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Physiol. Res. 70: 119-151, 2021 https://doi.org/10.33549/physiolres.934550 INVITED REVIEW The Effects of Spaceflight Microgravity on the Musculoskeletal System of Humans and Animals, with an Emphasis on Exercise as a Countermeasure: A Systematic Scoping Review Darya MOOSAVI1, David WOLOVSKY1, Angela DEPOMPEIS1, David UHER1, David LENNINGTON1, Roddy BODDEN1, Carol Ewing GARBER1 1Department of Biobehavioral Sciences, Teachers College, Columbia University. New York City, NY, United States Received July 29, 2020 Accepted February 18, 2021 Summary Existing studies have produced only limited data on the combined The purpose of this systematic review is twofold: 1) to identify, effects on bone and muscle of human spaceflight, despite the evaluate, and synthesize the heretofore disparate scientific likelihood that the effects on these two systems are complicated literatures regarding the effects of direct exposure to due to the components of the musculoskeletal system being microgravity on the musculoskeletal system, taking into account anatomically and functionally interconnected. Bone is directly for the first time both bone and muscle systems of both humans affected by muscle atrophy as well as by changes in muscle and animals; and 2) to investigate the efficacy and limitations of strength, notably at muscle attachments. Given this interplay, the exercise countermeasures on the musculoskeletal system under most effective exercise countermeasure is likely to be robust, microgravity in humans. The Framework for Scoping Studies individualized, resistive exercise, primarily targeting muscle mass (Arksey and O'Malley 2005) and the Cochrane Handbook for and strength. Systematic Reviews of Interventions (Higgins JPT 2011) were used to guide this review. The Preferred Reporting Items for Key words Systematic Reviews and Meta-Analyses (PRISMA) checklist was Microgravity • Musculoskeletal system • Exercise countermeasure utilized in obtaining the combined results (Moher, Liberati et al. • Spaceflight • Skeleton • Skeletal Muscle 2009). Data sources, PubMed, Embase, Scopus, and Web of Science were searched for published articles through October Corresponding author 2019 using the Mesh terms of microgravity, musculoskeletal Darya Moosavi, 525 W 120th St, New York, NY 10027, USA. system, and exercise countermeasures. A total of 84 references E-mail: [email protected] were selected, including 40 animal studies and 44 studies with human participants. The heterogeneity in the study designs, Introduction methodologies, and outcomes deemed this review unsuitable for a meta-analysis. Thus, we present a narrative synthesis of the With the prospect of sending humans to Mars results for the key domains under five categories: (and beyond), understanding the effects of physiological 1) Skeletal muscle responses to microgravity in humans changes on the health of astronauts is critical for 2) Skeletal muscle responses to microgravity in animals successful long-duration spaceflight (SF). Prolonged 3) Adaptation of the skeletal system to microgravity in humans exposure to microgravity (μG), is harmful to the bones 4) Adaptation of the skeletal system to microgravity in animals and muscles of the human body. When astronauts are in 5) Effectiveness of exercise countermeasures on the human a μG environment, they experience decreases in bone musculoskeletal system in microgravity. density and muscle volume, as well as changes in muscle PHYSIOLOGICAL RESEARCH • ISSN 1802-9973 (online) 2021 Institute of Physiology of the Czech Academy of Sciences, Prague, Czech Republic Fax +420 241 062 164, e-mail: [email protected], www.biomed.cas.cz/physiolres 120 Moosavi et al. Vol. 70 fiber properties (Trappe et al. 2009). A weakened Purpose musculoskeletal system comprises the ability of astronauts to perform mission-critical tasks both during The purpose of this systematic review is spaceflight and upon reentry to a gravitational twofold: 1) to identify, evaluate, and synthesize environment. While various exercise countermeasures heretofore disparate scientific literatures regarding the have been evaluated, one single successful method in effects of direct exposure to microgravity on the maintaining the integrity of the musculoskeletal system musculoskeletal system, taking into account for the first on long-duration spaceflight has not yet been found. time both bone and muscle systems of both humans and Since skeletal muscles, tendons, ligaments, and bones are animals; and 2) to investigate the efficacy and limitations anatomically and functionally interconnected, the of exercise countermeasures on the musculoskeletal reductionist approach that focuses on only one part of this system under microgravity in humans. complex system is inadequate for determining