Reduced energy availability: implications for bone health in physically active populations

Papageorgiou, Maria; Dolan, Eimear; Elliott‐Sale, Kirsty J.; Sale, Craig

doi:10.1007/s00394-017-1498-8

Cited by 90 publications

(61 citation statements)

References 127 publications

(210 reference statements)

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“…Evidence for the long-term effects of reduced energy availability on bone health in women is mostly provided by cross-sectional studies [5]; here we present, to our knowledge, the first longitudinal study examining changes in bone turnover, density, geometry, microarchitecture and estimated mechanical strength in response to a prolonged energy deficit for women.…”

Section: Discussionmentioning

confidence: 90%

“…Low energy availability directly impairs bone turnover and bone mass [1,5,9,13], through effects on cortisol, T3, leptin and IGF-1 [1,2,5,25]. We previously reported preserved thyroid function but reduced leptin following the expedition [18].…”

Section: Whole-body Areal Bone Mineral Densitymentioning

confidence: 99%

“…Reduced energy availability (energy intake minus exercise energy expenditure) and low oestrogen are likely mechanisms for altered bone turnover and reduced areal bone mineral density (aBMD) [1][2][3][4][5]. Low energy availability exerts indirect effects on bone by suppressing the hypothalamic pituitary gonadal (HPG) axis (leading to functional hypothalamic amenorrhoea [FHA]) [1,2,6], decreasing oestradiol, and stimulating bone resorption [2], although oestradiol is only decreased in severe energy deficit [7].…”

Section: Introductionmentioning

confidence: 99%

“…The changes in bone quantity and quality that accompany FHA increase stress fracture risk [8]. Conversely, low energy availability exerts direct effects on bone through 3,3,5-triiodothyronine (T3), leptin and insulin-like growth factor-1 (IGF-1) mediated suppression of bone formation [1,2,5,7]. Prospective laboratory studies have shown reduced amino-terminal propeptide of procollagen type 1 (P1NP, bone formation maker) and increased c-telopeptide cross-links of type 1 collagen (CTX, bone resorption maker) in women with reductions in energy availability over several days [5,7], although the long-term impact on bone density, geometry, microarchitecture and strength, has not been investigated.…”

Section: Introductionmentioning

confidence: 99%

“…Measurements of bone macro-and microstructure were not taken in US Army Ranger training [14]. To our knowledge, no studies have prospectively investigated the effect of a prolonged period of severe exercise stress and energy deficit on bone turnover, density, geometry, microarchitecture and mechanical strength in women, who are more prone to stress fractures than men [17] and possibly more susceptible to metabolic perturbations associated with reduced energy availability [5]. A prospective approach would aid our understanding of the pathophysiology of bone injuries for women.…”

Section: Introductionmentioning

confidence: 99%

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Skeletal responses to an all-female unassisted Antarctic traverse

O’Leary¹,

Gifford

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Section: Discussionmentioning

confidence: 90%

Section: Whole-body Areal Bone Mineral Densitymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Skeletal responses to an all-female unassisted Antarctic traverse

O’Leary¹,

Gifford

Double³

et al. 2019

Bone

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Tibial Macrostructure and Microarchitecture Adaptations in Women During 44 Weeks of Arduous Military Training

O’Leary

Wardle

Gifford

et al. 2020

Journal of Bone and Mineral Research

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Bone adapts to unaccustomed, high-impact loading but loses mechanosensitivity quickly. Short periods of military training (≤12 weeks) increase the density and size of the tibia in women. The effect of longer periods of military training, where the incidence of stress fracture is high, on tibial macrostructure and microarchitecture in women is unknown. This observational study recruited 51 women (age 19 to 30 years) at the start of 44 weeks of British Army Officer training. Tibial volumetric bone mineral density (vBMD), geometry, and microarchitecture were measured by high-resolution peripheral quantitative computed tomography (HRpQCT). Scans of the right tibial metaphysis (4% site) and diaphysis (30% site) were performed at weeks 1, 14, 28, and 44. Measures of whole-body areal bone mineral density (aBMD) were obtained using dual-energy X-ray absorptiometry (DXA). Blood samples were taken at weeks 1, 28, and 44, and were analyzed for markers of bone formation and resorption. Trabecular vBMD increased from week 1 to 44 at the 4% site (3.0%, p < .001). Cortical vBMD decreased from week 1 to 14 at the 30% site (−0.3%, p < .001). Trabecular area decreased at the 4% site (−0.4%); trabecular bone volume fraction (3.5%), cortical area (4.8%), and cortical thickness (4.0%) increased at the 4% site; and, cortical perimeter increased at the 30% site (0.5%) from week 1 to 44 (p ≤ .005). Trabecular number (3.5%) and thickness (2.1%) increased, and trabecular separation decreased (−3.1%), at the 4% site from week 1 to 44 (p < .001). Training increased failure load at the 30% site from week 1 to 44 (2.5%, p < .001). Training had no effect on aBMD or markers of bone formation or resorption. Tibial macrostructure and microarchitecture continued to adapt across 44 weeks of military training in young women. Temporal decreases in cortical density support a role of intracortical remodeling in the pathogenesis of stress fracture.

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Low energy availability surrogates associated with lower bone mineral density and bone stress injury site

Holtzman

Popp

Tenforde

et al. 2022

PM&R

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Background: Exercise is an osteogenic stimulus that should increase bone mineral density (BMD) and protect against injury. However, some female athletes have lower BMD and increased bone stress injury (BSI) risk. Impaired bone health seen in athletes may be explained by low energy availability as described by concepts of Relative Energy Deficiency in Sport (RED-S) and Female Athlete Triad (Triad). Objective: To elucidate the relationship between RED-S/Triad risk factors and BSI to high-risk (femoral neck, sacrum) and low-risk (other) bones. Design: Cross-sectional survey and retrospective chart review. Setting: Tertiary care academic center. Patients: Female athletes aged 15-30 years participating in ≥4 h/week of exercise presenting to sports medicine/orthopedics clinic who had a self-reported BSI and available dual-energy x-ray absorptiometry (DXA) measurement of BMD. Interventions: Not applicable. Main Outcome Measurements: Location of BSI. Results: In 127 athletes, high-risk BSI was associated with surrogates of low energy availability (p = .032) and having a DXA Z-score < À1 (p = .035) but not a current/past history of menstrual dysfunction (p = .348). Accumulating RED-S/Triad risk factors increase the odds of incurring a high-risk BSI (p = .048). Conclusions: Adolescent/young female athletes who sustain BSI at high-risk sites (femoral neck, sacrum) may have underlying risk factors (eg, low energy availability, poor overall bone health) that should prompt further workup and referral to optimize health in these athletes.

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Reduced energy availability: implications for bone health in physically active populations

Cited by 90 publications

References 127 publications

Skeletal responses to an all-female unassisted Antarctic traverse

Skeletal responses to an all-female unassisted Antarctic traverse

Tibial Macrostructure and Microarchitecture Adaptations in Women During 44 Weeks of Arduous Military Training

Low energy availability surrogates associated with lower bone mineral density and bone stress injury site

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