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Iron nutritional status in female karatekas, handball and basketball players, and runners
Physiology & Behavior, Vol. 59, No. 3, 449-453, 1996 Copyright © 1996 Elsevier Science Inc. Printed in the USA. All rights reserved 0031-9384/96 $15.00 + .00
ELSEVIER
0031-9384(95)02081-6
Iron Nutritional Status in Female Karatekas, Handball and Basketball Players, and Runners R A M O N JOSl~ NUVIALA, l M A R I A C A R M E N CASTILLO, M A R I A GLORIA L A P I E Z A AND JESI~IS F E R N A N D O ESCANERO
Clinical Biochemistry Department, University Hospital, 50009 Zaragoza, Spain Received 14 March 1995 NUVIALA, R. J., M. C. CASTILLO, M. G. LAPIEZA AND J. F. ESCANERO. Iron nutritional status in female karatekas, handball and basketball players, and runners. PHYSIOL BEHAV 59(3) 449-453, 1996.--The iron nutritional status was studied in 84 sportswomen (19 karatekas, 20 handball players, 20 basketball players, and 25 middle and long distance runners) and in 82 nonathletic females of similar characteristics (control group). After a 7-day nutritional survey by means of the food weighing method, it was found that iron intake was significantly higher in the handball players ( p < 0.05), basketball players ( p < 0.01), and runners ( p < 0.01) with regard to the control group; the basketball players were the only ones to cover the recommended minimum intake (15 mg/day). The heme iron intake was significantly greater in the handball and basketball players ( p < 0.01), who, together with the runners, reached the value of 1.5 mg/day, which is considered to be optimal. In relation to the control group, the karatekas and handball and basketball players had lower levels of serum ferritin, although their iron intake was greater, whereas the runners had higher values that were very similar to those of the control group, due to the iron supplementation they had received. Despite finding a marked prevalence of inadequate iron intake, both in the sportswomen and in the control group, the manifest cases of anemia are relatively scarce. The organic iron stores do not seem to depend exclusively on the iron intake but also on intimate mechanisms of intestinal absorption and diverse causes of iron loss. Females
ilron status
Heme iron
Karate
ALTHOUGH iron loss in sportswomen may have very diverse causes, it should be pointed out that the deficiency of this micronutrient seems to lae mainly caused by insufficient intake (4,6,18). Moreover, the absorption of iron does not depend only on the total quantity of iron intake, but also on the bioavailability of iron in food, with a different percentage of intestinal absorption according to whether it is heme or nonheme iron (11,15). All this leads to the concept that the diet must not only contain a minimum amount of iron (15 mg/day for women) but also that the heme iron intake must be sufficient (10% of the total intake), as established by the U.S. Recommended Dietary Allowances (17,23). Most studies related to the iron nutritional status in sportswomen have been performed on long distance runners (5,7,14,27); there are few conceming predominantly explosive sports or team sports, and those that do exist are somewhat incomplete (9,19). The aim of the present article was to study the iron nutritional status in women who practise an explosive sport such as karate,
Handball
Basketball
Runners
two team sports such as handball and basketball, and an endurance activity such as middle and long distance running, to establish the possible relationship between iron intake and its organic stores, and whether there are differences between the different groups of sportswomen. METHOD
Subjects Eighty-four female athletes between 16 and 29 years of age who took part in national and international competitions participated in the study (19 karatekas, 20 handball players, 20 basketball players, and 25 middle and long distance runners). At the same time, a group of 82 females of a similar age range who did not participate in physical activities was studied (control group). They were all previously informed of the aim of the study and gave written consent. They were interviewed personally as to the number of hours per week dedicated to training and to the
t Requests for reprints should be addressed to Ram6n Jos6 Nuviala, M.D., Serviciode BioqufmicaCffnica, Hospital Cl~nicoUniversitario,Avda. San Juan Bosco, 15, 50009 Zaragoza, Spain.
449
450
NUVIALA ET AL.
TABLE 1 PHYSICAL CHARACTERISTICS AND LEVEL OF TRAINING Control n Age (years) Weight (kg) Height (cm) Menarche age (years) Practice time (years) Training ( h / w e e k )
82 21.0 57.0 160.8 13.0 ---
5:2.8 5:7.6 _+ 5.2 5:1.3
Karate 19 20.1 56.7 160.7 12.6 6.8 5.8
5:3.4 + 5.0 + 6.0 +_ 1.2 5:3.4 5:3.0
Handball 20 19.9 62.3 164.3 12.8 8.9 7.9
5:3.6 5:7.8 5:4.3 5:1.2 5:2.0 5: 1.7
Basketball
Runners
20 19.2 _+ 2.3 67.1 5: 11.2 172.3 + 9.2 13.4_+ 1.3 8.1 5: 3.5 8.3 5: 2.2
25 20.0 _+ 3.6 54.1 5:4.9 165.3 + 6.0 13.5+ 1.9 7.2 + 3.1 t0.3 + 3.2
Values are mean + SD.
practice of their particular sport. To eliminate those presenting serious abnormalities, they were also required to note down the date of their menarche and the characteristics of their menstrual cycles as precisely as possible. If they were regular, they were asked their duration and the intensity of their menstrual hemorrhages. Finally, they were also asked if they took contraceptives.
