Nutrition for Older Athletes: Focus on Sex-Differences

r physical exercise and a healthy diet are major determinants of a healthy lifespan. Although aging is associated with declining endurance performance and muscle function, these components can favorably be modi ed by regular physical activity and especially by exercise training at all ages in both sexes. In addition, age-related changes in body composition and metabolism, which affect even highly trained masters athletes, can in part be compensated for by higher exercise metabolic ef ciency in active individuals. Accordingly, masters athletes are often considered as a role model for healthy aging and their physical capacities

activity and especially by exercise training at all ages in both sexes. In addition, age-related changes in body composition and metabolism, which affect even highly trained masters athletes, can in part be compensated for by higher exercise metabolic ef ciency in active individuals. Accordingly, masters athletes are often considered as a role model for healthy aging and their physical capacities are an impressive example of what is possible in aging individuals. In the present review, we rst discuss physiological changes, performance and trainability of older athletes with a focus on sex differences. Second, we describe the most important hormonal alterations occurring during aging pertaining regulation of appetite, glucose homeostasis and energy expenditure and the modulatory role of exercise training. The third part highlights nutritional aspects that may support health and physical performance for older athletes. Key nutrition-related concerns include the need for adequate energy and protein intake for preventing low bone and muscle mass and a higher demand for speci c nutrients (e.g., vitamin D and probiotics) that may reduce the infection burden in masters athletes. Fourth, we present important research ndings on the association between exercise, nutrition and the microbiota, which represents a rapidly developing eld in sports nutrition. Keywords: aging; cardiorespiratory system; exercise; hormones; masters athletes; muscle; nutrition; protein 1. Introduction Nutrition and physical activity (PA) are the two main modi able factors that deter- mine health and well-being in modern civilization. These two factors are often studied and considered as separate entities, although they are, in reality, inter-related in various ways. To give some examples of this interplay, PA can shift the nutrient spectrum that human metabolism utilizes; lack of PA leads to accumulation of ectopic fat in liver, muscle, and potentially other organs [1,2]; malnutrition hampers physical and mental performance; Nutrients2021,13, 1409.

Nutrients2021,13, 1409 2 of 34 overfeeding leads to expansion of fat deposits, thus increasing body inertia and deterio- rating physical tness [3]. One motivation for this review, therefore, is to raise awareness of the interplay between nutrition and PA/performance for readers with either of the two backgrounds. The topic of diet and PA becomes particularly relevant in combination with aging, as aging is generally associated with generalized in ammation and exaggerated disease burden [4]. Ample evidence suggests that regular exercise and optimized nutrition can help to reduce disease burden [5–7]. Therefore, the World Health Organization (WHO) has taken action to promote PA across the entire age spectrum [8], and many governments have developed national strategies also with the interest to mitigate age-related morbidity. However, older people become typically more and more sedentary with increasing age, and it is often challenging to engage them in regular physical exercise. In this sense, masters athletes can offer interesting insights. These people train for and compete in athletic events beyond the typical age of retirement from sports. Many of them follow rigorous training regimens, often over decades or even their entire adult life. Beyond their intrinsic motivation to be physically active, they are driven by the desire to excel in sports, but also to maintain their health. The scienti c literature has long neglected this topic, and only the past decade has seen an increasing number of publications on all aspects of masters athletics (Figure).Nutrients 2021, 13, x FOR PEER REVIEW 2 of 35 deteriorating physical fitness [3]. One motivation for this review, therefore, is to raise awareness of the interplay between nutrition and PA/performance for readers with either of the two backgrounds. The topic of diet and PA becomes particularly relevant in combination with aging, as aging is generally associated with generalized inflammation and exaggerated disease bur- den [4]. Ample evidence suggests that regular exercise and optimized nutrition can help to reduce disease burden [5–7]. Therefore, the World Health Organization (WHO) has taken action to promote PA across the entire age spectrum [8], and many governments have developed national strategies also with the

