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Findings on sperm alterations and DNA fragmentation, nutritional, hormonal and antioxidant status in an elite triathlete. Case report
Hallazgo de alteraciones en semen, nutricionales, hormonales, del estado antioxidante y fragmentación de ADN en un triatleta de élite. Caso clínico
Descoberta das alterações no sêmen, nutricionais, hormonais, o antioxidante status e fragmentação de DNA em triatleta de elite. Relato do caso
D. Vaamondea,
Corresponding author
, M.E. Da Silva-Grigolettob,c, J.M. Fernandezd, C. Algar-Santacruzc,d, J.M. García-Mansoe
a Morphological Sciences Department, School of Medicine, University of Cordoba, Spain
b Departamento de Educação Física, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe, Brazil
c Scientific Sport Association, Cordoba, Spain
d Nutrir, Nutrición Médica y Ejercicio, Cordoba, Spain
e Physical Education Department, School of Physical Activity and Sport Sciences, University of Las Palmas de Gran Canaria, Spain
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          "en" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Fluorescence and bright field microscopy images&#46; A macrophage can be seen along with several abnormal sperm in bright field &#40;A&#41;&#46; Fluorescence microscopy shows&#44; in the same field&#44; how several of these sperm cells are undergoing necrosis&#59; moreover&#44; several sperm cells &#40;red color&#41; have been phagocitized by the macrophage &#40;B&#41;&#46; &#40;For interpretation of the references to color in this figure legend&#44; the reader is referred to the web version of this article&#46;&#41;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">It has been recently postulated that exhaustive endurance exercise may be a factor altering the seminological and hormonal profiles in elite athletes&#46; Triathlon competition imposes great physical and mental demands on the athletes&#44; forcing them to undergo high training loads and long-duration competitions&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The Ironman is certainly one of the most extenuating competitions&#44; with athletes spending between 9 and 10<span class="elsevierStyleHsp" style=""></span>h in order to complete a 3&#46;86<span class="elsevierStyleHsp" style=""></span>km-swim&#44; 180<span class="elsevierStyleHsp" style=""></span>km-cycling&#44; and 42&#46;2<span class="elsevierStyleHsp" style=""></span>km-run&#46; Athletes aim in this competition to achieve the best possible position and scores&#46; As a result of the high training loads used by the triathletes&#44; the organism undergoes great physical and mental stress&#46; Moreover&#44; physical training may produce negative physiological changes that may lead to overreaching&#47;overtraining status&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">There are many studies that report a relationship between intense endurance exercise and hormonal &#40;suprarenal and gonadal&#41; and semen alterations&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> From the studies&#44; it has been observed that training volume is one of the characteristics most exerting an influence on hormone and semen parameters&#46; Some authors have even established a theory of a volume-threshold&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Previous studies have related triathlon practice to semen alterations&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#44;6</span></a> This relationship has been observed to be related to training volume&#46; However&#44; studies have suggested that training intensity may also be deleterious for hormone and semen profiles and may induce an oxidative status&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;8</span></a> Moreover&#44; inappropriate nutrition may also influence these parameters&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In line with this&#44; we have assessed semen&#44; hormone and total antioxidant capacity values in a high-intensity elite triathlete as well as careful nutritional surveillance in order to determine any possible alterations in the reproductive profile of this particular athlete&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Method</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Subject</span><p id="par0025" class="elsevierStylePara elsevierViewall">The athlete&#44; who was 26 years old&#44; had a VO<span class="elsevierStyleInf">2max</span> of 72&#46;11<span class="elsevierStyleHsp" style=""></span>ml&#47;kg&#47;min&#44; as measured by a gas analyzer &#40;Erich Jaeger&#44; Viasys Healthcare&#44; Germany&#41;&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">His mean annual weekly training regime is as follows&#58; 15<span class="elsevierStyleHsp" style=""></span>km of swimming&#44; 155&#46;4<span class="elsevierStyleHsp" style=""></span>km of cycling&#44; and 30<span class="elsevierStyleHsp" style=""></span>km of running&#46; With regards to cycling alone&#44; his mean annual weekly training characteristics were as follow&#58; 18&#46;5<span class="elsevierStyleHsp" style=""></span>h and a total covered distance of 155&#46;4<span class="elsevierStyleHsp" style=""></span>km&#46; His mean