Nutrition’s Role In Performance Enhancement And Post Exercise Recovery
Keywords: nutrition, diet, sport, athlete, supplements, hydration
Introduction To The Importance & Influence Of Nutrition On Exercise
Nutrition is increasingly recognized as a key component of optimal sporting performance, with both the science and practice of sports nutrition developing rapidly.1 Recent studies have found that a planned scientific nutritional strategy (consisting of fluid, carbohydrate, sodium, and caffeine) compared with a self-chosen nutritional strategy helped non-elite runners complete a marathon run faster2 and trained cyclists complete a time trial faster.3 Whereas training has the greatest potential to increase performance, it has been estimated that consumption of a carbohydrate�electrolyte drink or relatively low doses of caffeine may improve a 40 km cycling time trial performance by 32�42 and 55�84 seconds, respectively.4
Evidence supports a range of dietary strategies in enhancing sports performance. It is likely that combining several strategies will be of greater bene t than one strategy in isolation.5 Dietary strategies to enhance performance include optimizing intakes of macronutrients, micronutrients, and fluids, including their composition and spacing throughout the day. The importance of individualized or personalized dietary advice�is becoming increasingly recognized,6 with dietary strategies varying according to the individual athlete�s sport, personal goals, and practicalities (eg, food preferences). �Athlete� includes individuals competing in a range of sport types, such as strength and power (eg, weight-lifting), team (eg, football), and endurance (eg, marathon running). The use of dietary supplements can enhance performance, provided these are used appropriately. This manuscript provides an overview of dietary strategies used by athletes, the efficacy of these strategies, availability of nutrition information to athletes, and risks associated with dietary supplement intake.
Review Of Diet Strategies Employed By Athletes
Maximizing Muscle Glycogen Stores Prior To Exercise
Carbohydrate loading aims to maximize an athlete�s muscle glycogen stores prior to endurance exercise lasting longer than 90 minutes. Benefits include delayed onset of fatigue (approximately 20%) and improvement in performance of 2%�3%.7 Initial protocols involved a depletion phase (3 days of intense training and low carbohydrate intake) followed by a loading phase (3 days of reduced training and high carbo- hydrate intake).8,9 Further research showed muscle glycogen concentrations could be enhanced to a similar level without the glycogen-depletion phase,10 and more recently, that 24 hours may be sufficient to maximize glycogen stores.11,12 Current recommendations suggest that for sustained or intermittent exercise longer than 90 minutes, athletes should consume 10�12 g of carbohydrate per kg of body mass (BM) per day in the 36�48 hours prior to exercise.13
There appears to be no advantage to increasing pre- exercise muscle glycogen content for moderate-intensity cycling or running of 60�90 minutes, as signi cant levels of glycogen remain in the muscle following exercise.7 For exercise shorter than 90 minutes, 7�12 g of carbohydrate/kg of BM should be consumed during the 24 hours preceding.13 Some14,15 but not all16 studies have shown enhanced performance of intermittent high-intensity exercise of 60�90 minutes with carbohydrate loading.