with aging, as aging is generally associated with generalized inflammation and exaggerated disease bur- den [4]. Ample evidence suggests that regular exercise and optimized nutrition can help to reduce disease burden [5–7]. Therefore, the World Health Organization (WHO) has taken action to promote PA across the entire age spectrum [8], and many governments have developed national strategies also with the interest to mitigate age-related morbid- ity. However, older people become typically more and more sedentary with increasing age, and it is often challenging to engage them in regular physical exercise. In this sense, masters athletes can offer interesting insights. These people train for and compete in athletic events beyond the typical age of retirement from sports. Many of them follow rigorous training regimens, often over decades or even their entire adult life. Beyond their intrinsic motivation to be physically active, they are driven by the desire to excel in sports, but also to maintain their health. The scientific literature has long neglected this topic, and only the past decade has seen an increasing number of publications on all aspects of masters athletics (Figure 1). Figure 1. Publications on masters athletes, plotted against year of publication. Date are the result of a literature research on public Medline on 1 October 2021, using the following search terms: ((master athlete (Title/Abstract)) OR (masters athlete (Title/Abstract)) OR (veteran athlete (Title/Abstract)). Naturally, a plethora of questions arise with regard to the nutritional support for these aging athletes. Thus, as with any athlete, also the masters athletes wish to reduce their body fat, in order to optimize athletic performance. But what are the energetic re- quirements, given that resting metabolic rate (RMR) typically dwindles with age? How can the requirements for the intake of protein, vitamins and other micronutrients be met Figure 1. Publications on masters athletes, plotted against year of publication. Date are the result of a literature research on public Medline on 1 October 2021, using the following search terms: ((master athlete (Title/Abstract)) OR (masters athlete (Title/Abstract)) OR (veteran athlete (Title/Abstract)). Naturally, a plethora of questions arise with regard to the nutritional support for

and other micronutrients be met Figure 1. Publications on masters athletes, plotted against year of publication. Date are the result of a literature research on public Medline on 1 October 2021, using the following search terms: ((master athlete (Title/Abstract)) OR (masters athlete (Title/Abstract)) OR (veteran athlete (Title/Abstract)). Naturally, a plethora of questions arise with regard to the nutritional support for these aging athletes. Thus, as with any athlete, also the masters athletes wish to reduce their body fat, in order to optimize athletic performance. But what are the energetic re-

Nutrients2021,13, 1409 3 of 34 quirements, given that resting metabolic rate (RMR) typically dwindles with age? How can the requirements for the intake of protein, vitamins and other micronutrients be met when the total intake is reduced for the sake of body composition? Which nutrients are physiologically opportune for optimized performance, and which ones should be recommended to facilitate recovery and prevention of injury? The eld of nutritional support for athletes has traditionally focused on young elite athletes, and there is no clear answer to these and other questions pertinent to the topic. Hence, the present paper attempts to collate the relevant information in order to (a) provide recommen- dations where evidence is available, and to (b) ag the most important open question for future research. 2. Physiological Changes in Older Athletes 2.1. Oxygen Delivery and Utilization Systems The exercising skeletal muscles rely on continuous oxygen supply that is precisely matched to the metabolic requirements of the exercise intensity. If, at any intensity, the oxygen supply becomes limited, anaerobic metabolism compensates for the lacking oxygen, indicated by increasing lactate concentration [9,10]. Oxygen has to be transported from the ambient air to the oxygen-respiring mitochondria of the working muscles. This is involving a series of steps, namely oxygen diffusion (driven by the existing pressure gradient) from the alveoli into the pulmonary capillary blood, the oxygenated blood (oxygen is primarily bound to hemoglobin) is pumped by the heart to the skeletal muscles, where oxygen is converted to adenosine triphosphate (ATP), providing energy to power the working muscles (Figure). Oxygen delivery (DO 2) to the muscles is determined by the cardiac output (heart rate x stroke volume, Q), the hemoglobin concentration (Hb) and the level of its saturation (SaO2), according to the equation: DO2= Q Hb SaO2 K K indicates the Hüfner coefficient for hemoglobin-oxygen binding capacity which is 1.33 mL/g.Nutrients 2021, 13, x FOR PEER REVIEW 3 of 35 when the total intake is reduced for the sake of body composition? Which nutrients are physiologically opportune for optimized performance, and which ones should be recom- mended to facilitate recovery and prevention of

