Abstract

Physiological and pathological processes such as aging, diseases, treatments, and lactation can alter lacunar–canalicular network (LCN) morphology and perilacunar region properties. These modifications can impact the mechanical environment of osteocytes which in turn can influence osteocyte mechanosensitivity and the remodeling process. In this study, we aim to evaluate how the modifications in the canalicular morphology, lacunar density, and the perilacunar region properties influence the local mechanical environment of LCN and the apparent bone properties using three-dimensional finite element (FE) modeling. The simulation results showed that a 50% reduction in perilacunar elastic modulus led to about 7% decrease in apparent elastic modulus of the bone. The increase in canalicular density, length, and diameter did not influence the strain amplification in the models but they increased the amount of highly strained bone around LCN. Change in lacunar density did not influence the strain amplification and the amount of highly strained regions on LCN surfaces. Reduction in perilacunar elastic modulus increased both the strain amplification and the volume of highly strained tissue around and on the surface of LCN. The FE models of LCN in this study can be utilized to quantify the influence of modifications in canalicular morphology, lacunar density, and perilacunar region properties on the apparent bone properties and the local mechanical environment of LCN. Although this is a numerical study with idealized models, it provides important information on how mechanical environment of osteocytes is influenced by the modifications in LCN morphology and perilacunar region properties due to physiological and pathological processes.

References

1.
Marks
,
S. C.
, Jr.
, and
Popoff
,
S. N.
,
1988
, “
Bone Cell Biology: The Regulation of Development, Structure, and Function in the Skeleton
,”
Am. J. Anat.
,
183
(
1
), pp.
1
44
.10.1002/aja.1001830102
2.
Jahn
,
K.
,
Kelkar
,
S.
,
Zhao
,
H.
,
Xie
,
Y.
,
Tiede-Lewis
,
L. M.
,
Dusevich
,
V.
,
Dallas
,
S. L.
, and
Bonewald
,
L. F.
,
2017
, “
Osteocytes Acidify Their Microenvironment in Response to PTHrP in Vitro and in Lactating Mice in Vivo
,”
J. Bone Miner. Res.
,
32
(
8
), pp.
1761
1772
.10.1002/jbmr.3167
3.
Ashique
,
A. M.
,
Hart
,
L. S.
,
Thomas
,
C. D. L.
,
Clement
,
J. G.
,
Pivonka
,
P.
,
Carter
,
Y.
,
Mousseau
,
D. D.
, and
Cooper
,
D. M. L.
,
2017
, “
Lacunar-Canalicular Network in Femoral Cortical Bone Is Reduced in Aged Women and Is Predominantly Due to a Loss of Canalicular Porosity
,”
Bone Rep.
,
7
, pp.
9
16
.10.1016/j.bonr.2017.06.002
4.
Busse
,
B.
,
Djonic
,
D.
,
Milovanovic
,
P.
,
Hahn
,
M.
,
Puschel
,
K.
,
Ritchie
,
R. O.
,
Djuric
,
M.
, and
Amling
,
M.
,
2010
, “
Decrease in the Osteocyte Lacunar Density Accompanied by Hypermineralized Lacunar Occlusion Reveals Failure and Delay of Remodeling in Aged Human Bone
,”
Aging Cell
,
9
(
6
), pp.
1065
1075
.10.1111/j.1474-9726.2010.00633.x
5.
Carter
,
Y.
,
Thomas
,
C. D. L.
,
Clement
,
J. G.
, and
Cooper
,
D. M. L.
,
2013
, “
Femoral Osteocyte Lacunar Density, Volume and Morphology in Women Across the Lifespan
,”
J. Struct. Biol.
,
183
(
3
), pp.
519
526
.10.1016/j.jsb.2013.07.004
6.
Vashishth
,
D.
,
Verborgt
,
O.
,
Divine
,
G.
,
Schaffler
,
M.
, and
Fyhrie
,
D. P.
,
2000
, “
Decline in Osteocyte Lacunar Density in Human Cortical Bone Is Associated With Accumulation of Microcracks With Age
,”
Bone
,
26
(
4
), pp.
375
380
.10.1016/S8756-3282(00)00236-2
7.