training values for the last week of training were&#44; therefore&#44; diminished in comparison to the mean annual values &#40;4&#46;1<span class="elsevierStyleHsp" style=""></span>km of swimming&#44; 112&#46;8<span class="elsevierStyleHsp" style=""></span>km of cycling&#44; and 14<span class="elsevierStyleHsp" style=""></span>km of running&#41;&#46; Due to the athlete&#39;s own training regime&#44; he had not performed any cycling in the week of the testing &#40;performed on a Wednesday&#41;&#46; The intensity at which the athlete trained in the three different disciplines is as follows&#58; 75&#37; of maximum HR for swimming&#44; 75&#37; for cycling&#44; and 68&#37; for running&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">It has to be mentioned that the athlete completed a detailed fertility questionnaire which did not reveal any possible previous fertility-related issues&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Procedures</span><p id="par0040" class="elsevierStylePara elsevierViewall">The athlete underwent complete physical exam as well as completed a fertility&#44; a training and a nutritional questionnaire&#46; Routine blood analysis was performed with normal results for all common biochemical and physiological parameters &#40;no iron or zinc deficiency&#44; cholesterol&#44; 25-hydroxyvitamin D or glycemic alterations&#41;&#46; Semen&#44; hormone&#44; total antioxidant capacity &#40;TAC&#41;&#44; nutritional habits and training parameters were carefully analyzed&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">With regards to training&#44; the athlete was in a tapering period preparing for a non-official competition&#46; As previously described&#44; the week before testing was characterized by a low volume training&#46; All testing and questionnaires were done on the same day&#46; The athlete collected semen and afterwards he gave the saliva sample and answered the nutritional questionnaire&#46; For better semen characterization&#44; he gave another semen sample 3 days later&#46; He was asked to drastically lower the load 2 days before sample collection&#44; and to avoid any cycling exercise&#46; Moreover&#44; the day before the testing&#44; he decreased training volume to 50&#37; of the total of that week&#39;s volume&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Semen analysis</span><p id="par0050" class="elsevierStylePara elsevierViewall">The athlete kept the required abstinence for adequate sample collection &#40;4 days&#41;&#46; World Health Organization &#40;WHO&#41; values for volume&#44; number and velocity were chosen for sample normality assessment&#44; while Kruger&#39;s strict criteria were chosen for morphology normality assessment&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> Total motility &#40;PR&#43;NP&#41; was assessed and motility was graded as follows&#58; progressive motility &#40;PR&#41;&#44; non-progressive motility &#40;NP&#41; and immotile sperm &#40;IM&#41;&#46; For determination of leucocytes in the sample the leucoscreen test was used &#40;Fertipro&#44; Belgium&#41;&#46; For morphology&#44; two sperm smears were stained &#40;Diff Quick&#44; Panreac&#44; Barcelona&#44; Spain&#41; and observed at 100&#215; under oil&#46; DNA fragmentation evaluation was performed using a sperm chromatin dispersion test &#40;Halosperm<span class="elsevierStyleSup">&#174;</span>&#44; Halotech DNA S&#46;L&#46;&#44; Madrid&#44; Spain&#41;&#46; Apoptosis and necrosis determination was performed using the Annexin V testing &#40;Miltenyi Biotec&#44; Germany&#41; and observing sperm with a fluorescence microscope&#46; TAC determination was performed in seminal plasma after centrifugation by ELISA with commercially available kits &#40;Cayman Chemical&#44; Michigan&#44; USA&#41;&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Hormone analysis</span><p id="par0055" class="elsevierStylePara elsevierViewall">For saliva collection&#44; the athlete avoided any food or caffeine products for a period of at least 2<span class="elsevierStyleHsp" style=""></span>h before sampling&#46; Saliva collection was performed by inserting a collection pad inside the athlete&#39;s mouth and keeping it inside the mouth to absorb saliva during 2<span class="elsevierStyleHsp" style=""></span>min&#46; Afterwards&#44; the pad was removed and stored at &#8722;80<span class="elsevierStyleHsp" style=""></span>&#176;C until assayed&#46; Commercial kits for nonradioactive ELISA were used for hormonal assessment &#40;Salivary Testosterone EIA Kit and Salivary Cortisol EIA Kit&#44; Salimetrics LLC&#44; Suffolk&#44; UK&#41;&#46; Sensitivity was &#60;0&#46;003<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;dL for <span class="elsevierStyleItalic">Cs</span> and 1<span class="elsevierStyleHsp" style=""></span>pg&#47;ml for <span class="elsevierStyleItalic">Ts</span>&#46; With regards to reproducibility of measures&#44; the ICC was 0&#46;8 for <span class="elsevierStyleItalic">Ts</span> and 0&#46;78 for <span class="elsevierStyleItalic">Cs</span>&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Nutritional analysis</span><p id="par0060" class="elsevierStylePara elsevierViewall">The material used for data collection