Rapid suppression of bone formation marker in response to sleep restriction and circadian disruption in men

C. M. Swanson, W. M. Kohrt, P. Wolfe, K. P. Wright, Steven Shea, S. W. Cain, M. Munch, N. Vujović, C. A. Czeisler, Eric Orwoll, O. M. Buxton

Research output: Contribution to journalArticle

Abstract

Summary: We describe the time course of bone formation marker (P1NP) decline in men exposed to ~ 3 weeks of sleep restriction with concurrent circadian disruption. P1NP declined within 10 days and remained lower with ongoing exposure. These data suggest even brief exposure to sleep and circadian disruptions may disrupt bone metabolism. Introduction: A serum bone formation marker (procollagen type 1 N-terminal, P1NP) was lower after ~ 3 weeks of sleep restriction combined with circadian disruption. We now describe the time course of decline. Methods: The ~ 3-week protocol included two segments: “baseline,” ≥ 10-h sleep opportunity/day × 5 days; “forced desynchrony” (FD), recurring 28 h day (circadian disruption) with sleep restriction (~ 5.6-h sleep per 24 h). Fasted plasma P1NP was measured throughout the protocol in nine men (20–59 years old). We tested the hypothesis that PINP would steadily decline across the FD intervention because the magnitude of sleep loss and circadian misalignment accrued as the protocol progressed. A piecewise linear regression model was used to estimate the slope (β) as ΔP1NP per 24 h with a change point mid-protocol to estimate the initial vs. prolonged effects of FD exposure. Results: Plasma P1NP levels declined significantly within the first 10 days of FD (β^ = − 1.33 μg/L per 24 h, p < 0.0001) and remained lower than baseline with prolonged exposure out to 3 weeks (β^ = − 0.18 μg/L per 24 h, p = 0.67). As previously reported, levels of a bone resorption marker (C-telopeptide (CTX)) were unchanged. Conclusion: Sleep restriction with concurrent circadian disruption induced a relatively rapid decline in P1NP (despite no change in CTX) and levels remained lower with ongoing exposure. These data suggest (1) even brief sleep restriction and circadian disruption can adversely affect bone metabolism, and (2) there is no P1NP recovery with ongoing exposure that, taken together, could lead to lower bone density over time.

Original languageEnglish (US)
JournalOsteoporosis International
DOIs
StateAccepted/In press - Jan 1 2019

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Osteogenesis
Sleep
Linear Models
Bone and Bones
Bone Resorption
Collagen Type I
Bone Density
Serum

Keywords

  • Bone formation
  • Bone loss
  • Circadian disruption
  • P1NP
  • Sleep restriction

ASJC Scopus subject areas

  • Endocrinology, Diabetes and Metabolism

Cite this

Rapid suppression of bone formation marker in response to sleep restriction and circadian disruption in men. / Swanson, C. M.; Kohrt, W. M.; Wolfe, P.; Wright, K. P.; Shea, Steven; Cain, S. W.; Munch, M.; Vujović, N.; Czeisler, C. A.; Orwoll, Eric; Buxton, O. M.

In: Osteoporosis International, 01.01.2019.

Research output: Contribution to journalArticle

Swanson, C. M. ; Kohrt, W. M. ; Wolfe, P. ; Wright, K. P. ; Shea, Steven ; Cain, S. W. ; Munch, M. ; Vujović, N. ; Czeisler, C. A. ; Orwoll, Eric ; Buxton, O. M. / Rapid suppression of bone formation marker in response to sleep restriction and circadian disruption in men. In: Osteoporosis International. 2019.
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abstract = "Summary: We describe the time course of bone formation marker (P1NP) decline in men exposed to ~ 3 weeks of sleep restriction with concurrent circadian disruption. P1NP declined within 10 days and remained lower with ongoing exposure. These data suggest even brief exposure to sleep and circadian disruptions may disrupt bone metabolism. Introduction: A serum bone formation marker (procollagen type 1 N-terminal, P1NP) was lower after ~ 3 weeks of sleep restriction combined with circadian disruption. We now describe the time course of decline. Methods: The ~ 3-week protocol included two segments: “baseline,” ≥ 10-h sleep opportunity/day × 5 days; “forced desynchrony” (FD), recurring 28 h day (circadian disruption) with sleep restriction (~ 5.6-h sleep per 24 h). Fasted plasma P1NP was measured throughout the protocol in nine men (20–59 years old). We tested the hypothesis that PINP would steadily decline across the FD intervention because the magnitude of sleep loss and circadian misalignment accrued as the protocol progressed. A piecewise linear regression model was used to estimate the slope (β) as ΔP1NP per 24 h with a change point mid-protocol to estimate the initial vs. prolonged effects of FD exposure. Results: Plasma P1NP levels declined significantly within the first 10 days of FD (β^ = − 1.33 μg/L per 24 h, p < 0.0001) and remained lower than baseline with prolonged exposure out to 3 weeks (β^ = − 0.18 μg/L per 24 h, p = 0.67). As previously reported, levels of a bone resorption marker (C-telopeptide (CTX)) were unchanged. Conclusion: Sleep restriction with concurrent circadian disruption induced a relatively rapid decline in P1NP (despite no change in CTX) and levels remained lower with ongoing exposure. These data suggest (1) even brief sleep restriction and circadian disruption can adversely affect bone metabolism, and (2) there is no P1NP recovery with ongoing exposure that, taken together, could lead to lower bone density over time.",
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AU - Swanson, C. M.