Dietary Survey Subjects completed a 7-day dietary survey using the food weighing method. Prior to the survey, they were provided with a precision balance (Postal Power TM model) so that they could weigh all their food, both solid and liquid, with a total capacity of 2 kg, a resolution of l g, and a precision of + 1 % in each weighing operation. Furthermore, they were given the corresponding instructions that explained the correct way to weigh the different foodstuffs and it was emphasized that they should not modify their normal diet during the period of the dietary survey. The surveys were checked by two different specialists to see that they had been filled in correctly, and those that did not fulfil this condition were rejected. The evaluation of the foodstuffs was carried out by means of a computerized programme based on the food composition tables for the Spanish population (16). From the surveys the mean daily intake of total energy, total iron, and heine iron was calculated [the heine iron intake according to the U.S. Recommended Dietary Allowances (17), which consider it to be 40% of the total iron contained in meat, fish, and poultry]. Afterwards, the iron density per 1000 kcal was calculated. All subjects were asked if they took pharmacological supplements and, in particular, iron supplements.
in a vacuum tube (Vacutainer) to obtain the serum. This was stored at - 30°C until the moment of analysis. The samples with anticoagulant were processed immediately. The hematocrit was determined in triplicate by means of microcentrifugation. Hemoglobin and the red blood cell count were measured in a STKS model hematological cell counter (Coulter Electronics, Inc.). From these parameters the mean corpuscular volume (MCV), the mean corpuscular hemoglobin (MCH) and the mean corpuscular hemoglobin concentration (MCHC) were calculated. The serum iron was determined in the serum samples by means of the ferrozine method (26) in a Synchron CX5 autoanalyzer (Beckman). The serum ferritine was evaluated in duplicate by means of an enzyme-immunoassay (Boehringer Mannheim), calculating the mean value. Transferrin and haptoglobin were determined by kinetic immunonephelometry, Array 360 (Beckman).
Statistical Analysis It was carried out after the kurtosis calculation. When me value obtained was between + 1 and - 1 it was considered that the sample distribution was normal, in which case the Student's test was performed. If, on the other hand, the kurtosis value was outside this range, it was accepted that the sample distribution was not normal and the nonparametric Mann-Whitney U-test was used. In both cases the level of significance was established for p < 0.05 and p < 0.01. RESULTS
Hematological Analysis The analysis was carried out halfway through the dietary survey. The blood samples were taken in the laboratory after a minimum period of a 10-h fast. The samples obtained were divided into two tubes: one with an anticoagulant (K3-EDTA) for the determination of the hematological parameters, and the other
The physical characteristics and the level of training can be seen in Table 1. The mean age of the appearance of the menarche was slightly lower in the karatekas and handball players but no significant differences were found. Three members of the control group referred to amenorrhea experience and 6 of the 25 runners were found in the same situation. No differences in ferritin serum
TABLE 2 ENERGY AND TOTAL, HEME AND NONHEME IRON INTAKE Control Energy intake (kcal/day) Iron intake(rag/day) Irondensity(mg/1000kcal) Heme iron intake ( m g / d a y ) Heme iron intake (% of total) Nonheme iron intake ( m g / d a y )
1969.2 11.3 5.9 1.34 11.9 10.0
Values are mean + SD. *~"Student's test: * p < 0.01, f p < 0.05. .~ Mann-Whimey's test: ~ p < 0.01.
+ 437.9 5: 2.8 5: 1.4 5: 0.52 5: 4.0 5: 2.6
Karate 2008.7 5:495.1 12.7"5: 3.7 6.4 5: 1.7 1.45 5: 0.69 11.6 __. 4.8 11.2 5: 3.4
Handball 2284.6 12.9 5.8 1.75 13.3 11.2
+ 547.6* + 2.7t 5: 1.1 5: 0.51" + 2.1 + 2.3
Basketball 2560.6 15.8 6.3 2.15 13.7 13.7
+ 470.5* 5: 2.7 5: 1.3 5: 0.65~ 5: 4.0 5: 2.6*
Runners
2003.0 13.6 6.9 1.53 11.2 12.0
+ 506.9 5: 4.0* 5: 1.8~ 5: 0.73 5: 4.5 5: 3.7*
IRON NUTRITION IN F E M A L E ATHLETES
451
TABLE 3 HEMATOLOGICAL AND BIOCHEMICAL PARAMETERS RELATED TO IRON METABOLISM Hematocrit(%) Hemoglobin(g/dl) Red cell count (106/mm 3) MCV(Iz 3) MCH (pg) MCHC(g/dl) Iron (/xg/dl) Transferrin (mg/dl) TRF saturation (%) Ferritin (ng/ml) Haptoglobin (mg/dl)
Control
Karate
40.1 + 2.2 13.2 4- 0.8 4.33 ± 0.29 92.8 4- 4.8 30.5 4- 1.8 32.9 4- 1.1 89.7 4- 38.6 317.7 4- 52.6 29.3 + 13.9 36.1 4- 26.2 83.2 4- 35.6
39.9 + 2.1 12.9 4- 0.8 4.41 4- 0.35 91.0 4- 7.0 29.5 4- 2.5 32.4 4- 0.9 64.8 4- 25.0* 321.4 4- 45.3 20.7 4- 9.226.7 4- 17.3 84.6 + 31.9
Handball
39.9 + 13.2 ± 4.34± 92.2 ± 30.5 + 33.1 ± 86.9 + 305.8 + 28.8 ± 26.7 ± 64.3 +
2.1 0.8 0.28 4.8 1.2 1.1 35.9 40.4 12.1 18.2 23.6~
Basketl:mll
Runners
39.7 ± 3.2 12.8 ± 1.3 4.29± 0.32 92.8 ± 7.5 29.9 ± 3.1 32.2 + 1.8 73.9 + 38.0 330.7 + 44.3 23.7 ± 13.9 28.1 4- 22.9 65.7 4- 41.3-~
41.0 ± 2.7 13.4 + 0.8 4.35 ± 0.23 94.3 ± 4.6 30.9 ± 1.5 32.8 ± 1.0 86.9 5- 43.6 333.8 4- 48.8 27.5 ± 15.4 34.6 ± 23.0 59.4 4- 32.7~
Values are mean __.SD. *¢ Student's test: * p < 0.01, - p < 0.05. - Mann-Whitney's test: :~ p < 0.05.
