Some of these factors, such as genetics, race, age and sex are non-modifiable; but some lifestyle factors provide a potential modifiable effect on the bone. As such, manipulating the mode, duration and intensity of exercise could be useful ways to improve bone health in athletes.

This would require some manipulation of training schedules, and whilst there might often be scope to do this, that sort of advice rarely proves popular with coaches and athletes.

As such, there is a need to consider other modifiable options, such as diet and nutrition. The purpose of this narrative review is to provide an overview of the potential dietary and nutritional influences on bone health, with a specific focus on the athlete.

Bone is a nutritionally modulated tissue, which is evidenced by the acute reduction in bone metabolic markers that occurs with feeding in postmenopausal women [ 16 ]. Reductions in markers of bone formation also occur with nutrient feeding, although to a lower magnitude than for bone resorption markers [ 17 ].

In addition to modulating the daily rhythm of bone turnover [ 19 ], feeding can also moderate a number of hormones such as calcitropic hormones, incretin hormones, growth hormone and cortisol that are implicated in bone turnover in healthy postmenopausal women. Coverage of these responses is beyond the scope of the current review, but a detailed review is provided by Walsh and Henriksen [ 17 ].

What is clear is that nutrition has a significant influence on bone health across the lifespan, and this is well covered in the narrative review by Mitchell et al. In the main, the nutritional requirements to support the skeleton during growth and development and during ageing Table 1 are unlikely to be notably different between athletes and the general population.

In addition to these nutrients, the athlete should also ensure adequate intake of silicon [ 22 ], manganese, copper, boron, iron, zinc, vitamin A, vitamin K, vitamin C and the B vitamins [ 21 , 23 ], in order to support other metabolic processes important for bone health.

It is difficult to be specific on the recommended dietary intakes of particular nutrients for the athlete given that different countries have different recommendations for these intakes for examples, see the guidelines from the European Food Safety Authority, National Health and Medical Research Council and the Institute of Medicine.

What is also unclear is whether the hard training undertaken by athletes modifies these requirements for many of the nutrients relevant to bone health.

Of course, the majority of recommended dietary intake guidelines consider the potential for variation to allow them to meet the needs of the majority of the population, but many of these guidelines are focused upon preventing nutrient deficiencies, whereas the athlete is more focused upon supporting optimal function a useful resource here is Larson-Meyer et al.

As such, there might be a need for the athlete to consider a well conducted nutritional assessment of their dietary intake to identify whether or not they are consuming the required amounts of the key nutrients to underpin bone health, among other things, including optimal performance.

In terms of foods, most recommendations for good bone health include the consumption of dairy, fish, fruits and vegetables particularly of the green leafy kind , which are useful sources of the main nutrients supporting bone health. When the intake of particular nutrients of benefit to bone is difficult perhaps because of food intolerances or food preferences , some consideration could be given to the consumption of fortified foods or supplements.

The remainder of this review will focus upon what we consider to be the most pertinent, namely: energy availability, low carbohydrate availability, protein intake, vitamin D intake and dermal calcium and sodium losses.

The review will also briefly cover the effects of feeding around exercise on bone metabolism. Energy availability can be described as the amount of ingested energy remaining to support basic bodily functions and physiological processes, including growth, immune function, locomotion, and thermoregulation, once the energy needed for exercise has been utilised [ 25 ].

For a good overview of the myriad effects of low energy availability in the athlete, we direct the reader to the recent review by Logue et al. One of the major problems of identifying those athlete populations at risk of low energy availability and of identifying the causal links between low energy availability and bone health is the significant difficulty in collecting accurate data on energy intake and energy expenditure particularly during more intermittent types of exercise [ 27 ].

The low energy availabilities experienced by some athletes can have adverse effects on bone [ 28 ], including acute bony injuries and longer-term reduced bone mass and strength. It seems that many highly active individuals, particularly elite and recreational endurance athletes, might have some difficulties in matching their dietary energy intakes to their exercise energy expenditure, which inevitably results in low energy availability [ 29 , 30 ].

It is clear that this is also an issue that can affect male athletes as well as female athletes [ 31 ]. Although the relevance of some of these markers of bone metabolism was questioned they would not be considered the optimal markers of bone resorption and formation to use today [ 33 ] , this paper has been instrumental in raising the awareness of potential problems for the bone when energy availability is low.

