Abstract
Background
It is now well established that physical exercise is an effective preventive method to reduce and treat certain chronic diseases, particularly musculoskeletal disorders. At the bone level, running exercise is well known for its positive effects on various parameters of bone quality. There is, however, no consensus regarding the effects of different running exercise modalities on bone quality.
Aim
The objective of this study was to compare the effects of three treadmill running modalities: intermittent, moderate continuous, and a combination of both—on bone quality parameters in rats.
Methods
Thirty-nine, 5-week-old, male Wistar rats were randomly divided in 4 groups: sedentary control (SED; n = 10), intermittent running exercise (IE; n = 10), continuous running exercise (CE; n = 10) and combined running exercise (COME; n = 9). Rats in running groups were exercised 45 min/day, 5 days/week, for 8 consecutive weeks. Femoral micro-architectural parameters were assessed by micro-CT; femoral osteocyte apoptosis, osteoclast resorption and bone histomorphometry were assessed by histology.
Results
Femoral trabecular thickness in the combined running group was increased (p < 0.0001) compared to respective results in the other running groups (0.13 mm vs 0.11 mm). The cortical thickness, osteocyte lacunae occupancy rate in the whole femur, numbers of apoptotic osteocytes and osteoclastic resorption surfaces were not significantly different between groups. Statistical differences were occasionally noted depending on the femoral anatomical region.
Conclusion
These results suggest that the femur should not be considered as the better bone to study the effects of running protocols.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The dataset generated and analyzed during the current study are available from the corresponding author and reasonable request.
Abbreviations
- BV/TV::
-
Trabecular bone fraction
- Tb.Th::
-
Trabecular thickness
- Tb.N::
-
Trabecular number
- BMD::
-
Bone mineral density
- NTx::
-
Cross-linked N-Telopeptide of type I collagen
- BMI::
-
Body mass index
- SED::
-
Sedentary control
- IE::
-
Intermittent running exercise
- CE::
-
Continuous running exercise
- COME::
-
Combined running exercise
- MAS::
-
Maximal aerobic velocity
- ALP::
-
Alkaline phosphatase
- PTH::
-
Parathyroid hormone
- AP::
-
Antero-posterior
- LM::
-
Latero-medial
- µCT::
-
Micro-Computed Tomography
- VOI::
-
Volumes of interest
- ROI::
-
Region of interest
- Tb.BMD::
-
Trabecular BMD
- Tb.Sp::
-
Trabecular spacing
- TRAP::
-
Tartrate-Resistant Acid Phosphatase activity
- SD::
-
Standard deviation
- SEM::
-
Standard error of the mean
References
Barlet JP, Coxam V, Davicco MJ (1995) Physical exercise and the skeleton. Archiv Physiol Biochem 103(6):681–698. https://doi.org/10.3109/13813459508998138
Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26(2):229–238. https://doi.org/10.1002/jbmr.320
Bonewald LF, Johnson ML (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42(4):606–615. https://doi.org/10.1016/j.bone.2007.12.224
Boudenot A, Presle N, Uzbekov R, Toumi H, Pallu S, Lespessailles E (2014) Effect of interval-training exercise on subchondral bone in a chemically-induced osteoarthritis model. Osteoarthr Cartil 22(8):1176–1185. https://doi.org/10.1016/j.joca.2014.05.020
Boudenot A, Maurel DB, Pallu S, Ingrand I, Boisseau N, Jaffré C, Portier H (2015) Quick benefits of interval training versus continuous training on bone: a dual-energy X-ray absorptiometry comparative study. Int J Exp Pathol 96(6):370–377. https://doi.org/10.1111/iep.12155
Boudenot A, Pallu S, Uzbekov R, Dolleans E, Toumi H, Lespessailles E (2021) Free-fall landing and interval running have different effects on trabecular bone mass and microarchitecture, serum osteocalcin, biomechanical properties, SOST expression and on osteocyte-related characteristics. Appl Physiol Nutr Metab 46(12):1525–1534. https://doi.org/10.1139/apnm-2020-0683
Bourrin S, Genty C, Palle S, Gharib C, Alexandre C (1994) Adverse effects of strenuous exercise: a densitometric and histomorphometric study in the rat. J Appl Physiol 76(5):1999–2005. https://doi.org/10.1152/jappl.1994.76.5.1999