levels were found between amenorrheic and eumenorrheic runners. The energy intake was significantly greater in the handball and basketball players ( p < 0.01) in relation to the intake of the control group (Table 2). The total iron intake showed significantly higher levels in the handball players ( p < 0.05), the basketball players ( p < 0.01), and in the runners ( p < 0.0 I); the basketball players wen; the only ones to reach the minimum intake of 15 m g / d a y . The density of i r o n / 1 0 0 0 kcal was significantly greater in the runners ( p < 0.01). With regard to the heme iron intake, both the handball and basketball players showed significantly higher values ( p < 0.01) than the control group. The percentage of berne iron intake in relation to the total iron intake was higher in the handball and basketball players, but no significant differences were found with regard to the control group. Finally, the nonheme iron intake was significantly greater in the basketball players and the runners ( p < 0 . 0 1 ) . It should be underlined that none of the control group took iron supplements, whereas 11 of the 25 runners did take supplementation that ranged from 10 to 210 m g / d a y of elemental iron. The supplementary intake has not been included in the mean intake of this micronutrient. At the same time, no significant differences in the serum ferritin level were found between the runners taking iron supplementation (29.7 :± 17.8 n g / m l ) and those who did not (38.4 _+ 26.4 n g / m l ) . With regard to the hematological parameters (Table 3), the values found were very similar in all the groups studied, without significant differences between the sportswomen and the control group. Both the serum iiron ( p < 0.01) and the transferrin saturation percentage ( p < 0.05) had significantly lower values in the karatekas than in the control group. The levels of haptoglobin were significantly lower ( p < 0.05) in the handball and basketball players and in the runners, who showed the lowest value.
Seventy-three members of the control group (89.0%) did not reach the minimum iron intake of 15 m g / d a y (Table 4), whereas the total among the sportswomen was 53 (63%), with a greater percentage of deficiency in the handball players (80%). Twentyfive females from the control group (30.4%) had ferritin levels under 20 n g / m l and 32 sportswomen were in the same situation, with a higher percentage of iron deficiency among the karatekas (27.3%). Finally, five females from the control group (6.0%) and seven sportswomen (8.3%) presented a hemoglobin concentration under 12 g / d l . The anemia percentage was greater in the group of basketball players (20%). DISCUSSION The results of this study show a greater mean energy intake in the handball players and, above all, in the basketball players, which is the consequence of the greater energy output of these sportswomen. The intake of the basketball players is very similar to that reported by Short and Short (24), also on basketball players, whereas these authors found quite higher mean values of energy intake in a follow-up control performed 4 years later (24). On the other hand, Nowak et al. (19) report a much lower mean intake in female university basketball players. For the runners, the values are similar to those of Lampe et al. (14) in marathon runners and higher than those of Pate et al. (21). On the other hand, Faber and Benade (10) report a higher energy intake in field athletes. The iron intake of the sportswomen in this study seems to be related to the energy intake, with a greater value in the basketball players, who were the only ones to reach the recommended minimum intake of 15 m g / d a y (17). However, it was the runners who had a higher density of iron intake. A somewhat higher iron intake was found in the handball players than that reported by
TABLE 4 PREVALENCE OF INADEQUATE IRON INTAKE. IRON DEFICIENCY AND ANEMIA Iron Intake (< 15 mg/day) Ferritin (< 20 ng/ml) Hemoglobin [< 12 g / d l )
Control Karate Handball Basketball Runners Total athletes
Cases
%
Cases
%
Cases
%
73 12 16 8 17 53
89.0 63.1 80.0 40.0 68.0 63.0
25 9 7 9 7 32
30.4 47.3 35.0 45.0 28.0 38.0
5 2 1 4 0 7
6.0 10.5 5.0 20.0 -8.3
452
Erp-Baart et al. (9). Similarly, the intake of the basketball players was greater than that of the players studied by Nowak et al. (19), Short and Short (24), and than that reported by Perron and Endres (22) in volleyball players. Some authors (2,3,21,28) report mean iron intakes lower than those of the middle and long distance runners included in this study. On the other hand, other studies also performed on long distance runners (13,14,25) report values over the 13.6 m g / d a y found in this study. It should be pointed out that in none of these studies was the mean intake of 15 m g / d a y reached, which is considered it to be the optimal intake. Only Haymes and Spillman (13) found a mean intake of 15 m g / d a y in sprinters. With regards to the U.S. Recommended Dietary Allowances (RDA) (17), the iron intake of the control group was 75.8% of that recommended; in the sportswomen as a whole, it was 92%, with a value of 84.8% for the karatekas, 86.4% for the handball players, and 92% for the runners. The basketball players were the only ones who reached the RDA, with a mean intake of 105.9%. Nowak et al. (19) report an iron intake in female basketball players of 54%, Perron and Endres (22) a 60% intake in volleyball players, whereas Lampe et al. (14) and Pate et al. (21) found an intake of 78% and 58% in runners, respectively, taking into account that all these authors consider the minimum iron intake limit to be 18 m g / d a y . Faber and Benade (10), establishing this limit at 15 mg/day, as in this study, found an iron intake in their field athletes of 89% in relation to the RDA, which is a percentage similar to that found in our middle and long distance runners. Bearing in mind that