the most protective exercise protocols for astronauts. This Methods systematic review thus aims to synthesize for the first time the scientific literature regarding the effects of μG This systematic review was conducted in on both bone and muscle, describe exercise protocols that accordance with the methodological framework for have been used in μG, and identify crucial features of scoping studies (Arksey and O'Malley 2005) and the effective countermeasures to SF-induced atrophy. We guidelines of the Cochrane Handbook for Systematic review studies based on direct exposure to μG in both Reviews of Interventions (Higgins JPT 2011) to ensure humans and animals. This topic is of particular relevance, a transparent and complete investigation. Also, the especially amid the coronavirus (COVID-19) pandemic. PRISMA (Preferred Reporting Items for Systematic Patients with COVID-19 sustain muscle atrophy due to Reviews and Meta-analyses) checklist was used to report hospital-associated deconditioning. Likewise, astronauts the results (Moher et al. 2009). The scoping methodology experience muscular deterioration from long-term was employed because our research questions were broad inactivity and muscle unloading in the microgravity and complex. Additionally, this topic covers several environment. different study designs that could not be identified in advance. Table 1. PICOS eligibility criteria model Parameter Inclusion criteria Exclusion criteria Population Astronauts/cosmonauts and animals with no sex or age Populations with no direct exposure to restrictions spaceflight conditions Intervention or Direct exposure to μG for at least 24 hours or longer All other analogs such as bed rest, hind limb Exposure suspension, immobilization, disuse, and Countermeasure: physical activity/exercise training, parabolic flights including resistance training All other countermeasures including pharmacologic or dietary supplementation, electrical stimulation, hybrid, artificial gravity Comparator No exposure to μG (e.g., ground-based controls, bed rest, N/A etc.) No exercise countermeasure Outcomes Physiological changes in skeletal muscle (e.g., muscle No defined physiological outcomes related to the mass, strength, fiber types, etc.), and/or skeletal system musculoskeletal systém (e.g., bone density, structure, such as cortical thickness or porosity) All other non-physiological outcomes Physiological effects of exercise countermeasures (e.g., biomechanical and motor control) Study Design Primary studies including All nonexperimental designs including RCT, NRCT, and single group studies editorials, opinions, pilot studies, narrative reviews, meta-analyses 2021 Spaceflight Microgravity and Musculoskeletal System 121 Table 2. Search strategy Search # Keywords Terms and MeSH vocabulary 1 Microgravity Microgravity OR spaceflight OR weightlessness 2 Musculoskeletal Muscle OR bone OR musculoskeletal OR ‘skeletal muscle’ 3 Countermeasure Exercise OR training OR countermeasure 4 Combined search 1 AND 2 AND 3 1 AND 2 1 AND 3 Note. Medical Subject Headings (MeSH) as a comprehensive controlled vocabulary for the purpose of indexing journal articles and books in the life sciences were included in the search strategy. In the Pubmed advanced search builder either ‘Title/Abstract’ [tiab] was used. Eligibility criteria the term “hypogravity” or studies using it. Inclusion criteria included the population, Risk of bias in individual studies intervention, comparison, outcome, and study design (PICOS) model (Richardson 1995). The PICOS The Cochrane Collaboration's tool for assessing eligibility criteria are presented in Table 1. risk of bias was used to assess the quality of included studies (Moher et al. 2009). Two authors independently Search strategy for identification of studies assessed the risk of bias. Uncertainties or disagreements were resolved by consensus or discussed with a third The electronic searches were performed in reviewer when necessary. Risk of bias was evaluated as August 2018, by the first author with the assistance of low, high, or unclear, according to the following factors: a research librarian from the Augustus C. Long Health random sequence generation, allocation concealment, Sciences Library of Columbia University. blinding of participants and personnel, blinding of The literature search was conducted in English. outcome assessment, incomplete outcome data, and A range of medical subject headings (MeSH) (or selective outcome data, as well as other sources of bias. equivalent structured terms in other databases) and keywords related to μG, the musculoskeletal system, and Results exercise were used in various combinations. Searches were performed on PubMed, Embase, Scopus, and Web Study selection of Science (Table 2). The search
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