Swimming and cycling do not cause positive effects on bone mineral density: a systematic review

Abrahin, Odilon; Rodrigues, Rejane Pequeno; Marçal, Anderson Carlos; Alves, Erik Artur Cortinhas; Figueiredo, Rosa Costa; Sousa, Evitom Corrêa de

doi:10.1016/j.rbre.2016.02.013

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Review articles • Rev. Bras. Reumatol. 56 (4) • Jul-Aug 2016 • https://doi.org/10.1016/j.rbre.2016.02.013 copy

Swimming and cycling do not cause positive effects on bone mineral density: a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Osteoporosis is considered a common metabolic bone disease and its prevalence is increasing worldwide. In this context, physical activity has been used as a non-pharmacological tool for prevention and auxiliary treatment of this disease. The aim of this systematic review was to evaluate the effects of cycling and swimming practice on bone mineral density (BMD). This research was conducted in accordance with the recommendations outlined by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses. The studies were consulted in the period from 2004 to 2014, through major electronic databases: PubMed^®, SciELO^® and LILACS^®. Ten studies evaluated the effects of cycling on BMD, and the results showed that nine studies have linked the practice of professional cycling with low levels of BMD. Another 18 studies have reported that swimming has no positive effects on bone mass. We conclude that cycling and swimming do not cause positive effects on BMD; thus, these are not the most suitable exercises for prevention and treatment of osteoporosis.

Keywords:
Osteoporosis; Osteopenia; Bone density; Exercise; Physical activity

Author	Sample	Training time	Age	Study design	Results
Abe et al.¹³13 Abe T, Nahar VK, Young KC, Patterson KM, Stover CD, Lajza DG, et al. Skeletal muscle mass, bone mineral density, and walking performance in masters cyclists. Rejuvenat Res. 2014;17(3):291-6. (2014)	14 cycling (masters) 13 moderately active youngsters (M)	17 years of training	20–71	Cross-sectional	BMD in lower part of femoral neck of cyclists versus control. ND in BMD of lumbar spine.
Sherk et al.¹⁹19 Sherk VD, Barry DW, Villalon KL, Hansen KC, Wolfe P, Kohrt WM. Bone loss over 1 year of training and competition in female cyclists. Clin J Sport Med. 2014;24(4):331-6. (2014)	14 cycling (F)	>1 year of competition history	26–41	Longitudinal (1 year)	BMD of the hip decreases 1–2% after a year of training and competition.
Gómez-Bruton et al.²⁰20 Gómez-Bruton A, González-Agüero A, Olmedillas H, Gómez-Cabello A, Matute-Llorente A, Julián-Almárcegui C, et al. Do calcium and vitamin D intake influence the effect of cycling on bone mass through adolescence? Nutr Hosp. 2013;28(3):1136-9. (2013)	20 cycling 19 control (M)	10 h/wk	16.4 16.7	Cross-sectional	Lower BMD of young cyclists in some places.
Guillaume et al.¹⁴14 Guillaume G, Chappard D, Audran M. Evaluation of the bone status in high-level cyclists. J Clin Densitom. 2012;15(1):103-7. (2012)	29 cycling (M)	25,000–30,000 km/year	26–5	Descriptive	ND between groups on calcium and vitamin D intake
Nichols et al.¹⁵15 Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res. 2011;25(3):727-34. (2011)	19 cycling 18 control (M)	11.1 h/wk 4.5 h/wk	50–57	Longitudinal (7 years)	Cycling has not demonstrated positive effects on BMD. High rate of osteopenia/osteoporosis in cyclists (84.2% and 89.5% after seven years)
Olmedillas et al.¹⁶16 Olmedillas H, González-Agüero A, Moreno LA, Casajús JA, Vicente-Rodríguez G. Bone related health status in adolescent cyclists. PLoS ONE. 2011;6(9):e24841. (2011)	21 cycling 23 control (M)	10 h/wk 4 h/wk	15–21	Cross-sectional	Lower BMD of the hip, leg and pelvis of cyclists versus control
Campion et al.²¹21 Campion F, Nevill AM, Karlsson MK, Lounana J, Shabani M, Fardellone P, et al. Bone status in professional cyclists. Int J Sports Med. 2010;31(7):511-5. (2010)	30 cycling 30 control (M)	22–25 h/wk <1 h/wk	29 ± 3 28 ± 4	Cross-sectional	Professional cycling affected negatively BMD (femoral neck: −18%)
Penteado et al.¹⁷17 Penteado VS, Castro CH, Pinheiro MM, Santana M, Bertolino S, Mello MT, et al. Diet, body composition, and bone mass in well-trained cyclists. J Clin Densitom. 2010;13(1):43-50. (2010)	31 cycling 28 control	21 h/wk	20–30	Cross-sectional	ND in BMD versus control
Barry et al.¹⁰10 Barry DW, Kohrt WM. BMD decreases over the course of a year in competitive male cyclists. J Bone Miner Res. 2008;23(4):484-91. (2008)	14 cycling (M)	>450 h/y	27–44	Two groups: low and high doses of calcium supplementation during one year	Both groups decreased BMD of the hip and sub-regions, regardless of calcium intake
Rector et al.¹⁸18 Rector RS, Rogers R, Ruebel M, Hinton PS. Participation in road cycling vs running is associated with lower bone mineral density in men. Metabolism. 2008;57(2):226-32. (2008)	27 cycling 16 marathon (M)	≥6 h/wk ≥6 h/wk	20–59	Cross-sectional	63% of cyclists had lumbar spine osteopenia and were 7-fold times more likely to have osteopenia

