Journal of Health Science

p-ISSN: 2166-5966    e-ISSN: 2166-5990

2016;  6(5): 77-86

doi:10.5923/j.health.20160605.03

 

Hair Zinc Level Affects Nociception in Humans: A Cross-sectional Study

Eleana Tzoi 1, Evaggelos Paleologos 1, Panagiotis Lekkas 1, Konstantinos Krikonis 2, Demetrios Damigos 3, Vasiliki Kalfakakou 1

1Exp. Physiology Lab., Medical Dept., School of Health Sciences, Univ. of Ioannina, Ioannina Greece

2Data Analysis, Ioannina, Greece

3Medical Psycology, Medical Dept., School of Health Sciences, Univ. of Ioannina, Ioannina, Greece

Correspondence to: Eleana Tzoi , Exp. Physiology Lab., Medical Dept., School of Health Sciences, Univ. of Ioannina, Ioannina Greece.

Email:

Copyright © 2016 Scientific & Academic Publishing. All Rights Reserved.

This work is licensed under the Creative Commons Attribution International License (CC BY).
http://creativecommons.org/licenses/by/4.0/

Abstract

Purpose: This study aims to investigate the relationship between hair zinc levels and nociception/ pain tolerance in reference to dietary preferences, smoking and/or alcohol consumption and exercise in young men, aged 19-40 years old. Methods: Hair samples were collected from 42 recruited healthy soldiers, aged 19-40 years old. All subjects were asked to complete a detailed questionnaire including demographic data, education status, dietary preferences, smoking and alcohol use, exercise or athletic habits and then were submitted to a stress test. Data were subjected to statistical analysis via the SPPS program. Results: Zinc levels and pain tolerance were found linearly and positively correlated (r=0.293, sig<0.05), higher levels of zinc were observed in athletes (t=-2.534, sig<0.05) and a significant positive relation was registered between hair zinc levels (rho=0.366, sig<0.05), pain tolerance (rho=0.291, sig<0.05) and frequency of athletic activity. Foods providing high zinc levels, to the consumers, such as red meat (r=0.324, sig<0.05), white meat (r=0.361, sig<0.05) and legumes (r=0.346, sig<0.05) revealed higher correlation scores to pain tolerance, whereas consumption of red meat (r= 0.447, sig<0.05) and legumes (r=0.355, sig<0.05) showed also higher hair zinc levels. Persons performing athletic activity consumed more often red meat, legumes and seafood and presented higher zinc levels (r=0.430, sig<0.05) and higher pain tolerance (r=0.428, sig<0.05). Finally a negative relation between hair zinc levels and age (rho=-0.337, sig<0.05) was registered. Conclusions: Zinc seems to modulate somatosensory function, nociception and pain tolerance in relation to a variety of lifestyle parameters.

Keywords: Zinc, Nociception, Pain tolerance, Physical exercise, Smoking, Alcohol, Diet

Cite this paper: Eleana Tzoi , Evaggelos Paleologos , Panagiotis Lekkas , Konstantinos Krikonis , Demetrios Damigos , Vasiliki Kalfakakou , Hair Zinc Level Affects Nociception in Humans: A Cross-sectional Study, Journal of Health Science, Vol. 6 No. 5, 2016, pp. 77-86. doi: 10.5923/j.health.20160605.03.