Carpentier
,
V. T.
,
Wong
,
J.
,
Yeap
,
Y.
,
Gan
,
C.
,
Sutton-Smith
,
P.
,
Badiei
,
A.
,
Fazzalari
,
N. L.
, and
Kuliwaba
,
J. S.
,
2012
, “
Increased Proportion of Hypermineralized Osteocyte Lacunae in Osteoporotic and Osteoarthritic Human Trabecular Bone: Implications for Bone Remodeling
,”
Bone
,
50
(
3
), pp.
688
694
.10.1016/j.bone.2011.11.021
8.
Mullender
,
M. G.
,
Tan
,
S. D.
,
Vico
,
L.
,
Alexandre
,
C.
, and
Klein-Nulend
,
J.
,
2005
, “
Differences in Osteocyte Density and Bone Histomorphometry Between Men and Women and Between Healthy and Osteoporotic Subjects
,”
Calcif. Tissue Int.
,
77
(
5
), pp.
291
296
.10.1007/s00223-005-0043-6
9.
Qiu
,
S.
,
Rao
,
D. S.
,
Palnitkar
,
S.
, and
Parfitt
,
A. M.
,
2003
, “
Reduced Iliac Cancellous Osteocyte Density in Patients With Osteoporotic Vertebral Fracture
,”
J. Bone Miner. Res.
,
18
(
9
), pp.
1657
1663
.10.1359/jbmr.2003.18.9.1657
10.
van Hove
,
R. P.
,
Nolte
,
P. A.
,
Vatsa
,
A.
,
Semeins
,
C. M.
,
Salmon
,
P. L.
,
Smit
,
T. H.
, and
Klein-Nulend
,
J.
,
2009
, “
Osteocyte Morphology in Human Tibiae of Different Bone Pathologies With Different Bone Mineral Density–Is There a Role for Mechanosensing?
,”
Bone
,
45
(
2
), pp.
321
329
.10.1016/j.bone.2009.04.238
11.
Hemmatian
,
H.
,
Jalali
,
R.
,
Semeins
,
C. M.
,
Hogervorst
,
J. M.
,
van Lenthe
,
G. H.
,
Klein-Nulend
,
J.
, and
Bakker
,
A. D.
,
2018
, “
Mechanical Loading Differentially Affects Osteocytes in Fibulae From Lactating Mice Compared to Osteocytes in Virgin Mice: Possible Role for Lacuna Size
,”
Calcif. Tissue Int.
,
103
(
6
), pp.
675
685
.10.1007/s00223-018-0463-8
12.
Kaya
,
S.
,
Basta-Pljakic
,
J.
,
Seref-Ferlengez
,
Z.
,
Majeska
,
R. J.
,
Cardoso
,
L.
,
Bromage
,
T. G.
,
Zhang
,
Q.
,
Flach
,
C. R.
,
Mendelsohn
,
R.
,
Yakar
,
S.
,
Fritton
,
S. P.
, and
Schaffler
,
M. B.
,
2017
, “
Lactation‐Induced Changes in the Volume of Osteocyte Lacunar‐Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue
,”
J. Bone Miner. Res.
,
32
(
4
), pp.
688
697
.10.1002/jbmr.3044
13.
Qing
,
H.
,
Ardeshirpour
,
L.
,
Pajevic
,
P. D.
,
Dusevich
,
V.
,
Jähn
,
K.
,
Kato
,
S.
,
Wysolmerski
,
J.
,
Bonewald
,
L. F.
, and
Research
,
M.
,
2012
, “
Demonstration of Osteocytic Perilacunar/Canalicular Remodeling in Mice During Lactation
,”
Bone
,
27
(
5
), pp.
1018
1029
.10.1002/jbmr.1567
14.
Li
,
Y.
,
de Bakker
,
C. M. J.
,
Lai
,
X.
,
Zhao
,
H.
,
Parajuli
,
A.
,
Tseng
,
W.-J.
,
Pei
,
S.
,
Meng
,
T.
,
Chung
,
R.
,
Wang
,
L.
