Impact of Long-Term Swimming Exercise on Rat Femur Bone Quality

Abstract

Considering the conflicting evidence regarding the potential long-term detrimental effect of swimming during growth on femur quality and fracture risk, our aim was to investigate the effect of eight months of swimming on femur quality. Twenty male eight-week-old Wistar rats were assigned into a swimming (SW; n = 10; 2 h/day, 5 days/week) or active control group (CG; n = 10, housed with running wheel) for eight months. Plasma osteocalcin and C-terminal telopeptide of type I collagen concentrations (ELISA) were assessed at baseline, four, and eight months of protocol. Femur structure (micro-computed tomography), biomechanical properties (three-point bending), and cellular density (histology) were determined after the protocol. SW displayed a lower uncoupling index, suggesting higher bone resorption, lower empty lacunae density, cortical and trabecular femur mass, femur length and cortical thickness, and higher cortical porosity than CG (p < 0.05). Although both biomarkers' concentrations decreased in both groups throughout the experiment (p < 0.001), there were no significant differences between groups (p > 0.05). No differences were also found regarding biomechanical properties, bone marrow adiposity, and osteocyte and osteoclast densities (p > 0.05). Long-term swimming was associated with unbalanced bone turnover and compromised femur growth, lower femur mass, and deteriorated cortical bone microarchitecture. However, femur trabecular microarchitecture and biomechanical properties were not affected by swimming.

Keywords: bone growth; bone microarchitecture; bone mineral density; bone remodelling; non-weight bearing exercise.

Figure 1

Water adaptation and experimental exercise protocol of the swimming group (image created in https://www.biorender.com/ (accessed on 15 November 2023).

Figure 2

Trabecular mass and microarchitecture at distal femoral epiphysis in growing rats between the control (n = 10, except for trabeculae connectivity density n = 9 after removing the outliers) and swimming groups (n = 9, except for trabeculae connectivity density n = 7 after removing the outliers) after eight months of the experiment (C), with the representative micro-computed tomography images of the sagittal (A) and transverse planes (B). Data are displayed as mean ± SD. Legend: Active control group (CG); bone volume fraction (BV/TV); trabeculae connectivity density (Conn.D); trabecular bone mineral content (Tb.BMC); trabecular number (Tb.N); trabecular thickness (Tb.Th); trabecular separation (Tb.Sp); trabecular volumetric bone density (Tb.vBMD); * p < 0.05.

Figure 3

Cortical mass and microarchitecture at the femoral midshaft in growing rats between the control (n = 10, except for cortical porosity n = 9 after removing the outliers) and swimming (n = 9, except for cortical porosity n = 8 after removing the outliers) groups after eight months of the experiment (C), with the representative micro-computed tomography images of the sagittal (A) and transverse planes (B). Data are displayed as mean ± SD. Legend: Active control group (CG); cortical area fraction (Ct.Ar/Tt.Ar); cortical bone mineral content (Ct.BMC); cortical porosity (Ct.Po); cortical thickness cortical (Ct.Th); volumetric bone density (Ct.vBMD); swimming group (SW); * p < 0.05.

Figure 4

Bone turnover assessed by the biochemical markers and bone turnover uncoupling index (A) and femur osteocyte, lacunae, and osteoclast densities (B) between the control (n = 10) and swimming (n = 9) groups after eight months of the experiment, with representative images of haematoxylin and eosin staining for osteocyte, lacunae densities (B1), and bone marrow adiposity (B2), and tartrate-resistant acid phosphatase staining for osteoclast density (B3). Data are displayed as mean ± SD. Legend: Active control group (CG); bone marrow adiposity (Ad.Ar/Ma.Ar); C-terminal telopeptide of type I collagen (CTX); empty lacunae density (N.Lc/Ct.Ar); osteocyte density (N.Ot/Ct.Ar); osteoclast density (N.Oc/T.Ar); swimming group (SW); * p < 0.05.