1. Introduction

Zinc is a key element in the pyramid of micronutrients [1]. More than 500 enzymes and 3000 transcription factors need zinc for their actions, highlighting the importance of zinc in homeostasis, immune function, oxidative stress, apoptosis and aging [2-4]. Zinc also mediates transmission of nociceptive stimuli from peripheral (PNS) to central nervous system (CNS). As regards the peripheral nervous system, it affects a variety of receptors and ion channels involved in the transmission of noxious stimuli towards more central structures, such as GABA (gama-aminobutyric acid) receptors [5], glycine receptors [6], NMDA (N-Methyl-D-aspartic acid) receptors, purinergic receptor P2X [7], the ASIC (Acid-Sensing Ion Channel) channel and some of TRP (Transient Receptor Potential) channels and voltage-gated Ca2+ and Κ+ channels which are required for neuronal excitability and neurotransmitter release [8]. In the CNS, zinc stored in the vesicles of the final endings of glutamatergic neurons, is released along with glutamate in the synapses, adjusting signal and neural plasticity [9]. Levels of trace elements, such as Zn, in blood serum are related to gender, age, smoking, alcohol consumption, sports and frequency of exercising and in particular to the dietary intake of antioxidant nutrients [10].
Skin components’ (nails, hair) zinc level, reflect the recent exposure 2-3 months to the trace element and represent the body burden to Zn. [11].

2. Materials and Methods

2.1. Human Volunteers

Sixty two (62) recruited soldiers, 19-40 years old, voluntarily joined the research, after obtaining Institutional Ethical Approval, getting volunteers informed about the aim of the study and have them signing a declaration of consensus. Soldiers suffering any recent or chronic disease were excluded from this research. Finally, after careful inspection of the medical history, forty six (46) healthy persons were included and registered in the present study.

2.2. Questionnaire

a. General informations
Full name:
Somatometric/anthropometric data:
Age group:
Birth place:
Residence place during the last five (5) years:
Education level:
Graduate from
Occupation:
Where did you work the last two years?
b. Nutrition Habits
How often do you consume, in a weekly basis, each of the food categories below:
Food categories according to Zn content and bioavailability:
red meat (pork, calf), seafood (fishes, oysters, mussels), legumes, nuts
white meat, pasta, dairy products
vegetables fruits, whole grain cereals, oil/olives
c. Life Style Habits
Do you smoke? :
If the answer is yes, how many cigarettes do you smoke? :
If the answer is yes, when did you start smoking? :
ow often do you consume alcohol beverages? :
Only in social events and interactions:
hich kind of beverages do you prefer? :
Do you practice exercise / sport
(Basketball, football, volleyball, water polo, gym, etc):
If you do, how often? :
d. Medical History
Do you have you any recent health problems? :
If the answer is yes, what kind of?
Are you under any medical treatment? :
If the answer is yes, what kind of?
How long are you under medication? :
Do you take any Nutrition Supplements (NS)?:
If the answer is yes, what kind of?
How long do you take NS? :
Are you allergic to? :
medicaments:
food:
anything else:
Have you undergone any surgery? :
Do you suffer any chronic disease such as:
Does any member of your family suffer a health problem? :

2.3. Sample Collection, Preparation and Zn Detection

Hair samples, 2-3 cm long, were taken from the occipital protuberance of each participant and collected in plastic polyethylene containers (zip). The procedure was carried out using stainless scissors and disposable gloves. Each container was labelled with a code-number corresponding to each participant as well as to the questionnaire completed by him. Volunteers were submitted to a stress test, by repetitively lifting (1 lift/sec) a 5 kg dumbbell with the hand, after the application of 180 mm Hg tourniquet pressure around the left arm if the participant was right- handed and vice versa, by means of a sphygmomanometer’s cuff. Pain stimuli evoked due to ischemic fatigue and time between stress test initiation and pain perception were registered for each participant. Hair samples were analyzed in the laboratory of Physiology of the Medical Department of the University of Ioannina by Atomic Absorption Spectroscopy (AAS). Each hair sample was processed into acid digestion and then zinc content was detected. Reference material for the detection of the metal was Human Hair certified reference material NCS ZC81002b. Data were processed into statistical analysis, listed and coded by the SPPS program. Basic descriptive measures of position and dispersion (mean, standard deviation, median and minimum-maximum) were produced for quantitative - continuous variables, as well as frequency and relative frequency were calculated for each quantitive and nominal variable (smoking, educational level, etc.), Shapiro-Wilk test were used to identify if variables are normally distributed, as regards the independent variables, independent sample t-test was used to test the equality of the average of the answers, coefficient of correlation Pearson and Spearman was used to test bivariate correlations, the value of which shows the intensity of the linear relationship and their sign shows the direction of their relationship and finally the procedures were completed by graphical representations such as scatter diagrams and bar diagrams in the name of nominal and continuous variables respectively.

