Abstract
Purpose of Review: In view of the existing uncertainty about the implications of intentional weight loss in older obese adults, the present review (a) summarizes the available evidence from epidemiological and interventional studies concerning the effects of weight loss through lifestyle modifications on skeletal health parameters in older overweight/obese individuals, (b) proposes mechanisms that link weight loss to bone loss in this age group, and (c) identifies appropriate animal models. Main Findings and Future Directions: Based on prospective epidemiological studies, weight loss is associated with bone loss, impaired bone macro- and microstructure, and increased fracture risk in the elderly. Data from interventional studies confirm the negative effects of intentional weight loss achieved by lifestyle modifications on skeletal health outcomes in obese older individuals. These effects appear to be modest following a single weight loss attempt, but may persist in the longer term, and presumably, during subsequent weight loss efforts. Current evidence suggests that resistance exercise coupled with caloric restriction mitigates bone and muscle loss. However, alternative strategies do not exist for older individuals, especially those who are unable or unwilling to exercise. Clinical weight loss studies in obese older individuals and preclinical research in relevant animal models with obesity and osteoporosis are required. These will advance our understanding of the pathophysiology of weight-loss-associated skeletal alterations and provide evidence on how bone loss can be counteracted or prevented.
References
1.
Marques
A
, Peralta
M
, Naia
A
, Loureiro
N
, de Matos
MG
. Prevalence of adult overweight and obesity in 20 European countries, 2014
. Eur J Public Health
. 2018
Apr
;28
(2
):295
–300
.
[PubMed]
1101-12622.
Hales
CM
, Carroll
MD
, Fryar
CD
, Ogden
CL
. Prevalence of obesity among adults and youth: United States, 2015–2016. NCHS data brief, no 288
. Hyattsville (MD)
: National Center for Health Statistics
; 2017
.3.
Mathus-Vliegen
EM
, Basdevant
A
, Finer
N
, Hainer
V
, Hauner
H
, Micic
D
, et al.; Obesity Management Task Force of the European Association for the Study of Obesity
. Prevalence, pathophysiology, health consequences and treatment options of obesity in the elderly: a guideline
. Obes Facts
. 2012
;5
(3
):460
–83
.
[PubMed]
1662-40254.
Zamboni
M
, Mazzali
G
, Fantin
F
, Rossi
A
, Di Francesco
V
. Sarcopenic obesity: a new category of obesity in the elderly
. Nutr Metab Cardiovasc Dis
. 2008
Jun
;18
(5
):388
–95
.
[PubMed]
0939-47535.
Ilich
JZ
, Kelly
OJ
, Inglis
JE
. Osteosarcopenic obesity syndrome: what is it and how can it be identified and diagnosed?
Curr Gerontol Geriatr Res
. 2016
;2016
:7325973
.
[PubMed]
1687-70636.
7.
Darmon
P
. Intentional weight loss in older adults: useful or wasting disease generating strategy?
Curr Opin Clin Nutr Metab Care
. 2013
May
;16
(3
):284
–9
.
[PubMed]
1363-19508.
Shapses
SA
, Sukumar
D
. Bone metabolism in obesity and weight loss
. Annu Rev Nutr
. 2012
Aug
;32
(1
):287
–309
.
[PubMed]
0199-98859.
Zibellini
J
, Seimon
RV
, Lee
CM
, Gibson
AA
, Hsu
MS
, Shapses
SA
, et al. Does diet-Induced weight loss lead to bone loss in overweight or obese adults? A systematic review and meta-analysis of clinical trials
. J Bone Miner Res
. 2015
Dec
;30
(12
):2168
–78
.
[PubMed]
0884-043110.
Nguyen
TV
, Sambrook
PN
, Eisman
JA
. Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study
. J Bone Miner Res
. 1998
Sep
;13
(9
):1458
–67
.
[PubMed]
0884-043111.
Hannan
MT
, Felson
DT
, Dawson-Hughes
B
, Tucker
KL
, Cupples
LA
, Wilson
PW
, et al. Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study
. J Bone Miner Res
. 2000
Apr
;15
(4
):710
–20
.
[PubMed]
0884-043112.