the minimum iron intake in females should be 15 m g / d a y and that heme iron should make up about 10% of the former, the optimum mean intake of heine iron should be 1.5 rag/day. This figure is reached by the handball and basketball players and by the runners but not by the karatekas or the control group. Erp-Baart et al. (9) found a heine iron intake in female handball players of 3.2 m g / d a y and of 1.6 m g / d a y in runners, both values higher than those of the corresponding sportswomen in the present study. The analyses carried out on long distance runners show a heme iron intake lower than the recommended minimum (13,25,28). Only Haymes and Spillman (13) report a mean intake of 1.5 m g / d a y in sprinters. The importance of a sufficient heine iron intake is highlighted in the study performed by Snyder et al. (25), which, in long distance runners, compares the heme iron contained in a normal diet with that contained in a vegetarian diet, finding a clearly lower concentration of serum ferritin in the case of the sportswomen with a vegetarian diet, whose content of heme iron was very low. Heme iron represents between 7% and 10% of the total dietary iron intake of females in the United States (23). In the present study, a somewhat higher percentage, which varied between the 11.2% of the runners and the 13.7% of the basketball players, was found. The mean intake of the control group was 11.9% of the total iron. According to the different studies reviewed, there is a difference of criteria regarding the minimum serum ferritin concentration considered to be an indicator of an iron deficiency state. Harju et al. (12) found that with less than 20 n g / m l of ferritin there is an absence of iron in bone marrow, whereas Wick et al. (30) established a clear difference between the 20 n g / m l , which they considered as a deficiency of stored iron, and the 12 n g / m l , which would indicate, moreover, a deficiency in its transport. For this reason, we have considered a serum ferritin concentration of 20 n g / m l to indicate deficiency in iron stores. All groups of sportswomen in this study had mean ferritin concentrations over 20 n g / m l . The lowest values were those of
NUVIALA ET AL.
the karatekas and the handball and basketball players, whereas the runners had higher concentrations that were very similar to those of the control group. However, it should be taken into account that 11 of the 25 runners regularly took iron supplements, which clearly affected the serum ferritin concentration. The majority of studies performed on long distance runners show ferritin values lower than those found in our runners (3,5,7,13,14,20,25). Durstine et al. (8) report a concentration of ferritin in elite runners similar to that of those in the present study, pointing out that 50% of them took iron supplements. Finally, Weight et al. (29) found a mean ferritin figure in their runners of 45.2 n g / m l , which is clearly higher than that of all the sportswomen included in the present series. The levels of haptoglobin were significantly lower in the handball and basketball players and in the runners with respect to the control group, which corresponds to sports with repeated floor-foot impact. This finding is similar to that reported by Haymes and Spillman (13) in long distance runners, presenting, moreover, lower levels than those found in sprinters and particularly in the control group. Clement and Asmundson (3), also referring to long distance runners, report a mean concentration of haptoglobin of 95.0 m g / d l , which is far higher than that of the runners in this study. The high value of haptoglobin found in the karatekas, similar to that of the control group, is surprising, although it might be explained because they practised the " k a t a " discipline, in which no physical contact is produced, as opposite to the " k u m i t e " discipline in which there is contact. The elevated prevalence of inadequate iron intake, both in the control group (89.0%) and in the sportswomen (63%), contrasts with the scarcity of manifest cases of anemia. This is in agreement with the conclusions of Weight et al. (29). Among the sportswomen, the greater number of cases found in the basketball players stands out because they were the ones who had the highest mean intake of total iron and heme iron and the lowest percentage of prevalence of inadequate intake (40%). At the same time, it is surprising that two of the basketball players with manifest anemia had mean iron intakes higher than that of the recommended minimums (18.2 and 17.3 rag/day), whereas the rest of the anemic females, both those of the control group and the sportswomen, did not reach this minimum. Recent studies performed at the level of the serum transferrin receptor and of the iron responsive element binding protein (IRE-BP) may possibly explain, in the near future, some of the unknown factors concerning the absorption of iron at the intestinal level (1). In conclusion, it may be said that the karatekas and the handball and basketball players studied had lower levels of ferritin than the control group, although their iron intake was higher, whereas the middle and long distance runners showed higher values of ferritin, which may be explained in some cases by intake of iron supplements. The organic iron stores in the sportswomen do not seem to depend exclusively on iron intake and its bioavailability, but also the intimate mechanisms of intestinal iron aborption and the different causes of additional iron loss must be considered. Among the sportswomen studied, it was the group of basketball players who had the greatest total iron and heme iron intakes; moreover, they were the only ones who covered the minimum requirements established by the U.S. RDA. ACKNOWLEDGEMENTS This study has been financed by a grant from the Sanitary Research Fund of the Spanish National Health Service (FIS; Exp. 92/0598).