and analysis with regards to the nutritional intake was based on the completion of a food frequency questionnaire&#44; using a computerized support&#44; and an individual personal interview&#44; the purpose of which is to gather knowledge on the dietary habits before&#44; during and after training for the studied athlete&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">In order to assess the athlete&#39;s nutrition&#44; he was asked to complete&#44; during a personalized interview&#44; a food frequency survey obtained from the &#8220;<span class="elsevierStyleItalic">Study Predimed&#46; Nodo Pamplona AP-UNAV&#46; Epidemiology and Public Health&#44; University of Navarra</span>&#8221;&#46; By means of this survey&#44; knowledge is obtained about which foods are eaten&#44; how frequently and in what quantity&#46; The survey consists of 136 foods divided into seven groups &#40;dairy&#44; vegetables&#44; eggs&#8211;meats&#8211;fish&#44; fruits&#44; cereals&#8211;vegetables&#44; oils and fats&#44; and miscellaneous&#41;&#44; asking the athlete to refer his daily&#44; weekly and monthly intake of each one of them and even three seasonal categories can be differentiated &#40;Spring&#44; Fall&#8211;Winter and Summer&#41; for better assess met due to seasonal differences in obtaining certain foods&#46; In addition&#44; a manual with pictures of different foods and dishes&#44;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">11</span></a> and food replicas were used&#46; With all these data&#44; the portion size of each food consumed by the athlete was established so as to later determine the amount ingested&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">These surveys have been analyzed with the software V&#46;2&#46;0 Dietsource TM obtaining final data on micronutrients&#44; macronutrients and energy for the triathlete&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Results</span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">Semen and hormone values</span><p id="par0075" class="elsevierStylePara elsevierViewall">Values for semen physical parameters were within normal ranges&#44; as well as values for sperm concentration and velocity&#46; However&#44; both morphology and DNA fragmentation showed abnormal values &#40;3&#46;9&#37; and 38&#46;33&#37; respectively&#41;&#46; Moreover&#44; it was observed that the presence of round cells in semen was higher than normal &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Active macrophages were found to be present in the semen sample &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Hormonal values were within normal&#46; <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> also shows the values for TAC from seminal plasmas as well as the values obtained for salivary testosterone&#44; salivary cortisol&#44; and the <span class="elsevierStyleItalic">T</span>&#47;<span class="elsevierStyleItalic">C</span> ratio resulting from both hormones&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Nutritional values</span><p id="par0080" class="elsevierStylePara elsevierViewall">After analyzing the different dietary data obtained from the interview with the athlete&#44; the following observations were found &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#44; indicating an overall suitable nutritional intake for the requirements for the kind of the athlete studied&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Discussion</span><p id="par0085" class="elsevierStylePara elsevierViewall">The main finding of the present study is an altered value for sperm morphology and sperm DNA fragmentation despite adequate testosterone value and nutrition and TAC values&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Several studies have shown a potential relationship of exercise to hormonal and seminological alterations&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#8211;7</span></a> The characteristics observed in the present case seem to be in accordance with previously published observations&#44;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#8211;7&#44;12</span></a> the triathlete did not show any alterations for sperm number or velocity but showed significant alterations in sperm morphology and a great degree of sperm DNA fragmentation&#46; Significant alterations in morphology and sperm DNA fragmentation have been correlated with longer times to conception and less chances of live birth&#46;<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13&#44;14</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">In the present case&#44; the athlete is characterized by performing a high-intensity&#44; low-volume training&#59; when his training is compared to other triathletes is notorious his priority is intensity rather than volume&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Testosterone is essential for proper spermatogenesis to occur&#46; Our triathlete showed testosterone levels within the normal range for healthy male adults&#44; although somewhat lower than the values reported for other sports modalities&#44; especially with regards to strength sports&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Yet it has also been documented that Ironman