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Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents a
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Kathleen F. Janz , David Q. Thomas , M. Allison Ford & Skip M. Williams a
University of Iowa
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Illinois State University
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University of Mississippi Published online: 09 Feb 2015.
Click for updates To cite this article: Kathleen F. Janz, David Q. Thomas, M. Allison Ford & Skip M. Williams (2015) Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents, Research Quarterly for Exercise and Sport, 86:1, 5-12, DOI: 10.1080/02701367.2014.995019 To link to this article: http://dx.doi.org/10.1080/02701367.2014.995019
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Research Quarterly for Exercise and Sport, 86, 5–12, 2015 Copyright q SHAPE America ISSN 0270-1367 print/ISSN 2168-3824 online DOI: 10.1080/02701367.2014.995019
SPECIAL TOPICS: Top 10 Research Questions
Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents Downloaded by [Michigan State University] at 04:05 24 February 2015
Kathleen F. Janz University of Iowa
David Q. Thomas Illinois State University
M. Allison Ford University of Mississippi
Skip M. Williams Illinois State University
Evidence strongly supports a positive, causal effect of physical activity on bone strength and suggests long-term benefits of childhood physical activity to the prevention of osteoporosis. The contribution of healthy bone development in youth is likely to be as important to fracture prevention as the amount of late adulthood bone loss. Families, schools (particularly physical education), and communities are key settings for health promotion focused on boneenhancing physical activity. However, little research has explored the topic of health promotion and physical education as they pertain to bone health, so best practices are not known. Based on our understanding of the literature, we present the top 10 research questions in health promotion and physical education that should be answered to advance boneenhancing physical activity in children and adolescents. Keywords: childhood, exercise, mechanical (impulsive) loading, skeletal health
About 30% to 50% of women and 15% to 20% of men at age 50 years will sustain an osteoporotic fracture in their remaining lifetime (U.S. Department of Health and Human Services [USDHHS], 2004). This accumulative incidence rate is higher than that of breast cancer in women and prostate cancer in men. Osteoporotic fractures, particularly of the hip, spine, and wrist, have significant health consequences including chronic pain, loss of function, loss of independence, and early mortality (Burge et al., 2007; Magaziner et al., 1997). In 2010, there were 258,000 hip fractures and the rate for women was almost twice the rate for men (Centers for Disease Control and Prevention Correspondence should be addressed to Kathleen F. Janz, Department of Health and Human Physiology, University of Iowa, 130 Field House, Iowa City, IA 52242. E-mail: [email protected]
[CDC], 2013). Women, who sustain an osteoporotic hip fracture have a mortality rate that is 10% to 24% greater than that of their peers (Magaziner et al., 1997). Hip fractures are also among the most expensive conditions addressed in U.S. hospitals with an aggregated inpatient cost of $4.9 billion (Torio & Andrews, 2013). These health statistics convey the morbidity, mortality, and economic burden of bone disease during late adulthood; however, extrapolations from epidemiological studies suggest that a relatively small increase in bone strength during childhood could significantly reduce osteoporotic fracture risk later in life (Heaney et al., 2000). Furthermore, statistical projections indicate that the amount of peak bone mass achieved during adolescence and young adulthood is a strong predictor of osteoporosis risk in later life (Hernandez, Beaupre, & Carter, 2003). For example, Clark and
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colleagues have estimated an 89% increase in adult fracture risk per standard deviation decrease in bone mass during childhood (Clark, Ness, Bishop, & Tobias, 2006). The contribution of healthy bone development in youth is likely to be as important to fracture prevention as the amount of late adulthood bone loss (Baptista & Janz, 2012). There is apparently much to be gained by beginning osteoporosis prevention early and continuing with a lifetime of bone health strategies. Of all the lifestyle strategies for increasing bone strength during the growing years, physical activity is one of the most (if not the most) efficacious (Heaney et al., 2000). However, more than 50% of children aged 6 years to 11 years old and more than 90% of youngsters aged 12 years to 19 years old are not active enough to optimize the health benefits of physical activity (Troiano et al., 2008). It is particularly troubling that physical activity levels decline precipitously during adolescence because it is during this stage of growth that bone is accruing most rapidly and is most sensitive to the osteogenic effects of physical activity (Baptista & Janz, 2012). Specifically during the growing years, the outer surface of bone (periosteum) is covered with a greater proportion of active osteoblasts that initiate bone formation when stimulated mechanically by muscle forces and impact forces, which primarily occur during physical activity, linear growth, and weight gain. Whole bone becomes stronger with the addition of more bone (increased mass) and through expansion of the bone’s periosteal circumference (change in structure; Daly, 2007). These responses to mechanical loads are primarily local crosssectional changes (Daly, 2007). Adding more crosssectional mass predominantly improves the strength of bone when it is being compressed (e.g., falling straight onto the wrist), whereas changing the structure of bone improves its bending and torsional strength. Hip fractures are usually caused by sideway falls and the impact creates bending and compression of the proximal femur (Kaptoge et al., 2008). Physical activities that are dynamic and odd in nature, high in magnitude and rate, and short in duration are the most effective in increasing bone mass and changing its structure (Gunter, Almstedt, & Janz, 2012). Examples of these activities include jumping, hopping, and tumbling. Because of its importance in osteoporosis prevention (USDHHS, 2004), bone-strengthening physical activity has been included in the U.S. Physical Activity Guidelines for Americans, with the recommendation that children and adolescents include these activities as part of their 60 min of daily physical activity on at least 3 days per week (USDHHS, 2008). For the last two decades, research in physical activity and bone health in children and adolescents has focused on establishing the causal effect of physical activity on bone strength. Much of this research has recently been reviewed in narratives (Tan et al., 2014), systematic reviews (Hind & Burrows, 2007; Nogueira, Weeks, & Beck, 2014), and metaanalyses (Behringer, Gruetzner, McCourt, & Mester, 2014;
Ishikawa, Kim, Kang, & Morgan, 2013; Nogueira et al., 2014). Taken in total, the evidence strongly supports a positive, causal effect of physical activity on bone strength and suggests long-term benefits of childhood physical activity to the prevention of osteoporosis. Nevertheless, significant work remains to fully understand dose-repose relationships between physical activity and bone health. However, given the current evidence for physical activity’s positive effect on bone, declining rates of physical activity during early adolescence, and the considerable additional benefits of a physically active lifestyle, there is no reason to not act on what we already know to help children and adolescents optimize bone health via physical activity. In fact, it is surprising that so little has been done to better understand the determinants of bone-enhancing physical activity or to test novel strategies to implement successful bone health programs in the home, school, and community. Based on our understanding of the current literature, we present the top 10 research questions that should be answered to advance bone-enhancing physical activity in children and adolescents with an eye toward primary prevention of osteoporotic fractures via health promotion and physical education.
TOP 10 RESEARCH QUESTIONS 1. What Exactly Is the Best Bone-Enhancing Physical Activity Recommendation for Children and Adolescents? Current federal health recommendations recommend boneenhancing physical activities for children and adolescents 3 days per week as part of a 60-min–per-day physical activity recommendation (USDHHS, 2008). The exact duration and mechanical load of bone-enhancing physical activity is not described because, honestly, this information is unknown. Based on a review of successful randomized controlled studies, Gunter, Almstedt, Baptista, and Janz (2011) suggested an exercise prescription for bone health with an impact magnitude of 3.5 times body weight, 100 loads per session (approximately 10 min to 15 min), 3 days per week, for at least 7 months. However, there is great overlap in the dose of exercise in successful and unsuccessful randomized controlled trials (Anliker, Dick, Rawer, & Toigo, 2012; Greene, Wiebe, & Naughton, 2009; MacDonald et al., 2008; Petit et al., 2002). Clearly more work is needed to define magnitude, time, and frequency. However, to date, all successful randomized controlled trials testing exercise as a causal factor for bone strength have used jumping as the primary physical activity. This gross motor skill mechanically loads the clinically important site of the hip via muscle loading during takeoff and via impact loading during landing. Jumping imposes a greater anabolic stimulus on bone than commonly prescribed metabolic-loading activities of walking or running (Fuchs,
PHYSICAL ACTIVITY AND BONE HEALTH RESEARCH
Bauer, & Snow, 2001). Current national priorities for increasing physical activity levels in youth are focused on metabolic health, particularly in relation to combating childhood obesity instead of holistic lifetime health and fitness. Studies are needed to more precisely identify the best osteogenic exercise dose and an exercise dose that encompasses both metabolic and skeletal health priorities.