It is common for athletes to experience low energy availabilities of a similar order of magnitude to those used by Ihle and Loucks [ 32 ]. Indeed, Thong et al.

Despite this, examination of the individual data showed that some men responded to lower energy availability with a decrease in bone formation. Whilst this is in no way conclusive, there is the possibility that lower energy availability will affect bone metabolism by decreasing bone formation in men, but that it might take a lower level of energy availability to produce this response than in women.

This would be an interesting avenue for future research. One of the issues with examining the effects of reduced energy availability on bone metabolism in athletes and athletic populations in the laboratory is that this is usually achieved via a reduction in dietary intake and an increase in exercise energy expenditure.

Whilst this is probably relevant, it does not allow us to determine whether the effect of low energy availability on bone might be more as a result of dietary restriction or as a result of high exercise energy expenditures or whether this makes no difference. Low energy availability achieved through dietary energy restriction resulted in decreased bone formation, with no concomitant change in bone resorption.

Low energy availability achieved through exercise alone, on the other hand, did not significantly alter bone metabolism.

Taken together, these results might suggest some bone protective effect of the mechanical loading induced by exercise in the short term, even when this might result in low energy availability.

These results also suggest that the athlete must focus on adequate dietary intake during hard training periods. Given the potential for low energy availability to negatively influence the short-term responses of bone, it would seem sensible to suggest that if this state was maintained over longer periods, more serious consequences might be experienced.

This raises an important, but as yet unanswered, question over whether it is the magnitude of the low energy availability i.

there is a threshold below which there is a negative effect on the bone that is important or whether it is more an issue of continuous low energy availability over time that negatively influences bone health. Added to this is the evidence from the many studies conducted since relating to the female athlete triad [ 25 , 42 ].

More recently, this same group has also suggested the potential for a similar syndrome in male athletes referred to as the male athlete triad; see Tenforde et al. Whilst further discussion of these conditions the male athlete triad and RED-S is vitally important and would be highly relevant herein, these topics are covered more extensively in another article within this supplement.

Certainly, it seems unlikely that elite endurance athletes male or female would be able to attain these levels of energy availability given the high energy expenditures induced by training and the limited time for refuelling that their demanding training schedules allow.

Another complication here is that endurance athletes might be directly opposed to trying to maintain a balanced energy intake, since many consider an energy deficit as essential to drive the endurance phenotype.

Taken together, these points highlight the difficulty in maintaining balanced energy availabilities for the promotion of bone health in the endurance athlete when stacked against the competing interests of optimising their sporting performance. As such, further research is needed to identify whether or not there is a means to maintain bone health without compromising training practices to optimise endurance performance.

One possibility might be to periodise low energy availability into the training cycle to develop the endurance phenotype without the need to have constantly low energy availability, a recent approach suggested by Stellingwerff [ 46 ].

Further research is also required to tease out the nuances of the effects of energy and nutrient availability on bone. In the laboratory, energy intake is often limited by simply determining habitual dietary energy intake and then cutting this intake down by a certain percentage. The issue with this is that nutrient intake is also reduced by the same relative amount, which begs the question of whether the effects on bone are wholly energy availability dependent or whether the concomitant reduction in the availability of carbohydrate, protein, calcium, vitamin D and other micronutrients also contributes to the negative impact on bone.

In addition, there might also be an interaction between elements of the female athlete triad and certain nutrients that could exacerbate the effects on bone. For example, iron deficiency might directly interact with reduced energy availability to further disrupt thyroid function and to suppress anabolic factors for bone formation, as recently postulated by Petkus et al.

Whilst no studies have directly examined the effects of low carbohydrate availability on bone health parameters in athletes, it has been shown that carbohydrate feeding can reduce bone turnover [ 50 ].

Bjarnason et al. Similarly, the provision of carbohydrate has been shown to attenuate the bone resorption response to acute exercise in athletes involved in an 8-day overloaded endurance training trial [ 51 ]. Sale et al. There is some more direct information to suggest that following a low-carbohydrate diet would negatively affect bone health, albeit from animal models and when concomitantly followed with a high-fat diet [ 53 ].

Bielohuby et al. Conversely, in humans, albeit osteoarthritis patients and not athletes, there was no effect on bone turnover as assessed by urinary N-telopeptide and bone-specific alkaline phosphatase concentrations when patients were fed less than 20 g of carbohydrate per day for 1 month and then less than 40 g of carbohydrate per day for the next 2 months [ 54 ].

