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Medicine & Science in Sports & Exercise:
Basic Sciences: NASA Roundtable

Musculoskeletal adaptations to weightlessness and development of effective countermeasures

BALDWIN, KENNETH M. (CO-CHAIR); WHITE, TIMOTHY P. (CO-CHAIR); ARNAUD, SARA B.; EDGERTON, V. REGGIE; KRAEMER, WILLIAM J.; KRAM, RODGER; RAAB-CULLEN, DIANE; SNOW, CHRISTINE M.

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Author Information

Department of Physiology and Biophysics, University of California, Irvine, CA; College of Health and Human Performance, Oregon State University, Corvallis, OR; NASA-Ames Research Center, Moffett Field, CA; Department of Physiological Science, University of California, Los Angeles, CA; Center for Sports Medicine, Pennsylvania State University, University Park, PA; Department of Human Biodynamics, University of California, Berkeley, CA; Department of Medicine, Creighton University, Omaha, NE; Department of Exercise and Sport Science, Oregon State University, Corvallis, OR

Submitted for publication February 1996.

Accepted for publication April 1996.

Address for correspondence: Timothy P. White, Office of the Dean, College of Health and Human Performance, 123 WB, Oregon State University, Corvallis, OR 97331-6802.

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Abstract

A Research Roundtable, organized by the American College of Sports Medicine with sponsorship from the National Aeronautics and Space Administration, met in November 1995 to define research strategies for effective exercise countermeasures to weightlessness. Exercise was considered both independently of, and in conjunction with, other therapeutic modalities (e.g., pharmacological, nutritional, hormonal, and growth-related factors) that could prevent or minimize the structural and functional deficits involving skeletal muscle and bone in response to chronic exposure to weightlessness, as well as return to Earth baseline function if a degree of loss is inevitable. Musculoskeletal deficits and countermeasures are described with respect to: 1) muscle and connective tissue atrophy and localized bone loss, 2) reductions in motor performance, 3) potential proneness to injury of hard and soft tissues, and 4) probable interaction between muscle atrophy and cardiovascular alterations that contribute to the postural hypotension observed immediately upon return from space flight. In spite of a variety of countermeasure protocols utilized previously involving largely endurance types of exercise, there is presently no activity-specific countermeasure(s) that adequately prevent or reduce musculoskeletal deficiencies. It seems apparent that countermeasure exercises that have a greater resistance element, as compared to endurance activities, may prove beneficial to the musculoskeletal system. Many questions remain for scientific investigation to identify efficacious countermeasure protocols, which will be imperative with the emerging era of long-term space flight.

For several decades both human beings and laboratory animals have been exposed to the environment of weightlessness associated with space flight. During this time, a large body of evidence has been gathered to clearly show that exposure to such an environment of varying duration-days to weeks to months-results in structural and functional deficits in the musculoskeletal system.

These deficits could affect muscular function during space flight, particularly in activities requiring high precision and muscular force-such as is the case during extravehicular activity. However, the decrements become more significantly expressed as astronauts return to a partial-G or 1 G environment. These deficits could have catastrophic consequences, for example if the need arose for emergency egress upon return to a 1 G environment. The deficits also affect motor abilities requiring even modest amounts of strength, endurance, and coordination, such as required for locomotion. If the deficits in bone mass and strength are not restored after return to 1 G, then they may also have long-range consequences by increasing the risk of fracture with aging.

A Research Roundtable was organized by the American College of Sports Medicine (ACSM) with sponsorship from the National Aeronautics and Space Administration (NASA). The Roundtable met at the National Center of ACSM on November 7 and 8, 1995. The goal of this Roundtable was to define research strategies for exercise, both independently of and in conjunction with other therapeutic modalities (e.g., pharmacological, nutritional, hormonal, and growth-related factors) that could prevent or minimize the structural and functional deficits involving the skeletal muscle and bone in response to chronic exposure to weightlessness, as well as return to Earth baseline function if some degree of loss is inevitable.