3. Results

3.1. Correlation between Zinc Level and Time of Pain Display

According to the results, time of pain display and hair zinc level are linearly and positively correlated (r=0.293, sig<0.05), indicating that the higher the hair zinc level the more the time of pain display is registered in healthy young males, aged 19-40 years old.
Table 1. Correlation coefficient between time of pain display and hair zinc level in healthy male humans (19-40 y)
     
Figure 1. Hair Zn level vs time of pain display

3.2. Correlation between Time of Pain Display, Hair Zinc Level, Rate and Content of Alcohol Consumption, in Alcohol Consumers

Table 2. Correlation between time of pain display and hair zinc level and alcohol consumption and alcohol content. (Alcohol consumption 5 categories: never, often, daily, rarely, in social events)
     
Results presented above show that time of pain display is linearly and positively correlated to the rate of alcohol consumption (rho=0.363, sig<0.05) as well as to the alcohol content (rho=0.391, sig<0.05).
Figure 2. Comparative box plot of time of pain display and frequency of alcohol consumption

3.3. Correlation between Hair Zinc Level, Time of Pain Display and Exercise Practice

Table 3. Survey on the mean rates of time of pain display and hair zinc levels, between volunteers practicing ( + ) and not practicing ( - ) exercise
     
Statistical analysis via t-test for equality of means shows that significantly higher hair Zn level, is registered, in those participants who are practicing exercise (+) compared to those who are not (-) (t=-2.386, sig<0.05).

3.4. Correlation between Hair Zinc Level, Time of Pain Display and Frequency of Practicing Exercise

Table 4. Correlation between time of pain display, hair Zn level and frequency of practicing exercise
     
Results listed in table 4 show that there is statistically significant linear correlation between time of pain display and frequency of practicing exercise (rho= 0.291, sig<0.05). Statistically significant linear correlation is also registered between hair Zn level and frequency of practicing exercise (rho= 0.366, sig< 0.05).
Figure 3. Comparative box plot of frequency of practise and time of pain display

3.5. Correlation between Hair Zinc Level and Time of Pain Display in Smokers and Non Smokers

Table 5. Correlation of time of pain display, zinc level and number of cigarettes
     
Based on the results above, significant negative linear correlation was observed between zinc level and number of consumed cigarettes in smokers (24 persons) (rho=-0.44, sig<0.05). No significant differences were observed between smokers and non smokers, either to time of pain display or to zinc level (table 6).
Table 6. Means rates and standard deviation of time of pain display and zinc levels between smokers and non smokers
     

3.6. Correlation between Hair Zinc Level, Time of Pain Display and Diet

a. Food categories according to Zn content and bioavailability
Table 7α. Correlation between time of pain display, hair zinc level and food categories
     
Based on the results above (table 7a)significant positive linear correlation appeared between time of pain display and “red” colored nutritional products, rich in Zn (r=0.375, sig<0.05)as well as significant positive linear correlation between zinc level and “red” foods (r= 0,347, sig<0.05).
b. Foods
Table 7b. Correlation between time of pain display and zinc level and certain foods
     
Based on the results above important linear correlation was observed between time of pain display and consumption of red meat (r=0.324, sig<0.05), white meat (r=0.361, sig<0.05) and legumes (r=0.346, sig<0.05).
Significant linear correlation between zinc level and consumption of red meat (r=0.447, sig<0.05) or legumes (r=0.355, sig <0.05) was also registered.

3.7. Correlation between Zinc Level and Time of Pain Display and Age

Table 8. Correlation between time of pain display, zinc level and age
     
Significant negative linear correlation between zinc level and age (rho=-0.337, sig<0.05) was registered.