DO2= Q Hb SaO2 K K indicates the Hüfner coefficient for hemoglobin-oxygen binding capacity which is 1.33 mL/g.Nutrients 2021, 13, x FOR PEER REVIEW 3 of 35 when the total intake is reduced for the sake of body composition? Which nutrients are physiologically opportune for optimized performance, and which ones should be recom- mended to facilitate recovery and prevention of injury? The field of nutritional support for athletes has traditionally focused on young elite athletes, and there is no clear answer to these and other questions pertinent to the topic. Hence, the present paper attempts to collate the relevant information in order to (a) provide recommendations where evidence is available, and to (b) flag the most important open question for future research. 2. Physiological Changes in Older Athletes 2.1. Oxygen Delivery and Utilization Systems The exercising skeletal muscles rely on continuous oxygen supply that is precisely matched to the metabolic requirements of the exercise intensity. If, at any intensity, the oxygen supply becomes limited, anaerobic metabolism compensates for the lacking oxy- gen, indicated by increasing lactate concentration [9,10]. Oxygen has to be transported from the ambient air to the oxygen-respiring mitochondria of the working muscles. This is involving a series of steps, namely oxygen diffusion (driven by the existing pressure gradient) from the alveoli into the pulmonary capillary blood, the oxygenated blood (ox- ygen is primarily bound to hemoglobin) is pumped by the heart to the skeletal muscles, where oxygen is converted to adenosine triphosphate (ATP), providing energy to power the working muscles (Figure 2). Oxygen delivery (DO 2) to the muscles is determined by the cardiac output (heart rate x stroke volume, Q), the hemoglobin concentration (Hb) and the level of its saturation (SaO 2), according to the equation: DO 2 = Q × Hb × SaO2 × K K indicates the Hüfner coefficient for hemoglobin-oxygen binding capacity which is 1.33 mL/g. The extraction of oxygen utilized by the mitochondria is represented by the arterio- venous oxygen difference (a-v O 2 difference). As the need for oxygen is increasing with increasing exercise intensity, minute ventilation, cardiac output, muscle perfusion

DO 2 = Q × Hb × SaO2 × K K indicates the Hüfner coefficient for hemoglobin-oxygen binding capacity which is 1.33 mL/g. The extraction of oxygen utilized by the mitochondria is represented by the arterio- venous oxygen difference (a-v O 2 difference). As the need for oxygen is increasing with increasing exercise intensity, minute ventilation, cardiac output, muscle perfusion and ox- ygen extraction all have to increase. According to the Fick principle for individual aerobic capacity, the highest achievable rate of oxygen uptake (VO 2max) equals Q × a-v O2 extrac- tion. All organs involved in oxygen transport and utilization may contribute to VO 2max decline in the aging athlete. Figure 2. The lung–heart–muscle axis involved in oxygen delivery and utilization. Main cardi- orespiratory parameters specifying organ function at rest and during exercise: minute ventilation (VE), cardiac output (Q), and oxygen extraction in the skeletal muscle. Parameters listed below the Figure 2. The lung–heart–muscle axis involved in oxygen delivery and utilization. Main cardiores- piratory parameters specifying organ function at rest and during exercise: minute ventilation (VE), cardiac output (Q), and oxygen extraction in the skeletal muscle. Parameters listed below the organs represent those which are primarily affected by the aging process. Oxygen, O 2; carbon dioxide, CO 2; tidal volume, VT; breathing frequency, Bf; hemoglobin concentration, Hb; arterial oxygen saturation, SaO 2; heart rate, HR; adenosine triphosphate, ATP.

Nutrients2021,13, 1409 4 of 34 The extraction of oxygen utilized by the mitochondria is represented by the arterio- venous oxygen difference (a-v O2difference). As the need for oxygen is increasing with increasing exercise intensity, minute ventilation, cardiac output, muscle perfusion and oxygen extraction all have to increase. According to the Fick principle for individual aerobic capacity, the highest achievable rate of oxygen uptake (VO2max) equals Q a-v O2extraction. All organs involved in oxygen transport and utilization may contribute to VO2max decline in the aging athlete. 2.1.1. The Pulmonary System Although data on the breathing reserve (BR; maximal voluntary ventilation related to minute ventilation during maximal exercise) do not indicate a considerable ventilatory limitation of VO2max in healthy older individuals [11], it can become a limiting factor in some highly trained aged athletes [12]. In addition, diffusion capacity of the lung is predictive of marathon performance, and it decreases markedly with age, an effect from which masters athletes are not exempt [13]. Probably as a consequence of this, exercise- induced hypoxemia is more prevalent in highly t older individuals compared to the healthy general population and fatiguing work of the respiratory muscles may provoke vasoconstriction in the leg muscles and compromise Q [14]. Thus, VO2max restriction by the pulmonary system depends on the level of tness (the higher the more likely) and the age-related degree of decrease in respiratory function along with structural changes, i.e., declining respiratory muscle strength and endurance, enhanced rigidity of the chest wall, loss of elastic recoil, reduction of the alveolar surface area and the number of capillaries perfusing the lung [11,15,16]. A low BR, reduced forced expiratory volume in one second (FEV1) and exercise-induced hypoxemia are potential markers for pulmonary limitations of VO2max in the older athlete [17] (Figure). 2.1.2. The Cardiovascular System It is obvious that a precise interplay between pulmonary ventilation, DO2and the extraction of oxygen by the muscle tissue is a prerequisite for properly matching oxygen need and demand. The contribution of the cardiovascular system, in particular Qmax, is considered as the main determinant of VO2max in young people when including large skeletal