Future research work is required to determine whether low-carbohydrate dietary practices would negatively impact the bone health of athletes in the longer term. Athletes are often recommended to consume more protein than is recommended for the general population, in order to support the additional demands of athletic training.

The recommendations for athletes is to consume between 1. This may result in a conflict of interest, as there is a long-held belief that higher protein intakes may have a negative influence on bone health [ 56 , 57 ], a topic that has recently been covered in detail by Dolan and Sale [ 58 ]; herein we will summarise the salient points.

The theory suggests that, in order to protect the homeostatic state, the body increases the availability of alkaline minerals, such as calcium, most of which are stored within the bone tissue.

The calcium released from the bone in order to counteract a high potential renal acid load is also associated with increased losses of calcium in the urine, along with lower BMD and an increased rate of bone loss [ 60 ].

Taken together, the results of these studies would suggest that, as a result of the acid-ash hypothesis, an athlete consuming a high particularly animal protein diet would run the risk of inducing demineralisation of the bone over the longer term with potential adverse effects on bone health.

Taken alone, however, this theory does not provide a fully balanced account of the potential influences of a high protein intake on bone. The main negative effect of a high animal protein diet on bone according to the acid-ash hypothesis relies upon the clear assumption that the calcium used to neutralise the high potential renal acid load resulting from animal protein consumption comes from the bone and that any excess calcium subsequently excreted in the urine comes from the bone.

This might not, however, be the case given that Kerstetter et al. Of further consideration is the fact that dietary acid load could just as easily be influenced by a reduction in the intake of alkaline foods, such as fruits and vegetables, as by an increase in the intake of acidic foods, such as animal proteins.

This would compound the issue, especially given that alkaline foods are also rich in a wide range of micro- and phyto-nutrients that are important for bone health [ 21 ].

Therefore, it is possible that the poorer bone outcomes reported in those consuming an acidic diet [ 60 ] were not due to high protein, but were as a result of a shortage of nutrient rich fruits and vegetables. This gives further support to the point made in Sect.

It is equally important to consider the possibility that protein is, in fact, beneficial and not harmful to bone for a review, see Dolan and Sale [ 58 ]. As such, athletes need to consume sufficient protein to support the increased rate of bone turnover caused by athletic training.

Additionally, protein ingestion increases the production of a number of hormones and growth factors, such as IGF-1, which are also involved in the formation of bone. Of further relevance for the athlete is the fact that higher protein intakes also support the development of muscle mass and function [ 64 ]; the associated increases in muscular force would likely act upon the bone to enhance bone mass and strength [ 65 ].

On the balance of the available evidence it would seem unlikely that higher animal protein intakes, in the amounts recommended to athletes, are harmful to bone health.

This is evidenced by the results of a number of studies albeit not in athletes per se that have been well summarised and statistically combined in high-quality meta-analyses as summarised by Rizzoli et al. It might, however, be sensible to recommend to athletes that they maintain adequate calcium during periods of higher protein consumption to be sure of no negative effects on the bone.

A small positive effect of protein on BMD and fracture risk has been identified, suggesting that the protein intakes of athletes, which are usually in excess of the recommended daily allowance, might be ultimately beneficial to the bone, although this requires further specific research.

Numerous studies in the last 5—10 years have identified athlete groups who have deficient or insufficient levels of circulating vitamin D [ 67 ], although the specific definitions of vitamin D deficiency and insufficiency have been debated. Whilst the causes of vitamin D deficiency in the general population are clearly multifactorial, it is most likely that the main cause in the athletic population is a reduction of ultraviolet B radiation absorption into the skin, which is the major source of vitamin D [ 72 , 73 ].

Whilst this seems fairly obvious in relation to those athletes who largely train and compete indoors and those who live and train in latitudes furthest from the equator, it might also be of relevance to those who train and compete outside, but who have to wear a significant amount of equipment e.

A direct relationship between serum vitamin D levels and musculoskeletal outcomes is relatively clear [ 69 ] and makes sense given the important role for vitamin D in calcium and phosphorus metabolism. Miller et al.

Similarly, Maroon et al. Whilst not directly causal, low-fat dairy products and the major nutrients in milk calcium, vitamin D, and protein were associated with greater bone gains and lower stress fracture rates in young female runners [ 77 ].