Ensrud
KE
, Ewing
SK
, Stone
KL
, Cauley
JA
, Bowman
PJ
, Cummings
SR
; Study of Osteoporotic Fractures Research Group
. Intentional and unintentional weight loss increase bone loss and hip fracture risk in older women
. J Am Geriatr Soc
. 2003
Dec
;51
(12
):1740
–7
.
[PubMed]
0002-861413.
Knoke
JD
, Barrett-Connor
E
. Weight loss: a determinant of hip bone loss in older men and women. The Rancho Bernardo Study
. Am J Epidemiol
. 2003
Dec
;158
(12
):1132
–8
.
[PubMed]
0002-926214.
Blain
H
, Carrière
I
, Favier
F
, Jeandel
C
, Papoz
L
; EPIDOS Study Group
. Body weight change since menopause and percentage body fat mass are predictors of subsequent bone mineral density change of the proximal femur in women aged 75 years and older: results of a 5 year prospective study
. Calcif Tissue Int
. 2004
Jul
;75
(1
):32
–9
.
[PubMed]
0171-967X15.
Gudmundsdottir
SL
, Oskarsdottir
D
, Indridason
OS
, Franzson
L
, Sigurdsson
G
. Risk factors for bone loss in the hip of 75-year-old women: a 4-year follow-up study
. Maturitas
. 2010
Nov
;67
(3
):256
–61
.
[PubMed]
0378-512216.
Bleicher
K
, Cumming
RG
, Naganathan
V
, Travison
TG
, Sambrook
PN
, Blyth
FM
, et al. The role of fat and lean mass in bone loss in older men: findings from the CHAMP study
. Bone
. 2011
Dec
;49
(6
):1299
–305
.
[PubMed]
8756-328217.
Meyer
HE
, Søgaard
AJ
, Falch
JA
, Jørgensen
L
, Emaus
N
. Weight change over three decades and the risk of osteoporosis in men: the Norwegian Epidemiological Osteoporosis Studies (NOREPOS)
. Am J Epidemiol
. 2008
Aug
;168
(4
):454
–60
.
[PubMed]
0002-926218.
Ensrud
KE
, Fullman
RL
, Barrett-Connor
E
, Cauley
JA
, Stefanick
ML
, Fink
HA
, et al.; Osteoporotic Fractures in Men Study Research Group
. Voluntary weight reduction in older men increases hip bone loss: the osteoporotic fractures in men study
. J Clin Endocrinol Metab
. 2005
Apr
;90
(4
):1998
–2004
.
[PubMed]
0021-972X19.
Forsmo
S
, Aaen
J
, Schei
B
, Langhammer
A
. What is the influence of weight change on forearm bone mineral density in peri- and postmenopausal women? The health study of Nord-Trondelag, Norway
. Am J Epidemiol
. 2006
Nov
;164
(9
):890
–7
.
[PubMed]
0002-926220.
Schousboe
JT
, Vo
TN
, Langsetmo
L
, Taylor
BC
, Kats
AM
, Schwartz
AV
, et al.; Osteoporotic Fractures in Men (MrOS) Study Research Group
. Predictors of change of trabecular bone score (TBS) in older men: results from the Osteoporotic Fractures in Men (MrOS) Study
. Osteoporos Int
. 2018
Jan
;29
(1
):49
–59
.
[PubMed]
0937-941X21.
Lang
TF
, Sigurdsson
S
, Karlsdottir
G
, Oskarsdottir
D
, Sigmarsdottir
A
, Chengshi
J
, et al. Age-related loss of proximal femoral strength in elderly men and women: the Age Gene/Environment Susceptibility Study—Reykjavik
. Bone
. 2012
Mar
;50
(3
):743
–8
.
[PubMed]
8756-328222.
Liu
CT
, Sahni
S
, Xu
H
, McLean
RR
, Broe
KE
, Hannan
MT
, et al. Long-Term and Recent Weight Change Are Associated With Reduced Peripheral Bone Density, Deficits in Bone Microarchitecture, and Decreased Bone Strength: The Framingham Osteoporosis Study
. J Bone Miner Res
. 2018
Oct
;33
(10
):1851
–8
.
[PubMed]
0884-043123.
Cauley
JA
, Burghardt
AJ
, Harrison
SL
, Cawthon
PM
, Schwartz
AV
, Connor
EB
, et al.; Osteoporotic Fractures in Men (MrOS) Research Group
. Osteoporotic Fractures in Men (MrOS) Research Group. Accelerated bone loss in older men: effects on bone microarchitecture and strength
. J Bone Miner Res
. 2018
Oct
;33
(10
):1859
–69
.
