Calcium Bioavailability of Opuntia ficus-indica Cladodes in an Ovariectomized Rat Model of Postmenopausal Bone Loss

Abstract

Osteoporosis is a disease of the skeletal system characterized by low bone mass and bone weakening, which increase the risk of fracture. This disease is associated with menopause because hypoestrogenism induces the maturation and activation of osteoclasts. In addition, a low dietary intake of calcium leads to low bone mineral density and postmenopausal osteoporosis. The objectives of this work were to determine calcium bioavailability of Opuntia ficus-indica cladodes at a late maturity stage and to assess its contribution in improving bone health in an ovariectomized rat model. Two-month-old Wistar female rats (n = 35) were used and distributed in seven experimental groups: (i) control group (Crtl), (ii) sham group (SH), (iii) ovariectomized group (OVX), (iv) ovariectomized group supplemented with calcium citrate (CCa), (v) ovariectomized group supplemented with O. ficus-indica powder (NI), (vi) ovariectomized group supplemented with soluble fiber from O. ficus-indica (FS) and (vii) ovariectomized group supplemented with insoluble fiber from O. ficus-indica (FI). Our results showed that calcium in the soluble fiber of O. ficus-indica is bioavailable and contributes to improve the physical, densitometric, biomechanical and microstructural properties of bones in ovariectomized rats. These findings indicated that O. ficus-indica cladodes at a late maturity stage represent a good source of bioavailable calcium and consumption of these cladodes might be beneficial for the prevention of osteoporosis and other bone diseases.

Keywords: Opuntia ficus-indica; bone mineral density; calcium bioavailability; osteoporosis; ovariectomy; remodeling biomarkers.

Figure 1

Effect of ovariectomy in serum estrogen levels at the beginning and at the end of the treatment. The results represent the average ± SD of the experimental groups, n = 5 in control (Ctrl), sham (SH) and ovariectomized (OVX) groups. Means in bars with different letters indicate significant differences (p ≤ 0.05) between groups with Tukey’s test.

Figure 2

(a) Apparent calcium absorption and (b) calcium balance in experimental groups. The results represent the average ± SD of experimental groups, n = 5 rats/group. Means in bars with different letters indicate significant differences (p ≤ 0.05) between groups with Tukey’s test. Ctrl = control group, SH = sham group, OVX = ovariectomized group fed with AIN-93M, FS = ovariectomized group fed with diet supplemented with soluble fiber extracted from O. ficus-indica, CCa = ovariectomized group fed with diet supplemented with calcium citrate, NI = ovariectomized group fed with diet supplemented with O. ficus-indica powder, FI = ovariectomized group fed with diet supplemented with insoluble fiber extracted from O. ficus-indica.

Figure 3

Bone mineral density in experimental groups. The results represent the average ± SD of experimental groups, n = 5 rats/group. Means in bars with different letters indicate significant differences (p ≤ 0.05) between groups with Tukey’s test. Ctrl = control group, SH = sham group, OVX = ovariectomized group fed with AIN-93M, FS = ovariectomized group fed with diet supplemented with soluble fiber extracted from O. ficus-indica, CCa = ovariectomized group fed with diet supplemented with calcium citrate, NI = ovariectomized group fed with diet supplemented with O. ficus-indica powder, FI = ovariectomized group fed with diet supplemented with insoluble fiber extracted from O. ficus-indica.

Figure 4

(a) Cortical thickness (Ct.Wi), (b) trabecular thickness (Tb.Th) and (c) trabecular separation (Tb.Sp) in femoral bone of experimental groups. The results represent the average ± SD of the experimental groups, n = 5 rats/group. Means in bars with different letters indicate significant differences (p ≤ 0.05) between groups with Tukey’s test. Ctrl = control group, SH = sham group, OVX = ovariectomized group fed with AIN-93M, FS = ovariectomized group fed with diet supplemented with soluble fiber extracted from O. ficus-indica, CCa = ovariectomized group fed with diet supplemented with calcium citrate, NI = ovariectomized group fed with diet supplemented with O. ficus-indica powder, FI = ovariectomized group fed with diet supplemented with insoluble fiber extracted from O. ficus-indica.

Figure 5

Scanning electron micrographs of the inner part of the femur (longitudinal cut from the line between condyles in the direction to the diaphysis at 12X) of rats from the experimental groups. (a) Ctrl and sham (insert in the upper right) groups, (b) ovariectomized group fed with AIN-93M, (c) ovariectomized group fed with diet supplemented with soluble fiber extracted from O. ficus-indica, (d) ovariectomized group fed with diet supplemented with calcium citrate, (e) ovariectomized group fed with diet supplemented with insoluble fiber extracted from O. ficus-indica, (f) ovariectomized group fed with diet supplemented with O. ficus-indica powder.

Figure 6

Serum levels of remodeling bone biomarkers at the initial and final stages of the treatments (a) alkaline phosphatase (b-ALP), (b) osteocalcin (OC) and (c) amino-terminal procollagen (PNPC). The results represent the average ± SD of experimental groups, n = 5 rats/group. Means in bars with different letters indicate significant differences (p ≤ 0.05) between groups with Tukey’s test. Ctrl = control group, SH = sham group, OVX = ovariectomized group fed with AIN-93M, FS = ovariectomized group fed with diet supplemented with soluble fiber extracted from O. ficus-indica, CCa = ovariectomized group fed with diet supplemented with calcium citrate, NI = ovariectomized group fed with diet supplemented with O. ficus-indica powder, FI = ovariectomized group fed with diet supplemented with insoluble fiber extracted from O. ficus-indica.