3.8. Correlation between Zinc Level, Time of Pain Display and Food Consumption by Athletes

Table 9. Correlation between time of pain display, zinc level and food consumption by athletes
     
Both Zinc level and time of pain display presented significant positive correlation to consumption of “red” foods in subjects practicing exercise (r=0.430, sing<0.05), (r= 0.428, sing<0.05) respectively.

4. Discussion

Hair zinc level is positively correlated to pain endurance (r=0,293, sig<0,05) (Table 1, Fig. 1). Correlation between several forms of chronic pain and inadequacy of zinc as well as the beneficial role of zinc supplements in these maladies has been revealed by many researchers [12, 13]. Zinc administration in animals improved analgesia levels [14, 15]. Moreover, in vitro research has shown that zinc may provide a general mechanism regulating the neuronic stimulation in the central nervous system by inhibiting the NMDA receptors [16].
Our results showed that time of pain display is linearly and positively correlated to frequency of alcohol consumption (rho=0.363, sig<0.05) and to alcohol concentration of consumed beverages (rho=0.391, sig<0.05) (Table 2, Fig. 2). Alcohol affects a wide spectrum of neurotransmitters, most important of them being GABA and glutamic acid [17-19]. Chronic alcohol use leads to decrease of GABA’s receptors function and increase of the NMDA’s receptors activity resulting to neurodegeneration and neuronic damage [17].
The present study showed that zinc level differs among individuals practicing exercise compared to not practicing exercise (t=-2.386, sig<0.05) (Table 3). It was also shown that the higher the frequency of exercise the higher the hair zinc levels (rho=0.366, sig<0.05) and pain endurance (rho=0.291, sig<0.05) (Table 4, Fig. 3). Recent studies have shown that zinc’s plenty metabolic roles, such as energy production, immune defence system and organism protection towards oxidative stress [20, 21] were increased after high-intensity exercise [22-23] maybe due to lipids mobilization. Parallel increase of zinc and leptin also appears after intense exercise [24].
Regarding frequency of exercise and pain endurance, Scheef L et al, 2012 and Tesarz J. et al, 2013, showed through functional magnetic resonance imaging (fMRI) that exercise such as running but not walking leads to control of perception and pain resistance due to mediation of endogenous nociception mechanisms and specifically of opioids since increased b endorphins levels in the athletes blood were detected [25, 26].
In addition, our results showed that hair zinc levels were reduced inversely to the number of consumed cigarettes in smokers (rho=-0.44, sig<0.05) (Table 5, Table 6). Smoking intervenes in human metal homeostasis [27] affecting body mineral levels and especially zinc [28] resulting in disorders such as arterial hypertension, atherosclerosis [29] and male’s spermatic distortion [30].
The present study showed that consumers of red foods revealed higher zinc levels (r=0.347, sig<0.05) and higher pain resistance (r=0.375, sig<0.05) compared to white and green food consumers (Table 7a). In particular, consumers of red meat and legumes revealed higher pain resistance (r=0.324, sig<0.05) (r=0.346, sig<0.05) and higher zinc level (r=0.447, sig<0.05) (r=0.355, sig<0,05) respectively, compared to other groups of consumers (Table 7b). Recent research showed that meat-based diets such as seafood and shellfish, veal, beef and lamb meat, chickens, dairy, cereals and cereal products and their combination with legumes resulted to higher body zinc level in comparison to diets based on vegetables [31-33].
The present study showed that body zinc level is reduced during aging (rho=-0,337, sig <0.05) (Table 8). Research shows that serum zinc levels increase during the third decade and then decline [34], teenagers seem to hold the 80% of the appropriate zinc level while elders hold only the 37% [35]. Zinc’s decrease influences the human immune system and leads to susceptibility to immune function disorders [3] but this may be improved by zinc supplementation [34].
In conclusion, the present research showed that individuals practicing exercise and consuming red meat, legumes and seafood revealed higher hair zinc level (r=0.430, sig<0.05) and higher pain resistance (r=0.428, sig<0.05) comparatively to the other group of the study (Table 9). Our results corroborate to research findings showing that athletes often adopt an unusual diet in an attempt to enhance performance, which is an excessive increase in carbohydrates and low intake of foods rich in zinc such as meat, eggs and seafood, proteins and fat. As a result they appear having 90% zinc deficiency as well as deficiency of other minerals such as phosphorous, magnesium and iron [36-38].