, and
Liu
,
X. S.
,
2021
, “
Maternal Bone Adaptation to Mechanical Loading During Pregnancy, Lactation, and Post-Weaning Recovery
,”
Bone
,
151
, p.
116031
.10.1016/j.bone.2021.116031
15.
Milovanovic
,
P.
,
Zimmermann
,
E. A.
,
Hahn
,
M.
,
Djonic
,
D.
,
Püschel
,
K.
,
Djuric
,
M.
,
Amling
,
M.
, and
Busse
,
B.
,
2013
, “
Osteocytic Canalicular Networks: Morphological Implications for Altered Mechanosensitivity
,”
ACS Nano
,
7
(
9
), pp.
7542
7551
.10.1021/nn401360u
16.
Tiede-Lewis
,
L. M.
,
Xie
,
Y.
,
Hulbert
,
M. A.
,
Campos
,
R.
,
Dallas
,
M. R.
,
Dusevich
,
V.
,
Bonewald
,
L. F.
, and
Dallas
,
S. L.
,
2017
, “
Degeneration of the Osteocyte Network in the C57BL/6 Mouse Model of Aging
,”
Aging (Albany NY)
,
9
(
10
), pp.
2190
2208
.10.18632/aging.101308
17.
Kobayashi
,
K.
,
Nojiri
,
H.
,
Saita
,
Y.
,
Morikawa
,
D.
,
Ozawa
,
Y.
,
Watanabe
,
K.
,
Koike
,
M.
,
Asou
,
Y.
,
Shirasawa
,
T.
,
Yokote
,
K.
,
Kaneko
,
K.
, and
Shimizu
,
T.
,
2015
, “
Mitochondrial Superoxide in Osteocytes Perturbs Canalicular Networks in the Setting of Age-Related Osteoporosis
,”
Sci. Rep.
,
5
(
1
), p.
9148
.10.1038/srep09148
18.
Ciani
,
A.
,
Toumi
,
H.
,
Pallu
,
S.
,
Tsai
,
E. H. R.
,
Diaz
,
A.
,
Guizar-Sicairos
,
M.
,
Holler
,
M.
,
Lespessailles
,
E.
, and
Kewish
,
C. M.
,
2018
, “
Ptychographic X-Ray CT Characterization of the Osteocyte Lacuno-Canalicular Network in a Male Rat's Glucocorticoid Induced Osteoporosis Model
,”
Bone Rep.
,
9
, pp.
122
131
.10.1016/j.bonr.2018.07.005
19.
Schurman
,
C. A.
,
Verbruggen
,
S. W.
, and
Alliston
,
T.
,
2021
, “
Disrupted Osteocyte Connectivity and Pericellular Fluid Flow in Bone With Aging and Defective TGF-β Signaling
,”
Proc. Natl. Acad. Sci.
,
118
(
25
), p.
e2023999118
.10.1073/pnas.2023999118
20.
Hemmatian
,
H.
,
Conrad
,
S.
,
Furesi
,
G.
,
Mletzko
,
K.
,
Krug
,
J.
,
Faila
,
A. V.
,
Kuhlmann
,
J. D.
,
Rauner
,
M.
,
Busse
,
B.
, and
Jahn-Rickert
,
K.
,
2021
, “
Reorganization of the Osteocyte Lacuno-Canalicular Network Characteristics in Tumor Sites of an Immunocompetent Murine Model of Osteotropic Cancers
,”
Bone
,
152
, p.
116074
.10.1016/j.bone.2021.116074
21.
Lai
,
X.
,
Price
,
C.
,
Modla
,
S.
,
Thompson
,
W. R.
,
Caplan
,
J.
,
Kirn-Safran
,
C. B.
, and
Wang
,
L.
,
2015
, “
The Dependences of Osteocyte Network on Bone Compartment, Age, and Disease
,”
Bone Res.
,
3
, p.
15009
.10.1038/boneres.2015.9
22.
Dole
,
N. S.
,
Mazur
,
C. M.
,
Acevedo
,
C.
,
Lopez
,
J. P.
,
Monteiro
,
D. A.
,
Fowler
,
T. W.
,
Gludovatz
,
B.
,
Walsh
,
F.