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REFERENCES 1. Brittenham, G. M. New advances in iron metabolism, iron deficiency, and iron overload. Curr. Opin. Hematol. 1:101-106; 1994. 2. Brown, R. T.; Mcintosh, S. M.; Seabolt, V. R.; Daniel, W. A., Jr. Iron status of adolescent female athletes. J. Adolesc. Health Care 6:349-352; 1985. 3. Clement, D. B.; Asmundson, R. C. Nutritional intake and hematological parameters in endurance runners. Phys. Sportsmed. 10:37-43;
1982. 4. Clement, D. B.; Sawchuk, L. L. Iron status and sports performance. Sports Med. 1:65-74; 1984. 5. Colt, E.; Heyman, B. Low ferritin levels in runners. J. Sports Med. 24:13-17; 1984. 6. Dallman, P. R. Biochemical basis for the manifestations of iron deficiency. Annu. Rev. Nutr. 6:13-40; 1986. 7. Deuster, P. A.; Kyle, S. B.; Moser, P. B.; Vigersky, R. A.; Singh, A.; Schoomaker, E. B. Nutritional survey of highly trained women runners. Am. J. Clin. Nutr. 45:954-962; 1986. 8. Durstine, J. L.; Pate, R. R.; Spading, P. B.; et al. Lipid, lipoprotein, and iron status of elite women distance runners. Int. J. Sports Med. 8(Suppl. 2): 119-123; 1987. 9. Erp-Baart, A. M. J. van; Saris, W. M. H.; Binkhorst, R. A.; Vos, J. A.; Elvers, J. W. H. Nationwide survey on nutritional habits in elite athletes. Part II. Mineral and vitamin intake. Int. J. Sports Med. 10(Suppl. I):S11-S16; 1989. 10. Faber, M.; Benade, A. J. S. Mineral and vitamin intake in field athletes (discus-, hamraer-, javelin-throwers and shotputters). Int. J. Sports Med. 12:324-327; 1991. 11. Hallberg, L. Bioavailability of dietary iron in man. Annu. Rev. Nutr. 1:123-147; 1981. 12. Harju, E.; Pakarinen, A.; Larmi, T. A comparison between serum ferritin concentration and the amount of bone marrow stainable iron. Scand. J. Clin. Lab. Invest. 44:555-556; 1984. 13. Haymes, E. M.; Spillman, D. M. Iron status of women distance runners, sprinters, and control women. Int. J. Sports Med. 10:430433; 1989. 14. Lampe, J. W.; Slavin, J. L.; Apple, F. S. Poor iron status of women runners training for a marathon. Int. J. Sports Med. 7:111-114; 1986. 15. Monsen, E. R.; Hallberg, L.; Layrisse, M.; et al. Estimation of available dietary iron. Am. J. Clin. Nutr. 31:134-141; 1978.
16. Moreiras, O.; Carbajal, A.; Cabrera, M. L. La composici6n de los alimentos. Madrid: Eudema; 1992. 17. National Research Council. Commitee of Dietary Allowances. Recommended dietary allowances (10th ed.). Washington, DC: National Academy Press; 1989. 18. Newhouse, I. J.; Clement, D. B. Iron status in athletes. An update. Sports Med. 5:337-352; 1988. 19. Nowak, R. K.; Knudsen, K. S.; Schulz, L. O. Body composition and nutrient intakes of college men and women basketball players. J. Am. Diet. Assoc. 88:575-578; 1988. 20. Parr, R. B.; Bachman, L. A.; Moss, R. A. Iron deficiency in female athletes. Phys. Sportsmed. 12:81-86; 1984. 21. Pate, R. R.; Sargent, R. G.; Baldwin, C.; Burgess, M. L. Dietary intake of women runners. Int. J. Sports Med. 11:461-466; 1990. 22. Perron, M.; Endres, J. Knowledge, attitudes, and dietary practices of female athletes. J. Am. Diet. Assoc. 85:573-576; 1985. 23. Raper, N. R.; Rosenthal, J. C.; Woteki, C. E. Estimates of available iron in diets of individuals 1 year old and older in the Nationwide Food Consumption Survey. J. Am. Diet. Asocc. 84:783-787; 1984. 24. Short, S. H.; Short, W. R. Four-year study of university athlete's dietary intake. J. Am. Diet. Assoc. 82:632-645; 1983. 25. Snyder, A. C.; Dvorak, L. L.; Roepke, J. B. Influence of dietary iron source on measures of iron status among female runners. Meal. Sci. Sports Exerc. 21:7-10; 1989. 26. Stookey, L. Ferrozine--a new spectrophotometric reagent for iron. Ann. Chem. 42:779-781; 1970. 27. Watkin, V. A.; Myburgh, K. H.; Noakes, T. D. Low nutrient intake does not cause the menstrual cycle interval disturbances seen in some ultramarathon runners. Clin. J. Sports Med. 1:154-161; 1991. 28. Weight, L. M.; Jacobs, P.; Noakes, T. D. Dietary iron deficiency and sports anaemia. Br. J. Nutr. 68:253-260; 1992. 29. Weight, L. M.; Klein, M.; Noakes, T. D.; Jacobs, P. 'Sports anemia' - - A real or apparent phenomenon in endurance-trained athletes? lnt. J. Sports Med. 13:344-347; 1992. 30. Wick, M.; Pinggera, W.; Lehmann, P. Ferritin in iron metabolism. New York: Springer-Verlag Wien; 1991.