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2. How and Why Does the Dose Response of Physical Activity to Bone Mass and Structure Vary Between Children and Adolescents? Mechanical loads placed on bone via physical activity create deformation (strains) of whole bone (Forwood & Turner, 1995; Turner, Forwood, Rho, & Yoshikawa, 1994). These strains activate mechanosensitive cells that in turn activate osteoblasts (bone-building cells) and osteoclasts (bone-resorbing cells). Adaptation occurs in response to changes in physical activity (as well as other mechanical loads) that surpasses a threshold regulated by the habitual strain loading. Inactive children may respond to low-impact loading and improve bone mass or structure, while others will need a higher mechanical load to promote a skeletal response (Turner & Robling, 2003). In addition to habitual physical activity, the threshold appears to vary between individuals (and also bone sites) according to maturity, sex, and perhaps race/ethnicity. Peripubertal children show more dramatic effects due to exercise interventions than do latepubertal and postpubertal adolescents. Several studies suggest that even the timing of maturation may affect bone accretion, particularly in girls; specifically, girls who mature early are more likely to enter adulthood with greater bone mass than are late-maturing girls (Bass et al., 1998; Behringer et al., 2014; Gilsanz, Roe, Mora, Costin, & Goodman, 1991). Physical activity-induced increases in periosteal circumference and cortical area continue across and perhaps after puberty in boys, whereas physical activity seems to cause reduced endosteal circumference and cortical bone mineral density in peripubertal and postpubertal girls (Leonard et al., 2010). Sparse research has been done in African American, Asian American, and Latino youth, and the effect of race and ethnicity as a moderating factor is almost unexplored, though it is expected to be significant. A better understanding of the variation in response to similar mechanical-loading conditions by children and adolescents will advance our ability to develop personalized prescriptions and set realistic goals for exercise training. 3. How Should Physical Activity and Bone Strength Dose-Response Relationships Be Measured? To more precisely understand how bone adapts to mechanical loading, measurement methods must capture physical activity dimensions (intensity, frequency, time) as
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well as the mass and structure of whole bone. In intervention studies, the physical activity dimension of intensity can be objectively measured with force plates to provide acceleration (m/s2) and power output (Watts; Fuchs et al., 2001; Ja¨msa¨, Ahola, & Korpelainen, 2011). Frequency and time are measured via observation. Quantifying physical activity dose in school- and community-based settings is more challenging. However, newer accelerometers directly provide acceleration gravitational units (m/s2), which may provide a relevant index of mechanical intensity. An additional accelerometer parameter, jerk or change in acceleration (g/s), has recently been shown to improve the prediction of physical activity dose as related to bone outcomes (Ja¨msa¨ et al., 2011). Because bone can adapt to short bouts of mechanical loading if the load is of high intensity (Turner et al., 1994), the time-stamped feature of accelerometers is important. Finally, accelerometers worn at the waist are sensitive to the clinically significant skeletal site of the hip (Gunter et al., 2012). Until the last decade, dual-energy X-ray absorptiometry (DXA) was almost entirely used to quantify bone outcomes. This two-dimensional imaging technology measures the attenuation of X-ray beams as they pass through tissues of varying density and sorts the body into three tissue compartments—muscle, fat, and bone. Software algorithms are then used to estimate areal bone mineral density (aBMD; g/cm2) and bone mineral content (BMC; g). Because DXA is fast, involves low radiation exposure (, 1 mrem per scan), and is widely available, it continues to be commonly used in pediatric research (Adams, Engelke, Zemel, & Ward, 2014; Gunter et al., 2012). When paired with algorithms, DXA measures can be used to estimate the structure of the proximal femur and, as such, can provide a more complete index of bone strength. However, because DXA does not measure depth of bone, it systematically overestimates density for children larger in size (when compared with their peers; Adams et al., 2014). A relatively new advancement in bone imaging, peripheral quantitative computed tomography (pQCT), provides three-dimensional imaging at distal bone locations such as the lower arm and lower leg. This technique also uses the attenuation of X-rays (, 10 mrem per scan; Gunter et al., 2012). In addition to providing a true measure of volumetric density (g/cm3), pQCT can separate cortical bone from trabecular bone and can provide measures of structural strength in compression, bending, and torsion (i.e., bone strength index, section modulus, and stress-strain index, respectively). Recently, high-resolution pQCT scanners have become available for use in clinical research. The resolution with these scanners can be used to measure additional bone strength features including cortical porosity and trabecular plate and rod microstructures (Adams et al., 2014). Of critical importance to dose-response studies is the measure of muscle crosssectional area (MCSA; cm2) and lean body mass (kg) because muscle is a strong and consistent predictor of bone
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strength (Lorbergs, Farthing, Baxter-Jones, & Kontulainen, 2011; MacDonald et al., 2008; Schoenau, Neu, Beck, Manz, & Rauch, 2002). Muscle also mediates the relationship between physical activity and bone strength. More consistent use of objective measurement systems for physical activity (force plates, accelerometers) and measurement systems for multiple outcomes including muscle will advance our understanding of the dose of physical activity needed to improve bone strength. Physical activity measures should capture mechanical loading (intensity, frequency, time), and bone-imaging measures should capture mass, structure, and surrounding muscle. 4. What Is the Interaction Between Physical Activity and Diet on Bone Health? Bone mineral tissue is composed of hydroxyapatite, a calcium-phosphate compound with magnesium and trace amounts of other minerals. Of the nutrients necessary for healthy bone development, calcium is one of the most important micronutrients, and it is the nutrient most likely to be insufficient during childhood and especially adolescence when milk consumption is typically replaced by soft drinks. Milk and other dairy products provide most of the calcium and vitamin D in the diet of U.S. children and adolescents (Krebs-Smith, Guenther, Subar, Kirkpatrick, & Dodd, 2010). Dairy products also provide protein and macronutrients important to bone metabolism including magnesium and potassium. However, approximately 66% of adolescent boys and 80% of adolescent girls do not meet the recommended intake of milk (Krebs-Smith et al., 2010). Though limited in number, most of the randomized controlled trials that have examined the effect of calcium and exercise combined report a significantly greater effect on bone mass, density, and structure compared with the intervention arm of calcium or exercise alone (Bass et al., 2007; Courteix, Jaffre´, Lespessailles, & Benhamou, 2005; Iuliano-Burns, Saxon, Naughton, Gibbons, & Bass, 2003; Specker & Binkley, 2003). Results suggest that the full effects of physical activity are realized only with a calciumrich diet. At this time, more work is needed to quantify the interaction between physical activity and calcium intake as well as the possible interaction between physical activity and other nutrients. 5. Are the Effects of Physical Activity on Bone Sustained From Childhood Through Adulthood to Old Age? Results from animal studies indicate that early exerciseinduced changes to bone strength persist through maturity and significantly reduce fracture risk in older animals (Warden, Fuchs, Castillo, Nelson, & Turner, 2007). The sustained effect of children’s physical activity into adolescence and even young adulthood has been demon-
strated in several observational studies (Baxter-Jones, Kontulainen, Faulkner, & Bailey, 2008; Janz et al., 2010); and at least two randomized controlled trials have shown a persistence of effects 1 year (Binkley & Specker, 2004) and 7 years (Gunter, Baxter-Jones, Mirwald, Almstedt, Fuchs, et al., 2008) postintervention. However, we do not know if bone-enhancing physical activity in children and adolescents is sustained so that it influences bone strength in older adults when fracture risk is greatest. Retrospective observational studies report positive associations between youth physical activity and older-adult bone mineral density (Bass et al., 1998; Nilsson et al., 2014; Tervo, Nordstrom, Neovius, & Nordstrom, 2008). However, these studies are likely to be confounded by present (adult) physical activity and (unknown) bone strength during youth. On the other hand, one prospective observational study, the University of Saskatchewan Pediatric Bone Mineral Accrual Study (Baxter-Jones et al., 2008), revealed positive associations between a self-reported general level of physical activity in youth and bone mineral density in adulthood. Investigators in this study controlled for present physical activity and early bone outcomes. When compared with less active peers, participants who were physically active at ages 8 to 15 years had 8% to 10% more hip BMC than young adults (ages 23– 30 years old; Baxter-Jones et al., 2008). This study suggested the possibility of long-term sustained benefits of childhood physical activity on adult bone health. We do not know what is more important for bone health in older adults—past, present, or persistent physical activity. 6. What Determines if Children and Adolescents Participate in Bone-Enhancing Physical Activity? Although the literature on physical activity determinants in youth is large and increasingly more theoretical and sophisticated, we were unable to identify any research on why children and youth specifically participate in the types of physical activities known to enhance bone health. Many osteogenic gross motor skills (e.g., skipping, hopping, jumping, tumbling) can be classified as play and are engaged in not for their health benefits but purely for enjoyment and for the opportunity to socialize with friends (Fitzgerald, Fitzgerald, & Aherne, 2012; Humbert et al., 2008). For those boys and girls involved in organized or recreational sports, games, and activities that require muscle loading and impact loading (e.g., volleyball, basketball, gymnastics, dance), bone health benefits have not been associated with reasons for participation (McCarthy & Jones, 2007; Schneider & Cooper, 2011; Wallhead & Buckworth, 2004). It is likely that physical education and perhaps public health campaigns (e.g., the CDC’s Best Bones Forever) are the venues that provide youth with overt reasons and specific skill sets to participate in boneenhancing physical activities. To the best of our knowledge, strategies for how to most effectively educate youth about
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bone-enhancing physical activities have not been systematically tested.