[PubMed]
0884-043124.
Ensrud
KE
, Vo
TN
, Burghardt
AJ
, Schousboe
JT
, Cauley
JA
, Taylor
BC
, et al.; Osteoporotic Fractures in Men (MrOS) Research Group
. Weight loss in men in late life and bone strength and microarchitecture: a prospective study
. Osteoporos Int
. 2018
Jul
;29
(7
):1549
–58
.
[PubMed]
0937-941X25.
Langlois
JA
, Harris
T
, Looker
AC
, Madans
J
. Weight change between age 50 years and old age is associated with risk of hip fracture in white women aged 67 years and older
. Arch Intern Med
. 1996
May
;156
(9
):989
–94
.
[PubMed]
0003-992626.
Langlois
JA
, Mussolino
ME
, Visser
M
, Looker
AC
, Harris
T
, Madans
J
. Weight loss from maximum body weight among middle-aged and older white women and the risk of hip fracture: the NHANES I epidemiologic follow-up study
. Osteoporos Int
. 2001
;12
(9
):763
–8
.
[PubMed]
0937-941X27.
Omsland
TK
, Schei
B
, Grønskag
AB
, Langhammer
A
, Forsén
L
, Gjesdal
CG
, et al. Weight loss and distal forearm fractures in postmenopausal women: the Nord-Trøndelag health study, Norway
. Osteoporos Int
. 2009
Dec
;20
(12
):2009
–16
.
[PubMed]
0937-941X28.
Crandall
CJ
, Yildiz
VO
, Wactawski-Wende
J
, Johnson
KC
, Chen
Z
, Going
SB
, et al. Postmenopausal weight change and incidence of fracture: post hoc findings from Women’s Health Initiative Observational Study and Clinical Trials
. BMJ
. 2015
Jan
;350
jan27 6
:h25
.
[PubMed]
0959-813829.
Compston
JE
, Wyman
A
, FitzGerald
G
, Adachi
JD
, Chapurlat
RD
, Cooper
C
, et al. Increase in Fracture Risk Following Unintentional Weight Loss in Postmenopausal Women: The Global Longitudinal Study of Osteoporosis in Women
. J Bone Miner Res
. 2016
Jul
;31
(7
):1466
–72
.
[PubMed]
0884-043130.
Mussolino
ME
, Looker
AC
, Madans
JH
, Langlois
JA
, Orwoll
ES
. Risk factors for hip fracture in white men: the NHANES I Epidemiologic Follow-up Study
. J Bone Miner Res
. 1998
Jun
;13
(6
):918
–24
.
[PubMed]
0884-043131.
Armamento-Villareal
R
, Sadler
C
, Napoli
N
, Shah
K
, Chode
S
, Sinacore
DR
, et al. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training
. J Bone Miner Res
. 2012
May
;27
(5
):1215
–21
.
[PubMed]
0884-043132.
Fogelholm
M
, Sievänen
H
, Heinonen
A
, Virtanen
M
, Uusi-Rasi
K
, Pasanen
M
, et al. Association between weight cycling history and bone mineral density in premenopausal women
. Osteoporos Int
. 1997
;7
(4
):354
–8
.
[PubMed]
0937-941X33.
Søgaard
AJ
, Meyer
HE
, Ahmed
LA
, Jørgensen
L
, Bjørnerem
A
, Joakimsen
RM
, et al. Does recalled dieting increase the risk of non-vertebral osteoporotic fractures? The Tromsø Study
. Osteoporos Int
. 2012
Dec
;23
(12
):2835
–45
.
[PubMed]
0937-941X34.
French
SA
, Folsom
AR
, Jeffery
RW
, Zheng
W
, Mink
PJ
, Baxter
JE
. Weight variability and incident disease in older women: the Iowa Women’s Health Study
. Int J Obes Relat Metab Disord
. 1997
Mar
;21
(3
):217
–23
.
[PubMed]
35.
Søgaard
AJ
, Meyer
HE
, Tonstad
S
, Håheim
LL
, Holme
I
. Weight cycling and risk of forearm fractures: a 28-year follow-up of men in the Oslo Study
. Am J Epidemiol
. 2008
Apr
;167
(8
):1005
–13
.