,
Regan
,
J. N.
,
Messina
,
S.
,
Evans
,
D. S.
,
Lang
,
T. F.
,
Zhang
,
B.
,
Ritchie
,
R. O.
,
Mohammad
,
K. S.
, and
Alliston
,
T.
,
2017
, “
Osteocyte-Intrinsic TGF-β Signaling Regulates Bone Quality Through Perilacunar/Canalicular Remodeling
,”
Cell Rep.
,
21
(
9
), pp.
2585
2596
.10.1016/j.celrep.2017.10.115
23.
Tokarz
,
D.
,
Martins
,
J. S.
,
Petit
,
E. T.
,
Lin
,
C. P.
,
Demay
,
M. B.
, and
Liu
,
E. S.
,
2018
, “
Hormonal Regulation of Osteocyte Perilacunar and Canalicular Remodeling in the Hyp Mouse Model of X-Linked Hypophosphatemia
,”
J. Bone Miner. Res.
,
33
(
3
), pp.
499
509
.10.1002/jbmr.3327
24.
Rux
,
C. J.
,
Vahidi
,
G.
,
Darabi
,
A.
,
Cox
,
L. M.
, and
Heveran
,
C. M.
,
2022
, “
Perilacunar Bone Tissue Exhibits Sub-Micrometer Modulus Gradation Which Depends on the Recency of Osteocyte Bone Formation in Both Young Adult and Early-Old-Age Female C57Bl/6 Mice
,”
Bone
,
157
, p.
116327
.10.1016/j.bone.2022.116327
25.
Lane
,
N. E.
,
Yao
,
W.
,
Balooch
,
M.
,
Nalla
,
R. K.
,
Balooch
,
G.
,
Habelitz
,
S.
,
Kinney
,
J. H.
, and
Bonewald
,
L. F.
,
2006
, “
Glucocorticoid‐Treated Mice Have Localized Changes in Trabecular Bone Material Properties and Osteocyte Lacunar Size That Are Not Observed in Placebo‐Treated or Estrogen‐Deficient Mice
,”
J. Bone Miner. Res.
,
21
(
3
), pp.
466
476
.10.1359/JBMR.051103
26.
Damrath
,
J. G.
,
Moe
,
S. M.
, and
Wallace
,
J. M.
,
2022
, “
Calcimimetics Alter Periosteal and Perilacunar Bone Matrix Composition and Material Properties in Early Chronic Kidney Disease
,”
J. Bone Miner. Res.
,
37
(
7
), pp.
1297
1306
.10.1002/jbmr.4574
27.
Stern
,
A. R.
,
Yao
,
X.
,
Wang
,
Y.
,
Berhe
,
A.
,
Dallas
,
M.
,
Johnson
,
M. L.
,
Yao
,
W.
,
Kimmel
,
D. B.
, and
Lane
,
N. E.
,
2018
, “
Effect of Osteoporosis Treatment Agents on the Cortical Bone Osteocyte Microenvironment in Adult Estrogen-Deficient, Osteopenic Rats
,”
Bone Rep.
,
8
, pp.
115
124
.10.1016/j.bonr.2018.02.005
28.
Nicolella
,
D. P.
,
Moravits
,
D. E.
,
Gale
,
A. M.
,
Bonewald
,
L. F.
, and
Lankford
,
J.
,
2006
, “
Osteocyte Lacunae Tissue Strain in Cortical Bone
,”
J. Biomech.
,
39
(
9
), pp.
1735
1743
.10.1016/j.jbiomech.2005.04.032
29.
Verbruggen
,
S. W.
,
Mc Garrigle
,
M. J.
,
Haugh
,
M. G.
,
Voisin
,
M. C.
, and
McNamara
,
L. M.
,
2015
, “
Altered Mechanical Environment of Bone Cells in an Animal Model of Short- and Long-Term Osteoporosis
,”
Biophys. J.
,
108
(
7
), pp.
1587
1598
.10.1016/j.bpj.2015.02.031
30.
Burr
,
D. B.
,
Milgrom
,
C.
,
Fyhrie
,
D.
,
Forwood
,
M.
,
Nyska
,
M.
,
Finestone
,
A.
