Bone Turnover Markers After Sleep Restriction and Circadian Disruption: A Mechanism for Sleep-Related Bone Loss in Humans

Christine M. Swanson, Steven A. Shea, Pamela Wolfe, Sean W. Cain, Mirjam Munch, Nina Vujovic, Charles A. Czeisler, Orfeu M. Buxton, Eric S. Orwoll

Research output: Research - peer-reviewArticle

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Abstract

Context: Sleep abnormalities are associated with low bone mineral density. Underlying mechanisms are unknown.

Objective: Investigate the impact of sleep restriction with circadian disruption on bone biomarkers.

Design: Intervention study.

Participants and Methods: Four bone biomarkers [C-terminal cross-linked telopeptide of type I collagen (CTX) = bone resorption, N-terminal propeptide of type I procollagen (P1NP) = bone formation, sclerostin and fibroblast growth factor 23 = osteocyte function] were measured in bihourly serum samples over 24 hours at baseline and after ∼3 weeks of sleep restriction (5.6 hours sleep/24 hours) with concurrent circadian disruption (recurring 28-hour "day" in dim light) in 10 men (age groups: 20 to 27 years, n = 6; 55 to 65 years, n = 4). The effects of sleep/circadian disruption and age on bone biomarker levels were evaluated using maximum likelihood estimation in a mixed model for repeated measures.

Results: P1NP levels were lower after intervention compared with baseline (P < 0.001); the decrease in P1NP was greater for younger compared with older men (28.0% vs 18.2%, P < 0.001). There was no change in CTX (Δ = 0.03 ± 0.02 ng/mL, P = 0.10). Sclerostin levels were higher postintervention in the younger men only (Δ = 22.9% or 5.64 ± 1.10 pmol/L, P < 0.001).

Conclusions: These data suggest that 3 weeks of circadian disruption with concurrent sleep restriction can lead to an uncoupling of bone turnover wherein bone formation is decreased but bone resorption is unchanged. Circadian disruption and sleep restriction may be most detrimental to bone in early adulthood.

LanguageEnglish (US)
Pages3722-3730
Number of pages9
JournalThe Journal of clinical endocrinology and metabolism
Volume102
Issue number10
DOIs
StatePublished - Oct 1 2017

Fingerprint

Bone Remodeling
Sleep
Bone and Bones
Bone
Biomarkers
Bone Resorption
Collagen Type I
Osteogenesis
Osteocytes
Bone Density
Age Groups
Light
Serum
fibroblast growth factor 23
Maximum likelihood estimation
Minerals

ASJC Scopus subject areas

  • Endocrinology, Diabetes and Metabolism
  • Biochemistry
  • Endocrinology
  • Clinical Biochemistry
  • Biochemistry, medical

Cite this

Bone Turnover Markers After Sleep Restriction and Circadian Disruption : A Mechanism for Sleep-Related Bone Loss in Humans. / Swanson, Christine M.; Shea, Steven A.; Wolfe, Pamela; Cain, Sean W.; Munch, Mirjam; Vujovic, Nina; Czeisler, Charles A.; Buxton, Orfeu M.; Orwoll, Eric S.

In: The Journal of clinical endocrinology and metabolism, Vol. 102, No. 10, 01.10.2017, p. 3722-3730.

Research output: Research - peer-reviewArticle

Swanson, Christine M. ; Shea, Steven A. ; Wolfe, Pamela ; Cain, Sean W. ; Munch, Mirjam ; Vujovic, Nina ; Czeisler, Charles A. ; Buxton, Orfeu M. ; Orwoll, Eric S./ Bone Turnover Markers After Sleep Restriction and Circadian Disruption : A Mechanism for Sleep-Related Bone Loss in Humans. In: The Journal of clinical endocrinology and metabolism. 2017 ; Vol. 102, No. 10. pp. 3722-3730
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T2 - Journal of Clinical Endocrinology and Metabolism

AU - Swanson,Christine M.

AU - Shea,Steven A.

AU - Wolfe,Pamela

AU - Cain,Sean W.

AU - Munch,Mirjam

AU - Vujovic,Nina

AU - Czeisler,Charles A.

AU - Buxton,Orfeu M.

AU - Orwoll,Eric S.

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Y1 - 2017/10/1

N2 - Context: Sleep abnormalities are associated with low bone mineral density. Underlying mechanisms are unknown.Objective: Investigate the impact of sleep restriction with circadian disruption on bone biomarkers.Design: Intervention study.Participants and Methods: Four bone biomarkers [C-terminal cross-linked telopeptide of type I collagen (CTX) = bone resorption, N-terminal propeptide of type I procollagen (P1NP) = bone formation, sclerostin and fibroblast growth factor 23 = osteocyte function] were measured in bihourly serum samples over 24 hours at baseline and after ∼3 weeks of sleep restriction (5.6 hours sleep/24 hours) with concurrent circadian disruption (recurring 28-hour "day" in dim light) in 10 men (age groups: 20 to 27 years, n = 6; 55 to 65 years, n = 4). The effects of sleep/circadian disruption and age on bone biomarker levels were evaluated using maximum likelihood estimation in a mixed model for repeated measures.Results: P1NP levels were lower after intervention compared with baseline (P < 0.001); the decrease in P1NP was greater for younger compared with older men (28.0% vs 18.2%, P < 0.001). There was no change in CTX (Δ = 0.03 ± 0.02 ng/mL, P = 0.10). Sclerostin levels were higher postintervention in the younger men only (Δ = 22.9% or 5.64 ± 1.10 pmol/L, P < 0.001).Conclusions: These data suggest that 3 weeks of circadian disruption with concurrent sleep restriction can lead to an uncoupling of bone turnover wherein bone formation is decreased but bone resorption is unchanged. Circadian disruption and sleep restriction may be most detrimental to bone in early adulthood.

AB - Context: Sleep abnormalities are associated with low bone mineral density. Underlying mechanisms are unknown.Objective: Investigate the impact of sleep restriction with circadian disruption on bone biomarkers.Design: Intervention study.Participants and Methods: Four bone biomarkers [C-terminal cross-linked telopeptide of type I collagen (CTX) = bone resorption, N-terminal propeptide of type I procollagen (P1NP) = bone formation, sclerostin and fibroblast growth factor 23 = osteocyte function] were measured in bihourly serum samples over 24 hours at baseline and after ∼3 weeks of sleep restriction (5.6 hours sleep/24 hours) with concurrent circadian disruption (recurring 28-hour "day" in dim light) in 10 men (age groups: 20 to 27 years, n = 6; 55 to 65 years, n = 4). The effects of sleep/circadian disruption and age on bone biomarker levels were evaluated using maximum likelihood estimation in a mixed model for repeated measures.Results: P1NP levels were lower after intervention compared with baseline (P < 0.001); the decrease in P1NP was greater for younger compared with older men (28.0% vs 18.2%, P < 0.001). There was no change in CTX (Δ = 0.03 ± 0.02 ng/mL, P = 0.10). Sclerostin levels were higher postintervention in the younger men only (Δ = 22.9% or 5.64 ± 1.10 pmol/L, P < 0.001).Conclusions: These data suggest that 3 weeks of circadian disruption with concurrent sleep restriction can lead to an uncoupling of bone turnover wherein bone formation is decreased but bone resorption is unchanged. Circadian disruption and sleep restriction may be most detrimental to bone in early adulthood.

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