[PubMed]
0002-926236.
Villareal
DT
, Chode
S
, Parimi
N
, Sinacore
DR
, Hilton
T
, Armamento-Villareal
R
, et al. Weight loss, exercise, or both and physical function in obese older adults
. N Engl J Med
. 2011
Mar
;364
(13
):1218
–29
.
[PubMed]
0028-479337.
Shah
K
, Armamento-Villareal
R
, Parimi
N
, Chode
S
, Sinacore
DR
, Hilton
TN
, et al. Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones
. J Bone Miner Res
. 2011
Dec
;26
(12
):2851
–9
.
[PubMed]
0884-043138.
Kelleher
JL
, Beavers
DP
, Henderson
RM
, Yow
D
, Crotts
C
, Kiel
J
, et al. Weighted vest use during dietary weight loss on bone health in older adults with obesity
. J Osteoporos Phys Act
. 2017
;5
(4
):210
.
[PubMed]
2329-950939.
Beavers
KM
, Walkup
MP
, Weaver
AA
, Lenchik
L
, Kritchevsky
SB
, Nicklas
BJ
, et al. Effect of exercise modality during weight loss on bone health in older adults with obesity and cardiovascular disease or metabolic syndrome: a randomized controlled trial
. J Bone Miner Res
. 2018
Dec
;33
(12
):2140
–9
.
[PubMed]
0884-043140.
Chao
D
, Espeland
MA
, Farmer
D
, Register
TC
, Lenchik
L
, Applegate
WB
, et al. Effect of voluntary weight loss on bone mineral density in older overweight women
. J Am Geriatr Soc
. 2000
Jul
;48
(7
):753
–9
.
[PubMed]
0002-861441.
Haywood
CJ
, Prendergast
LA
, Purcell
K
, Le Fevre
L
, Lim
WK
, Galea
M
, et al. Very low calorie diets for weight loss in obese older adults-a randomized trial
. J Gerontol A Biol Sci Med Sci
. 2017
Dec
;73
(1
):59
–65
.
[PubMed]
1079-500642.
Villareal
DT
, Shah
K
, Banks
MR
, Sinacore
DR
, Klein
S
. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial
. J Clin Endocrinol Metab
. 2008
Jun
;93
(6
):2181
–7
.
[PubMed]
0021-972X43.
Daly
RM
, Dunstan
DW
, Owen
N
, Jolley
D
, Shaw
JE
, Zimmet
PZ
. Does high-intensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes?
Osteoporos Int
. 2005
Dec
;16
(12
):1703
–12
.
[PubMed]
0937-941X44.
Villareal
DT
, Aguirre
L
, Gurney
AB
, Waters
DL
, Sinacore
DR
, Colombo
E
, et al. Armamento-Villareal R1, Qualls C. Aerobic or resistance exercise, or both, in dieting obese older adults
. N Engl J Med
. 2017
May
;376
(20
):1943
–55
.
[PubMed]
0028-479345.
Beavers
KM
, Beavers
DP
, Martin
SB
, Marsh
AP
, Lyles
MF
, Lenchik
L
, et al. Change in bone mineral density during weight loss with resistance versus aerobic exercise training in older adults
. J Gerontol A Biol Sci Med Sci
. 2017
Oct
;72
(11
):1582
–5
.
[PubMed]
1079-500646.
Schoell
SL
, Beavers
KM
, Beavers
DP
, Lenchik
L
, Marsh
AP
, Rejeski
WJ
, et al. Prediction of lumbar vertebral body compressive strength of overweight and obese older adults using morphed subject-specific finite-element models to evaluate the effects of weight loss
. Aging Clin Exp Res
. 2018
.
[PubMed]
1594-066747.
Waters
DL
, Vawter
R
, Qualls
C
, Chode
S
, Armamento-Villareal
R
, Villareal
DT
. Long-term maintenance of weight loss after lifestyle intervention in frail, obese older adults
. J Nutr Health Aging
. 2013
Jan
;17
(1
):3
–7
.
[PubMed]
1279-770748.