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BACKGROUND

The driving force behind a Roundtable specifically focusing on the integrative theme of weightlessness, exercise, and the musculoskeletal system stems from an evolving data base derived from both biological and biomedical ground-based and space-related research. These data strongly suggest that, in spite of a variety of countermeasure protocols being utilized that involve largely aerobic types of exercise (in which exercise is performed with a bias to many muscular contractions against relatively low loads), there is presently no activity-specific countermeasure that adequately prevents or reduces identified deficiencies in the musculoskeletal system.

The musculoskeletal deficits include, but are not limited to, the following: 1) muscle and connective tissue atrophy and localized bone loss, 2) reductions in motor performance, 3) potential proneness to injury involving both hard and soft tissues, and 4) probable interaction between muscle atrophy processes and cardiovascular alterations that collectively contribute to the postural hypotension observed upon immediate return from space flight.

Because NASA is entering into a new era of long-term space flight, the deficits in musculoskeletal structure and function, which were tolerable to some degree with shorter flights, become intolerable with flights that extend to months or years. It seems apparent that countermeasure exercises that have a greater resistance element, when compared to endurance activities, may prove beneficial to the structure and function of skeletal muscle and bone.

The Roundtable was structured to involve leading researchers in the related fields of muscle and bone biology, biomechanics, exercise physiology, and clinical medicine. These individuals reviewed and discussed currently available information on what is known and unknown concerning musculoskeletal plasticity and function in response to interventions such as: 1) different types of physical activity of varying intensity, duration, and frequency; 2) exposure to space flight of varying duration; and 3) ground-based models designed to simulate weightlessness such as immobilization, water immersion, bed rest, and limb suspension. The review of information included analyses of both human and animal models.

As a result of these deliberations, the Roundtable participants identified a number of key observations that were coupled to a series of recommendations, both general and specific. The recommendations are intended to guide future research on musculoskeletal structure and function in the context of states of unloading, and for the development of effective countermeasures. These recommendations are aimed at both basic and directed research involving both humans and research animals, with the ultimate objective of preserving the functional integrity of not only the musculoskeletal system, but other physiological systems also heavily impacted by chronic exposure to states of weightlessness.

Moreover, the Roundtable participants were cognizant of the fact that information gained from such a research focus would have a tremendous impact on aging and a variety of health problems associated with physical inactivity, debilitating diseases and injury, and rehabilitation.

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OBSERVATIONS AND RECOMMENDATIONS

I. Overview of Issues Concerning Future Research Directions
I-A. Observations:

1. Based on the data analyzed by the Roundtable participants, it is apparent that exercise protocols of the endurance type (i.e., cycling, simulated running, and rowing) that are currently used in space flight missions of varying duration to counteract a variety of cardiovascular deficits (and likely other systems as well), are insufficient for the musculoskeletal system and do not fully maintain normal motor control of posture and locomotion, muscle and bone mass, and regulatory processes that prevent postural hypotension. These deficits both individually and collectively could potentially impair the performance of a variety of tasks carried out during space flight (e.g., extravehicular activity) and upon landing in either 1 G or partial-G environments.

2. Available information further suggests that a single uniform exercise protocol is likely to be insufficient to fully maintain the structural and functional integrity of those systems impacting motor activity, musculoskeletal function, and circulatory homeostasis.

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I-A. Recommendations:

1. A broad-based research plan must evolve with an overall strategy of designing a battery of exercise countermeasures aimed at preserving integrated physiological processes necessary for maintaining total body homeostasis during both space flight and upon return to a partial-G or 1 G environment. While the Roundtable participants focused more specifically on the musculoskeletal system, it recognized the importance of the interactions with other systems as well, e.g., the cardiovascular system and particularly its peripheral vascular control.

2. A minimum of four types of activity paradigms should be developed and configured for the space environment that will likely be experienced on either the shuttle and/or space station. These paradigms are defined herein relative to the desired performance outcomes. a) Routine motor skills (tasks) suitable for maintaining posture and basic locomotor function. Motor control tasks should be designed for both the upper (trunk) and lower body. Preferably this activity paradigm should be developed in conjunction with equipment or devices that could restore partial gravity forces on the body. b) Heavy resistance paradigms, involving isometric, concentric, and eccentric muscular actions, should be designed to optimally load the lower extremity and trunk musculature to maintain a positive protein balance in these muscle groups. c) Activities that generate either a high impact or produce sufficient strain on bone to maintain its structure and mineral density also need to be developed. Where possible, activities that create simultaneous maintenance of the above properties of both bone and muscle should be prioritized. d) An element of aerobic activity should be included in the training regimens with the primary objective of maintaining cardiovascular function and homeostasis, e.g., plasma volume. In all preventive and therapeutic activity paradigms, attention should be paid to the incidence of, and proneness for, injury to soft and hard tissues, and short- and long-term consequences of such injury should be determined.