Carbohydrate eaten in the hours prior to exercise (com- pared with an overnight fast) has been shown to increase muscle glycogen stores and carbohydrate oxidation,17 extend cycle time to exhaustion,5 and improve exercise performance.5,18 Specific recommendations for exercise of longer than 60 minutes include 1�4 g of carbohydrate/kg of BM in the 1�4 hours prior.13 Most studies have not found improvements in performance from consuming low glycemic�index (GI) foods prior to exercise.19 Any metabolic or performance effects from low GI foods appear to be attenuated when carbohydrate is consumed during exercise.20,21
Carbohydrate Intake During The Event
Carbohydrate ingestion has been shown to improve performance in events lasting approximately 1 hour.6 A growing body of evidence also demonstrates beneficial effects of a carbohydrate mouth rinse on performance.22 It is thought that receptors in the oral cavity signal to the central nervous system to positively modify motor output.23
In longer events, carbohydrate improves performance primarily by preventing hypoglycemia and maintaining high levels of carbohydrate oxidation.6 The rate of exogenous carbohydrate oxidation is limited by the small intestine�s ability to absorb carbohydrate.6 Glucose is absorbed by the sodium- dependent transporter (SGLT1), which becomes saturated with an intake of approximately 1 g/minute. The simultaneous ingestion of fructose (absorbed via glucose transporter 5�[GLUT5]), enables oxidation rates of approximately 1.3 g/minute,24 with performance benefits apparent in the third hour of exercise.6 Recommendations reflect this, with 90 g of carbohydrate from multiple sources recommended for events longer than 2.5 hours, and 60 g of carbohydrate from either single or multiple sources recommended for exercise of 2�3 hours� duration (Table 1). For slower athletes exercising at a lower intensity,�carbohydrate requirements will be less due to lower carbohydrate oxidation.6 Daily training with high carbohydrate availability has been shown to increase exogenous carbohydrate oxidation rates.25
The �Train-Low, Compete-High� Approach
The �train-low, compete-high� concept is training with low carbohydrate availability to promote adaptations such as�enhanced activation of cell-signaling pathways, increased mitochondrial enzyme content and activity, enhanced lipid oxidation rates, and hence improved exercise capacity.26 However, there is no clear evidence that performance is improved with this approach.27 For example, when highly trained cyclists were separated into once-daily (train-high) or twice-daily (train-low) training sessions, increases in resting muscle glycogen content were seen in the low-carbohydrate- availability group, along with other selected training adaptations.28 However, performance in a 1-hour time trial after 3 weeks of training was no different between groups. Other research has produced similar results.29 Different strategies have been suggested (eg, training after an overnight fast, training twice per day, restricting carbohydrate during recovery),26 but further research is needed to establish optimal dietary periodization plans.27
Fat As A Fuel During Endurance Exercise
There has been a recent resurgence of interest in fat as a fuel, particularly for ultra endurance exercise. A high-carbohydrate strategy inhibits fat utilization during exercise,30 which may not be beneficial due to the abundance of energy stored in the body as fat. Creating an environment that optimizes fat oxidation potentially occurs when dietary carbohydrate is reduced to a level that promotes ketosis.31 However, this strategy may impair performance of high-intensity activity, by contributing to a reduction in pyruvate dehydrogenase activity and glycogenolysis. 32 The lack of performance benefits seen in studies investigating �high-fat� diets may be attributed to inadequate carbohydrate restriction and time for adaptation.31 Research into the performance effects of high fat diets continues.
Nutrition: Protein
While protein consumption prior to and during endurance and resistance exercise has been shown to enhance rates of muscle protein synthesis (MPS), a recent review found protein ingestion alongside carbohydrate during exercise does not improve time�trial performance when compared with the ingestion of adequate amounts of carbohydrate alone.33
Fluid And Electrolytes
The purpose of fluid consumption during exercise is primarily to maintain hydration and thermoregulation, thereby benefiting performance. Evidence is emerging on increased risk of oxidative stress with dehydration.34 Fluid consumption prior to exercise is recommended to ensure that the athlete is well-hydrated prior to commencing exercise.35 In addition,�carefully planned hyperhydration ( fluid overloading) prior to an event may reset fluid balance and increase fluid retention, and consequently improve heat tolerance.36 However, fluid overloading may increase the risk of hyponatremia 37 and impact negatively on performance due to feelings of fullness and the need to urinate.