AU - Kohrt, W. M.

AU - Wolfe, P.

AU - Wright, K. P.

AU - Shea, Steven

AU - Cain, S. W.

AU - Munch, M.

AU - Vujović, N.

AU - Czeisler, C. A.

AU - Orwoll, Eric

AU - Buxton, O. M.

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N2 - Summary: We describe the time course of bone formation marker (P1NP) decline in men exposed to ~ 3 weeks of sleep restriction with concurrent circadian disruption. P1NP declined within 10 days and remained lower with ongoing exposure. These data suggest even brief exposure to sleep and circadian disruptions may disrupt bone metabolism. Introduction: A serum bone formation marker (procollagen type 1 N-terminal, P1NP) was lower after ~ 3 weeks of sleep restriction combined with circadian disruption. We now describe the time course of decline. Methods: The ~ 3-week protocol included two segments: “baseline,” ≥ 10-h sleep opportunity/day × 5 days; “forced desynchrony” (FD), recurring 28 h day (circadian disruption) with sleep restriction (~ 5.6-h sleep per 24 h). Fasted plasma P1NP was measured throughout the protocol in nine men (20–59 years old). We tested the hypothesis that PINP would steadily decline across the FD intervention because the magnitude of sleep loss and circadian misalignment accrued as the protocol progressed. A piecewise linear regression model was used to estimate the slope (β) as ΔP1NP per 24 h with a change point mid-protocol to estimate the initial vs. prolonged effects of FD exposure. Results: Plasma P1NP levels declined significantly within the first 10 days of FD (β^ = − 1.33 μg/L per 24 h, p < 0.0001) and remained lower than baseline with prolonged exposure out to 3 weeks (β^ = − 0.18 μg/L per 24 h, p = 0.67). As previously reported, levels of a bone resorption marker (C-telopeptide (CTX)) were unchanged. Conclusion: Sleep restriction with concurrent circadian disruption induced a relatively rapid decline in P1NP (despite no change in CTX) and levels remained lower with ongoing exposure. These data suggest (1) even brief sleep restriction and circadian disruption can adversely affect bone metabolism, and (2) there is no P1NP recovery with ongoing exposure that, taken together, could lead to lower bone density over time.

AB - Summary: We describe the time course of bone formation marker (P1NP) decline in men exposed to ~ 3 weeks of sleep restriction with concurrent circadian disruption. P1NP declined within 10 days and remained lower with ongoing exposure. These data suggest even brief exposure to sleep and circadian disruptions may disrupt bone metabolism. Introduction: A serum bone formation marker (procollagen type 1 N-terminal, P1NP) was lower after ~ 3 weeks of sleep restriction combined with circadian disruption. We now describe the time course of decline. Methods: The ~ 3-week protocol included two segments: “baseline,” ≥ 10-h sleep opportunity/day × 5 days; “forced desynchrony” (FD), recurring 28 h day (circadian disruption) with sleep restriction (~ 5.6-h sleep per 24 h). Fasted plasma P1NP was measured throughout the protocol in nine men (20–59 years old). We tested the hypothesis that PINP would steadily decline across the FD intervention because the magnitude of sleep loss and circadian misalignment accrued as the protocol progressed. A piecewise linear regression model was used to estimate the slope (β) as ΔP1NP per 24 h with a change point mid-protocol to estimate the initial vs. prolonged effects of FD exposure. Results: Plasma P1NP levels declined significantly within the first 10 days of FD (β^ = − 1.33 μg/L per 24 h, p < 0.0001) and remained lower than baseline with prolonged exposure out to 3 weeks (β^ = − 0.18 μg/L per 24 h, p = 0.67). As previously reported, levels of a bone resorption marker (C-telopeptide (CTX)) were unchanged. Conclusion: Sleep restriction with concurrent circadian disruption induced a relatively rapid decline in P1NP (despite no change in CTX) and levels remained lower with ongoing exposure. These data suggest (1) even brief sleep restriction and circadian disruption can adversely affect bone metabolism, and (2) there is no P1NP recovery with ongoing exposure that, taken together, could lead to lower bone density over time.

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