3. Because time available for the astronaut corps that is dedicated to exercise is such a premium, it is apparent that in order to seek more economical exercise countermeasure strategies, research should be undertaken to explore other interventions (pharmacological, hormonal, and growth factors) that could independently or in conjunction with exercise stimuli maintain musculoskeletal structure and function.

4. Future research should incorporate both basic (mechanistic) and directed research programs that utilize both animal and human models in addition to the experimental resources that will be available on the space station. Experiments should be designed around acceptable models of unloading, such as bed rest and unilateral lower extremity suspension for humans and the hind limb suspension model for animals (rodents).

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II. Observations and Recommendations on Neuromotor Control
II-A. Observation:

The ability to accurately control movement in changing gravitational environments reflects a remarkable ability to rapidly change the adaptive strategies of the neural control system. Furthermore, prolonged exposure to a new gravitational environment results in a range of continuing adaptations of the neuromotor system. These adaptations encompass a long list of well-documented physiological, biochemical, and morphological changes in muscle, connective, and neural tissues, as well as in highly integrative functions such as posture, locomotion, and the control of fine movement.

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II-A. Recommendations:

1. Define the adaptations of the motor output strategies of movements requiring flexion and extension of joints of the upper limbs, lower limbs, and trunk and neck in varying gravitational environments.

2. Characterize the sequences of adaptations specific for the control of movement that occur from early to prolonged exposure to 0 G.

3. Define the physiological, biochemical, and molecular events in neural, muscular, and connective tissues, which underlie the adaptive strategies to varying gravitational environments.

4. Define the altered neuromotor control strategies that can be attributed to the changing output properties of skeletal muscle and connective tissues vs the neural control systems.

5. Define the peripheral sensory systems involved in movement control that are altered by varying gravitational environments.

6. Determine to what extent an altered peripheral sensory system can be attributed to changes in afferent receptors and spinal and supraspinal processing of afferent information.

7. Ascertain to what extent altered neural control strategies in varying gravitational environments can be attributed to the output (efferent) properties of the neural control system.

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III. Observations and Recommendations on Muscle Resistance Training
III-A. Observation:

A combination of isometric (i.e., muscle length essentially fixed during contraction), concentric (i.e., muscle shortening during contraction), and eccentric (i.e., muscle lengthening during contraction) repetitions during resistance training appears to optimally enhance muscle strength and hypertrophy.

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III-A. Recommendations:

1. Determine the optimal combination of isometric, eccentric, and concentric contractions that will prevent or attenuate muscle atrophy in weightless environments, and will best maintain neuromuscular function in weightless environments and upon return to partial-G or 1 G forces. Components of this research shall be focused on defining the mechanisms through which the stretch-shortening cycle of muscle could induce neuromuscular adaptations, and determine how the intrinsic properties of muscle fibers and connective tissue adapt as a function of time and intensity.

2. Characterize motor unit recruitment relative to movement specificity during exercise in normal gravity and the time course of change upon exposure to 0 G, and upon return to partial-G and 1 G.

3. Determine to what extent training of various types prior to exposure to 0 G might prevent, minimize, or even enhance deleterious changes occuring with exposure to 0 G, and/or enhance the effect of training during 0 G on preventing or minimizing the degree of muscle atrophy.

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III-B. Observation:

The neuroendocrine response to training is specific to the type of exercise performed.

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III-B. Recommendations:

1. Determine the interaction over time of autocrine, paracrine, and endocrine responses to resistance and other forms of exercise in the context of changes in the intrinsic properties of muscle structure and function. Determine these relationships in 0 and 1 G environments.