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7. What Is the Effect of Traditional Physical Education on Bone Health? Schools are in an ideal setting to influence children’s participation in bone-strengthening physical activity due to the amount of time children spend at school and the physical activity instruction that takes place in schools (American Alliance for Health, Physical Education, Recreation and Dance, 2013). Comprehensive, quality physical education programs should include bone-enhancing curricula tailored for student age and developmental needs (National Association for Sport and Physical Education & American Heart Association, 2012). For example, the goal within elementary school physical education is to teach students the gross motor skills necessary to move and control their bodies in an effective manner. During the learning of skills such as hopping, skipping, and galloping, students are participating in activities that have been shown to improve bone strength (Gunter, Baxter-Jones, Mirwald, Almstedt, Fuchs, et al., 2008). During middle school and high school, curricula shifts from learning basic movement skills to participation in sports and fitness activities. Many of the skills within sports and fitness units (e.g., jumping, running) are excellent for bone health. However, the potential educational link between these muscle-loading and impactloading activities and bone health is (seldom) made and little is known as to how much these specific activities contribute to bone health. In short, research is needed on how intermittent, nontargeted participation in boneenhancing activities during physical education contributes to bone health. 8. How Can Physical Education Instruction Be Altered to Be More Effective in Enhancing Bone Health? Some (Linden, Ahlborg, Besjakov, Gardsell, & Karlsson, 2006; Lofgren, Dencker, Nilsson, & Karlsson, 2012; Valdimarsson, Linden, Johnell, Gardsell, & Karlsson, 2006), though not all (Alwis et al., 2008; Detter et al., 2014), intervention studies where bone-enhancing exercises such as jumping were infused in the physical education curriculum have been successful in improving bone strength (when compared with controls). These exercise trials support the efficacy of using physical education as a means to improve bone heath. What is now needed is an innovative approach to consistently include bone-enhancing activities within the physical education curriculum with the acknowledgement that the curriculum is already filled with other, equally important, objectives. For example, there may be value in incorporating a variety of bone-enhancing physical activities during the warm-up or during waiting periods of physical education lessons. Appropriate osteo-
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genic warm-up activities for middle and high school programs include burpees, squat and jump, jumping jacks, tuck jumps, single-leg hops, single-leg/double-leg lateral ski hops, and rope skipping (Walter, Quint, Fischer, & Kiger, 2011). Small-sided games during sports-based lessons in basketball and volleyball provide bone-enhancing activities and active participation for all. The main lessons in tumbling and gymnastics provide exceptional osteogenic opportunities. In the end, physical education curricula that incorporate multiple motor skills (e.g., soccer, tumbling, tennis) and provide diverse physical activity choices throughout the school year including osteogenic warm-ups are most likely to satisfy physical education priorities and enhance bone strength. Research should test curricular approaches for efficacy and efficiency. 9. How Can Communities Facilitate Youth Participation in Bone-Enhancing Physical Activities? While most children’s bone-related physical activity interventions have occurred in school settings, there is also a need for interventions within the community. Communities provide an excellent setting for intervention programs for several reasons. Programs within communities more easily incorporate parents and other adults (when compared with the school setting). These adults can serve as role models as well as organizers to help ensure the sustained effect of an intervention (Ornelas, Perreira, & Ayala, 2007; Pate et al., 2000). The engagement of parents and community members in bone health programming is important given findings of a study conducted at the University of Michigan C. S. Mott Children’s Hospital (2013). When adults were asked to list the top health concerns for youth in their communities, smoking, drugs, and obesity were cited most often. Bone health was never mentioned even though 30% to 50% of youth will experience a bone fracture prior to adulthood (Mayranpaa, Makitie, & Kallio, 2010). Communities also should provide the recreational space critical for youth physical activity programs. Adolescents report athletic playing fields/courts, indoor recreation facilities, walk/run trails, and parks as their most commonly used recreation sites (Davison & Lawson, 2006; Grafova, 2008). Similarly, children report public parks, playgrounds, and athletic playing fields/courts among their most commonly used recreation sites (Grow et al., 2008). Little work has been done to explore how community programming in these recreational spaces might enhance bone health. However, Gunter and Kasianchuk (2011) showed early pubertal girls realized an increase in BMC after a 9-month community running program. Similarly, a study among adolescent (nonelite) community tennis players revealed higher femoral neck aBMD compared with their age-matched controls (Ermin, Owens, Ford, & Bass, 2012). Running and tennis are lifetime leisure activities and are likely to be more sustainable than
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jumping-based activities. Because community-based physical activity programs augment and support school-based programs (Bryant et al., 2010), bridging community-based with school-based interventions may provide the most effective intervention strategies. Research examining community settings and programs that facilitate boneenhancing physical activity is warranted.
supportive environments to ensure continued physical activity with age. Families, schools (particularly physical education), and communities are key settings for successful bone-related health promotion.
REFERENCES
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10. How Do We Assess and Track Efforts to Promote Bone Health? Finding answers to the nine research questions presented in this article is likely to improve health promotion and physical education efforts to increase bone-enhancing physical activity in youth. However, quantifying success (or identifying failure) will require nonclinical measures of changes in bone mass and structure or at least proxy measures that are strongly associated with osteogenic changes. During physical activity, muscle forces account for the majority of bone strains leading to increases in bone strength (Robling, 2009). The connection between muscle force and bone strength is summarized in Harold Frost’s mechanostat theory (Frost, 1987), indicating that the greater the force on the bone by muscles, the greater the bone adaptation. Muscle power is considered a performancerelated physical fitness attribute, yet it is not assessed in our national health-related fitness testing battery, FITNESSGRAMw (Meredith & Welk, 2010). However, recent research suggests muscle power may prove to be a useful surrogate for bone (Robling, 2009). Although the U.S. Physical Activity Guidelines for Americans (USDHHS, 2008) recommend bone-enhancing physical activities for children and adolescents, surprisingly, these activities are not even tracked in our national Youth Risk Behavior Surveillance System. It is time for research targeting our national assessment of physical fitness and tracking physical activity in youth to examine what is missing when bone health is left out.
