Bone marrow metabolism is affected by body weight and response to exercise training varies according to anatomical location

Abstract

AimHigh body weight is a protective factor against osteoporosis, but obesity also suppresses bone metabolism and whole‐body insulin sensitivity. However, the impact of body weight and regular training on bone marrow (BM) glucose metabolism is unclear. We studied the effects of regular exercise training on bone and BM metabolism in monozygotic twin pairs discordant for body weight.MethodsWe recruited 12 monozygotic twin pairs (mean ± SD age 40.4 ± 4.5 years; body mass index 32.9 ± 7.6, mean difference between co‐twins 7.6 kg/m2; eight female pairs). Ten pairs completed the 6‐month long training intervention. We measured lumbar vertebral and femoral BM insulin‐stimulated glucose uptake (GU) using 18F‐FDG positron emission tomography, lumbar spine bone mineral density and bone turnover markers.ResultsAt baseline, heavier co‐twins had higher lumbar vertebral BM GU (p < .001) and lower bone turnover markers (all p < .01) compared with leaner co‐twins but there was no significant difference in femoral BM GU, or bone mineral density. Training improved whole‐body insulin sensitivity, aerobic capacity (both p < .05) and femoral BM GU (p = .008). The training response in lumbar vertebral BM GU was different between the groups (time × group, p = .02), as GU tended to decrease in heavier co‐twins (p = .06) while there was no change in leaner co‐twins.ConclusionsIn this study, regular exercise training increases femoral BM GU regardless of weight and genetics. Interestingly, lumbar vertebral BM GU is higher in participants with higher body weight, and training counteracts this effect in heavier co‐twins even without reduction in weight. These data suggest that BM metabolism is altered by physical activity.

Evaluation of bone marrow glucose uptake and adiposity in male rats after diet and exercise interventions

“…Our data agrees with this finding, which is reflected by higher BMGU in the sternum than in humerus. The same phenomenon can be seen in humans when comparing vertebral and femoral BMGU ( 14 , 15 , 28 ). In humans, lumbar vertebral BM is more hematopoietically active while femoral BM cavity serves mainly as a specialized fat depot ( 14 , 15 , 28 ).…”

“…We have previously shown that BMAT-enriched femoral BM insulin-stimulated glucose uptake (GU) and fasting free fatty acid uptake are impaired in insulin resistance in humans ( 14 ). Further, lumbar vertebral BM metabolism is affected by body weight ( 15 ). We also showed that BMGU is affected by exercise training and the effects of short- and long-term exercise training on BMGU varied according to anatomical location ( 14 , 15 ).…”

“…Further, lumbar vertebral BM metabolism is affected by body weight ( 15 ). We also showed that BMGU is affected by exercise training and the effects of short- and long-term exercise training on BMGU varied according to anatomical location ( 14 , 15 ). Femoral insulin-stimulated BMGU was increased already after two weeks of cycling exercise and associated positively with whole-body insulin sensitivity and bone turnover rate at baseline.…”

“…Femoral insulin-stimulated BMGU was increased already after two weeks of cycling exercise and associated positively with whole-body insulin sensitivity and bone turnover rate at baseline. On the contrary, lumbar vertebral BMGU remained unaffected by short-term exercise training, but was higher in participants with high body weight while six months of regular exercise training decreased lumbar vertebral BMGU to the level of leaner participants even without reduction in body weight or BM adiposity ( 15 ).…”

“…In our previous studies in humans, we used positron emission tomography (PET) to assess the changes in BM metabolism ( 3 , 14 , 15 ). This imaging modality allowed us to study the metabolism of the BM niche as a whole.…”