Hydration requirements are closely linked to sweat loss, which is highly variable (0.5�2.0 L/hour) and dependent on type and duration of exercise, ambient temperature, and athletes� individual characteristics.35 Sodium losses linked to high temperature can be substantial, and in events of long duration or in hot temperatures, sodium must be replaced along with fluid to reduce risk of hyponatremia. 35
It has long been suggested that fluid losses greater than 2% of BM can impair performance,35 but there is controversy over the recommendation that athletes maintain BM by fluid ingestion throughout an event.37 Well-trained athletes who �drink to thirst� have been found to lose as much as 3.1% of BM with no impairment of performance in ultra-endurance events.38 Ambient temperature is important, and a review illustrated that exercise performance was preserved if loss was restricted to 1.8% and 3.2% of BM in hot and temperate conditions, respectively.39
Dietary Supplementation: Nitrates, Beta-Alanine & Vitamin D
Performance supplements shown to enhance performance include caffeine, beetroot juice, beta-alanine (BA), creatine, and bicarbonate.40 Comprehensive reviews on other supplements including caffeine, creatine, and bicarbonate can be found elsewhere.41 In recent years, research has focused on the role of nitrate, BA, and vitamin D and performance. Nitrate is most commonly provided as sodium nitrate or beetroot juice.42 Dietary nitrates are reduced (in mouth and stomach) to nitrites, and then to nitric oxide. During exercise, nitric oxide potentially influences skeletal muscle function through regulation of blood ow and glucose homeostasis, as well as mitochondrial respiration.43 During endurance exercise, nitrate supplementation has been shown to increase exercise efficiency (4%�5% reduction in VO at a steady attenuate oxidative stress.42 Similarly, a 4.2% improvement in performance was shown in a test designed to simulate a football game.44
BA is a precursor of carnosine, which is thought to have a number of performance-enhancing functions including the reduction of acidosis, regulation of calcium, and antioxidant properties.45 Supplementation with BA has been shown to�2�state; 0.9% improvement in time trials), reduce fatigue, and�augment intracellular carnosine concentration.45 A systematic review concluded that BA may increase power output and working capacity and decrease feelings of fatigue, but that there are still questions about safety. The authors suggest caution in the use of BA as an ergogenic aid.46
Vitamin D is essential for the maintenance of bone health and control of calcium homeostasis, but is also important for muscle strength,47,48 regulation of the immune system,49 and cardiovascular health.50 Thus inadequate vitamin D status has potential implications for the overall health of athletes and performance. A recent review found that the vitamin D status of most athletes reflects that of the population in their locality, with lower levels in winter, and athletes who train predominantly indoors are at greater risk of deficiency.51 There are no dietary vitamin D recommendations for athletes; however, for muscle function, bone health, and avoidance of respiratory infections, current evidence supports maintenance of serum 25-hydroxy vitamin D (circulating form) concentrations of 80�100 nmol/L.51
Diets Specific For Post Exercise
Recovery from a bout of exercise is integral to the athlete�s training regimen. Without adequate recovery of carbohydrate, protein, fluids, and electrolytes, beneficial adaptations and performance may be hampered.
Muscle Glycogen Synthesis
Consuming carbohydrates immediately post exercise to coincide with the initial rapid phase of glycogen synthesis has been used as a strategy to maximize rates of muscle glycogen synthesis. An early study found delaying feeding by 2 hours after glycogen-depleting cycling exercise reduced glycogen synthesis rates.52 However the importance of this early enhanced rate of glycogen synthesis has been questioned in the context of extended recovery periods with sufficient carbohydrate consumption. Enhancing the rate of glycogen synthesis with immediate carbohydrate consumption after exercise appears most relevant when the next exercise session is within 8 hours of the first.53,54 Feeding frequency is also irrelevant with extended recovery; by 24 hours post exercise, consumption of carbohydrate as four large meals or 16 small snacks had comparable effects on muscle glycogen storage.55
With less than 8 hours between exercise sessions, it is recommended that for maximal glycogen synthesis, 1.0�1.2 g/kg/hour is consumed for the first 4 hours, followed by resumption of daily carbohydrate requirements.13 Additional protein has been shown to enhance glycogen�synthesis rates when carbohydrate intake is suboptimal.56 The consumption of moderate to high GI foods post exercise is recommended;13 however, when either a high-GI or low-GI meal was consumed after glycogen-depleting exercise, no performance differences were seen in a 5 km cycling time trial 3 hours later.57
Muscle Protein Synthesis
An acute bout of intense endurance or resistance exercise can induce a transient increase in protein turnover, and, until feeding, protein balance remains negative. Protein consumption after exercise enhances MPS and net protein balance,58 predominantly by increasing mitochondrial protein fraction with endurance training, and myofibrillar protein fraction with resistance training.59
Only a few studies have investigated the effect of timing of protein intake post exercise. No significant difference in MPS was observed over 4 hours post exercise when a mixture of essential amino acids and sucrose was fed 1 hour versus 3 hours after resistance exercise.60 Conversely, when a protein and carbohydrate supplement was provided immediately versus 3 hours after cycling exercise, leg protein synthesis increased threefold over 3 hours.61 A meta-analysis found timed post exercise protein intake becomes less important with longer recovery periods and adequate protein intake,62 at least for resistance training.