,
Hoshaw
,
S.
,
Saiag
,
E.
, and
Simkin
,
A.
,
1996
, “
In Vivo Measurement of Human Tibial Strains During Vigorous Activity
,”
Bone
,
18
(
5
), pp.
405
410
.10.1016/8756-3282(96)00028-2
31.
Yang
,
P.
,
Brüggemann
,
G.-P.
, and
Rittweger
,
J.
,
2011
, “
What Do We Currently Know From in Vivo Bone Strain Measurements in Humans?
,”
J. Musculoskeletal Neuronal Interact.
,
11
(
1
), pp.
8
20
.https://www.ismni.org/jmni/pdf/43/02YANG.pdf
32.
Bonivtch
,
A. R.
,
Bonewald
,
L. F.
, and
Nicolella
,
D. P.
,
2007
, “
Tissue Strain Amplification at the Osteocyte Lacuna: A Microstructural Finite Element Analysis
,”
J. Biomech.
,
40
(
10
), pp.
2199
2206
.10.1016/j.jbiomech.2006.10.040
33.
Cen
,
H.
,
Yao
,
Y.
,
Liu
,
H.
,
Jia
,
S.
, and
Gong
,
H.
,
2021
, “
Multiscale Mechanical Responses of Young and Elderly Human Femurs: A Finite Element Investigation
,”
Bone
,
153
, p.
116125
.10.1016/j.bone.2021.116125
34.
Wang
,
L.
,
Dong
,
J.
, and
Xian
,
C. J.
,
2015
, “
Strain Amplification Analysis of an Osteocyte Under Static and Cyclic Loading: A Finite Element Study
,”
BioMed Res. Int.
,
2015
, p.
376474
.10.1155/2015/376474
35.
Verbruggen
,
S. W.
,
Vaughan
,
T. J.
, and
McNamara
,
L. M.
,
2016
, “
Mechanisms of Osteocyte Stimulation in Osteoporosis
,”
J. Mech. Behav. Biomed. Mater.
,
62
, pp.
158
168
.10.1016/j.jmbbm.2016.05.004
36.
Varga
,
P.
,
Hesse
,
B.
,
Langer
,
M.
,
Schrof
,
S.
,
Männicke
,
N.
,
Suhonen
,
H.
,
Pacureanu
,
A.
,
Pahr
,
D.
,
Peyrin
,
F.
, and
Raum
,
K.
,
2015
, “
Synchrotron X-Ray Phase Nano-Tomography-Based Analysis of the Lacunar–Canalicular Network Morphology and Its Relation to the Strains Experienced by Osteocytes In Situ as Predicted by Case-Specific Finite Element Analysis
,”
Biomech. Model. Mechanobiol.
,
14
(
2
), pp.
267
282
.10.1007/s10237-014-0601-9
37.
Verbruggen
,
S. W.
,
Vaughan
,
T. J.
, and
McNamara
,
L. M.
,
2012
, “
Strain Amplification in Bone Mechanobiology: A Computational Investigation of the In Vivo Mechanics of Osteocytes
,”
J. R. Soc., Interface
,
9
(
75
), pp.
2735
2744
.10.1098/rsif.2012.0286
38.
Kola
,
S. K.
,
Begonia
,
M. T.
,
Tiede-Lewis
,
L. M.
,
Laughrey
,
L. E.
,
Dallas
,
S. L.
,
Johnson
,
M. L.
, and
Ganesh
,
T.
,
2020
, “
Osteocyte Lacunar Strain Determination Using Multiscale Finite Element Analysis
,”
Bone Rep.
,
12
, p.
100277
.10.1016/j.bonr.2020.100277
39.
Vaughan
,
T. J.
,
Verbruggen
,
S. W.
, and
McNamara
,
L. M.
,
2013
, “
Are All Osteocytes Equal? Multiscale Modelling of Cortical Bone to Characterise the Mechanical Stimulation of Osteocytes
,”
Int. J. Numer. Methods Biomed. Eng.
,
29
(
12
), pp.
1361
1372
.10.1002/cnm.2578
40.
Hemmatian
,
H.