competitors&#44; and even other endurance athletes &#40;running&#44; cycling&#44; rowing&#44; swimming&#41;&#44; may present lowered testosterone values&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> especially immediately after competition&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a></p><p id="par0105" class="elsevierStylePara elsevierViewall">Although endurance athletes may have <span class="elsevierStyleItalic">T</span> values below normal range&#44;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> the triathlete in this study showed normal values&#44; even greater than those observed in other triathletes&#59; this may be because he is characterized by a high-intensity training&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Intensity defined as &#8220;high-intensity training&#8221; has been shown to be the key factor in modulating endocrine response as increase in <span class="elsevierStyleItalic">T</span> and decrease in <span class="elsevierStyleItalic">C</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Moreover&#44; an increase in salivary <span class="elsevierStyleItalic">T</span> could be associated with a greater metabolic efficiency toward the pre-competition and competition phases&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> Zahavi and Perel<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> reported an improvement in the efficiency of the mitochondrial proton pump when producing ATP&#44; despite suggesting that this metabolic advantage could be associated to an increase in oxidative damage&#46; The fact that TAC values are somewhat low&#44; can refer to the subject not having an appropriate antioxidant defense and&#44; therefore&#44; he may not be able to mitigate the oxidative damage&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">In highly trained male athletes&#44; as in female athletes<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> exercise is usually associated with a decrease in the hypothalamic&#8211;pituitary&#8211;suprarrenal axis&#44; although basal cortisol levels are usually greater than normal&#44; reflecting a chronic response to training&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">Macrophage presence was observed in the athlete&#39;s semen&#46; Although macrophages should not be present in semen&#44; phosphatidylserine exposure&#44; like in the case of apoptotic cells&#44; serves as a triggering signal for macrophages<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a>&#59; this may also be true for removing defective sperm&#59; in fact&#44; some authors have reported presence of macrophages along impaired sperm parameters in men&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> Macrophages may&#44; thus&#44; have a function in the differentiated tissues of the reproductive system&#46; In this regard&#44; we have observed high numbers of sperm with morphological anomalies as well as with fragmented DNA and undergoing apoptosis and necrosis&#46; Other authors have observed a direct relationship between the presence of macrophages and the number of sperm exhibiting denatured DNA&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> High-load endurance training promotes the appearance of muscle injury markers along with an increased white cell count in blood&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> During inflammation&#44; additional circulating macrophages help testes-residing macrophages by arriving and invading the site of inflammation&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">Nonetheless&#44; the number of round cells is elevated&#44; with the presence not only of macrophages and other leucoytic cells but also a greater than normal presence of germinal cells&#46; This fact may indicate a moderate alteration of spermatogenesis&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">When analyzing the micronutrient intake with regards established recommendations&#44;<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">9&#44;28&#44;29</span></a> it can be observed that the athlete has a deficit in the intake of calcium&#44; iodine and vitamin B12&#44; as shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; In addition&#44; it can be observed there is a high consumption of Niacin&#44; Riboflavin &#40;Vitamin B2&#41;&#44; Vitamin B6&#44; Vitamin C&#44; Folate and Vitamin E&#44; Iron and Zinc&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The observed excess can lead to oxidative DNA damage in testicular and epididymal sperm&#44; as well as a significant increase in 8-oxodG&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> Especially&#44; an accumulation of certain minerals&#44; such as iron and zinc&#44; can produce damage in sperm and other reproduction-related cells&#44; as well as degeneration of the germinal epithelium of the testes&#44; multinucleated giant cell formation&#44; and lack of mature sperm&#44; along with a decrease in spermatogenesis and sperm motility with subsequent reduction of fertility&#46;<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">31&#44;32</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">The intake and use of vitamin C and vitamin E &#40;with