Dose�response studies suggest approximately 20 g of high-quality protein is sufficient to maximize MPS at rest,63 following resistance,63,64 and after high-intensity aerobic exercise.65 Rate of MPS has been found to approximately triple 45�90 minutes after protein consumption at rest, and then return to baseline levels, even with continued availability of circulating essential amino acids (termed the �muscle full� effect).66 Since exercise-induced protein synthesis is elevated for 24�48 hours following resistance exercise67and 24�28 hours following high-intensity aerobic exercise,68 and feeding protein post exercise has an additive effect,58,64 then multiple feedings over the day post exercise might maximize muscle growth. In fact, feeding 20 g of whey protein every 3 hours was subsequently found to maximally stimulate muscle myofibrillar protein synthesis following resistance exercise.69,70
In resistance training, where post exercise intake of protein was balanced by protein intake later in the day, increased adaptation of muscle hypertrophy resulted in equivocal strength performance effects.71,72 Most studies have not found a subsequent bene t to aerobic performance with post exercise protein consumption.73,74 However, in two�well controlled studies in which post exercise protein intake was balanced by protein intake later in the day, improvements were seen in cycling time to exhaustion75 and in cycling sprint performance.76
Fluids And Electrolyte Balance
Fluid and electrolyte replacement after exercise can be achieved through resuming normal hydration practices. However, when euhydration is needed within 24 hours or substantial body weight has been lost (.5% of BM), a more structured response may be warranted to replace fluids and electrolytes.77
Availability Of Nutritional Information To Athletes At Varying Levels
The availability of nutrition information for athletes varies. Younger or recreational athletes are more likely to receive generalized nutritional information of poorer quality from individuals such as coaches.78 Elite athletes are more likely to have access to specialized sports-nutrition input from qualified professionals. A range of sports science and medicine support systems are in place in different countries to assist elite athletes,1 and nutrition is a key component of these services. Some countries have nutrition programs embedded within sports institutes (eg, Australia) or alternatively have National Olympic Committees that support nutrition programs (eg, United States of America).1 However, not all athletes at the elite level have access to sports-nutrition services. This may be due to financial constraints of the sport, geographical issues, and a lack of recognition of the value of a sports-nutrition service.78
Athletes eat several times per day, with snacks contributing to energy requirements.79 Dietary intake differs across sports, with endurance athletes more likely to achieve energy and carbohydrate requirements compared to athletes in weight-conscious sports.79 A review found daily intakes of carbohydrate were 7.6 g/kg and 5.7 g/kg of BM for male and female endurance athletes, respectively.80 Ten elite Kenyan runners met macronutrient recommendations but not guide- lines for fluid intake.81 A review of fluid strategies showed a wide variability of intake across sports, with several factors influencing intake, many outside the athlete�s control.82
Nutrition information may be delivered to athletes by a range of people (dietitians, nutritionists, medical practitioners, sports scientists, coaches, trainers) and from a variety of sources (nutrition education programs, sporting magazines, the media and Internet).83 Of concern is the provision of�nutrition advice from outside various professional�s scope of practice. For example, in Australia 88% of registered exercise professionals provided nutrition advice, despite many not having adequate nutrition training.84 A study of Canadian high-performance athletes from 34 sports found physicians ranked eighth and dietitians, 16th as choice of source of dietary supplement information.85
Risks Of Contravening The Doping Regulations
Supplement use is widespread in athletes.86,87 For example, 87.5% of elite athletes in Australia used dietary supplements88 and 87% of Canadian high-performance athletes took dietary supplements within the past 6 months85 (Table 2). It is difficult to compare studies due to differences in the criteria used to define dietary supplements, variations in assessing supplement intake, and disparities in the populations studied.85
Athletes take supplements for many reasons, including for proposed performance benefits, for prevention or treatment of a nutrient deficiency, for convenience, or due to fear of �missing out� by not taking a particular supplement.41
The potential benefits (eg, improved performance) of taking a dietary supplement must outweigh the risks.86,87 There are few permitted dietary supplements available that have an ergogenic effect.87,89 Dietary supplementation cannot compensate for poor food choices.87 Other concerns include lack of efficacy, safety issues (toxicity, medical concerns), negative nutrient interactions, unpleasant side effects, ethical issues, financial expense, and lack of quality control.41,86,87 Of major concern, is the consumption of prohibited substances by the World Anti-Doping Agency (WADA).