5. Conclusions

Zinc is correlated to nociception and pain resistance and may be used in the treatment of various painful conditions. Alcohol consumption extends the time of pain display. Long term smoking influences negatively zinc levels due to toxic metal accumulation and competition to zinc. Consumption of red meat and legumes-combined to protein foods leads to increased body zinc level. Moreover, an inverse correlation between age and body zinc level plays an important role in human immune system regulation. Exercise is correlated to high hair zinc level and individuals, exercising systematically and regularly, appear to have higher pain resistance compared to other groups. Regarding athletes, high rate ignorance is observed concerning their nutrition sources and is necessary a proper diet plan accompanied with the right nutrition and mineral taking for the improvement of their preparation and their health. In conclusion, results of the present study highlight zinc’s role in nociception and pain resistance, in correlation to significant lifestyle parameters.

References

[1]  King JC, Shames DM, Woodhouse LR Zinc homeostasis in humans. J. Nutr. 2000 May; 130(5S Suppl):1360S-6S.
[2]  Livingstone C. Zinc: physiology, deficiency, and parenteral nutrition. Nutr Clin Pract. 2015 Jun; 30(3):371-82.
[3]  Maywald M, Rink L. Zinc homeostasis and immunosenescence. J Trace Elem Med Biol. 2015 Jan; 29:24-30.
[4]  Bonaventura P, Benedetti G, Albarède F, Miossec P. Zinc and its role in immunity and inflammation. Autoimmun Rev. 2015 Apr; 14(4):277-85.
[5]  Grauert Antonia, Engel Dominique and Ruiz Arnaud J. Endogenous zinc depresses GABAergic transmission via T-type Ca2+ channels and broadens the time window for integration of glutamatergic inputs in dentate granule cells. J Physiol. 2014 Jan 1; 592(1): 67–86.
[6]  Chorin E, Vinograd O, et al. Upregulation of KCC2 activity by zinc-mediated neurotransmission via the mZnR/GPR39 receptor. J. Neurosci. 2011; 31(36):12916–12926.
[7]  Li C, Peoples RW, Weight FF. Inhibition of ATP-activated current by zinc in dorsal root ganglion neurones of bullfrog. J. Physiol. 1997 Dec 15; 505 (Pt 3):641-53.
[8]  Uchida Kunitoshi and Tominaga Makoto. Extracellular Zinc Ion Regulates Transient Receptor Potential Melastatin 5 (TRPM5) Channel Activation through Its Interaction with a Pore Loop Domain. Biol Chem. Sep 6, 2013; 288(36): 25950–25955.
[9]  Nozaki C, Vergnano AM, Filliol D, Ouagazzal AM, Le Goff A, Carvalho S, Reiss D, Gaveriaux-Ruff C, Neyton J, Paoletti P, Kieffer BL. Zinc alleviates pain through high-affinity binding to the NMDA receptor NR2A subunit. Nat Neurosci. 2011 Jul 3; 14(8): 1017-22.
[10]  Galan P, Viteri FE, Bertrais S, Czernichow S, Faure H, Arnaud J, Ruffieux D, Chenal S, Arnault N, Favier A, Roussel AM, Hercberg S. Serum concentrations of beta-carotene, vitamins C and E, zinc and selenium are influenced by sex, age, diet, smoking status, alcohol consumption and corpulence in a general French adult population. Eur J Clin Nutr. 2005 Oct; 59(10):1181-90.