different modes of action&#41; as antioxidants should be carefully considered because&#44; even though they have a protective effect on the polyunsaturated acids &#40;PUFAs&#41; present in the sperm membrane<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> with a subsequent improvement in sperm function&#44; in some cases &#40;with the concurrent presence of metals such as Fe and Cu&#44; etc&#46;&#41; these vitamins can act as potent prooxidants&#46; In fact&#44; it has been reported that continued Vitamin C supplementation in athletes may alter performance and elevate oxidative markers&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> In the present case&#44; the athlete showed an elevated intake of both vitamin C and Iron and this imbalance may lead to a pro-oxidative state&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">The macronutrients intake analysis reveals high protein intake and&#44; to a lesser extent&#44; of carbohydrates&#46; High consumption of meat and dairy products has been associated with the incorporation of xenoestrogens&#44; powerful endocrine disruptors&#44; and thus to a deterioration in semen quality&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> Overall daily energy intake for this athlete is estimated at 4311&#46;28<span class="elsevierStyleHsp" style=""></span>kcal&#47;day&#46; Although this energy value is much higher than for normal individuals&#44; it is adequate for a high-level athlete&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">In the present case&#44; it can be observed how training load&#44; even if training volume is not high&#44; promotes alterations in semen parameters and leucocytic profiles&#46; Sperm DNA fragmentation&#44; as well as morphology&#44; are affected by high-intensity endurance exercise&#46; Further studies are needed to clarify this fact and to seek for preventive measures in this specific population&#46; Moreover&#44; even though nutrition seems to be appropriate&#44; despite slight excess and deficiency of some specific nutrients and a slight excess protein intake&#44; this parameter needs to be further assessed with regards to the relation of exercise and fertility&#46; Moreover&#44; appropriate nutritional strategies should be assessed for avoiding the deleterious effects on the reproductive system that are associated to sports practice&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Financial support</span><p id="par0155" class="elsevierStylePara elsevierViewall">Grant &#40;IMD2010SC0001&#41; from the <span class="elsevierStyleGrantSponsor" id="gs1">Consejeria de Turismo&#44; Comercio y Deporte de la Junta de Andalucia</span>&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0155">Conflict of interest</span><p id="par0160" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Objective</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The present case study analyzes semen quality&#44; nutritional patterns&#44; and hormonal and oxidative status of an international high-level triathlete with a low-volume&#44; high-intensity training load&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Method</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The athlete was 26 years old&#44; having participated in competitions since he was 13 years old&#44; and practiced professional triathlon for the last five years&#46; The qualitative sperm parameters analyzed were volume&#44; sperm count&#44; motility&#44; morphology&#44; and DNA fragmentation &#40;additional testing performed as needed&#41;&#46; Salivary hormones measured were <span class="elsevierStyleItalic">T</span>&#44; <span class="elsevierStyleItalic">C</span>&#44; and <span class="elsevierStyleItalic">T</span>&#47;<span class="elsevierStyleItalic">C</span>&#46; Seminal plasma total antioxidant capacity was measured&#46; Maximum oxygen consumption and training characteristics were assessed&#46; To determine habitual food intake and its possible repercussion on oxidative status&#44; a quali-quantitative frequency questionnaire of 136 different foods was used and subsequently analyzed using specific software&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Hormonal and physical semen parameters were within normal ranges&#46; Sperm morphology and DNA fragmentation showed abnormal values &#40;3&#46;9&#37; and 38&#46;33&#37;&#41;&#46; Round cells in semen were higher than normal &#40;2&#46;3<span class="elsevierStyleHsp" style=""></span>million&#47;ml&#41;&#44; with presence of macrophages&#46; Apoptotic and necrotic events were observed&#46; Total antioxidant capacity&#44; although not compromised&#44; was low&#46; Dietetic intake was characterized by excess protein and appropriate overall antioxidant intake &#40;with slight deficit and excess of some specific nutrients&#41; according to recommended values&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">In this high-intensity endurance athlete&#44; sperm parameters&#44; mainly sperm morphology and DNA fragmentation&#44; are altered&#46; Further knowledge is needed with regards nutritional antioxidant intake and other dietetic strategies oriented toward avoiding oxidative damage in semen of high-performance triathletes&#46; Moreover&#44; adequate