Inadequate regulation in the supplement industry (com- pounded by widespread Internet sales) makes it difficult for athletes to choose supplements wisely.41,86,87 In 2000�2001, a study of 634 different supplements from 13 countries found that 94 (14.8%) contained undeclared steroids, banned by WADA.90 Many contaminated supplements were routinely used by athletes (eg, vitamin and mineral supplements).86 Several studies have confirmed these findings. 41,86,89
A positive drug test in an athlete can occur with even a minute quantity of a banned substance.41,87 WADA maintains a �strict liability� policy, whereby every athlete is responsible for any substance found in their body regardless of how it got there.41,86,87,89 The World Anti-Doping Code (January 1, 2015) does recognize the issue of contaminated supplements.91 Whereas the code upholds the principle of strict liability, athletes may receive a lesser ban if they can��show �no significant fault� to demonstrate they did not intend to cheat. The updated code imposes longer bans on those who cheat intentionally, includes athlete support personnel (eg, coaches, medical staff), and has an increased focus on anti-doping education.91,99
In an effort to educate athletes about sports-supplement use, the Australian Institute of Sport�s sports-supplement program categorizes supplements according to evidence�of efficacy in performance and risk of doping outcome.40 Category A supplements have sound evidence for use and include sports foods, medical supplements, and performance supplements. Category D supplements should not be used by athletes, as they are banned or are at high risk for contamination. These include stimulants, pro-hormones and hormone boosters, growth hormone releasers, peptides, glycerol, and colostrum.40
Conclusion
Athletes are always looking for an edge to improve their performance, and there are a range of dietary strategies available. Nonetheless, dietary recommendations should be individualized for each athlete and their sport and provided by an appropriately qualified professional to ensure optimal performance. Dietary supplements should be used with caution and as part of an overall nutrition and performance plan.
Disclosure
The authors report no conflicts of interest in this work.
Kathryn L Beck1 Jasmine S Thomson2 Richard J Swift1 Pamela R von Hurst1
1School of Food and Nutrition, Massey institute of Food Science and Technology, College of Health, Massey University Albany, Auckland, 2School of Food and Nutrition, Massey institute of Food Science and Technology, College of Health, Massey University Manawatu, Palmerston North, New Zealand
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Chronic undernutrition is characterized by a progressive reduction of the�fat-free mass (FFM) and fat mass (FM)�and �which has deleterious consequences on health. Undernutrition is insufficiently screened and treated in hospitalized or at-risk patients despite its high prevalence and negative impact on mortality, morbidity, length of stay (LOS), quality of life, and costs [1�4]. The risk of underestimating hospital undernutrition is likely to worsen in the next decades because of the increasing prevalence of overweight, obesity, and chronic diseases and the increased number of elderly subjects. These clinical conditions are associated with FFM loss (sarcopenia). Therefore, an increased number of patients with FFM loss and sarcopenic obesity will be seen in the future.
Academic societies encourage systematic screening of undernutrition at hospital admission and during the hospital stay [14]. The detection of undernutrition is generally based on measurements of weight and height, calculations of BMI, and the percentage of weight loss. Nevertheless, screening of undernutrition is infrequent in hospitalized or nutritionally at-risk ambulatory patients. For example, in France, surveys performed by the French Health Authority [15] indicate that: (i) weight alone, (ii) weight with BMI or percentage of weight loss, and (iii) weight, BMI,�and percentage of weight loss are reported in only 55, 30, and 8% of the hospitalized patients� records, respectively. Several issues, which could be improved by specific educational programs, explain the lack of implementation of nutritional screening in hospitals (table 1). In addition, the accuracy of the clinical screening of undernutrition could be limited at hospital admission. Indeed, patients with undernutrition may have the same BMI as sex- and age- matched healthy controls but a significantly decreased FFM hidden by an expansion of the FM and the total body water which can be measured by bioelectrical impedance analysis (BIA) [13]. This example illustrates that body composition evaluation allows a more accurate identification of FFM loss than body weight loss or BMI decrease. The lack of sensitivity and specificity of weight, BMI, and percentage of weight loss argue for the need for other methods to evaluate the nutritional status.