Interestingly, a higher potassium intake was also associated with greater gains in hip and whole-body BMD. It would seem relatively clear that the avoidance of vitamin D deficiency and insufficiency is important for the athlete to protect their bone health.

Athletes who undertake a high volume of prolonged exercise, particularly when that exercise is not weight bearing, are at risk of having lower BMDs [ 79 , 80 ]. One of the potential contributors to this might be an increase in bone resorption mediated by the activation of parathyroid hormone due to reductions in serum calcium levels, which, in turn, occur as the result of dermal calcium losses [ 81 ].

It is likely that the level of dermal calcium loss required to cause a decline in serum calcium concentrations, which is sufficient to activate parathyroid hormone secretion and thus bone demineralisation, would only occur during prolonged hard exercise.

Given that calcium plays an important role in many cellular processes that occur while exercising, the body vigorously defends serum calcium concentrations, predominantly by the demineralisation of bone, which, in turn could lead to a reduction in bone mass over time.

As such, Barry et al. Barry et al. Twenty male endurance athletes completed a km cycling time trial on three occasions having consumed either 1 mg of calcium 20 min before exercise and a placebo during exercise; 2 a placebo before exercise and mg of calcium every 15 min during exercise; or 3 a placebo before and during exercise.

The results showed that when mg of calcium was ingested as a single bolus prior to exercise, there was an attenuated parathyroid hormone response to the subsequent exercise bout.

There was a smaller attenuation of the parathyroid hormone response when calcium was supplemented during exercise, and this did not reach statistical significance. This latter possibility has not been explored and future research is required. In line with this, there is also the possibility that the challenge to fluid and sodium homeostasis that would occur under these circumstances might influence bone metabolism and health.

This, to our knowledge, has not been directly or well-studied in relation to the athlete, but there is some suggestion from the osteoporosis focussed literature suggesting that bone might be negatively affected by hyponatraemia.

Verbalis et al. The same paper also reported on a cross-sectional analysis of human adults from the Third National Health and Nutrition Examination Survey, showing that mild hyponatraemia was associated with significantly increased odds of osteoporosis, in line with the rodent data presented.

This might be explained by novel sodium signalling mechanisms in osteoclasts resulting in the release of sodium from bone stores during prolonged hyponatraemia [ 84 ].

Nutrient ingestion around acute exercise can alter the bone resorption marker response to that exercise bout. Many athletes exercise in the morning after an overnight fast, which has the potential to promote an increase in bone turnover.

Scott et al. As anticipated, the ingestion of food reduced pre-exercise bone resorption as measured by β-CTX , but, contrary to what was proposed, the bone resorption response to exercise was greater in the fed condition than in the fasted condition and, over time, there was no difference in the response between fasting and feeding.

As such, it seemed that the mechanical loading induced by exercise might have provided a more powerful stimulus than that of pre-exercise feeding. In line with this theory, Sale et al. Carbohydrate feeding attenuated bone resorption β-CTX and formation P1NP in the hours but not days following exercise, indicating an acute effect of carbohydrate feeding on bone turnover.

The total amount of glucose ingested was Given the fact that the post-exercise period might provide a longer timeframe and a greater scope for intervention, Townsend et al. There were three trials conducted in this study: 1 placebo: ingested immediately and 2 h post-exercise; 2 immediate feeding: carbohydrate plus protein 1.

When carbohydrate plus protein was ingested immediately post-exercise, there was a suppression of the exercise-induced bone resorption β-CTX response when compared to the control trial, along with a smaller increase in the bone formation P1NP response 3—4 h post-exercise.

It would seem clear that feeding around exercise can moderate the bone metabolic response to that exercise bout, with the post-exercise period being perhaps the most useful timeframe for intervention. Longer-term studies are therefore required to determine whether or not these shorter-term or acute responses to feeding around exercise are positive for bone health.

The studies in this area have largely been conducted in men, and it would be of interest to determine whether the same effects are seen in exercising women. Bone health is an important issue for some athletes, particularly those who are at a greater risk of low or lower BMD.

These athletes should develop strategies to take care of their bones, particularly during adolescence and early adulthood, even at the expense of their training and performance, given that trying to overcome an already low bone mass in later life is extremely difficult.