Author	Sample	Training time	Age	Study design	Results
Czeczelewski et al.²²22 Czeczelewski J, Długołęcka B, Czeczelewska E, Raczyńska B. Intakes of selected nutrients, bone mineralisation and density of adolescent female swimmers over a three-year period. Biol Sport. 2013;30(1):17-20. (2013)	20 swimming 20 control (F)	2.3 ± 1.2 training years	11–13	Longitudinal (3 years)	Both groups increased BMD of lumbar spine during a 3-year follow-up, despite insufficient intake of calcium by these groups
Ferry et al.²³23 Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D. Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Joint Bone Spine. 2013;80(1):57-63. (2013)	26 swimming	10 h/wk	15.9	Longitudinal (8 months)	Swimmers <BDM versus footballers
	32 soccer	10 h/wk	16.2		Swimmers <BDM versus footballers
	15 control (F)		16.3
Maïmoun et al.²⁴24 Maïmoun L, Coste O, Philibert P, Briot K, Mura T, Galtier F, et al. Peripubertal female athletes in high-impact sports show improved bone mass acquisition and bone geometry. Metabolism. 2013;62(8):1088-98. (2013)	20 swimming	14.5 h/wk	10–18	Cross-sectional	Swimmers <BDM versus RG (except skull)
	20 RG	21 h/wk		Cross-sectional	Swimmers <BDM versus RG (except skull)
	20 AG	20 h/wk
	20 control (F)	2.5 h/wk
Maïmoun et al.²⁵25 Maïmoun L, Coste O, Mura T, Philibert P, Galtier F, Mariano-Goulart D, et al. Specific bone mass acquisition in elite female athletes. J Clin Endocrinol Metab. 2013;98(7):2844-53. (2013)	24 swimming 24 RG 24 control (F)	>5 training years	11–18	Longitudinal (1 year)	RG >BMD versus swimming and control group. ND between swimmers and control in studied locations. ND in BMD between groups after one year
Andreoli et al.²⁶26 Andreoli A, Celi M, Volpe SL, Sorge R, Tarantino U. Long-term effect of exercise on bone mineral density and body composition in post-menopausal ex-elite athletes: a retrospective study. Eur J Clin Nutr. 2012;66(1):69-74. (2012)	12 swimming	30 h/wk	54–73	Retrospective	Total body BMD lower in the control group versus athletes. Marathon > BMD of lumbar spine versus control. Marathon > BMD of legs versus swimming
	12 marathon	22 h/wk
	24 control (F)	2 h/wk
Czeczuk et al.²⁷27 Czeczuk A, Huk-Wieliczuk E, Michalska A, Bylina D, Sołtan J, Zofia D. The effect of menopause on bone tissue in former swimmers and in non-athletes. Adv Clin Exp Med. 2012;21(5):645-52. (2012)	11 swimming I	4.8 h/wk	52 ± 3	Longitudinal (1 year)	Swimming I and control I >BMD of both groups II. Swimming I and control I reduced BMD after one year (−2% and −2.8%, respectively)
	7 swimming II	6.3 h/wk	63 ± 4	Longitudinal (1 year)
	11 control I	1.4 h/wk	50 ± 2
	7 control II (F)	0.6 h/wk	60 ± 2
Greenway et al.²⁸28 Greenway KG, Walkley JW, Rich PA. Does long-term swimming participation have a deleterious effect on the adult female skeleton? Eur J Appl Physiol. 2012;112(9):3217-25. (2012)	43 swimming	>2 h/wk (last 5 years)	40 ± 8	Retrospective	ND in BMD and calcium intake between groups
	44 control (F)		44 ± 7		ND in BMD and calcium intake between groups
Hind et al.²⁹29 Hind K, Gannon L, Whatley E, Cooke C, Truscott J. Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: a hip-structural analysis study. Eur J Appl Physiol. 2012;112(2):535-41. (2012)	10 swimming	>5 h/wk	18–35	Cross-sectional	Gymnastics and marathon >BMD versus control group
	31 marathon	>5 h/wk		Cross-sectional	Gymnastics and marathon >BMD versus control group
	14 gymnastics	>5 h/wk
	22 control (M)
Ferry et al.³⁰30 Ferry B, Duclos M, Burt L, Therre P, Le Gall F, Jaffré C, et al. Bone geometry and strength adaptations to physical constraints inherent in different sports: comparison between elite female soccer players and swimmers. J Bone Miner Metab. 2011;29(3):342-51. (2011)	26 swimming	10 h/wk	16 ± 2	Cross-sectional	Soccer >BMD versus swimming in total body, lumbar spine and hip. Swimmers (F) consumed more calcium that footballers (F)