[11]  Ozmen Habibe, Akarsu Saadet, Polat Fatih and Cukurovali Alaaddin. The Levels of Calcium and Magnesium, and of Selected Trace Elements, in Whole Blood and Scalp Hair of Children with Growth Retardation. Iran J. Pediatr. 2013 Apr; 23(2): 125–130.
[12]  Temiye EO, Duke ES, Owolabi MA, Renner JK. Relationship between Painful Crisis and Serum Zinc Level in Children with Sickle Cell Anaemia. Anemia. 2011; 2011:698586.
[13]  Ciubotariu Diana, Ghiciuc Cristina Mihaela and Lupușoru Cătălina Elena. Zinc involvement in opioid addiction and analgesia – should zinc supplementation be recommended for opioid-treated persons? Subst Abuse Treat Prev Policy. 2015; 10: 29.
[14]  Matsunami M, Kirishi S, Okui T, Kawabata A Chelating luminal zinc mimics hydrogen sulfide-evoked colonic pain in mice: possible involvement of T-type calcium channels. Neuroscience. 2011 May 5; 181: 257-64.
[15]  Tamba BI, Leon MM, Petreus T. Common trace elements alleviate pain in an experimental mouse model. J Neurosci Res. 2013 Apr; 91(4):554-61.
[16]  Anderson Charles T., Radford Robert J., Zastrow Melissa L., Zhang Daniel Y., Apfel Ulf-Peter, Lippard Stephen J. and Tzounopoulos Thanos. Modulation of extrasynaptic NMDA receptors by synaptic and tonic zinc. Proc Natl Acad Sci U S A. 2015 May 19; 112(20): 2705–2714.
[17]  Krystal JH, Staley J, Mason G, et al. Gamma-aminobutyric acid type A receptors and alcoholism: intoxication, dependence, vulnerability, and treatment. Archives of General Psychiatry. 2006; 63:957–968.
[18]  Hicklin TR, Wu PH, Radcliff PA, Freud RK, Goebel-Goody SM, Correa PR, Proctor WR, Lombroso PJ, Browning MD. Alcohol inhibition of the NMDA receptor function, long-term potentiation, and fear learning requires striatanal-enriched protein tyrosine phosphatase. Proc Natl Acad Sci USA. 2011 Apr 19; 108(16):6650-5.
[19]  Gutierrez Carlos A and Staehle Mary M. A control system analysis of the dynamic response of N-methyl-D-aspartate glutamate receptors to alcoholism and alcohol withdrawal. Theor Biol Med Model. 2015; 12:8.
[20]  Speich M, Pineau A, Ballereau F. Minerals, trace elements and related biological variables in athletes and during physical activity. Clin Chim Acta. 2001 Oct; 312(1-2):1-11.
[21]  Chu A, Petocz P, Samman S. Immediate Effects of Aerobic Exercise on Plasma/Serum Zinc Levels: A Meta-analysis. Med Sci Sports Exerc. 2015 Nov 4.
[22]  Savas S, Senel O, Okan I, Aksu ML. Effect of acute maximal aerobic exercise upon the trace element levels in blood. Neuro Endocrinol Lett. 2007 Oct; 28(5):675-80.
[23]  Somboonwong J, Traisaeng S, Saguanrungsirikul S, Moderate-intensity exercise training elevates serum and pancreatic zinc levels and pancreatic ZnT8 expression in streptozotocin-induced diabetic rats. Life Sci. 2015 Oct 15; 139:46-51.
[24]  Zhao J, Fan B, Wu Z, Xu M, Luo Y. Serum zinc is associated with plasma leptin and Cu-Zn SOD in elite male basketball athletes. J Trace Elem Med Biol. 2015 Apr; 30:49-53.
