Biological Tissues
,”
Arch. Appl. Mech.
,
92
(
2
), pp.
491
511
.10.1007/s00419-020-01851-8
39.
de Onis
,
M.
, and
WHO Multicentre Growth Reference Study Group
,
2006
, “
WHO Child Growth Standards Based on Length/Height, Weight and Agetandards Based on Length/Height, Weight and Age
,”
Acta Paediatr.
,
95
(
S450
), pp.
76
85
.10.1111/j.1651-2227.2006.tb02378.x
40.
Liao
,
J. B.
,
Buhimschi
,
C. S.
, and
Norwitz
,
E. R.
,
2005
, “
Normal Labor: Mechanism and Duration
,”
Obstet. Gynecol. Clin. North Am.
,
32
(
2
), pp.
145
164
.10.1016/j.ogc.2005.01.001
41.
Hume
,
R.
, and
Weyers
,
E.
,
1971
, “
Relationship Between Total Body Water and Surface Area in Normal and Obese Subjects
,”
J. Clin. Pathol.
,
24
(
3
), pp.
234
238
.10.1136/jcp.24.3.234
42.
Huiskes
,
R.
,
Weinans
,
H.
,
Grootenboer
,
H. J.
,
Dalstra
,
M.
,
Fudala
,
B.
, and
Slooff
,
T. J.
,
1987
, “
Adaptive Bone-Remodeling Theory Applied to Prosthetic-Design Analysis
,”
J. Biomech.
,
20
(
11–12
), pp.
1135
1150
.10.1016/0021-9290(87)90030-3
43.
Weinans
,
H.
,
Huiskes
,
R.
, and
Grootenboer
,
H. J.
,
1992
, “
The Behavior of Adaptive Bone-Remodeling Simulation Models
,”
J. Biomech.
,
25
(
12
), pp.
1425
1441
.10.1016/0021-9290(92)90056-7
44.
National Research Council (US)
,
1989
,
Recommended Dietary Allowances
, 10th ed.,
National Academy Press
,
Washington, DC
.
45.
Cyron
,
C. J.
,
Aydin
,
R. C.
, and
Humphrey
,
J. D.
,
2016
, “
A Homogenized Constrained Mixture (and Mechanical Analog) Model for Growth and Remodeling of Soft Tissue
,”
Biomech. Model. Mechanobiol.
,
15
(
6
), pp.
1389
1403
.10.1007/s10237-016-0770-9
46.
Cyron
,
C. J.
, and
Humphrey
,
J. D.
,
2017
, “
Growth and Remodeling of Load-Bearing Biological Soft Tissues
,”
Meccanica
,
52
(
3
), pp.
645
664
.10.1007/s11012-016-0472-5
47.
Valentín
,
A.
, and
Humphrey
,
J. D.
,
2009
, “
Evaluation of Fundamental Hypotheses Underlying Constrained Mixture Models of Arterial Growth and Remodelling
,”
Philos. Trans. R. Soc., A
,
367
(
1902
), pp.
3585
–3
606
.10.1098/rsta.2009.0113
48.
Holmes
,
J. W.
,
2019
, “
Model First and Ask Questions Later: Confessions of a Reformed Experimentalist
,”
ASME J. Biomech. Eng.
,
141
(
7
), p.
074701
.10.1115/1.4043432
49.
Maas
,
S. A.
,
Ellis
,
B. J.
,
Ateshian
,
G. A.
, and
Weiss
,
J. A.
,
2012
, “
FEBio: Finite Elements for Biomechanics
,”
ASME J. Biomech. Eng.
,
134
(
1
), p.
011005
.10.1115/1.4005694
50.
Bonet
,
J.
, and
Wood
,
R. D.
,
1997
,
Nonlinear Continuum Mechanics for Finite Element Analysis
,
Cambridge University Press
,
Cambridge, UK
.
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