Batsis
JA
, Gill
LE
, Masutani
RK
, Adachi-Mejia
AM
, Blunt
HB
, Bagley
PJ
, et al. Weight loss interventions in older adults with obesity: a systematic review of randomized controlled trials since 2005
. J Am Geriatr Soc
. 2017
Feb
;65
(2
):257
–68
.
[PubMed]
0002-861449.
Frost
HM
. Why the ISMNI and the Utah paradigm? Their role in skeletal and extraskeletal disorders
. J Musculoskelet Neuronal Interact
. 2000
Sep
;1
(1
):5
–9
.
[PubMed]
1108-716150.
Lee
JS
, Visser
M
, Tylavsky
FA
, Kritchevsky
SB
, Schwartz
AV
, Sahyoun
N
, et al.; Health ABC Study
. Weight loss and regain and effects on body composition: the Health, Aging, and Body Composition Study
. J Gerontol A Biol Sci Med Sci
. 2010
Jan
;65
(1
):78
–83
.
[PubMed]
1079-500651.
Tagliaferri
C
, Wittrant
Y
, Davicco
MJ
, Walrand
S
, Coxam
V
. Muscle and bone, two interconnected tissues
. Ageing Res Rev
. 2015
May
;21
:55
–70
.
[PubMed]
1568-163752.
Liu
Y
, Song
CY
, Wu
SS
, Liang
QH
, Yuan
LQ
, Liao
EY
. Novel adipokines and bone metabolism
. Int J Endocrinol
. 2013
;2013
:895045
.
[PubMed]
1687-833753.
Veldhuis-Vlug
AG
, Rosen
CJ
. Clinical implications of bone marrow adiposity
. J Intern Med
. 2018
Feb
;283
(2
):121
–39
.
[PubMed]
0954-682054.
Scheller
EL
, Khoury
B
, Moller
KL
, Wee
NK
, Khandaker
S
, Kozloff
KM
, et al. Changes in skeletal integrity and marrow adiposity during high-fat diet and after weight loss
. Front Endocrinol (Lausanne)
. 2016
Jul
;7
(7
):102
.
[PubMed]
1664-239255.
Kim
TY
, Schwartz
AV
, Li
X
, Xu
K
, Black
DM
, Petrenko
DM
, et al. Bone marrow fat changes after gastric bypass surgery are associated with loss of bone mass
. J Bone Miner Res
. 2017
Nov
;32
(11
):2239
–47
.
[PubMed]
0884-043156.
Ferrucci
L
, Baroni
M
, Ranchelli
A
, Lauretani
F
, Maggio
M
, Mecocci
P
, et al. Interaction between bone and muscle in older persons with mobility limitations
. Curr Pharm Des
. 2014
;20
(19
):3178
–97
.
[PubMed]
1381-612857.
Talbott
SM
, Cifuentes
M
, Dunn
MG
, Shapses
SA
. Energy restriction reduces bone density and biomechanical properties in aged female rats
. J Nutr
. 2001
Sep
;131
(9
):2382
–7
.
[PubMed]
0022-316658.
Ricci
TA
, Chowdhury
HA
, Heymsfield
SB
, Stahl
T
, Pierson
RN
Jr, Shapses
SA
. Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women
. J Bone Miner Res
. 1998
Jun
;13
(6
):1045
–50
.
[PubMed]
0884-043159.
Thorpe
MP
, Jacobson
EH
, Layman
DK
, He
X
, Kris-Etherton
PM
, Evans
EM
. A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults
. J Nutr
. 2008
Jun
;138
(6
):1096
–100
.
[PubMed]
0022-316660.
Fontana
L
, Villareal
DT
, Das
SK
, Smith
SR
, Meydani
SN
, Pittas
AG
, et al.; CALERIE Study Group
. Effects of 2-year calorie restriction on circulating levels of IGF-1, IGF-binding proteins and cortisol in nonobese men and women: a randomized clinical trial
. Aging Cell
. 2016
Feb
;15
(1
):22
–7
.
[PubMed]
1474-971861.
Biver
E
, Salliot
C
, Combescure
C
, Gossec
L
, Hardouin
P
, Legroux-Gerot
I
, et al. Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis
. J Clin Endocrinol Metab
. 2011
Sep
;96
(9
):2703
–13
.
[PubMed]
0021-972X62.