2. Ascertain the impact of age and gender on the neuroendocrine response to different exercise training protocols.

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III-C. Observation:

The time course of improvements in the force production capabilities of muscle in response to resistance training that can be attributed to neural control components and muscle output potential differ substantially.

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III-C. Recommendations:

1. Determine the relative contributions and time course of neural and muscle output mechanisms, which determine the force production potential and which occur under experimental conditions resulting in atrophic responses, and the interaction with resistance exercise. Determine the influences of gender and age on the adaptive responses.

2. Determine the neural, endocrine, and muscle-related mechanisms that mediate the maintenance of the forcegenerating potential when the musculoskeletal system is unloaded, as during bed rest, limb suspension, and space flight. These studies should be performed in the context of recommendations outlined above for isometric/concentric/eccentric training programs.

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IV. Observations and Recommendations on Postural Hypotension
IV-A. Observation:

A majority of individuals returning to 1 G from exposure to 0 G experience postural hypotension while assuming an upright posture. This problem appears to be manifest in altered reflex activity involving sympathetic nervous system responses targeting the peripheral resistance vessels supplying skeletal muscle. Based on research that links the mechanical activity of skeletal muscle to the reflex control of sympathetic activity, there is mounting evidence to suggest that deficiencies in skeletal muscle function contribute to the postural hypotension occurring following space flight. Adaptations involving skeletal muscle may also be linked to the inability to maintain adequate circulating blood volumes.

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IV-A. Recommendations:

1. Ascertain to what extent reductions in skeletal motor activity, and specifically the role of muscle atrophy, contribute to the alterations in blood pressure regulation associated with microgravity exposure to 0 G and return to partial-G and 1 G. A determination of how skeletal muscle regulates extracellular fluid volume and distribution, vascular capacitance, and total vascular conductance should be included in this research.

2. Determine whether resistance training ameliorates orthostatic intolerance and whether this training modality affects plasma volume. Identify the underlying mechanisms impacting this adaptive process.

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V. Observations and Recommendations on Muscle Injury and Repair
V-A. Observations:

1. Skeletal muscle fiber degeneration and subsequent regeneration occur after damage to fibers induced by a variety of insults, including mechanical and chemical trauma, ischemia, and exposure to extreme heat and cold. Focal areas of degeneration-regeneration in skeletal muscle can result from bouts of seemingly modest exercise following chronic unloading (i.e., muscle weightlessness), as well as excessive stretch and specific types and duration of exercise (particularly those with a bias toward lengthening contractions).

2. When muscle is unloaded during regenerative repair following injury, significant impairments in regenerative growth occur.

3. The adaptation of skeletal muscle to 0 G results in structural atrophy and functional impairments. Effective preventive countermeasures should prevent or attenuate the atrophy, while not inducing injury to hard and soft tissues. Effective therapeutic exercises upon return to partial-G or 1 G should likewise return control structure and function without inducing injury. Prior resistance exercise appears to have some degree of prophylactic value in subsequent susceptibility to injury.

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V-A. Recommendations:

1. Identify characteristics of a threshold exercise dose that results in a response characterized by injury and/or failure in normal muscle and muscle atrophied by short-and long-term unloading. The exercise dose should be quantified with respect to force-velocity factors, duration, work-rest relationships, and the duty cycles during the work phases. The degree of injury should be quantified with respect to function, morphology, and identification of the contractile, regulatory, and structural proteins involved.

2. The implications of injury and impaired recovery for contractile properties in vitro and in vivo should be determined, including force, velocity, power, endurance and accuracy, particularly upon return to partial-G or 1 G environments.

3. Determine to what extent muscle injury occurs during space flight of short and long duration, and particularly upon return to partial-G or 1 G environments, in humans involved in routine activities and extravehicular activities.

4. Determine whether there is a limit to the duration of impaired regeneration by unloading on subsequent successful regeneration when loading is reintroduced.

5. Determine the optimal therapeutic activity patterns to restore normal structure and function following short-and long-term unloading. The activity patterns should be quantified with respect to force-velocity factors, duration, and to work-rest duty cycles.

6. Determine the pharmacological, growth factor, and therapeutic treatments that enhance the regenerative recovery following injury. Identify molecular and cellular mechanisms by which these putative ergogenic interventions work.