,
Bakker
,
A. D.
,
Klein-Nulend
,
J.
, and
van Lenthe
,
G. H.
,
2021
, “
Alterations in Osteocyte Lacunar Morphology Affect Local Bone Tissue Strains
,”
J. Mech. Behav. Biomed. Mater.
,
123
, p.
104730
.10.1016/j.jmbbm.2021.104730
41.
Sang
,
W.
, and
Ural
,
A.
,
2022
, “
Quantifying How Altered Lacunar Morphology and Perilacunar Tissue Properties Influence Local Mechanical Environment of Osteocyte Lacunae Using Finite Element Modeling
,”
J. Mech. Behav. Biomed. Mater.
,
135
, p.
105433
.10.1016/j.jmbbm.2022.105433
42.
Yu
,
B.
,
Pacureanu
,
A.
,
Olivier
,
C.
,
Cloetens
,
P.
, and
Peyrin
,
F.
,
2020
, “
Assessment of the Human Bone Lacuno-Canalicular Network at the Nanoscale and Impact of Spatial Resolution
,”
Sci. Rep.
,
10
(
1
), pp.
1
12
.10.1038/s41598-020-61269-8
43.
Bach-Gansmo
,
F. L.
,
Brüel
,
A.
,
Jensen
,
M. V.
,
Ebbesen
,
E. N.
,
Birkedal
,
H.
, and
Thomsen
,
J. S.
,
2016
, “
Osteocyte Lacunar Properties and Cortical Microstructure in Human Iliac Crest as a Function of Age and Sex
,”
Bone
,
91
, pp.
11
19
.10.1016/j.bone.2016.07.003
44.
Nicolella
,
D.
,
Feng
,
J.
,
Moravits
,
D.
,
Bonivitch
,
A.
,
Wang
,
Y.
,
Dusecich
,
V.
,
Yao
,
W.
,
Lane
,
N.
, and
Bonewald
,
L.
,
2008
, “
Effects of Nanomechanical Bone Tissue Properties on Bone Tissue Strain: Implications for Osteocyte Mechanotransduction
,”
J. Musculoskeletal Neuronal Interact.
,
8
(
4
), pp.
330
331
.https://ismni.org/jmni/pdf/34/22NICOLELLA.pdf
45.
Koester
,
K. J.
,
Ager
,
J.
, and
Ritchie
,
R.
,
2008
, “
The True Toughness of Human Cortical Bone Measured With Realistically Short Cracks
,”
Nat. Mater.
,
7
(
8
), pp.
672
677
.10.1038/nmat2221
46.
Yeni
,
Y. N.
,
Vashishth
,
D.
, and
Fyhrie
,
D. P.
,
2001
, “
Estimation of Bone Matrix Apparent Stiffness Variation Caused by Osteocyte Lacunar Size and Density
,” ASME
J. Biomech. Eng.
,
123
(
1
), pp.
10
17
.10.1115/1.1338123
47.
Hbaieb
,
K.
,
Wang
,
Q.
,
Chia
,
Y.
, and
Cotterell
,
B.
,
2007
, “
Modelling Stiffness of Polymer/Clay Nanocomposites
,”
Polymer
,
48
(
3
), pp.
901
909
.10.1016/j.polymer.2006.11.062
48.
Yin
,
A.
,
Yang
,
X.
,
Zhang
,
C.
,
Zeng
,
G.
, and
Yang
,
Z.
,
2015
, “
Three-Dimensional Heterogeneous Fracture Simulation of Asphalt Mixture Under Uniaxial Tension With Cohesive Crack Model
,”
Constr. Build. Mater.
,
76
, pp.
103
117
.10.1016/j.conbuildmat.2014.11.065
49.
Grassl
,
P.
, and
Jirásek
,
M.
,
2010
, “
Meso-Scale Approach to Modelling the Fracture Process Zone of Concrete Subjected to Uniaxial Tension
,”
Int. J. Solids Struct.
,
47
(
7–8
), pp.
957
968
.10.1016/j.ijsolstr.2009.12.010
50.
Vaughan
,
T.
,
Mullen
,
C.
,
Verbruggen
,
S.
, and
McNamara
,
L.