CONCLUSIONS Optimal bone health is a key reason for promoting physical activity during the growing years when approximately 40% of bone mass is achieved (Bailey, McKay, Mirwald, Crocker, & Faulkner, 1999). Bone mass and structure appear to track through childhood, adolescence, and (at least) young adulthood (Baxter-Jones et al., 2008), suggesting that improving bone strength early in life may have sustained effects. Intervention strategies for bone health should begin during childhood when bone appears most sensitive to the effects of physical activity. These interventions must be designed to change the factors that keep children and adolescents from engaging in boneenhancing physical activity and must provide skills and
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PHYSICAL ACTIVITY AND BONE HEALTH RESEARCH Centers for Disease Control and Prevention. (2013). Hip fractures among older adults. Retrieved from http://www.cdc.gov/HomeandRecreationalSafety/Falls/adulthipfx.html Clark, E. M., Ness, A. R., Bishop, N. J., & Tobias, J. H. (2006). Association between bone mass and fractures in children: A prospective cohort study. Journal of Bone and Mineral Research, 21, 1489– 1495. Courteix, D., Jaffre´, C., Lespessailles, E., & Benhamou, L. (2005). Cumulative effects of calcium supplementation and physical activity on bone accretion in premenarchal children: A double-blind randomised placebo-controlled trial. International Journal of Sports Medicine, 26, 332–338. Daly, R. (2007). Optimizing bone mass and strength: The role of physical activity and nutrition during growth. In M. A. Petit & R. Daly (Eds.), The effect of exercise on bone mass and structural geometry during growth (pp. 33–49). Basel, Switzerland: Karger. Davison, K. K., & Lawson, C. T. (2006). Do attributes in the physical environment influence children’s physical activity? A review of the literature. International Journal of Behavioral Nutrition & Physical Activity, 3, 19. doi:10.1186/1479-5868-3-19 Detter, F., Rosengren, B. E., Dencker, M., Lorentzon, M., Nilsson, J. A., & Karlsson, M. K. (2014). A 6-year exercise program improves skeletal traits without affecting fracture risk: A prospective controlled study of 2621 children. Journal of Bone and Mineral Research, 29, 1325–1336. Ermin, K., Owens, S., Ford, M. A., & Bass, M. (2012). Bone mineral density of female adolescent tennis players and non-tennis players. Journal of Osteoporosis, 2012, Article ID 423910, 5 pages. doi:10.1155/ 2012/423910 Fitzgerald, A., Fitzgerald, N., & Aherne, C. (2012). Do peers matter? A review of peer and/or friends’ influence on physical activity among American adolescents. Journal of Adolescence, 35, 941 –958. Forwood, M. R., & Turner, C. H. (1995). Skeletal adaptations of mechanical usage: Results from tibial loading studies in rats. Bone, 17(Suppl. 4), 197S–205S. Frost, H. M. (1987). The mechanostat: A proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Mineral, 2, 73– 85. Fuchs, R. K., Bauer, J. J., & Snow, C. M. (2001). Jumping improves hip and lumbar spine bone mass in prepubescent children: A randomized controlled trial. Journal of Bone and Mineral Research, 16, 148– 156. Gilsanz, V., Roe, T. F., Mora, S., Costin, G., & Goodman, W. G. (1991). Changes in vertebral bone density in Black girls and White girls during childhood and puberty. New England Journal of Medicine, 325, 1597–1600. Grafova, I. B. (2008). Overweight children: Assessing the contribution of the built environment. Preventative Medicine, 47, 304 –308. Greene, D. A., Wiebe, P. N., & Naughton, G. A. (2009). Influence of droplanding exercises on bone geometry and biomechanical properties in prepubertal girls: A randomized controlled study. Calcified Tissue International, 85, 94– 103. Grow, H. M., Saelens, B. E., Kerr, J., Durant, N. H., Norman, G. J., & Sallis, J. F. (2008). Where are youth active? Roles of proximity, active transport, and built environment. Medicine & Science in Sports & Exercise, 40, 2071–2079. Gunter, K. B., Almstedt, H. C., Baptista, F., & Janz, K. F. (2011). The importance of physical activity for optimal lifelong bone health. President’s Council on Fitness, Sports & Nutrition Research Digest, 12(4), 1–8. Gunter, K. B., Almstedt, H. C., & Janz, K. F. (2012). Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exercise and Sports Science Reviews, 40, 13 –21. Gunter, K., Baxter-Jones, A. D., Mirwald, R. L., Almstedt, H., Fuchs, R. K., Durski, S., & Snow, C. (2008). Impact exercise increases BMC during growth: An 8-year longitudinal study. Journal of Bone and Mineral Research, 23, 986 –993.
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Gunter, K., Baxter-Jones, A. D., Mirwald, R. L., Almstedt, H., Fuller, A., Durski, S., & Snow, C. (2008). Jump starting skeletal health: A 4-year longitudinal study assessing the effects of jumping on skeletal development in pre and circum pubertal children. Bone, 42, 710 –718. Gunter, K. B., & Kasianchuk, A. (2011). Examining the influence of participation in a community-based running program on skeletal health in growing girls. Osteoporosis International, 22(Suppl. 2), S417–S439. Heaney, R. P., Abrams, S., Dawson-Hughes, B., Looker, A., Marcus, R., Matkovic, V., & Weaver, C. (2000). Peak bone mass. Osteoporosis International, 11, 985 –1009. Hernandez, C. J., Beaupre, G. S., & Carter, D. R. (2003). A theoretical analysis of the relative influences of peak BMD, age related bone loss and menopause on the development of osteoporosis. Osteoporosis International, 14, 843 –847. Hind, K., & Burrows, M. (2007). Weight-bearing exercise and bone mineral accrual in children and adolescents: A review of controlled trials. Bone, 40, 14 –27. Humbert, L. M., Chad, K. E., Bruner, M. W., Spink, K. S., Muhajarine, N., Anderson, K. D., . . . Gryba, C. R. (2008). Using a naturalistic ecological approach to examine the factors influencing youth physical activity across Grades 7 –12. Health Education Behavior, 35, 158–173. Ishikawa, S., Kim, Y., Kang, M., & Morgan, D. W. (2013). Effects of weight-bearing exercise on bone health in girls: A meta-analysis. Sports Medicine, 43, 875–892. Iuliano-Burns, S., Saxon, L., Naughton, G., Gibbons, K., & Bass, S. L. (2003). Regional specificity of exercise and calcium during skeletal growth in girls: A randomized controlled trial. Journal of Bone and Mineral Research, 18, 156–162. Ja¨msa¨, T., Ahola, R., & Korpelainen, R. (2011). Measurement of osteogenic exercise—how to interpret accelerometer data? Frontiers in Physiology, 2, 73. doi:10.3389/fphys.2011.00073 Janz, K. F., Letuchy, E. M., Eichenberger Gilmore, J. M., Burns, T. L., Torner, J. C., Willing, M. C., & Levy, S. M. (2010). Early physical activity provides sustained bone health benefits later in childhood. Medicine & Science in Sports & Exercise, 42, 1072–1078. Kaptoge, S., Beck, T. J., Reeve, J., Stone, K. L., Hillier, T. A., Cauley, J. A., & Cummings, S. R. (2008). Prediction of incident hip fracture risk by femur geometry variables measured by hip structural analysis in the study of osteoporotic fractures. Journal of Bone and Mineral Research, 23, 1892–1904. Krebs-Smith, S. M., Guenther, P. M., Subar, A. F., Kirkpatrick, S. I., & Dodd, K. W. (2010). Americans do not meet federal dietary recommendations. Journal of Nutrition, 140, 1832–1838. Leonard, M. B., Elmi, A., Mostoufi-Moab, S., Shults, J., Burnham, J. M., Thayu, M., . . . Zemel, B. S. (2010). Effects of sex, race, and puberty on cortical bone and the functional muscle bone unit in children, adolescents, and young adults. Journal of Clinical Endocrinology & Metabolism, 95, 1681–1689. Linden, C., Ahlborg, H. G., Besjakov, J., Gardsell, P., & Karlsson, M. K. (2006). A school curriculum-based exercise program increases bone mineral accrual and bone size in prepubertal girls: Two-year data from the Pediatric Osteoporosis Prevention (POP) Study. Journal of Bone and Mineral Research, 21, 829–835. Lofgren, B., Dencker, M., Nilsson, J. A., & Karlsson, M. K. (2012). A 4year exercise program in children increases bone mass without increasing fracture risk. Pediatrics, 129, e1468–e1476. Lorbergs, A. L., Farthing, J. P., Baxter-Jones, A. D., & Kontulainen, S. A. (2011). Forearm muscle size, strength, force, and power in relation to pQCT-derived bone strength at the radius in adults. Applied Physiology, Nutrition, and Metabolism, 36, 618–625. MacDonald, H. M., Kontulainen, S. A., Petit, M. A., Beck, T. J., Khan, K. M., & McKay, H. A. (2008). Does a novel school-based physical activity model benefit femoral neck bone strength in pre- and early pubertal children? Osteoporosis International, 19, 1445–1456.