7. Determine the influence of age, gender, and nutritional status on susceptibility to injury, degree of recovery, and efficacy of therapeutic exercises.

8. Ascertain the relationship among mechanical, paracrine, auotocrine, endocrine, and neural factors in initiating injury, subsequent regenerative repair, and therapeutic exercise in 0 G, partial-G, and 1 G.

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VI. Observations and Recommendations on Bone
VI-A. Observation:

When the skeleton is unloaded as in space flight, bone mass is lost in weight-bearing bones. This bone loss is more localized than originally predicted and shows individual variation, ranging from none to 10.1% of preflight values in the spine, 1.3-11.4% in the femoral neck, and 0.4-9.5% in the tibia bone of cosmonauts after long-duration flights. The bone loss associated with microgravity can be accelerated by age-related bone loss and changes in reproductive hormone levels, and there is no evidence that the bone loss is recoverable. Potential consequences of significant bone loss include fractures on reentry-particularly in a situation of emergency egress-and accelerated osteoporosis

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VI-A. Recommendations:

1. Determine site-specific rates and magnitudes of bone loss at 0 G and differences according to gender, age, endocrine, and nutritional status.

2. Determine whether individual variations in rates of bone loss are dependent upon factors-such as gender, age, hormonal status, preflight bone status-that could be used to identify individuals at risk for excessive bone loss at 0 G and consequent risk for fracture.

3. Assess the efficacy of preflight training protocols to mitigate skeletal loss during space flight. For example, determine if bone mass values that are substantially above the mean prior to liftoff may allow the astronaut to withstand bone loss and not be at risk for fractures. These protocols should be developed in a gender-specific manner.

4. Establish time course and degree of bone restoration upon return to 1 G and determine its relationship to flight duration, exercise done in space, age, and gender.

5. Relate density variations to typical loading patterns to assess fracture risk prior to, during, and postflight.

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VI-B. Observation:

The endocrine system has profound effects on bone metabolism, and there is evidence that space travel alters hormone secretion. Low levels of reproductive hormones (i.e., estrogen and testosterone) and high levels of corticosteroids result in bone loss, whereas increased levels of insulin-like growth factors are associated with higher bone and lean mass.

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VI-B. Recommendations:

1. Define the endocrine profile in long duration space flight for men and women. Identify these changes as central or peripheral processes.

2. Investigate the interaction between reproductive hormones and reduced mechanical forces on bone loss in 0 G.

3. Determine the effect of weight-bearing exercise, which promotes muscle strength and power development, on insulin-like growth factors and bone mass. Evaluate the responses according to gender.

4. Evaluate the efficacy of anti-resorptive agents (e.g., bisphosphonates) on reduction in loading-related, hormonal, and age-related bone loss in space according to gender.

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VI-C. Observation:

The structural capacity of whole bones depend on bone geometry(cross-sectional area and moments of inertia) and material properties(strength and modulus) of both cortical and trabecular bone. While age-related and hypogravitational changes in the material properties of diaphyseal cortical bone appear to be compensated for by geometric increases in moment of inertia, material properties of trabecular bone follow strong, power law functions of density. Trabecular density in turn is strongly associated with measures of trabecular morphology such as average trabecular width, spacing, and connectivity. Issues of bone “quality” that may be related to weightlessness are now focusing on mineralization, collagen content, and damage accumulation, and there is some evidence that these factors may be influenced by space flight.

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VI-C. Recommendations:

1. Develop noninvasive techniques to estimate trabecular bone strength; for example using peripheral quantitative computed tomography (pQCT), dual energy x-ray absorptiometry (DEXA), ultrasound, and mechanical response tissue analyzer (MRTA) technologies.

2. Use these techniques to track the strength of bone systematically from preflight, in-flight, postflight, and long-term recovery upon return to normal weight bearing.

3. Determine differences in morphology and material properties of bones remodeled in space compared with those remodeled on Earth.