Bourrin S, Palle S, Pupier R, Vico L, Alexandre C (1995) Effect of physical training on bone adaptation in three zones of the rat tibia. J Bone Miner Res 10(11):1745–1752. https://doi.org/10.1002/jbmr.5650101118
Bourzac C, Bensidhoum M, Manassero M, Chappard C, Michoux N, Pallu S, Portier H (2020) Preventive moderate continuous running-exercise conditioning improves the healing of non-critical size bone defects in male Wistar rats: a pilot study using ΜCT. Life 10(12):E308. https://doi.org/10.3390/life10120308
Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25(7):1468–1486. https://doi.org/10.1002/jbmr.141
Chae C-H, Kim H-T (2009) Forced, moderate-intensity treadmill exercise suppresses apoptosis by increasing the level of NGF and stimulating phosphatidylinositol 3-kinase signaling in the hippocampus of induced aging rats. Neurochem Int 55(4):208–213. https://doi.org/10.1016/j.neuint.2009.02.024
Chang Ting-Kuo, Huang Chang-Hung, Huang Chun-Hsiung, Chen Hsuan-Chiang, Cheng Cheng-Kung (2010) The influence of long-term treadmill exercise on bone mass and articular cartilage in ovariectomized rats. BMC Musculoskelet Disord 11(août):185. https://doi.org/10.1186/1471-2474-11-185
Chen X, Aoki H, Fukui Y (2004) Effect of exercise on the bone strength, bone mineral density, and metal content in rat femurs. Bio-Med Mater Eng 14(1):53–59
Fan Y, Bergmann A (2010) The cleaved-caspase-3 antibody is a marker of caspase-9-like DRONC activity in drosophila. Cell Death and Differ 17(3):534–539. https://doi.org/10.1038/cdd.2009.185
Filgueira L (2004) Fluorescence-based staining for tartrate-resistant acidic phosphatase (TRAP) in osteoclasts combined with other fluorescent dyes and protocols. J Histochem Cytochem 52(3):411–414. https://doi.org/10.1177/002215540405200312
Fonseca H, Moreira-Gonçalves D, Coriolano HJA, Duarte JA (2014) Bone quality: the determinants of bone strength and fragility. Sports Med 44(1):37–53. https://doi.org/10.1007/s40279-013-0100-7
Gao J, Fang J, Gong He, Gao B (2017) Morphological and microstructural alterations of the articular cartilage and bones during treadmill exercises with different additional weight-bearing levels. J Healthc Eng 2017:8696921. https://doi.org/10.1155/2017/8696921
George D, Pallu S, Bourzac C, Wazzani R, Allena R, Rémond Y, Portier H (2022) Prediction of cortical bone thickness variations in the tibial diaphysis of running rats. Life 12(2):233. https://doi.org/10.3390/life12020233
Hamann N, Kohler T, Müller R, Brüggemann G-P, Niehoff A (2012) The effect of level and downhill running on cortical and trabecular bone in growing rats. Calcif Tissue Int 90(5):429–437. https://doi.org/10.1007/s00223-012-9593-6
Iijima H, Aoyama T, Ito A, Yamaguchi S, Nagai M, Tajino J, Zhang X, Kuroki H (2015) Effects of short-term gentle treadmill walking on subchondral bone in a rat model of instability-induced osteoarthritis. Osteoarthr Cartil 23(9):1563–1574. https://doi.org/10.1016/j.joca.2015.04.015
Ip TY, Peterson J, Byrner R, Tou JC (2009) Bone responses to body weight and moderate treadmill exercising in growing male obese (Fa/Fa) and lean Zucker rats. J Musculoskelet Neuronal Interact 9(3):155–166
Iwamoto J, Yeh JK, Aloia JF (1999) Differential effect of treadmill exercise on three cancellous bone sites in the young growing rat. Bone 24(3):163–169. https://doi.org/10.1016/s8756-3282(98)00189-6
Joo Y-I, Sone T, Fukunaga M, Lim S-G, Onodera S (2003) Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 33(4):485–493. https://doi.org/10.1016/s8756-3282(03)00212-6
Li KC, Zernicke RF, Barnard RJ, Li AF (1991) Differential response of rat limb bones to strenuous exercise. J Appl Physiol 70(2):554–60. https://doi.org/10.1152/jappl.1991.70.2.554
Maurel DB, Boisseau N, Ingrand I, Dolleans E, Benhamou C-L, Jaffre C (2011) Combined effects of chronic alcohol consumption and physical activity on bone health: study in a rat model. Eur J Appl Physiol 111(12):2931–2940. https://doi.org/10.1007/s00421-011-1916-1
Maurel DB, Boisseau N, Pallu S, Rochefort GY, Benhamou C-L, Jaffre C (2013) Regular exercise limits alcohol effects on trabecular, cortical thickness and porosity, and osteocyte apoptosis in the rat. Jt Bone Spine 80(5):492–498. https://doi.org/10.1016/j.jbspin.2012.12.005