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Magaziner, J., Lydick, E., Hawkes, W., Fox, K. M., Zimmerman, S. I., Epstein, R. S., & Hebel, J. R. (1997). Excess mortality attributable to hip fracture in White women aged 70 years and older. American Journal of Public Health, 87, 1630– 1636. Mayranpaa, M. K., Makitie, O., & Kallio, P. E. (2010). Decreasing incidence and changing pattern of childhood fractures: A populationbased study. Journal of Bone and Mineral Research, 25, 2752–2759. McCarthy, P. J., & Jones, M. V. (2007). A qualitative study of sport enjoyment in the sampling years. The Sport Psychologist, 21, 400–416. Meredith, M. D., & Welk, G. J. (2010). Fitnessgram & Activitygram test administration manual (4th ed.). Champaign, IL: Human Kinetics. National Association for Sport and Physical Education & American Heart Association. (2012). Shape of the nation report: Status of physical education in the USA. Reston, VA: American Alliance for Health, Physical Education, Recreation and Dance. Nilsson, M., Sundh, D., Ohlsson, C., Karlsson, M., Mellstom, D., & Lorentzon, M. (2014). Exercise during growth and young adulthood is independently associated with cortical bone size and strength in old Swedish men. Journal of Bone and Mineral Research, 29, 1795–1804. Nogueira, R. C., Weeks, B. K., & Beck, B. R. (2014). Exercise to improve pediatric bone and fat: A systematic review and meta-analysis. Medicine & Science in Sports & Exercise, 46, 610–621. Ornelas, I. J., Perreira, K. M., & Ayala, G. X. (2007). Parental influences on adolescent physical activity: A longitudinal study. International Journal of Behavioral Nutrition and Physical Activity, 4, 3. doi:10.1186/14795868-4-3 Pate, R. P., Trost, S. G., Mullis, R., Sallis, J. F., Wechsler, H., & Brown, D. R. (2000). Community interventions to promote proper nutrition and physical activity among youth. Preventative Medicine, 31, S138–S149. Petit, M. A., McKay, H. A., MacKelvie, K. J., Heinonen, A., Khan, K. M., & Beck, T. J. (2002). A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: A hip structural analysis study. Journal of Bone and Mineral Research, 17, 363 –372. Robling, A. G. (2009). Is bone’s response to mechanical signals dominated by muscle forces? Medicine & Science in Sports & Exercise, 41, 2044–2049. Schneider, M., & Cooper, D. M. (2011). Enjoyment of exercise moderates the impact of a school-based physical activity intervention. Journal of Behavioral Nutrition and Physical Activity, 8, 64. doi:10.1186/14795868-8-64 Schoenau, E., Neu, C. M., Beck, B., Manz, F., & Rauch, F. (2002). Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. Journal of Bone and Mineral Research, 17, 1095–1101.
Specker, B., & Binkley, T. (2003). Randomized trial of physical activity and calcium supplementation on bone mineral content in 3- to 5-year-old children. Journal of Bone and Mineral Research, 18, 885–892. Tan, V. P., MacDonald, H. M., Kim, S., Nettlefold, L., Gabel, L., Ashe, M. C., & McKay, H. A. (2014). Influence of physical activity on bone strength in children and adolescents: A systematic review and narrative synthesis. Journal of Bone and Mineral Research, 29, 2161–2181. Tervo, T., Nordstrom, P., Neovius, M., & Nordstrom, A. (2008). Constant adaptation of bone to current physical activity level in men: A 12-year longitudinal study. Journal of Clinical Endocrinology & Metabolism, 93, 4873– 4879. Torio, C. M., & Andrews, R. M. (2013). National inpatient hospital costs: The most expensive conditions by payer, 2011 (HCUP statistical brief #160). Retrieved from http://www.hcup-us.ahrq.gov/reports/statbriefs/ sb160.pdf Troiano, R. P., Berrigan, D., Dodd, K. W., Masse, L. C., Tilert, T., & McDowell, M. (2008). Physical activity in the United States measured by accelerometer. Medicine & Science in Sports & Exercise, 40, 181 –188. Turner, C. H., Forwood, M. R., Rho, J. Y., & Yoshikawa, T. (1994). Mechanical loading thresholds for lamellar and woven bone formation. Journal of Bone and Mineral Research, 9, 87– 97. Turner, C. H., & Robling, A. G. (2003). Designing exercise regimens to increase bone strength. Exercise and Sport Sciences Reviews, 31, 45–50. University of Michigan C.S. Mott Children’s Hospital. (2013, August 19). C. S. Mott Children’s Hospital National Poll on Children’s Health: Top child health concerns: Obesity, drug abuse & smoking. Retrieved from http://mottnpch.org/sites/default/files/documents/081913Top10.pdf U.S. Department of Health and Human Services. (2004). Bone health and osteoporosis: A report of the Surgeon General. Rockville, MD: Office of the Surgeon General. U.S. Department of Health and Human Services. (2008). Physical Activity Guidelines Advisory Committee report. Washington, DC: Author. Valdimarsson, O., Linden, C., Johnell, O., Gardsell, P., & Karlsson, M. K. (2006). Daily physical education in the school curriculum in prepubertal girls during 1 year is followed by an increase in bone mineral accrual and bone width: Data from the Prospective Controlled Malmo Pediatric Osteoporosis Prevention Study. Calcified Tissue International, 78, 65 –71. Wallhead, T. L., & Buckworth, J. (2004). The role of physical education in the promotion of youth physical activity. Quest, 56, 285 –301. Walter, T., Quint, A., Fischer, K., & Kiger, J. (2011). Active movement warm-up routines. Journal of Physical Education, Recreation and Dance, 82(3), 23–31. Warden, S. J., Fuchs, R. K., Castillo, A. B., Nelson, I. R., & Turner, C. H. (2007). Exercise when young provides lifelong benefits to bone structure and strength. Journal of Bone and Mineral Research, 22, 251 –259.
Research Quarterly for Exercise and Sport Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/urqe20
Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents a
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Kathleen F. Janz , David Q. Thomas , M. Allison Ford & Skip M. Williams a
University of Iowa
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Illinois State University
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University of Mississippi Published online: 09 Feb 2015.