,
2015
, “
Bone Cell Mechanosensation of Fluid Flow Stimulation: A Fluid–Structure Interaction Model Characterising the Role Integrin Attachments and Primary Cilia
,”
Biomech. Model. Mechanobiol.
,
14
(
4
), pp.
703
718
.10.1007/s10237-014-0631-3
51.
Han
,
Y.
,
Cowin
,
S. C.
,
Schaffler
,
M. B.
, and
Weinbaum
,
S.
,
2004
, “
Mechanotransduction and Strain Amplification in Osteocyte Cell Processes
,”
Proc. Natl. Acad. Sci.
,
101
(
47
), pp.
16689
16694
.10.1073/pnas.0407429101
52.
Lai
,
X.
,
Chung
,
R.
,
Li
,
Y.
,
Liu
,
X. S.
, and
Wang
,
L.
,
2021
, “
Lactation Alters Fluid Flow and Solute Transport in Maternal Skeleton: A Multiscale Modeling Study on the Effects of Microstructural Changes and Loading Frequency
,”
Bone
,
151
, p.
116033
.10.1016/j.bone.2021.116033
53.
Zhou
,
X.
,
Novotny
,
J. E.
, and
Wang
,
L.
,
2009
, “
Anatomic Variations of the Lacunar-Canalicular System Influence Solute Transport in Bone
,”
Bone
,
45
(
4
), pp.
704
710
.10.1016/j.bone.2009.06.026
54.
Burra
,
S.
,
Nicolella
,
D. P.
,
Francis
,
W. L.
,
Freitas
,
C. J.
,
Mueschke
,
N. J.
,
Poole
,
K.
, and
Jiang
,
J. X.
,
2010
, “
Dendritic Processes of Osteocytes Are Mechanotransducers That Induce the Opening of Hemichannels
,”
Proc. Natl. Acad. Sci.
,
107
(
31
), pp.
13648
13653
.10.1073/pnas.1009382107
55.
Milovanovic
,
P.
,
Zimmermann
,
E. A.
,
Riedel
,
C.
,
Vom Scheidt
,
A.
,
Herzog
,
L.
,
Krause
,
M.
,
Djonic
,
D.
,
Djuric
,
M.
,
Püschel
,
K.
,
Amling
,
M.
,
Ritchie
,
R. O.
, and
Busse
,
B.
,
2015
, “
Multi-Level Characterization of Human Femoral Cortices and Their Underlying Osteocyte Network Reveal Trends in Quality of Young, Aged, Osteoporotic and Antiresorptive-Treated Bone
,”
Biomaterials
,
45
, pp.
46
55
.10.1016/j.biomaterials.2014.12.024
56.
Allison
,
H.
,
O'Sullivan
,
L. M.
, and
McNamara
,
L. M.
,
2022
, “
Temporal Changes in Cortical Microporosity During Estrogen Deficiency Associated With Perilacunar Resorption and Osteocyte Apoptosis: A Pilot Study
,”
Bone Rep.
,
16
, p.
101590
.10.1016/j.bonr.2022.101590
57.
Hesse
,
B.
,
Varga
,
P.
,
Langer
,
M.
,
Pacureanu
,
A.
,
Schrof
,
S.
,
Männicke
,
N.
,
Suhonen
,
H.
,
Maurer
,
P.
,
Cloetens
,
P.
,
Peyrin
,
F.
, and
Raum
,
K.
,
2015
, “
Canalicular Network Morphology Is the Major Determinant of the Spatial Distribution of Mass Density in Human Bone Tissue: Evidence by Means of Synchrotron Radiation Phase-Contrast Nano-CT
,”
J. Bone Miner. Res.
,
30
(
2
), pp.
346
356
.10.1002/jbmr.2324
58.
Nango
,
N.
,
Kubota
,
S.
,
Hasegawa
,
T.
,
Yashiro
,
W.
,
Momose
,
A.
, and
Matsuo
,
K.
,
2016
, “
Osteocyte-Directed Bone Demineralization Along Canaliculi
,”
Bone
,
84
, pp.
279
288
.10.1016/j.bone.2015.12.006
You do not currently have access to this content.