ELSEVIER
0031-9384(95)02081-6
Iron Nutritional Status in Female Karatekas, Handball and Basketball Players, and Runners R A M O N JOSl~ NUVIALA, l M A R I A C A R M E N CASTILLO, M A R I A GLORIA L A P I E Z A AND JESI~IS F E R N A N D O ESCANERO
Clinical Biochemistry Department, University Hospital, 50009 Zaragoza, Spain Received 14 March 1995 NUVIALA, R. J., M. C. CASTILLO, M. G. LAPIEZA AND J. F. ESCANERO. Iron nutritional status in female karatekas, handball and basketball players, and runners. PHYSIOL BEHAV 59(3) 449-453, 1996.--The iron nutritional status was studied in 84 sportswomen (19 karatekas, 20 handball players, 20 basketball players, and 25 middle and long distance runners) and in 82 nonathletic females of similar characteristics (control group). After a 7-day nutritional survey by means of the food weighing method, it was found that iron intake was significantly higher in the handball players ( p < 0.05), basketball players ( p < 0.01), and runners ( p < 0.01) with regard to the control group; the basketball players were the only ones to cover the recommended minimum intake (15 mg/day). The heme iron intake was significantly greater in the handball and basketball players ( p < 0.01), who, together with the runners, reached the value of 1.5 mg/day, which is considered to be optimal. In relation to the control group, the karatekas and handball and basketball players had lower levels of serum ferritin, although their iron intake was greater, whereas the runners had higher values that were very similar to those of the control group, due to the iron supplementation they had received. Despite finding a marked prevalence of inadequate iron intake, both in the sportswomen and in the control group, the manifest cases of anemia are relatively scarce. The organic iron stores do not seem to depend exclusively on the iron intake but also on intimate mechanisms of intestinal absorption and diverse causes of iron loss. Females
ilron status
Heme iron
Karate
ALTHOUGH iron loss in sportswomen may have very diverse causes, it should be pointed out that the deficiency of this micronutrient seems to lae mainly caused by insufficient intake (4,6,18). Moreover, the absorption of iron does not depend only on the total quantity of iron intake, but also on the bioavailability of iron in food, with a different percentage of intestinal absorption according to whether it is heme or nonheme iron (11,15). All this leads to the concept that the diet must not only contain a minimum amount of iron (15 mg/day for women) but also that the heme iron intake must be sufficient (10% of the total intake), as established by the U.S. Recommended Dietary Allowances (17,23). Most studies related to the iron nutritional status in sportswomen have been performed on long distance runners (5,7,14,27); there are few conceming predominantly explosive sports or team sports, and those that do exist are somewhat incomplete (9,19). The aim of the present article was to study the iron nutritional status in women who practise an explosive sport such as karate,
Handball
Basketball
Runners
two team sports such as handball and basketball, and an endurance activity such as middle and long distance running, to establish the possible relationship between iron intake and its organic stores, and whether there are differences between the different groups of sportswomen. METHOD
Subjects Eighty-four female athletes between 16 and 29 years of age who took part in national and international competitions participated in the study (19 karatekas, 20 handball players, 20 basketball players, and 25 middle and long distance runners). At the same time, a group of 82 females of a similar age range who did not participate in physical activities was studied (control group). They were all previously informed of the aim of the study and gave written consent. They were interviewed personally as to the number of hours per week dedicated to training and to the
t Requests for reprints should be addressed to Ram6n Jos6 Nuviala, M.D., Serviciode BioqufmicaCffnica, Hospital Cl~nicoUniversitario,Avda. San Juan Bosco, 15, 50009 Zaragoza, Spain.
449
450
NUVIALA ET AL.
TABLE 1 PHYSICAL CHARACTERISTICS AND LEVEL OF TRAINING Control n Age (years) Weight (kg) Height (cm) Menarche age (years) Practice time (years) Training ( h / w e e k )
82 21.0 57.0 160.8 13.0 ---
5:2.8 5:7.6 _+ 5.2 5:1.3
Karate 19 20.1 56.7 160.7 12.6 6.8 5.8
5:3.4 + 5.0 + 6.0 +_ 1.2 5:3.4 5:3.0
Handball 20 19.9 62.3 164.3 12.8 8.9 7.9
5:3.6 5:7.8 5:4.3 5:1.2 5:2.0 5: 1.7
Basketball
Runners
20 19.2 _+ 2.3 67.1 5: 11.2 172.3 + 9.2 13.4_+ 1.3 8.1 5: 3.5 8.3 5: 2.2
25 20.0 _+ 3.6 54.1 5:4.9 165.3 + 6.0 13.5+ 1.9 7.2 + 3.1 t0.3 + 3.2
Values are mean + SD.
practice of their particular sport. To eliminate those presenting serious abnormalities, they were also required to note down the date of their menarche and the characteristics of their menstrual cycles as precisely as possible. If they were regular, they were asked their duration and the intensity of their menstrual hemorrhages. Finally, they were also asked if they took contraceptives.
Dietary Survey Subjects completed a 7-day dietary survey using the food weighing method. Prior to the survey, they were provided with a precision balance (Postal Power TM model) so that they could weigh all their food, both solid and liquid, with a total capacity of 2 kg, a resolution of l g, and a precision of + 1 % in each weighing operation. Furthermore, they were given the corresponding instructions that explained the correct way to weigh the different foodstuffs and it was emphasized that they should not modify their normal diet during the period of the dietary survey. The surveys were checked by two different specialists to see that they had been filled in correctly, and those that did not fulfil this condition were rejected. The evaluation of the foodstuffs was carried out by means of a computerized programme based on the food composition tables for the Spanish population (16). From the surveys the mean daily intake of total energy, total iron, and heine iron was calculated [the heine iron intake according to the U.S. Recommended Dietary Allowances (17), which consider it to be 40% of the total iron contained in meat, fish, and poultry]. Afterwards, the iron density per 1000 kcal was calculated. All subjects were asked if they took pharmacological supplements and, in particular, iron supplements.
in a vacuum tube (Vacutainer) to obtain the serum. This was stored at - 30°C until the moment of analysis. The samples with anticoagulant were processed immediately. The hematocrit was determined in triplicate by means of microcentrifugation. Hemoglobin and the red blood cell count were measured in a STKS model hematological cell counter (Coulter Electronics, Inc.). From these parameters the mean corpuscular volume (MCV), the mean corpuscular hemoglobin (MCH) and the mean corpuscular hemoglobin concentration (MCHC) were calculated. The serum iron was determined in the serum samples by means of the ferrozine method (26) in a Synchron CX5 autoanalyzer (Beckman). The serum ferritine was evaluated in duplicate by means of an enzyme-immunoassay (Boehringer Mannheim), calculating the mean value. Transferrin and haptoglobin were determined by kinetic immunonephelometry, Array 360 (Beckman).