Pietschmann
P
, Mechtcheriakova
D
, Meshcheryakova
A
, Föger-Samwald
U
, Ellinger
I
. Immunology of Osteoporosis: A Mini-Review
. Gerontology
. 2016
;62
(2
):128
–37
.
[PubMed]
0304-324X63.
Forsythe
LK
, Wallace
JM
, Livingstone
MB
. Obesity and inflammation: the effects of weight loss
. Nutr Res Rev
. 2008
Dec
;21
(2
):117
–33
.
[PubMed]
0954-422464.
Calder
PC
, Bosco
N
, Bourdet-Sicard
R
, Capuron
L
, Delzenne
N
, Doré
J
, et al. Health relevance of the modification of low grade inflammation in ageing (inflammageing) and the role of nutrition
. Ageing Res Rev
. 2017
Nov
;40
:95
–119
.
[PubMed]
1568-163765.
Sipos
W
, Rauner
M
, Skalicky
M
, Viidik
A
, Hofbauer
G
, Schett
G
, et al. Running has a negative effect on bone metabolism and proinflammatory status in male aged rats
. Exp Gerontol
. 2008
Jun
;43
(6
):578
–83
.
[PubMed]
0531-556566.
Waters
DL
, Ward
AL
, Villareal
DT
. Weight loss in obese adults 65years and older: a review of the controversy
. Exp Gerontol
. 2013
Oct
;48
(10
):1054
–61
.
[PubMed]
0531-556567.
Jilka
RL
. The relevance of mouse models for investigating age-related bone loss in humans
. J Gerontol A Biol Sci Med Sci
. 2013
Oct
;68
(10
):1209
–17
.
[PubMed]
1079-500668.
Lutz
TA
, Woods
SC
. Overview of animal models of obesity.
Curr Protoc Pharmacol. 2012
;Chapter 5:Unit5 61. 69.
Lutz
TA
, Bueter
M
. The Use of Rat and Mouse Models in Bariatric Surgery Experiments
. Front Nutr
. 2016
Aug
;3
:25
.
[PubMed]
2296-861X70.
Sanderson
JP
, Binkley
N
, Roecker
EB
, Champ
JE
, Pugh
TD
, Aspnes
L
, et al. Influence of fat intake and caloric restriction on bone in aging male rats
. J Gerontol A Biol Sci Med Sci
. 1997
Jan
;52
(1
):B20
–5
.
[PubMed]
1079-500671.
LaMothe
JM
, Hepple
RT
, Zernicke
RF
. Selected contribution: Bone adaptation with aging and long-term caloric restriction in Fischer 344 x Brown-Norway F1-hybrid rats. J Appl Physiol (1985). 2003
;95(4):1739-45.72.
Westerbeek
ZW
, Hepple
RT
, Zernicke
RF
. Effects of aging and caloric restriction on bone structure and mechanical properties
. J Gerontol A Biol Sci Med Sci
. 2008
Nov
;63
(11
):1131
–6
.
[PubMed]
1079-500673.
Mardon
J
, Zangarelli
A
, Walrand
S
, Davicco
MJ
, Lebecque
P
, Demigné
C
, et al. Impact of energy and casein or whey protein intake on bone status in a rat model of age-related bone loss
. Br J Nutr
. 2008
Apr
;99
(4
):764
–72
.
[PubMed]
0007-114574.
Behrendt
AK
, Kuhla
A
, Osterberg
A
, Polley
C
, Herlyn
P
, Fischer
DC
, et al. dietary restriction-induced alterations in bone phenotype: effects of lifelong versus short-term caloric restriction on femoral and vertebral bone in C57BL/6 mice
. J Bone Miner Res
. 2016
Apr
;31
(4
):852
–63
.
[PubMed]
0884-043175.
Shen
CL
, Zhu
W
, Gao
W
, Wang
S
, Chen
L
, Chyu
MC
. Energy-restricted diet benefits body composition but degrades bone integrity in middle-aged obese female rats
. Nutr Res
. 2013
Aug
;33
(8
):668
–76
.
[PubMed]
0271-531776.
Gerbaix
M
, Metz
L
, Mac-Way
F
, Lavet
C
, Guillet
C
, Walrand
S
, et al. A well-balanced diet combined or not with exercise induces fat mass loss without any decrease of bone mass despite bone micro-architecture alterations in obese rat
. Bone
. 2013
Apr
;53
(2
):382
–90
.