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VI-D. Observation:

The current exercise modalities typically used during space flight are inadequate to maintain bone mass. Weight-bearing activities performed at 1 G, which incorporate impact loading and which increase muscle mass, power, and strength (e.g., gymnastics, wrestling), also increase bone mass. In 1 G environments, running or hopping in place provide substantially higher impact loads (and thus bone strain) than do activities such as cycling, walking, or resistance training exercises. In external loading animal models, thresholds for bone maintenance and increase have been shown for loading variables such as strain magnitude, strain rate, frequency (Hz), strain distribution, and number of loading repetitions.

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VI-D. Recommendations:

1. Characterize actual bone strains at clinically relevant sites in humans during specific movement patterns (including cycling, treadmill walking and running, jumping in place, and resistance training exercises) and determine the relationship of strain to age, size, and gender.

2. Determine mechanical loading thresholds for bone mass maintenance in adults and determine whether these protocols are specific to age, bone size, or gender.

3. Determine exercise prescriptions and other mechanical interventions that are sufficient to maintain bone mass during weightlessness and determine whether these protocols are specific to age, bone size, or gender.

4. Determine the molecular and cellular signals associated with bone loss due to decreased loading as observed in disuse and weightlessness, and determine how these signals compare with signals for bone hypertrophy.

5. Determine to what extent the bone loss that occurs during 0 G exposure is due to the lack of mechanical load and to what extent systemic change (e.g., fluid shifts, hormone expression) can modulate the response to unloading.

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VI-E. Observation:

Nutrition is important for bone health, independent of its influence on body weight. Specific nutrients, such as calcium and phosphorus, are essential components of bone crystals. In addition, there are other nutrients-such as vitamin D, magnesium, and protein-that are known to impact bone mass.

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VI-E. Recommendations:

1. Define the protein, mineral, and energy requirements for bone maintenance.

2. Determine to what extent astronauts in space have adequate energy, vitamin, and mineral intake and absorption, and to what extent exercise regimens alter these needs and intakes.

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VI-F. Observations:

1. Experimental models for the musculoskeletal system are classically human adults who volunteer for bed rest of varying periods of time, and for upright models in which some muscles of one leg are unloaded. These models appear to be valid for space flight, but direct comparisons of many measurements from ground-based studies with those made during space flight are lacking.

2. Small animal models currently in use for space flight experiments have generated a great deal of information on responses to 0 G and bone-muscle unloading. However, little information has been obtained on mature animal models.

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VI-F. Recommendations:

1. Make direct comparisons of measurements from ground-based studies with those made during space flight.

2. Compare the responses to unloading in mature animals to those of younger animals of the same species in both ground based and in-flight experiments. Incorporate the differences in maturity for bone and muscle into experimental design (i.e., 95% of the skeleton in the male rat is acquired by 6 months of age, yet muscle experiments typically consider 4-month-old rats to be mature).

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SUMMARY AND CONCLUSIONS

Research aimed at understanding the adaptive processes of human beings in response to the environment of weightlessness is both complex and difficult to perform. This is due to the inherent problems associated with using humans as research subjects, because they must adhere to a variety of operational medical procedures and perform a wide variety of duties during a given mission. These factors often ultimately compromise the variables being investigated, thus making the interpretation of the experiments difficult. Furthermore, the availability of the microgravity environment of space travel often precludes an ideal experimental design, particularly in controlling the important variable of duration and transient high G forces on ascent and descent.

Therefore, it is essential that future research focus both on human and animal subjects that can be configured into ground-based models simulating chronic states of weightlessness in order to examine both the mechanistic and applied components of the scientific issues raised in this report.

It seems highly unlikely that a single exercise paradigm will evolve that effectively ameliorates the important structural and functional deficits occurring in bone, muscle, and connective tissue identified in this report. Thus, it is imperative that a systematic and highly integrated research strategy evolve to ensure the likelihood that a multifaceted exercise prescription is established to maintain the functional integrity of the various components of the musculoskeletal system when they are challenged by the debilitating environment of weightlessness.

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SKELETAL MUSCLE ATROPHY; LOCALIZED BONE LOSS; HUMAN; RAT; RESISTANCE TRAINING; EXERCISE; MUSCLE ADAPTATIONS; BONE ADAPTATIONS; BONE MINERAL DENSITY; HYPOTENSION; ORTHOSTATIC INTOLERANCE

©1996The American College of Sports Medicine

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