[25]  Scheef L, Jankowski J, Daamen M, Weyer G, Klingenberg M, Renner J, Mueckter S, Schürmann B, Musshoff F, Wagner M, Schild HH, Zimmer A, Boecker H. An fMRI study on the acute effects of exercise on pain processing in trained athletes. Pain. 2012 Aug; 153(8):1702-14.
[26]  Tesarz J, Gerhardt A, Schommer K, Treede RD, Eich W. Alterations in endogenous pain modulation in endurance athletes: an experimental study using quantitative sensory testing and the cold-pressor task. Pain. 2013 Jul; 154(7): 1022-9.
[27]  Afridi HI, Talpur FN, Kazi TG, Brabazon D. Estimation of toxic elements in the samples of different cigarettes and their effect on the essential elemental status in the biological samples of Irish smoker rheumatoid arthritis consumers. Environ Monit Assess. 2015 Apr; 187(4):157.
[28]  Morales-Suárez-Varela María, Llopis-González Agustín, González-Albert Verónica, López-Izquierdo Raúl, González-Manzano Isabel, Cháves Javier, Huerta-Biosca Vicente and Martin-Escudero Juan C. Correlation of Zinc with Oxidative Stress Biomarkers. Int J Environ Res Public Health. 2015 Mar; 12(3): 3060–3076.
[29]  Afridi HI, Kazi TG, Kazi NG, Jamali MK, Arain MB, Sirajuddin, Baig J A, Kandhro GA, Wadhwa SK and Shah AQ. Evaluation of cadmium, lead, nickel and zinc status in biological samples of smokers and nonsmokers hypertensive patients. J. Hum Hypertens. 2010 Jan; 24(1): 34–43.
[30]  Liu RZ, Gao JC, Zhang HG, Wang RX, Zhang ZH, Liu XY. Seminal plasma zinc level may be associated with the effect of cigarette smoking on sperm parameters. J Int Med Res. 2010 May-Jun; 38(3):923-8.
[31]  Lönnerdal B. Dietary factors influencing zinc absorption. J Nutr. 2000 May; 130 (5S Suppl):1378S-83S.
[32]  Karen H. C. Lim, Lynn J. Riddell, Caryl A. Nowson, Alison O. Booth, and Ewa A. Szymlek-Gay. Iron and Zinc Nutrition in the Economically-Developed World: A Review. Nutrients. 2013 Aug; 5(8): 3184–3211.
[33]  Foster M, Samman S. Vegetarian diets across the lifecycle: impact on zinc intake and status. Adv Food Nutr Res. 2015; 74:93-131.
[34]  Haase Hajo and Rink Lothar. The immune system and the impact of zinc during aging. Immun Ageing. 2009; 6:9.
[35]  Mariani E, Cornacchiola V, Polidori MC, Mangialasche F, Malavolta M, Cecchetti R, Bastiani P, Baglioni M, Mocchegiani E, Mecocci P. Antioxidant enzyme activities in healthy old subjects: influence of age, gender and zinc status: results from the Zincage Project. Biogerontology. 2006 Oct-Dec; 7(5-6):391-8.
[36]  Hoogenboom Barbara J, Morris Jennifer, Morris Chad and Schaefer Katharine. Nutritional Knowledge and Eating Behaviors of Female, Collegiate Swimmers. N Am J Sports Phys Ther. 2009 Aug; 4(3): 139–148.
[37]  Dwyer Johanna, Eisenberg Alanna, Prelack Kathy, Song Won O, Sonneville Kendrin, and Ziegler Paula. Eating attitudes and food intakes of elite adolescent female figure skaters: a cross sectional study. J Int Soc Sports Nutr.2012; 9:53.
[38]  García-Rovés Pablo M, García-Zapico Pedro, Patterson Ángeles M. and Iglesias-Gutiérrez Eduardo. Nutrient Intake and Food Habits of Soccer Players: Analyzing the Correlates of Eating Practice. Nutrients. 2014 Jul; 6(7): 2697–2717.