Statistical Analysis It was carried out after the kurtosis calculation. When me value obtained was between + 1 and - 1 it was considered that the sample distribution was normal, in which case the Student's test was performed. If, on the other hand, the kurtosis value was outside this range, it was accepted that the sample distribution was not normal and the nonparametric Mann-Whitney U-test was used. In both cases the level of significance was established for p < 0.05 and p < 0.01. RESULTS
Hematological Analysis The analysis was carried out halfway through the dietary survey. The blood samples were taken in the laboratory after a minimum period of a 10-h fast. The samples obtained were divided into two tubes: one with an anticoagulant (K3-EDTA) for the determination of the hematological parameters, and the other
The physical characteristics and the level of training can be seen in Table 1. The mean age of the appearance of the menarche was slightly lower in the karatekas and handball players but no significant differences were found. Three members of the control group referred to amenorrhea experience and 6 of the 25 runners were found in the same situation. No differences in ferritin serum
TABLE 2 ENERGY AND TOTAL, HEME AND NONHEME IRON INTAKE Control Energy intake (kcal/day) Iron intake(rag/day) Irondensity(mg/1000kcal) Heme iron intake ( m g / d a y ) Heme iron intake (% of total) Nonheme iron intake ( m g / d a y )
1969.2 11.3 5.9 1.34 11.9 10.0
Values are mean + SD. *~"Student's test: * p < 0.01, f p < 0.05. .~ Mann-Whimey's test: ~ p < 0.01.
+ 437.9 5: 2.8 5: 1.4 5: 0.52 5: 4.0 5: 2.6
Karate 2008.7 5:495.1 12.7"5: 3.7 6.4 5: 1.7 1.45 5: 0.69 11.6 __. 4.8 11.2 5: 3.4
Handball 2284.6 12.9 5.8 1.75 13.3 11.2
+ 547.6* + 2.7t 5: 1.1 5: 0.51" + 2.1 + 2.3
Basketball 2560.6 15.8 6.3 2.15 13.7 13.7
+ 470.5* 5: 2.7 5: 1.3 5: 0.65~ 5: 4.0 5: 2.6*
Runners
2003.0 13.6 6.9 1.53 11.2 12.0
+ 506.9 5: 4.0* 5: 1.8~ 5: 0.73 5: 4.5 5: 3.7*
IRON NUTRITION IN F E M A L E ATHLETES
451
TABLE 3 HEMATOLOGICAL AND BIOCHEMICAL PARAMETERS RELATED TO IRON METABOLISM Hematocrit(%) Hemoglobin(g/dl) Red cell count (106/mm 3) MCV(Iz 3) MCH (pg) MCHC(g/dl) Iron (/xg/dl) Transferrin (mg/dl) TRF saturation (%) Ferritin (ng/ml) Haptoglobin (mg/dl)
Control
Karate
40.1 + 2.2 13.2 4- 0.8 4.33 ± 0.29 92.8 4- 4.8 30.5 4- 1.8 32.9 4- 1.1 89.7 4- 38.6 317.7 4- 52.6 29.3 + 13.9 36.1 4- 26.2 83.2 4- 35.6
39.9 + 2.1 12.9 4- 0.8 4.41 4- 0.35 91.0 4- 7.0 29.5 4- 2.5 32.4 4- 0.9 64.8 4- 25.0* 321.4 4- 45.3 20.7 4- 9.226.7 4- 17.3 84.6 + 31.9
Handball
39.9 + 13.2 ± 4.34± 92.2 ± 30.5 + 33.1 ± 86.9 + 305.8 + 28.8 ± 26.7 ± 64.3 +
2.1 0.8 0.28 4.8 1.2 1.1 35.9 40.4 12.1 18.2 23.6~
Basketl:mll
Runners
39.7 ± 3.2 12.8 ± 1.3 4.29± 0.32 92.8 ± 7.5 29.9 ± 3.1 32.2 + 1.8 73.9 + 38.0 330.7 + 44.3 23.7 ± 13.9 28.1 4- 22.9 65.7 4- 41.3-~
41.0 ± 2.7 13.4 + 0.8 4.35 ± 0.23 94.3 ± 4.6 30.9 ± 1.5 32.8 ± 1.0 86.9 5- 43.6 333.8 4- 48.8 27.5 ± 15.4 34.6 ± 23.0 59.4 4- 32.7~
Values are mean __.SD. *¢ Student's test: * p < 0.01, - p < 0.05. - Mann-Whitney's test: :~ p < 0.05.
levels were found between amenorrheic and eumenorrheic runners. The energy intake was significantly greater in the handball and basketball players ( p < 0.01) in relation to the intake of the control group (Table 2). The total iron intake showed significantly higher levels in the handball players ( p < 0.05), the basketball players ( p < 0.01), and in the runners ( p < 0.0 I); the basketball players wen; the only ones to reach the minimum intake of 15 m g / d a y . The density of i r o n / 1 0 0 0 kcal was significantly greater in the runners ( p < 0.01). With regard to the heme iron intake, both the handball and basketball players showed significantly higher values ( p < 0.01) than the control group. The percentage of berne iron intake in relation to the total iron intake was higher in the handball and basketball players, but no significant differences were found with regard to the control group. Finally, the nonheme iron intake was significantly greater in the basketball players and the runners ( p < 0 . 0 1 ) . It should be underlined that none of the control group took iron supplements, whereas 11 of the 25 runners did take supplementation that ranged from 10 to 210 m g / d a y of elemental iron. The supplementary intake has not been included in the mean intake of this micronutrient. At the same time, no significant differences in the serum ferritin level were found between the runners taking iron supplementation (29.7 :± 17.8 n g / m l ) and those who did not (38.4 _+ 26.4 n g / m l ) . With regard to the hematological parameters (Table 3), the values found were very similar in all the groups studied, without significant differences between the sportswomen and the control group. Both the serum iiron ( p < 0.01) and the transferrin saturation percentage ( p < 0.05) had significantly lower values in the karatekas than in the control group. The levels of haptoglobin were significantly lower ( p < 0.05) in the handball and basketball players and in the runners, who showed the lowest value.