In 2008, twelve and thirty percent of the worldwide adult population was obese or overweight; this is two times higher than in 1980 [16]. The prevalence of overweight and obesity is also increasing in hospitalized patients. A 10-year comparative survey performed in a European hospital showed an increase in patients� BMI, together with a shorter LOS [17]. The BMI increase masks undernutrition and FFM loss at hospital admission. The increased prevalence of obesity in an aging population has led to the recognition of a new nutritional entity: �sarcopenic obesity� [18]. Sarcopenic obesity is characterized by increased FM and reduced FFM with a normal or high body weight. The emergence of the concept of sarcopenic obesity will increase the number of situations associated with a lack of sensitivity of the calculations of BMI and�body weight change for the early detection of FFM loss. This supports a larger use of body composition evaluation for the assessment and follow-up of nutritional status in clinical practice (fig. 1).
Fig. 2. Current and potential applications of body composition evaluation in clinical practice. The applications are indicated in the boxes, and the body composition methods that could be used for each application are indicated inside the circles. The most used application of body composition evaluation is the measurement of bone mineral density by DEXA for the diagnosis and management of osteoporosis. Although a low FFM is associated with worse clinical outcomes, FFM evaluation is not yet implemented enough in clinical practice. However, by allowing early detection of undernutrition, body composition evaluation could improve the clinical outcome. Body composition evaluation could also be used to follow up nutritional status, calculate energy needs, tailor nutritional support, and assess fluid changes during perioperative period and renal insufficiency. Recent evidence indicates that�a low FFM is associated with a higher toxicity of some chemo- therapy drugs in cancer patients. Thus, by allowing tailoring of the chemotherapy doses to the FFM in cancer patients, body com- position evaluation should improve the tolerance and the efficacy of chemotherapy. BIA, L3-targeted CT, and DEXA could be used for the assessment of nutritional status, the calculation of energy needs, and the tailoring of nutritional support and therapy. Further studies are warranted to validate BIA as an accurate method for fluid balance measurement. By integrating body composition evaluation into the management of different clinical conditions, all of these potential applications would lead to a better recognition of nutritional care by the medical community, the health care facilities, and the health authorities, as well as to an increase in the medico-economic benefits of the nutritional evaluation.
Body Composition Techniques For FFM Measurement
Body composition evaluation allows measurement of the major body compartments: FFM (including bone mineral tissue), FM, and total body water. Table 2 shows indicative values of the body composition of a healthy subject weighing 70 kg. In several clinical situations, i.e. hospital admission, chronic obstructive pulmonary dis- ease (COPD) [21�23], dialysis [24�26], chronic heart failure [27], amyotrophic lateral sclerosis [28], cancer [5, 29], liver transplantation [30], nursing home residence [31], and Alzheimer�s disease [32], changes in body compartments are detected with the techniques of body composition evaluation. At hospital admission, body composition evaluation could be used for the detection of FFM loss and undernutrition. Indeed, FFM and the FFM index (FFMI) [FFM (kg)/height (m2)] measured by BIA are significantly lower in hospitalized patients (n = 995) than in age-, height-, and sex-matched controls (n = 995) [3]. Conversely, clinical tools of nutritional status assessment, such as BMI, subjective global assessment, or mini-nutritional assessment, are not accurate enough to estimate FFM loss and nutritional status [30, 32�34]. In 441 patients with non-small cell lung cancer, FFM loss deter- mined by computerized tomography (CT) was observed in each BMI category [7], and in young adults with all�types of cancer, an increase in FM together with a de- crease in FFM were reported [29]. These findings reveal the lack of sensitivity of BMI to detect FFM loss. More- over, the FFMI is a more sensitive determinant of LOS than a weight loss over 10% or a BMI below 20 [3]. In COPD, the assessment of FFM by BIA is a more sensitive method to detect undernutrition than anthropometry [33, 35]. BIA is also more accurate at assessing nutrition- al status in children with severe neurologic impairment than the measurement of skin fold thickness [36].