Click for updates To cite this article: Kathleen F. Janz, David Q. Thomas, M. Allison Ford & Skip M. Williams (2015) Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents, Research Quarterly for Exercise and Sport, 86:1, 5-12, DOI: 10.1080/02701367.2014.995019 To link to this article: http://dx.doi.org/10.1080/02701367.2014.995019
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Research Quarterly for Exercise and Sport, 86, 5–12, 2015 Copyright q SHAPE America ISSN 0270-1367 print/ISSN 2168-3824 online DOI: 10.1080/02701367.2014.995019
SPECIAL TOPICS: Top 10 Research Questions
Top 10 Research Questions Related to Physical Activity and Bone Health in Children and Adolescents Downloaded by [Michigan State University] at 04:05 24 February 2015
Kathleen F. Janz University of Iowa
David Q. Thomas Illinois State University
M. Allison Ford University of Mississippi
Skip M. Williams Illinois State University
Evidence strongly supports a positive, causal effect of physical activity on bone strength and suggests long-term benefits of childhood physical activity to the prevention of osteoporosis. The contribution of healthy bone development in youth is likely to be as important to fracture prevention as the amount of late adulthood bone loss. Families, schools (particularly physical education), and communities are key settings for health promotion focused on boneenhancing physical activity. However, little research has explored the topic of health promotion and physical education as they pertain to bone health, so best practices are not known. Based on our understanding of the literature, we present the top 10 research questions in health promotion and physical education that should be answered to advance boneenhancing physical activity in children and adolescents. Keywords: childhood, exercise, mechanical (impulsive) loading, skeletal health
About 30% to 50% of women and 15% to 20% of men at age 50 years will sustain an osteoporotic fracture in their remaining lifetime (U.S. Department of Health and Human Services [USDHHS], 2004). This accumulative incidence rate is higher than that of breast cancer in women and prostate cancer in men. Osteoporotic fractures, particularly of the hip, spine, and wrist, have significant health consequences including chronic pain, loss of function, loss of independence, and early mortality (Burge et al., 2007; Magaziner et al., 1997). In 2010, there were 258,000 hip fractures and the rate for women was almost twice the rate for men (Centers for Disease Control and Prevention Correspondence should be addressed to Kathleen F. Janz, Department of Health and Human Physiology, University of Iowa, 130 Field House, Iowa City, IA 52242. E-mail: [email protected]
[CDC], 2013). Women, who sustain an osteoporotic hip fracture have a mortality rate that is 10% to 24% greater than that of their peers (Magaziner et al., 1997). Hip fractures are also among the most expensive conditions addressed in U.S. hospitals with an aggregated inpatient cost of $4.9 billion (Torio & Andrews, 2013). These health statistics convey the morbidity, mortality, and economic burden of bone disease during late adulthood; however, extrapolations from epidemiological studies suggest that a relatively small increase in bone strength during childhood could significantly reduce osteoporotic fracture risk later in life (Heaney et al., 2000). Furthermore, statistical projections indicate that the amount of peak bone mass achieved during adolescence and young adulthood is a strong predictor of osteoporosis risk in later life (Hernandez, Beaupre, & Carter, 2003). For example, Clark and
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colleagues have estimated an 89% increase in adult fracture risk per standard deviation decrease in bone mass during childhood (Clark, Ness, Bishop, & Tobias, 2006). The contribution of healthy bone development in youth is likely to be as important to fracture prevention as the amount of late adulthood bone loss (Baptista & Janz, 2012). There is apparently much to be gained by beginning osteoporosis prevention early and continuing with a lifetime of bone health strategies. Of all the lifestyle strategies for increasing bone strength during the growing years, physical activity is one of the most (if not the most) efficacious (Heaney et al., 2000). However, more than 50% of children aged 6 years to 11 years old and more than 90% of youngsters aged 12 years to 19 years old are not active enough to optimize the health benefits of physical activity (Troiano et al., 2008). It is particularly troubling that physical activity levels decline precipitously during adolescence because it is during this stage of growth that bone is accruing most rapidly and is most sensitive to the osteogenic effects of physical activity (Baptista & Janz, 2012). Specifically during the growing years, the outer surface of bone (periosteum) is covered with a greater proportion of active osteoblasts that initiate bone formation when stimulated mechanically by muscle forces and impact forces, which primarily occur during physical activity, linear growth, and weight gain. Whole bone becomes stronger with the addition of more bone (increased mass) and through expansion of the bone’s periosteal circumference (change in structure; Daly, 2007). These responses to mechanical loads are primarily local crosssectional changes (Daly, 2007). Adding more crosssectional mass predominantly improves the strength of bone when it is being compressed (e.g., falling straight onto the wrist), whereas changing the structure of bone improves its bending and torsional strength. Hip fractures are usually caused by sideway falls and the impact creates bending and compression of the proximal femur (Kaptoge et al., 2008). Physical activities that are dynamic and odd in nature, high in magnitude and rate, and short in duration are the most effective in increasing bone mass and changing its structure (Gunter, Almstedt, & Janz, 2012). Examples of these activities include jumping, hopping, and tumbling. Because of its importance in osteoporosis prevention (USDHHS, 2004), bone-strengthening physical activity has been included in the U.S. Physical Activity Guidelines for Americans, with the recommendation that children and adolescents include these activities as part of their 60 min of daily physical activity on at least 3 days per week (USDHHS, 2008). For the last two decades, research in physical activity and bone health in children and adolescents has focused on establishing the causal effect of physical activity on bone strength. Much of this research has recently been reviewed in narratives (Tan et al., 2014), systematic reviews (Hind & Burrows, 2007; Nogueira, Weeks, & Beck, 2014), and metaanalyses (Behringer, Gruetzner, McCourt, & Mester, 2014;
Ishikawa, Kim, Kang, & Morgan, 2013; Nogueira et al., 2014). Taken in total, the evidence strongly supports a positive, causal effect of physical activity on bone strength and suggests long-term benefits of childhood physical activity to the prevention of osteoporosis. Nevertheless, significant work remains to fully understand dose-repose relationships between physical activity and bone health. However, given the current evidence for physical activity’s positive effect on bone, declining rates of physical activity during early adolescence, and the considerable additional benefits of a physically active lifestyle, there is no reason to not act on what we already know to help children and adolescents optimize bone health via physical activity. In fact, it is surprising that so little has been done to better understand the determinants of bone-enhancing physical activity or to test novel strategies to implement successful bone health programs in the home, school, and community. Based on our understanding of the current literature, we present the top 10 research questions that should be answered to advance bone-enhancing physical activity in children and adolescents with an eye toward primary prevention of osteoporotic fractures via health promotion and physical education.
TOP 10 RESEARCH QUESTIONS 1. What Exactly Is the Best Bone-Enhancing Physical Activity Recommendation for Children and Adolescents? Current federal health recommendations recommend boneenhancing physical activities for children and adolescents 3 days per week as part of a 60-min–per-day physical activity recommendation (USDHHS, 2008). The exact duration and mechanical load of bone-enhancing physical activity is not described because, honestly, this information is unknown. Based on a review of successful randomized controlled studies, Gunter, Almstedt, Baptista, and Janz (2011) suggested an exercise prescription for bone health with an impact magnitude of 3.5 times body weight, 100 loads per session (approximately 10 min to 15 min), 3 days per week, for at least 7 months. However, there is great overlap in the dose of exercise in successful and unsuccessful randomized controlled trials (Anliker, Dick, Rawer, & Toigo, 2012; Greene, Wiebe, & Naughton, 2009; MacDonald et al., 2008; Petit et al., 2002). Clearly more work is needed to define magnitude, time, and frequency. However, to date, all successful randomized controlled trials testing exercise as a causal factor for bone strength have used jumping as the primary physical activity. This gross motor skill mechanically loads the clinically important site of the hip via muscle loading during takeoff and via impact loading during landing. Jumping imposes a greater anabolic stimulus on bone than commonly prescribed metabolic-loading activities of walking or running (Fuchs,
PHYSICAL ACTIVITY AND BONE HEALTH RESEARCH
Bauer, & Snow, 2001). Current national priorities for increasing physical activity levels in youth are focused on metabolic health, particularly in relation to combating childhood obesity instead of holistic lifetime health and fitness. Studies are needed to more precisely identify the best osteogenic exercise dose and an exercise dose that encompasses both metabolic and skeletal health priorities.