athlete [17] (Figure). 2.1.2. The Cardiovascular System It is obvious that a precise interplay between pulmonary ventilation, DO2and the extraction of oxygen by the muscle tissue is a prerequisite for properly matching oxygen need and demand. The contribution of the cardiovascular system, in particular Qmax, is considered as the main determinant of VO2max in young people when including large skeletal muscle groups, e.g., leg cycling, running or cross-country skiing [18,19]. The demand of oxygen by these working muscles increases tremendously (about 10 to 20-fold, depending on the individual tness) from rest to maximal work [10]. Consequently, a large amount of oxygenated blood has to be transported to muscles driven by the pumping heart. Thus, a 72% contribution of Qmax to VO2max changes has been demonstrated in sedentary young and older subjects of both sexes, and the Qmax increased to 81–89% in trained young and older subjects of both sexes [18]. The age-related decrease in cardiovascular function (particularly decline of Q which is HR x SV) will considerably affect VO2max. HRmax decreases according to the formula (208 (beats per min)—0.7 age) in healthy sedentary and trained subjects, probably due to the decrease in intrinsic heart rate [20]. In addition, lower SV associated with reduced left ventricular (LV) compliance (diminished diastolic function) was shown in healthy sedentary people but seems to be preserved in masters athletes [21]. Impaired ability to modulate sympathetic vasoconstrictor activity (functional sympatholysis) and a reduced exercise hyperemia are also characteristics of aging. Again, regular PA was shown to offset these impairments [22]. 2.1.3. Skeletal Muscle and Mitochondria Capillarization of skeletal muscles and muscle oxidative capacity decrease likewise with aging at least in rather sedentary subjects [23,24]. However, long-term engaging in endurance sports can largely prevent the reduction in muscle capillarization and muscle oxidative enzymatic activity with aging, e.g., in 65- to 75-year-old athletes [25]. The oxida- tive capacity of skeletal muscles is not considered as an important limitation of VO2max because it exceeds the amount of oxygen consumed during whole body exercise [26]. Thus,

muscle capillarization and muscle oxidative enzymatic activity with aging, e.g., in 65- to 75-year-old athletes [25]. The oxida- tive capacity of skeletal muscles is not considered as an important limitation of VO2max because it exceeds the amount of oxygen consumed during whole body exercise [26]. Thus,

Nutrients2021,13, 1409 5 of 34 bene ts of regular training on adaptations in the skeletal muscle rather promote improved submaximal exercise performance than VO2max. Such adaptations include increases in capillary supply and mitochondrial key enzyme activities favoring a higher rate of fat oxidation and a concomitant reduction in the glycolytic ux, as well as a tighter control of the acid-base status [10]. Consequently, the anaerobic threshold (submaximal endurance performance) declines at a slower rate with aging (especially in trained individuals) than VO2max [27,28]. A noteworthy observation is the inverse relationship between mechanical ef ciency and VO2max (shown in elite cyclers), which was attributed to variations in the amount of ef cient type I and less ef cient type II bers of working muscles [29]. 2.2. Body Composition and Metabolism Although aging is generally associated with a loss of lean muscle mass, exercise can modulate such losses. According to population-based studies, the prevalence of sarcopenia in healthy adults aged 60 years and older is about 10% for men and 10% for women, respectively [30]. Intriguingly, in a cross-sectional study including 156 female and male masters athletes aged between 40–79 years, no individual was categorized as sarcopenic, i.e., below normal levels of muscle mass and muscle strength or performance, according to the de nition of the European Working Group for Sarcopenia in Older People [31,32]. Data from cross-sectional studies indicate that lean muscle mass and muscle strength did not decline with age in individuals aged 40–81 years who trained 4 to 5 times per week [33]. These data could indicate that declines in physical function may not be related to age alone but are rather confounded by muscle disuse and decreased levels of PA in the elderly general population [34]. On the other hand, two previous cross-sectional studies based on an anthropometric assessment of lower limb muscle volume [35] in male 115 track and eld masters [36] and in 54 male master weight lifters [37] indicated a volume reduction of approximately 6% per age decade. This gure has been con rmed by a recent longitudinal study in 71 track-and- eld master athletes

Review on nutrition and physiological changes in older athletes, focusing on sex differences.