[PubMed]
8756-328277.
Nebot
E
, Aparicio
VA
, Coll-Risco
I
, Camiletti-Moirón
D
, Schneider
J
, Kapravelou
G
, et al. Effects of a moderately high-protein diet and interval aerobic training combined with strength-endurance exercise on markers of bone metabolism, microarchitecture and turnover in obese Zucker rats
. Bone
. 2016
Nov
;92
:116
–23
.
[PubMed]
8756-328278.
Hawkins
J
, Cifuentes
M
, Pleshko
NL
, Ambia-Sobhan
H
, Shapses
SA
. Energy restriction is associated with lower bone mineral density of the tibia and femur in lean but not obese female rats
. J Nutr
. 2010
Jan
;140
(1
):31
–7
.
[PubMed]
0022-316679.
Reinwald
S
, Burr
D
. Review of nonprimate, large animal models for osteoporosis research
. J Bone Miner Res
. 2008
Sep
;23
(9
):1353
–68
.
[PubMed]
0884-043180.
Kleinert
M
, Clemmensen
C
, Hofmann
SM
, Moore
MC
, Renner
S
, Woods
SC
, et al. Animal models of obesity and diabetes mellitus
. Nat Rev Endocrinol
. 2018
Mar
;14
(3
):140
–62
.
[PubMed]
1759-502981.
Halade
GV
, Rahman
MM
, Williams
PJ
, Fernandes
G
. High fat diet-induced animal model of age-associated obesity and osteoporosis
. J Nutr Biochem
. 2010
Dec
;21
(12
):1162
–9
.
[PubMed]
0955-286382.
Hamann
C
, Picke
AK
, Campbell
GM
, Balyura
M
, Rauner
M
, Bernhardt
R
, et al. Effects of parathyroid hormone on bone mass, bone strength, and bone regeneration in male rats with type 2 diabetes mellitus
. Endocrinology
. 2014
Apr
;155
(4
):1197
–206
.
[PubMed]
0013-722783.
Hamrick
MW
. Leptin, bone mass, and the thrifty phenotype
. J Bone Miner Res
. 2004
Oct
;19
(10
):1607
–11
.
[PubMed]
0884-043184.
Halloran
BP
, Ferguson
VL
, Simske
SJ
, Burghardt
A
, Venton
LL
, Majumdar
S
. Changes in bone structure and mass with advancing age in the male C57BL/6J mouse
. J Bone Miner Res
. 2002
Jun
;17
(6
):1044
–50
.
[PubMed]
0884-043185.
Ferguson
VL
, Ayers
RA
, Bateman
TA
, Simske
SJ
. Bone development and age-related bone loss in male C57BL/6J mice
. Bone
. 2003
Sep
;33
(3
):387
–98
.
[PubMed]
8756-328286.
Houtkooper
RH
, Argmann
C
, Houten
SM
, Cantó
C
, Jeninga
EH
, Andreux
PA
, et al. The metabolic footprint of aging in mice
. Sci Rep
. 2011
;1
(1
):134
.
[PubMed]
2045-232287.
Pietschmann
P
, Skalicky
M
, Kneissel
M
, Rauner
M
, Hofbauer
G
, Stupphann
D
, et al. Bone structure and metabolism in a rodent model of male senile osteoporosis
. Exp Gerontol
. 2007
Nov
;42
(11
):1099
–108
.
[PubMed]
0531-556588.
Gordon
CJ
, Jarema
K
, Johnstone
AF
, Phillips
PM
. Effect of genetic strain and gender on age-related changes in body composition of the laboratory rat
. J Toxicol Environ Health A
. 2016
;79
(8
):376
–92
.
[PubMed]
1528-739489.
Takeda
T
, Hosokawa
M
, Higuchi
K
. Senescence-accelerated mouse (SAM): a novel murine model of senescence
. Exp Gerontol
. 1997
Jan-Apr
;32
(1-2
):105
–9
.
[PubMed]
0531-556590.
Silva
MJ
, Brodt
MD
, Ettner
SL
. Long bones from the senescence accelerated mouse SAMP6 have increased size but reduced whole-bone strength and resistance to fracture
. J Bone Miner Res
. 2002
Sep
;17
(9
):1597
–603
.
[PubMed]
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2019
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