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2. How and Why Does the Dose Response of Physical Activity to Bone Mass and Structure Vary Between Children and Adolescents? Mechanical loads placed on bone via physical activity create deformation (strains) of whole bone (Forwood & Turner, 1995; Turner, Forwood, Rho, & Yoshikawa, 1994). These strains activate mechanosensitive cells that in turn activate osteoblasts (bone-building cells) and osteoclasts (bone-resorbing cells). Adaptation occurs in response to changes in physical activity (as well as other mechanical loads) that surpasses a threshold regulated by the habitual strain loading. Inactive children may respond to low-impact loading and improve bone mass or structure, while others will need a higher mechanical load to promote a skeletal response (Turner & Robling, 2003). In addition to habitual physical activity, the threshold appears to vary between individuals (and also bone sites) according to maturity, sex, and perhaps race/ethnicity. Peripubertal children show more dramatic effects due to exercise interventions than do latepubertal and postpubertal adolescents. Several studies suggest that even the timing of maturation may affect bone accretion, particularly in girls; specifically, girls who mature early are more likely to enter adulthood with greater bone mass than are late-maturing girls (Bass et al., 1998; Behringer et al., 2014; Gilsanz, Roe, Mora, Costin, & Goodman, 1991). Physical activity-induced increases in periosteal circumference and cortical area continue across and perhaps after puberty in boys, whereas physical activity seems to cause reduced endosteal circumference and cortical bone mineral density in peripubertal and postpubertal girls (Leonard et al., 2010). Sparse research has been done in African American, Asian American, and Latino youth, and the effect of race and ethnicity as a moderating factor is almost unexplored, though it is expected to be significant. A better understanding of the variation in response to similar mechanical-loading conditions by children and adolescents will advance our ability to develop personalized prescriptions and set realistic goals for exercise training. 3. How Should Physical Activity and Bone Strength Dose-Response Relationships Be Measured? To more precisely understand how bone adapts to mechanical loading, measurement methods must capture physical activity dimensions (intensity, frequency, time) as
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well as the mass and structure of whole bone. In intervention studies, the physical activity dimension of intensity can be objectively measured with force plates to provide acceleration (m/s2) and power output (Watts; Fuchs et al., 2001; Ja¨msa¨, Ahola, & Korpelainen, 2011). Frequency and time are measured via observation. Quantifying physical activity dose in school- and community-based settings is more challenging. However, newer accelerometers directly provide acceleration gravitational units (m/s2), which may provide a relevant index of mechanical intensity. An additional accelerometer parameter, jerk or change in acceleration (g/s), has recently been shown to improve the prediction of physical activity dose as related to bone outcomes (Ja¨msa¨ et al., 2011). Because bone can adapt to short bouts of mechanical loading if the load is of high intensity (Turner et al., 1994), the time-stamped feature of accelerometers is important. Finally, accelerometers worn at the waist are sensitive to the clinically significant skeletal site of the hip (Gunter et al., 2012). Until the last decade, dual-energy X-ray absorptiometry (DXA) was almost entirely used to quantify bone outcomes. This two-dimensional imaging technology measures the attenuation of X-ray beams as they pass through tissues of varying density and sorts the body into three tissue compartments—muscle, fat, and bone. Software algorithms are then used to estimate areal bone mineral density (aBMD; g/cm2) and bone mineral content (BMC; g). Because DXA is fast, involves low radiation exposure (, 1 mrem per scan), and is widely available, it continues to be commonly used in pediatric research (Adams, Engelke, Zemel, & Ward, 2014; Gunter et al., 2012). When paired with algorithms, DXA measures can be used to estimate the structure of the proximal femur and, as such, can provide a more complete index of bone strength. However, because DXA does not measure depth of bone, it systematically overestimates density for children larger in size (when compared with their peers; Adams et al., 2014). A relatively new advancement in bone imaging, peripheral quantitative computed tomography (pQCT), provides three-dimensional imaging at distal bone locations such as the lower arm and lower leg. This technique also uses the attenuation of X-rays (, 10 mrem per scan; Gunter et al., 2012). In addition to providing a true measure of volumetric density (g/cm3), pQCT can separate cortical bone from trabecular bone and can provide measures of structural strength in compression, bending, and torsion (i.e., bone strength index, section modulus, and stress-strain index, respectively). Recently, high-resolution pQCT scanners have become available for use in clinical research. The resolution with these scanners can be used to measure additional bone strength features including cortical porosity and trabecular plate and rod microstructures (Adams et al., 2014). Of critical importance to dose-response studies is the measure of muscle crosssectional area (MCSA; cm2) and lean body mass (kg) because muscle is a strong and consistent predictor of bone
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strength (Lorbergs, Farthing, Baxter-Jones, & Kontulainen, 2011; MacDonald et al., 2008; Schoenau, Neu, Beck, Manz, & Rauch, 2002). Muscle also mediates the relationship between physical activity and bone strength. More consistent use of objective measurement systems for physical activity (force plates, accelerometers) and measurement systems for multiple outcomes including muscle will advance our understanding of the dose of physical activity needed to improve bone strength. Physical activity measures should capture mechanical loading (intensity, frequency, time), and bone-imaging measures should capture mass, structure, and surrounding muscle. 4. What Is the Interaction Between Physical Activity and Diet on Bone Health? Bone mineral tissue is composed of hydroxyapatite, a calcium-phosphate compound with magnesium and trace amounts of other minerals. Of the nutrients necessary for healthy bone development, calcium is one of the most important micronutrients, and it is the nutrient most likely to be insufficient during childhood and especially adolescence when milk consumption is typically replaced by soft drinks. Milk and other dairy products provide most of the calcium and vitamin D in the diet of U.S. children and adolescents (Krebs-Smith, Guenther, Subar, Kirkpatrick, & Dodd, 2010). Dairy products also provide protein and macronutrients important to bone metabolism including magnesium and potassium. However, approximately 66% of adolescent boys and 80% of adolescent girls do not meet the recommended intake of milk (Krebs-Smith et al., 2010). Though limited in number, most of the randomized controlled trials that have examined the effect of calcium and exercise combined report a significantly greater effect on bone mass, density, and structure compared with the intervention arm of calcium or exercise alone (Bass et al., 2007; Courteix, Jaffre´, Lespessailles, & Benhamou, 2005; Iuliano-Burns, Saxon, Naughton, Gibbons, & Bass, 2003; Specker & Binkley, 2003). Results suggest that the full effects of physical activity are realized only with a calciumrich diet. At this time, more work is needed to quantify the interaction between physical activity and calcium intake as well as the possible interaction between physical activity and other nutrients. 5. Are the Effects of Physical Activity on Bone Sustained From Childhood Through Adulthood to Old Age? Results from animal studies indicate that early exerciseinduced changes to bone strength persist through maturity and significantly reduce fracture risk in older animals (Warden, Fuchs, Castillo, Nelson, & Turner, 2007). The sustained effect of children’s physical activity into adolescence and even young adulthood has been demon-
strated in several observational studies (Baxter-Jones, Kontulainen, Faulkner, & Bailey, 2008; Janz et al., 2010); and at least two randomized controlled trials have shown a persistence of effects 1 year (Binkley & Specker, 2004) and 7 years (Gunter, Baxter-Jones, Mirwald, Almstedt, Fuchs, et al., 2008) postintervention. However, we do not know if bone-enhancing physical activity in children and adolescents is sustained so that it influences bone strength in older adults when fracture risk is greatest. Retrospective observational studies report positive associations between youth physical activity and older-adult bone mineral density (Bass et al., 1998; Nilsson et al., 2014; Tervo, Nordstrom, Neovius, & Nordstrom, 2008). However, these studies are likely to be confounded by present (adult) physical activity and (unknown) bone strength during youth. On the other hand, one prospective observational study, the University of Saskatchewan Pediatric Bone Mineral Accrual Study (Baxter-Jones et al., 2008), revealed positive associations between a self-reported general level of physical activity in youth and bone mineral density in adulthood. Investigators in this study controlled for present physical activity and early bone outcomes. When compared with less active peers, participants who were physically active at ages 8 to 15 years had 8% to 10% more hip BMC than young adults (ages 23– 30 years old; Baxter-Jones et al., 2008). This study suggested the possibility of long-term sustained benefits of childhood physical activity on adult bone health. We do not know what is more important for bone health in older adults—past, present, or persistent physical activity. 6. What Determines if Children and Adolescents Participate in Bone-Enhancing Physical Activity? Although the literature on physical activity determinants in youth is large and increasingly more theoretical and sophisticated, we were unable to identify any research on why children and youth specifically participate in the types of physical activities known to enhance bone health. Many osteogenic gross motor skills (e.g., skipping, hopping, jumping, tumbling) can be classified as play and are engaged in not for their health benefits but purely for enjoyment and for the opportunity to socialize with friends (Fitzgerald, Fitzgerald, & Aherne, 2012; Humbert et al., 2008). For those boys and girls involved in organized or recreational sports, games, and activities that require muscle loading and impact loading (e.g., volleyball, basketball, gymnastics, dance), bone health benefits have not been associated with reasons for participation (McCarthy & Jones, 2007; Schneider & Cooper, 2011; Wallhead & Buckworth, 2004). It is likely that physical education and perhaps public health campaigns (e.g., the CDC’s Best Bones Forever) are the venues that provide youth with overt reasons and specific skill sets to participate in boneenhancing physical activities. To the best of our knowledge, strategies for how to most effectively educate youth about
PHYSICAL ACTIVITY AND BONE HEALTH RESEARCH
bone-enhancing physical activities have not been systematically tested.