Taking care of their diet and nutrition might help athletes to better protect their bones against the demands of their sport. Dietary advice for athletes in this regard should remain in line with the advice given to the general population, with some consideration given to where there would be a need for higher intakes to match the needs of the sport and to optimise function, although there are several specific challenges that certain athletes might face over and above those faced by the general population.

In this review, we have attempted to acknowledge some of these potential issues and highlight the information that is currently available to support these views. There is, however, a dearth of information relating to the effects particularly the longer-term effects of different dietary and nutritional practices on bone health in athletes, and significant research effort is required on this topic in the future.

There is still a requirement to clearly define which types of athlete are and which types of athlete are not at risk of longer-term bone health issues, such as osteopenia and osteoporosis.

Further research is needed to determine the wider implications of reduced energy availability, beyond bone, as suggested by the RED-S syndrome; currently these are not well researched.

It remains to be clearly established whether there is or is not a male athlete triad and whether the bone health implications of reduced energy availability are seen at the same level as in females or whether males are a little more resistant to the effects of low energy availability.

Further research is required into the periodisation of low energy availabilities in endurance athletes, such that they can benefit from the positive effects of calorie restriction on the endurance phenotype but without putting their bone health at risk.

More work is required in athletes to determine the effects of nutrient availability particularly of carbohydrate separately from energy availability on bone health. The amounts of calcium lost during training in endurance and ultra-endurance athletes are still not well known, nor is the amount of calcium lost during more passive sweating, particularly in hot environments, such as might be performed by weight-making athletes.

No research has been conducted in athletes to determine whether or not there is an effect of sweat sodium loss on bone. Longer-term studies are needed to determine whether or not the shorter-term or acute responses of bone metabolism to feeding are positive for bone health.

These studies should also seek to determine whether feeding should be periodised around hard training blocks rather than constant so as not to reduce the potential adaptation of the bone to exercise training. Santos L, Elliott-Sale KJ, Sale C.

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This may simply be due to overtraining, or increasing training too quickly without giving the bones adequate time to adapt. Stress fractures can also be due to a lower bone mineral density, which means it takes less force to cause damage.

This often is the result of the female athlete triad — a direct result of not eating enough, or not eating enough of the right foods. If we can educate our youth on the importance of maintaining a healthy diet and supplying their active bodies with the energy they need, then we can prevent many of these injuries and maybe even reduce the chances that a woman develops osteoporosis later in life.

We know exercise is important. We know that a healthy weight is important. But what may not get enough attention is the fact that eating healthy calories to replenish and fuel the body is vital to athletes' health, in particular for strong and resilient bones.

Remember, bones are also a girl's best friends. And they should be like diamonds — strong and dense. We need to work to make sure they are. As a service to our readers, Harvard Health Publishing provides access to our library of archived content. Please note the date of last review or update on all articles.

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Recent Blog Articles. Flowers, chocolates, organ donation — are you in? A state of low energy availability can place athletes at risk of poor performance, low BMD and at a higher risk of osteoporotic fractures 6. If an athlete sustains a fracture, they are at risk of detrimentally impacting athletic performance, quality of life, and losing time out of training or failing to progress in their sporting careers 4.

Assessment of bone health should begin with a comprehensive history to screen for relevant risk factors. There are several blood tests that can be considered when investigating for causes of low BMD. In routine clinical practice primary care or SEM these may include the following blood tests prior to specialist referral:.

Newer blood tests have been developed to look at markers of bone turnover E. P1NP, CTX-1, Sclerostin, Osteocalcin. However, there is no definitive consensus on how they should be used in athletes and as a result their use is often restricted to either research studies or in specialist bone centres 5.

It is generally accepted that vitamin D plays a key role for the athlete in order to prevent stress fractures and muscle injury 6. The role of vitamin D supplementation and athletic performance has been debated extensively in the medical literature, however there is a lack of robust evidence to support widespread routine use 7.

Vitamin D measurement in asymptomatic patients is not routinely advised by NICE but may be considered in patients with significant risk factors for low BMD. Calcium supplementation is also not routinely recommended in the athlete and generally should only be considered if dietary intake is less than mg daily or less than mg a day in those with diagnoses osteoporosis 8.

Dual energy x-ray absorptiometry DEXA measures the amount of bone mineral per unit area of volume of bone tissue and is the main imaging modality used in the UK to assess BMD 9. Standard protocols measure the lumbar spine BMD to monitor treatment and hip BMD to predict fracture risk.