nutritional strategies must be found and nutritional advice given to athletes so as to palliate or dampen the effects of exercise on semen quality&#46;</p></span>"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Objetivo</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El presente estudio de caso analiza la calidad de semen&#44; patrones nutricionales y status hormonal y oxidativo de un triatleta internacional de alto nivel con carga de entrenamiento de bajo volumen y alta intensidad&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todo</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Atleta de 26 a&#241;os de edad&#44; con una pr&#225;ctica deportiva competitiva desde los 13 a&#241;os&#44; y cinco a&#241;os de triatl&#243;n profesional&#46; Los par&#225;metros cualitativos analizados en semen fueron&#58; volumen&#44; contaje esperm&#225;tico&#44; motilidad&#44; morfolog&#237;a&#44; y fragmentaci&#243;n de ADN&#44; con pruebas adicionales seg&#250;n necesidad&#46; Las hormonas salivares cuantificadas fueron&#58; T&#44; C&#44; y T&#47;C&#46; La capacidad antioxidante total fue medida en plasma seminal&#46; Tambi&#233;n se analiz&#243; el consumo m&#225;ximo de ox&#237;geno y caracter&#237;sticas de entrenamiento&#46; Para determinar la ingesta alimentaria habitual y su posible repercusi&#243;n sobre el estado oxidativo&#44; se utiliz&#243; un cuestionario de frecuencia de consumo cuali-cuantitativa&#44; de 136 alimentos&#44; analizado mediante software inform&#225;tico&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Los valores hormonales y par&#225;metros f&#237;sicos seminales estaban dentro de la normalidad&#46; La morfolog&#237;a y fragmentaci&#243;n de ADN esperm&#225;tico mostraron valores anormales &#40;3&#46;9&#37; y 38&#46;33&#37;&#41;&#46; Aparec&#237;a un elevado n&#250;mero de c&#233;lulas redondas &#40;2&#46;3 millones&#47;mL&#41;&#44; con presencia de macr&#243;fagos&#46; Se observaron eventos apopt&#243;ticos y necr&#243;ticos&#46; La capacidad antioxidante total&#44; aunque no alterada&#44; estaba baja&#46; La ingesta diet&#233;tica se caracteriz&#243; por un exceso proteico y consumo adecuado de antioxidantes &#40;con ligero d&#233;ficit y exceso de algunos nutrientes espec&#237;ficos&#41;&#44; seg&#250;n valores recomendados&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">El ejercicio de resistencia de alta intensidad altera los par&#225;metros esperm&#225;ticos&#44; principalmente morfolog&#237;a y fragmentaci&#243;n de ADN&#46; Es necesario obtener mayor informaci&#243;n sobre el efecto de antioxidantes y otras estrategias diet&#233;ticas con relaci&#243;n al da&#241;o oxidativo en el semen de triatletas de alto rendimiento&#44; al igual que hallar estrategias nutricionales adecuadas para paliar o amortiguar los efectos del ejercicio sobre la calidad del semen&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0025"
            "titulo" => "Objetivo"
          ]
          1 => array:2 [
            "identificador" => "abst0030"
            "titulo" => "M&#233;todo"
          ]
          2 => array:2 [
            "identificador" => "abst0035"
            "titulo" => "Resultados"
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          3 => array:2 [
            "identificador" => "abst0040"
            "titulo" => "Conclusiones"
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      "pt" => array:3 [
        "titulo" => "Resumo"
        "resumen" => "<span id="abst0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Objetivo</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">O presente estudo de caso analisa a qualidade de s&#234;men&#44; padr&#245;es nutricionais&#44; estado hormonal e oxidativo de um triatleta internacional de alto n&#237;vel com carga de treinamento de baixo volume e alta intensidade&#46;</p></span> <span id="abst0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">M&#233;todo</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Atleta de 26 anos de idade&#44; com uma pratica esportiva desde os 13 anos e cinco anos de tri&#225;tlon profissional&#46; Os par&#226;metros qualitativos analisados no s&#234;men foram&#58; volume&#44; contagem esperm&#225;tica&#44; motilidade&#44; morfologia&#44; e fragmenta&#231;&#227;o de DNA com testes adicionais dada necessidade&#46; Os testes hormonais salivares foram&#58; Testosterona&#44; Cortisol e a raz&#227;o testosterona&#47;cortisol&#46; A capacidade antioxidante total foi medida no plasma seminal&#46; Tamb&#233;m foi analisado o consumo m&#225;ximo de oxig&#234;nio e caracter&#237;sticas do treinamento&#46; Para determinar a ingesta alimentar habitual e sua poss&#237;vel repercuss&#227;o sobre o estado oxidativo&#44; foi utilizado um question&#225;rio de frequ&#234;ncia de consumo quali-quantitativo de 136 alimentos&#44; a partir do uso de um software especifico&#46;</p></span> <span id="abst0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Resultados</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">os valores e par&#226;metros hormonais e f&#237;sicos seminais estavam dentro da normalidade&#46; A morfologia e fragmenta&#231;&#227;o do DNA esperm&#225;tico mostraram valores anormais &#40;3&#44;9&#37; e 38&#44;33&#37;&#41;&#46; Apresentando um elevado n&#250;mero de c&#233;lulas redondas &#40;2&#44;3 milhoes&#47;mL&#41;&#44; com presen&#231;a de macr&#243;fagos&#46; Se observaram eventos apopt&#243;ticos e necr&#243;ticos&#46; A capacidade antioxidante total&#44; ainda que n&#227;o alterada&#44; estava baixa&#46; A ingesta diet&#233;tica foi caracterizada por um excesso proteico e consumo adequado de antioxidantes &#40;com ligeiro d&#233;ficit excesso de alguns nutrientes espec&#237;ficos&#41; segundo valores recomendados&#46;</p></span> <span id="abst0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Conclus&#245;es</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">o exerc&#237;cio de resist&#234;ncia de alta intensidade altera os par&#226;metros esperm&#225;ticos&#44; principalmente morfologia e fragmenta&#231;&#227;o do DNA&#46; Faz-se necess&#225;rio obter maiores informa&#231;&#245;es sobre o efeito de antioxidantes e outras estrat&#233;gias diet&#233;ticas com rela&#231;&#227;o ao dano oxidativo no s&#234;men de triatletas de alto rendimento&#44; e tra&#231;ar estrat&#233;gias nutricionais adequadas para atenuar os efeitos do exerc&#237;cio sobre a qualidade do s&#234;men&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "abst0045"
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          1 => array:2 [
            "identificador" => "abst0050"
            "titulo" => "M&#233;todo"
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          2 => array:2 [
            "identificador" => "abst0055"
            "titulo" => "Resultados"
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          3 => array:2 [
            "identificador" => "abst0060"
            "titulo" => "Conclus&#245;es"
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    ]
    "multimedia" => array:3 [
      0 => array:7 [
        "identificador" => "fig0005"
        "etiqueta" => "Fig&#46; 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
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          "en" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Fluorescence and bright field microscopy images&#46; A macrophage can be seen along with several abnormal sperm in bright field &#40;A&#41;&#46; Fluorescence microscopy shows&#44; in the same field&#44; how several of these sperm cells are undergoing necrosis&#59; moreover&#44; several sperm cells &#40;red color&#41; have been phagocitized by the macrophage &#40;B&#41;&#46; &#40;For interpretation of the references to color in this figure legend&#44; the reader is referred to the web version of this article&#46;&#41;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Parameter&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Value&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Reference values&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Volume &#40;ml&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;1&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Concentration &#40;10<span class="elsevierStyleSup">6</span><span class="elsevierStyleHsp" style=""></span>ml<span class="elsevierStyleSup">&#8722;1</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">69&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;15&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Total number &#40;10<span class="elsevierStyleSup">6</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">138&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;39&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Progressive motility &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">47&#46;83&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;32&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Non-progressive motility &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">7&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Immotile &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">44&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8804;40&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Morphology &#40;&#37;normal forms&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">3&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8805;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">&#37; DNA fragmentation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">38&#46;33&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8804;15&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Round cells &#40;10<span class="elsevierStyleSup">6</span><span class="elsevierStyleHsp" style=""></span>ml<span class="elsevierStyleSup">&#8722;1</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8804;10<span class="elsevierStyleSup">6</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Apoptotic &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;20&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">Necrotic &#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">6&#46;83&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top">TAC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2580&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">T</span> &#40;pg&#47;ml&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">163&#46;28&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">50&#8211;210&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C</span> &#40;&#956;g&#47;dL&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0&#46;8843&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;3&#8211;1&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">T</span>&#47;<span class="elsevierStyleItalic">C</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">18&#46;464&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Seminological and hormonal values of the studied athlete&#46;</p>"