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7. What Is the Effect of Traditional Physical Education on Bone Health? Schools are in an ideal setting to influence children’s participation in bone-strengthening physical activity due to the amount of time children spend at school and the physical activity instruction that takes place in schools (American Alliance for Health, Physical Education, Recreation and Dance, 2013). Comprehensive, quality physical education programs should include bone-enhancing curricula tailored for student age and developmental needs (National Association for Sport and Physical Education & American Heart Association, 2012). For example, the goal within elementary school physical education is to teach students the gross motor skills necessary to move and control their bodies in an effective manner. During the learning of skills such as hopping, skipping, and galloping, students are participating in activities that have been shown to improve bone strength (Gunter, Baxter-Jones, Mirwald, Almstedt, Fuchs, et al., 2008). During middle school and high school, curricula shifts from learning basic movement skills to participation in sports and fitness activities. Many of the skills within sports and fitness units (e.g., jumping, running) are excellent for bone health. However, the potential educational link between these muscle-loading and impactloading activities and bone health is (seldom) made and little is known as to how much these specific activities contribute to bone health. In short, research is needed on how intermittent, nontargeted participation in boneenhancing activities during physical education contributes to bone health. 8. How Can Physical Education Instruction Be Altered to Be More Effective in Enhancing Bone Health? Some (Linden, Ahlborg, Besjakov, Gardsell, & Karlsson, 2006; Lofgren, Dencker, Nilsson, & Karlsson, 2012; Valdimarsson, Linden, Johnell, Gardsell, & Karlsson, 2006), though not all (Alwis et al., 2008; Detter et al., 2014), intervention studies where bone-enhancing exercises such as jumping were infused in the physical education curriculum have been successful in improving bone strength (when compared with controls). These exercise trials support the efficacy of using physical education as a means to improve bone heath. What is now needed is an innovative approach to consistently include bone-enhancing activities within the physical education curriculum with the acknowledgement that the curriculum is already filled with other, equally important, objectives. For example, there may be value in incorporating a variety of bone-enhancing physical activities during the warm-up or during waiting periods of physical education lessons. Appropriate osteo-
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genic warm-up activities for middle and high school programs include burpees, squat and jump, jumping jacks, tuck jumps, single-leg hops, single-leg/double-leg lateral ski hops, and rope skipping (Walter, Quint, Fischer, & Kiger, 2011). Small-sided games during sports-based lessons in basketball and volleyball provide bone-enhancing activities and active participation for all. The main lessons in tumbling and gymnastics provide exceptional osteogenic opportunities. In the end, physical education curricula that incorporate multiple motor skills (e.g., soccer, tumbling, tennis) and provide diverse physical activity choices throughout the school year including osteogenic warm-ups are most likely to satisfy physical education priorities and enhance bone strength. Research should test curricular approaches for efficacy and efficiency. 9. How Can Communities Facilitate Youth Participation in Bone-Enhancing Physical Activities? While most children’s bone-related physical activity interventions have occurred in school settings, there is also a need for interventions within the community. Communities provide an excellent setting for intervention programs for several reasons. Programs within communities more easily incorporate parents and other adults (when compared with the school setting). These adults can serve as role models as well as organizers to help ensure the sustained effect of an intervention (Ornelas, Perreira, & Ayala, 2007; Pate et al., 2000). The engagement of parents and community members in bone health programming is important given findings of a study conducted at the University of Michigan C. S. Mott Children’s Hospital (2013). When adults were asked to list the top health concerns for youth in their communities, smoking, drugs, and obesity were cited most often. Bone health was never mentioned even though 30% to 50% of youth will experience a bone fracture prior to adulthood (Mayranpaa, Makitie, & Kallio, 2010). Communities also should provide the recreational space critical for youth physical activity programs. Adolescents report athletic playing fields/courts, indoor recreation facilities, walk/run trails, and parks as their most commonly used recreation sites (Davison & Lawson, 2006; Grafova, 2008). Similarly, children report public parks, playgrounds, and athletic playing fields/courts among their most commonly used recreation sites (Grow et al., 2008). Little work has been done to explore how community programming in these recreational spaces might enhance bone health. However, Gunter and Kasianchuk (2011) showed early pubertal girls realized an increase in BMC after a 9-month community running program. Similarly, a study among adolescent (nonelite) community tennis players revealed higher femoral neck aBMD compared with their age-matched controls (Ermin, Owens, Ford, & Bass, 2012). Running and tennis are lifetime leisure activities and are likely to be more sustainable than
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jumping-based activities. Because community-based physical activity programs augment and support school-based programs (Bryant et al., 2010), bridging community-based with school-based interventions may provide the most effective intervention strategies. Research examining community settings and programs that facilitate boneenhancing physical activity is warranted.
supportive environments to ensure continued physical activity with age. Families, schools (particularly physical education), and communities are key settings for successful bone-related health promotion.
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10. How Do We Assess and Track Efforts to Promote Bone Health? Finding answers to the nine research questions presented in this article is likely to improve health promotion and physical education efforts to increase bone-enhancing physical activity in youth. However, quantifying success (or identifying failure) will require nonclinical measures of changes in bone mass and structure or at least proxy measures that are strongly associated with osteogenic changes. During physical activity, muscle forces account for the majority of bone strains leading to increases in bone strength (Robling, 2009). The connection between muscle force and bone strength is summarized in Harold Frost’s mechanostat theory (Frost, 1987), indicating that the greater the force on the bone by muscles, the greater the bone adaptation. Muscle power is considered a performancerelated physical fitness attribute, yet it is not assessed in our national health-related fitness testing battery, FITNESSGRAMw (Meredith & Welk, 2010). However, recent research suggests muscle power may prove to be a useful surrogate for bone (Robling, 2009). Although the U.S. Physical Activity Guidelines for Americans (USDHHS, 2008) recommend bone-enhancing physical activities for children and adolescents, surprisingly, these activities are not even tracked in our national Youth Risk Behavior Surveillance System. It is time for research targeting our national assessment of physical fitness and tracking physical activity in youth to examine what is missing when bone health is left out.
CONCLUSIONS Optimal bone health is a key reason for promoting physical activity during the growing years when approximately 40% of bone mass is achieved (Bailey, McKay, Mirwald, Crocker, & Faulkner, 1999). Bone mass and structure appear to track through childhood, adolescence, and (at least) young adulthood (Baxter-Jones et al., 2008), suggesting that improving bone strength early in life may have sustained effects. Intervention strategies for bone health should begin during childhood when bone appears most sensitive to the effects of physical activity. These interventions must be designed to change the factors that keep children and adolescents from engaging in boneenhancing physical activity and must provide skills and
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