Mujika I, Chatard JC, Busso T, Geyssant A, Barale F, Lacoste L (1995) Effects of training on performance in competitive swimming. Can J Appl Physiol 20(4):395–406. https://doi.org/10.1139/h95-031
Nakajima D, Kim CS, Oh TW, Yang CY, Naka T, Igawa S, Ohta F (2001) Suppressive effects of genistein dosage and resistance exercise on bone loss in ovariectomized rats. J Physiol Anthropol Appl Hum Sci 20(5):285–291. https://doi.org/10.2114/jpa.20.285
Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376(6535):37–43. https://doi.org/10.1038/376037a0
Nordsletten L, Kaastad TS, Madsen JE, Reikerås O, Ovstebø R, Strømme JH, Falch J (1994) The development of femoral osteopenia in ovariectomized rats is not reduced by high intensity treadmill training: a mechanical and densitometric study. Calcif Tissue Int 55(6):436–442. https://doi.org/10.1007/BF00298557
Novelli ELB, Diniz YS, Galhardi CM, Ebaid GMX, Rodrigues HG, Mani F, Fernandes AAH, Cicogna AC, Novelli Filho JLVB (2007) Anthropometrical parameters and markers of obesity in rats. Lab Anim 41(1):111–19. https://doi.org/10.1258/002367707779399518
Patch LD, Brooks GA (1980) Effects of training on VO2 max and VO2 during two running intensities in rats. Pflugers Arch 386(3):215–219. https://doi.org/10.1007/BF00587471
Portier H, Benaitreau D, Pallu S (2020) Does physical exercise always improve bone quality in rats? Life 10(10):E217. https://doi.org/10.3390/life10100217
Rubin CT, Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J Bone Jt Surg Am 66(3):397–402
Schneider CA, Rasband WS, Eliceiri KW(2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-5. https://doi.org/10.1038/nmeth.2089.
Scott JM, Swallow EA, Metzger CE, Kohler R, Wallace JM, Stacy AJ, Allen MR, Gasier HG (2021) Iron deficiency and high-intensity running interval training do not impact femoral or tibial bone in young female rats. Br J Nutr. https://doi.org/10.1017/S0007114521004426
Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S (1997) Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res 12(9):1480–1485. https://doi.org/10.1359/jbmr.1997.12.9.1480
Umemura Y, Baylink DJ, Wergedal JE, Mohan S, Srivastava AK (2002) A time course of bone response to jump exercise in C57BL/6J mice. J Bone Miner Metab 20(4):209–215. https://doi.org/10.1007/s007740200030
Vicente Wagner S, dos Reis Luciene M, Graciolli Rafael G, Graciolli Fabiana G, Dominguez Wagner V, Wang Charles C, Fonseca Tatiana L et al (2013) Bone plasticity in response to exercise is sex-dependent in rats. PLoS One 8(5):e64725. https://doi.org/10.1371/journal.pone.0064725
Wolff J (1986) The law of bone remodelling. Springer-Verlag, Berlin Heidelberg, https://doi.org/10.1007/978-3-642-71031-5.
Yao Z, Lafage-Proust M-H, Plouët J, Bloomfield S, Alexandre C, Vico L (2004) Increase of both angiogenesis and bone mass in response to exercise depends on VEGF. J Bone Miner Res 19(9):1471–1480. https://doi.org/10.1359/JBMR.040517
Acknowledgements
The authors would like to acknowledge all the participants in this study. We thank Christine Chappard, Morad Bensidhoum, Sara Krim and Louis Lebreton for technical support.
Funding
This research was funded by “EnvA appel à projet 2018” and “Mecanobiology project” CNRS.
Author information
Authors and Affiliations
Contributions
RW, CB, SP, CJ, and HP contributed to the design of the study. RW, CB, PG, SA and HE contributed to the acquisition, collection, and assembly of data. RW, CB, PG, SA, HE, SP, CJ, and HP contributed to reagents/materials/analysis tools. RW, CB, SP, CJ, and HP wrote the main manuscript text. All authors contributed to revising the manuscript and approved the final version to be submitted.
Corresponding author
Ethics declarations
Conflict of interest
No conflicts of interest are declared by the authors.
Additional information
Communicated by Olivier Seynnes.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wazzani, R., Bourzac, C., Elhafci, H. et al. Comparative effects of various running exercise modalities on femoral bone quality in rats. Eur J Appl Physiol 124, 761–773 (2024). https://doi.org/10.1007/s00421-023-05293-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-023-05293-2