FFM loss is correlated with survival in different clinical settings [5, 21�28, 37]. In patients with amyotrophic lateral sclerosis, an FM increase, but not an FFM in- crease, measured by BIA, was correlated with survival during the course of the disease [28]. The relation between body composition and mortality has not yet been demonstrated in the intensive care unit. The relation between body composition and mortality has been demonstrated with anthropometric methods, BIA, and CT. Measurement of the mid-arm muscle circumference is an easy tool to diagnose sarcopenia [38]. The mid-arm muscle circumference has been shown to be correlated with survival in patients with cirrhosis [39, 40], HIV infection [41], and COPD in a stronger way than BMI [42]. The relation between FFM loss and mortality has been extensively shown with BIA [21�28, 31, 37], which is the most used method. Recently, very interesting data suggest that CT could evaluate the disease prognosis in relation to muscle wasting. In obese cancer patients, sarcopenia as assessed by CT measurement of the total skeletal muscle cross-sectional area is an independent predictor of the survival of patients with bronchopulmonary [5, 7], gastrointestinal [5], and pancreatic cancers [6]. FFM assessed by measurement of the mid-thigh muscle cross- sectional area by CT is also predictive of mortality in COPD patients with severe chronic respiratory insufficiency [43]. In addition to mortality, a low FFMI at hospital admission is significantly associated with an in- creased LOS [3, 44]. A bicentric controlled population study performed in 1,717 hospitalized patients indicates that both loss of FFM and excess of FM negatively affect the LOS [44]. Patients with sarcopenic obesity are most at risk of increased LOS. This study also found that ex- cess FM reduces the sensitivity of BMI to detect nutritional depletion [44]. Together with the observation that the BMI of hospitalized patients has increased during the last decade [17], these findings suggest that FFM and�FFMI measurement should be used to evaluate nutritional status in hospitalized patients.
Numerous methods of body composition evaluation have been developed: anthropometry, including the 4-skinfold method [58], hydrodensitometry [58], in vivo neutron activation analysis [59], anthropogammametry from total body potassium-40 [60], nuclear magnetic resonance [61], dual-energy X-ray absorptiometry (DEXA) [62, 63], BIA [45, 64�66], and more recently CT [7, 43, 67]. DEXA, BIA, and CT appear to be the most convenient methods for clinical practice (fig. 2), while the other methods are reserved for scientific use.
The evaluation of FFM could be used for the calculation of energy needs, thus allowing the optimization of nutritional intakes according to nutritional needs. This could be of great interest in specific situations, such as severe neurologic disability, overweight, and obesity. In 61 children with severe neurologic impairment and intellectual disability, an equation integrating body composition had good agreement with the doubly labeled water method. It gave a better estimation of energy expenditure than did the Schofield predictive equation [36]. However, in 9 anorexia nervosa patients with a mean BMI of 13.7, pre- diction formulas of resting energy expenditure including FFM did not allow accurate prediction of the resting energy expenditure measured by indirect calorimetry [76]. In overweight or obese patients, the muscle catabolism in response to inflammation was the same as that observed�in patients with normal BMI. Indeed, despite a higher BMI, the FFM of overweight or obese individuals is similar (or slightly increased) to that of patients with normal BMI. Thus, the use of actual weight for the assessment of the energy needs of obese patients would result in over- feeding and its related complications. Therefore, the ex- perts recommend the use of indirect calorimetry or calculation of the energy needs of overweight or obese patients as follows: 15 kcal/kg actual weight/day or 20�25 kcal/kg ideal weight/day [77, 78], although these predictive formulas could be inaccurate in some clinical conditions [79]. In a US prospective study conducted in 33 ICU medical and surgical ventilated ICU patients, daily measurement of the active cell mass (table 2) by BIA was used to assess the adequacy between energy/protein intakes and needs. In that study, nutritional support with 30 kcal/ kg actual body weight/day energy and 1.5 g/kg/day protein allowed stabilization of the active cell mass [75]. Thus, follow-up of FFM by BIA could help optimize nutritional intakes when indirect calorimetry cannot be performed.