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        "tabla" => array:2 [
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Dietary variables&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Value&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Recommended intake&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " colspan="3" align="left" valign="top"><span class="elsevierStyleItalic">Caloric distribution</span></td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Total calories &#40;kcal&#47;day&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4311&#46;28&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2564<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>&#37; Carbohydrates&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">56&#46;19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">55&#8211;65&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Carbohydrates &#40;gr&#47;kg&#47;day&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9&#46;44&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&#8211;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>&#37; Protein&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">14&#46;89&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">12&#8211;15&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>&#37; Fat&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">28&#46;90&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">20&#8211;33&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="3" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="3" align="left" valign="top"><span class="elsevierStyleItalic">Vitamins</span></td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Vitamin C &#40;mg&#47;day&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">365&#46;25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">200&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Vitamin A &#40;mg&#47;Eq&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1064&#46;53&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">700&#8211;900&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Vitamin E &#40;mg&#47;day&#41;&nbsp;\t\t\t\t\t\t\n
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Article information
ISSN: 18887546
Original language: English
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2023 November 55 13 68
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2023 September 52 3 55
2023 August 25 3 28
2023 July 26 5 31
2023 June 40 2 42
2023 May 65 3 68
2023 April 32 0 32
2023 March 35 2 37
2023 February 26 3 29
2023 January 25 1 26
2022 December 40 10 50
2022 November 29 7 36
2022 October 25 7 32
2022 September 31 7 38
2022 August 23 12 35
2022 July 27 7 34
2022 June 16 5 21
2022 May 24 14 38
2022 April 24 10 34
2022 March 31 9 40
2022 February 19 6 25
2022 January 29 6 35
2021 December 50 13 63
2021 November 27 11 38
2021 October 56 11 67
2021 September 64 15 79
2021 August 33 10 43
2021 July 101 10 111
2021 June 32 11 43
2021 May 25 5 30
2021 April 112 14 126
2021 March 26 7 33
2021 February 16 6 22
2021 January 31 6 37
2020 December 22 12 34
2020 November 18 9 27
2020 October 14 5 19
2020 September 21 7 28
2020 August 35 5 40
2020 July 20 7 27
2020 June 12 6 18
2020 May 29 9 38
2020 April 28 4 32
2020 March 23 6 29
2020 February 20 6 26
2020 January 28 3 31
2019 December 30 11 41
2019 November 24 4 28
2019 October 50 3 53
2019 September 35 8 43
2019 August 32 11 43
2019 July 42 10 52
2019 June 58 31 89
2019 May 147 34 181
2019 April 74 4 78
2019 March 15 5 20
2019 February 20 7 27
2019 January 14 4 18
2018 December 16 5 21
2018 November 28 5 33
2018 October 32 12 44
2018 September 7 5 12
2018 August 6 0 6
2018 July 9 7 16
2018 June 2 0 2
2018 May 7 3 10
2018 April 25 1 26
2018 March 14 3 17
2018 February 7 3 10
2018 January 10 3 13
2017 December 9 0 9
2017 November 20 3 23
2017 October 12 6 18
2017 September 6 7 13
2017 August 19 13 32
2017 July 12 8 20
2017 June 72 18 90
2017 May 30 11 41
2017 April 29 23 52
2017 March 40 66 106
2017 February 29 2 31
2017 January 17 6 23
2016 December 40 8 48
2016 November 39 8 47
2016 October 67 8 75
2016 September 58 11 69
2016 August 30 8 38
2016 July 31 5 36
2016 June 35 11 46
2016 May 22 7 29
2016 April 25 1 26
2016 March 20 22 42
2016 February 28 19 47
2016 January 39 21 60
2015 December 19 14 33
2015 November 18 18 36
2015 October 30 19 49
2015 September 12 7 19
2015 August 38 25 63
2015 July 26 19 45
2015 June 18 20 38
2015 May 35 10 45
2015 April 30 17 47
2015 March 25 13 38
2015 February 108 16 124
2015 January 143 42 185
2014 December 89 36 125
2014 November 13 5 18
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos