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Electrical Stimulation of Denervated Rat Skeletal Muscle Ameliorates Bone Fragility and Muscle Loss in Early-Stage Disuse Musculoskeletal Atrophy

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Abstract

We tested whether daily muscle electrical stimulation (ES) can ameliorate the decrease in cortical bone strength as well as muscle and bone geometric and material properties in the early stages of disuse musculoskeletal atrophy. 7-week-old male F344 rats were randomly divided into three groups: age-matched control group (Cont); a sciatic denervation group (DN); and a DN + direct electrical stimulation group (DN + ES). Denervated tibialis anterior (TA) muscle in the DN + ES group received ES with 16 mA at 10 Hz for 30 min/day, 6 days/week. Micro CT, the three-point bending test, and immunohistochemistry were used to characterize cortical bone mechanical, structural, and material properties of tibiae. TA muscle in the DN + ES group showed significant improvement in muscle mass and myofiber cross-sectional area relative to the DN group. Maximal load and stiffness of tibiae, bone mineral density estimated by micro CT, and immunoreactivity of DMP1 in the cortical bone tissue were also significantly greater in the DN + ES group than in the DN group. These results suggest that daily ES-induced muscle contraction treatment reduced the decrease in muscle mass and cortical bone strength in early-stage disuse musculoskeletal atrophy and is associated with a beneficial effect on material properties such as mineralization of cortical bone tissue.

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Acknowledgements

This study was supported in part by a Grant-in-Aid for Scientific Research (KAKENHI Grant Nos. 25350829, 25282163, 16K13021), and by a Grant-in-Aid for Developed Research from the Niigata University of Health and Welfare. The authors are grateful to the Niigata Bone Science Institute for technical support.

Author Contributions

Author HT designed the study and prepared the first draft of the paper; Authors HT, KY, FO, KN, and NK performed experiments; Authors HT, KS, and HK analyzed data; Authors HT, HO, and NY interpreted results of experiments; Authors HT and HK prepared figures; Authors HT, HO, and NK edited and revised manuscript; All authors approved the final version of the manuscript.

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Authors and Affiliations

  1. Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, 1398 Shimami, Kita-ku, Niigata, 950-3198, Japan

    Hiroyuki Tamaki, Keishi Hayao, Kouki Nakagawa, Hikari Kirimoto, Hideaki Onishi & Noriaki Yamamoto

  2. National Institute of Fitness and Sports in Kanoya, 1 Shiromizu, Kanoya, Kagoshima, 891-2393, Japan

    Kengo Yotani & Futoshi Ogita

  3. Tohoku Fukushi University, 1‑8‑1 Kunimi, Aoba‑ku, Sendai, Miyagi, 981‑8522, Japan

    Kazuhiro Sugawara

  4. Aichi University of Education, 1 Hirosawa, Igaya, Kariya, Aichi, 448-8542, Japan

    Norikatsu Kasuga

  5. Niigata Rehabilitation Hospital, 761 Kisaki, Kita-ku, Niigata, 950-3304, Japan

    Noriaki Yamamoto

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  1. Hiroyuki Tamaki
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  2. Kengo Yotani
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Correspondence to Hiroyuki Tamaki.

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Hiroyuki Tamaki, Kengo Yotani, Futoshi Ogita, Keishi Hayao, Kouki Nakagawa, Kazuhiro Sugawara, Hikari Kirimoto, Hideaki Onishi, Norikatsu Kasuga, and Noriaki Yamamoto declare no conflict of interest.

Human and Animal Rights and Informed Consent

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Tamaki, H., Yotani, K., Ogita, F. et al. Electrical Stimulation of Denervated Rat Skeletal Muscle Ameliorates Bone Fragility and Muscle Loss in Early-Stage Disuse Musculoskeletal Atrophy. Calcif Tissue Int 100, 420–430 (2017). https://doi.org/10.1007/s00223-017-0250-y

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