Body composition evaluation allows a qualitative assessment of body weight variations. The evaluation of body composition may help to document the efficiency of nutritional support during a patient�s follow-up of numerous clinical conditions, such as surgery [59], anorexia nervosa [76, 80], hematopoietic stem cell transplantation [81], COPD [82], ICU [83], lung transplantation [84], ulcerative colitis [59], Crohn�s disease [85], cancer [86, 87], HIV/AIDS [88], and acute stroke in elderly patients [89]. Body composition evaluation could be used for the follow-up of healthy elderly subjects [90]. Body composition evaluation allows characterization of the increase in body mass in terms of FFM and FM [81, 91]. After hematopoietic stem cell transplantation, the increase in BMI is the result of the increase in FM, but not of the increase in FFM [81]. Also, during recovery after an acute illness, weight gain 6 months after ICU discharge could be mostly related to an increase in FM (+7 kg) while FFM only increased by 2 kg; DEXA and air displacement plethysmography were used to measure the FM and FFM [91]. These two examples suggest that body composition evaluation could be helpful to decide the modification and/or the renewal of nutritional support. By identifying the patients gaining weight but reporting no or insufficient FFM, body composition evaluation could contribute to influencing the medical decision of continuing nutrition- al support that would have been stopped in the absence of body composition evaluation.
In clinical situations when weight and BMI do not reflect the FFM, the evaluation of body composition should be used to adapt drug doses to the FFM and/or FM absolute values in every patient. This point has been recently illustrated in oncology patients with sarcopenic obesity. FFM loss was determined by CT as described above. In cancer patients, some therapies could affect body com- position by inducing muscle wasting [92]. In patients with advanced renal cell carcinoma [92], sorafenib induces a significant 8% loss of skeletal muscular mass at 12 months. In turn, muscle wasting in patients with BMI less than 25 was significantly associated with sorafenib toxicity in patients with metastatic renal cancer [8]. In metastatic breast cancer patients receiving capecitabine treatment, and in patients with colorectal cancer receiving 5-fluorouracile, using the convention of dosing per unit of body surface area, FFM loss was the determinant of chemotherapy toxicity [9, 10] and time to tumor progression [10]. In colorectal cancer patients administered 5-fluoruracil, low FFM is a significant predictor of toxicity only in female patients [9]. The variation in toxicity between women and men may be partially explained by the fact that FFM was lower in females. Indeed, FFM rep- resents the distribution volume of most cytotoxic chemo- therapy drugs. In 2,115 cancer patients, the individual variations in FFM could change by up to three times the distribution volume of the chemotherapy drug per body area unit [5]. Thus, administering the same doses of chemotherapy drugs to a patient with a low FFM compared to a patient with a normal FFM would increase the risk of chemotherapy toxicity [5]. These data suggest that FFM loss could have a direct impact on the clinical outcome of cancer patients. Decreasing chemotherapy doses in case of FFM loss could contribute to improving cancer patients� prognosis through the improvement of the tolerance of chemotherapy. These findings justify the systematic evaluation of body composition in all cancer patients in order to detect FFM loss, tailor chemotherapy doses according to FFM values, and then improve the efficacy- tolerance and cost-efficiency ratios of the therapeutic strategies [93]. Body composition evaluation should also be used to tailor the doses of drugs which are calculated based on patients� weight, e.g. corticosteroids, immuno-suppressors (infliximab, azathioprine or methotrexate), or sedatives (propofol).
The implementation of body composition evaluation in routine care presents a challenge for the next decades. Indeed the concomitant increases in elderly subjects and patients with chronic diseases and cancer, and in the prevalence of overweight and obesity in the population, will increase the number of patients nutritionally at risk or undernourished, particularly those with sarcopenic obesity. Body composition evaluation should be used to improve the screening of undernutrition in hospitalized patients. The results of body composition should be based on the same principle as BMI calculation, towards the systematic normalization for body height of FFM (FFMI) and FM [FM (kg)/height (m)2 = FM index] [94]. The results could be expressed according to previously de- scribed percentiles of healthy subjects [95, 96]. Body com- position evaluation should be performed at the different stages of the disease, during the course of treatments and the rehabilitation phase. Such repeated evaluations of body composition could allow assessment of the nutritional status, adjusting the calculation of energy needs as kilocalories/kilogram FFM, following the efficacy of 
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