	32 soccer (F)	10 h/wk	16 ± 1	Cross-sectional
Silva et al.³¹31 Silva CC, Goldberg TBL, Teixeira AS, Dalmas JC. The impact of different types of physical activity on total and regional bone mineral density in young Brazilian athletes. J Sports Sci. 2011;29(3):227-34. (2011)	12 swimming	17 h/wk	10–18	Cross-sectional	Swimming and control <BMD in the femur versus soccer and tennis. ND in BMD between swimming and control
	10 soccer	16 h/wk
	10 tennis	15 h/wk
	14 control (M)
Carbuhn et al.³²32 Carbuhn AF, Fernandez TE, Bragg AF, Green JS, Crouse SF. Sport and training influence bone and body composition in women collegiate athletes. J Strength Cond Res. 2010;24(7):1710-7. (2010)	16 swimming	–	19 ± 1	Longitudinal (1 year)	Swimming <BDM versus other sports (pre- and post-season).
	17 softball		20 ± 1	Longitudinal (1 year)	Swimming <BDM versus other sports (pre- and post-season).
	10 basketball		20 ± 1
	7 volleyball (F)		19 ± 1
Gruodyte et al.³³33 Gruodytė R, Jürimäe J, Cicchella A, Stefanelli C, Passariello C, Jürimäe T. Adipocytokines and bone mineral density in adolescent female athletes. Acta Pædiatrica. 2010;99(12):1879-84. (2010)	24 swimming	9 h/wk	13–15	Cross-sectional	Swimming <BMD in femoral neck versus gymnastics.
	49 SG	5 h/wk		Cross-sectional	Swimming <BMD in femoral neck versus gymnastics.
	24 sprinter	5 h/wk
	23 gymnastics	9 h/wk
	17 CCS	6 h/wk
	33 control (F)
Kemper et al.³⁴34 Kemper C, Oliveira RJ, Bottaro M, Moreno R, Bezerra LMA, Guido M, et al. Effects of swimming and resistance training on bone mineral density of older women. Rev Bras Med Esporte. 2009;15(1):10-3. (2009)	13 swimming	–	66 ± 5	Experimental (6 months)	No changes in BMD after six months of intervention in either group.
	13 resisted exercise		61 ± 6	Experimental (6 months)
Velez et al.³⁶36 Velez NF, Zhang A, Stone B, Perera S, Miller M, Greenspan SL. The effect of moderate impact exercise on skeletal integrity in master athletes. Osteoporos Int. 2008;19(10):1457-64. (2008)	43 swimming	–	≥65	Cross-sectional	ND in BMD between swimming and control. Marathon >BMD of total body versus swimming and control
	44 marathon
	87 control (M/F)
Magkos et al.³⁷37 Magkos F, Kavouras SA, Yannakoulia M, Karipidou M, Sidossi S, Sidossis LS. The bone response to non-weight-bearing exercise is sport-, site-, and sex-specific. Clin J Sport Med. 2007;17(2):123-8. (2007)	26 swimming	>3 h/day	17–34	Cross-sectional	Swimming <Total and leg BMD versus control.
	43 water polo	>3 h/day		Cross-sectional	Swimming <Total and leg BMD versus control.
	30 control (M/F)
Magkos et al.⁹9 Magkos F, Yannakoulia M, Kavouras SA, Sidossis LS. The type and intensity of exercise have independent and additive effects on bone mineral density. Int J Sports Med. 2007;28(9):773-9. (2007)	7 swimming (endurance)	>3 h/day	19 ± 2	Cross-sectional	Swimming <BMD of leg and body versus control
	9 swimming (sprint)	>3 h/day	21 ± 2
	10 marathon	>3 h/day	23 ± 4
	11 sprint	>3 h/day	23 ± 3
	15 control (M/F)		22 ± 3
Mudd et al.³⁸38 Mudd LM, Fornetti W, Pivarnik JM. Bone mineral density in collegiate female athletes: comparisons among sports. J Athl Train. 2007;42(3):403-8. (2007)	9 swimming	–	20 ± 1	Cross-sectional	Swimming <BMD of leg versus other sports (except marathon and rowing).
	8 gymnastics			Cross-sectional
	14 softball
	25 marathon
	8 sprinter
	10 hockey
	10 soccer
	15 rowing (F)
Maïmoun et al.³⁹39 Maïmoun L, Mariano-Goulart D, Couret I, Manetta J, Peruchon E, Micallef JP, et al. Effects of physical activities that induce moderate external loading on bone metabolism in male athletes. J Sports Sci. 2004;22(9):875-83. (2004)	13 swimming	10 h/wk	18–39	Cross-sectional	ND in BMD between groups. Cyclists consumed more calcium versus control group.
	11 cycling	10 h/wk
	14 triathlon	15 h/wk
	10 control (M)

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[1] *Corresponding author. E-mail: odilonsalim@hotmail.com (O. Abrahin).