Seventy-three members of the control group (89.0%) did not reach the minimum iron intake of 15 m g / d a y (Table 4), whereas the total among the sportswomen was 53 (63%), with a greater percentage of deficiency in the handball players (80%). Twentyfive females from the control group (30.4%) had ferritin levels under 20 n g / m l and 32 sportswomen were in the same situation, with a higher percentage of iron deficiency among the karatekas (27.3%). Finally, five females from the control group (6.0%) and seven sportswomen (8.3%) presented a hemoglobin concentration under 12 g / d l . The anemia percentage was greater in the group of basketball players (20%). DISCUSSION The results of this study show a greater mean energy intake in the handball players and, above all, in the basketball players, which is the consequence of the greater energy output of these sportswomen. The intake of the basketball players is very similar to that reported by Short and Short (24), also on basketball players, whereas these authors found quite higher mean values of energy intake in a follow-up control performed 4 years later (24). On the other hand, Nowak et al. (19) report a much lower mean intake in female university basketball players. For the runners, the values are similar to those of Lampe et al. (14) in marathon runners and higher than those of Pate et al. (21). On the other hand, Faber and Benade (10) report a higher energy intake in field athletes. The iron intake of the sportswomen in this study seems to be related to the energy intake, with a greater value in the basketball players, who were the only ones to reach the recommended minimum intake of 15 m g / d a y (17). However, it was the runners who had a higher density of iron intake. A somewhat higher iron intake was found in the handball players than that reported by
TABLE 4 PREVALENCE OF INADEQUATE IRON INTAKE. IRON DEFICIENCY AND ANEMIA Iron Intake (< 15 mg/day) Ferritin (< 20 ng/ml) Hemoglobin [< 12 g / d l )
Control Karate Handball Basketball Runners Total athletes
Cases
%
Cases
%
Cases
%
73 12 16 8 17 53
89.0 63.1 80.0 40.0 68.0 63.0
25 9 7 9 7 32
30.4 47.3 35.0 45.0 28.0 38.0
5 2 1 4 0 7
6.0 10.5 5.0 20.0 -8.3
452
Erp-Baart et al. (9). Similarly, the intake of the basketball players was greater than that of the players studied by Nowak et al. (19), Short and Short (24), and than that reported by Perron and Endres (22) in volleyball players. Some authors (2,3,21,28) report mean iron intakes lower than those of the middle and long distance runners included in this study. On the other hand, other studies also performed on long distance runners (13,14,25) report values over the 13.6 m g / d a y found in this study. It should be pointed out that in none of these studies was the mean intake of 15 m g / d a y reached, which is considered it to be the optimal intake. Only Haymes and Spillman (13) found a mean intake of 15 m g / d a y in sprinters. With regards to the U.S. Recommended Dietary Allowances (RDA) (17), the iron intake of the control group was 75.8% of that recommended; in the sportswomen as a whole, it was 92%, with a value of 84.8% for the karatekas, 86.4% for the handball players, and 92% for the runners. The basketball players were the only ones who reached the RDA, with a mean intake of 105.9%. Nowak et al. (19) report an iron intake in female basketball players of 54%, Perron and Endres (22) a 60% intake in volleyball players, whereas Lampe et al. (14) and Pate et al. (21) found an intake of 78% and 58% in runners, respectively, taking into account that all these authors consider the minimum iron intake limit to be 18 m g / d a y . Faber and Benade (10), establishing this limit at 15 mg/day, as in this study, found an iron intake in their field athletes of 89% in relation to the RDA, which is a percentage similar to that found in our middle and long distance runners. Bearing in mind that the minimum iron intake in females should be 15 m g / d a y and that heme iron should make up about 10% of the former, the optimum mean intake of heine iron should be 1.5 rag/day. This figure is reached by the handball and basketball players and by the runners but not by the karatekas or the control group. Erp-Baart et al. (9) found a heine iron intake in female handball players of 3.2 m g / d a y and of 1.6 m g / d a y in runners, both values higher than those of the corresponding sportswomen in the present study. The analyses carried out on long distance runners show a heme iron intake lower than the recommended minimum (13,25,28). Only Haymes and Spillman (13) report a mean intake of 1.5 m g / d a y in sprinters. The importance of a sufficient heine iron intake is highlighted in the study performed by Snyder et al. (25), which, in long distance runners, compares the heme iron contained in a normal diet with that contained in a vegetarian diet, finding a clearly lower concentration of serum ferritin in the case of the sportswomen with a vegetarian diet, whose content of heme iron was very low. Heme iron represents between 7% and 10% of the total dietary iron intake of females in the United States (23). In the present study, a somewhat higher percentage, which varied between the 11.2% of the runners and the 13.7% of the basketball players, was found. The mean intake of the control group was 11.9% of the total iron. According to the different studies reviewed, there is a difference of criteria regarding the minimum serum ferritin concentration considered to be an indicator of an iron deficiency state. Harju et al. (12) found that with less than 20 n g / m l of ferritin there is an absence of iron in bone marrow, whereas Wick et al. (30) established a clear difference between the 20 n g / m l , which they considered as a deficiency of stored iron, and the 12 n g / m l , which would indicate, moreover, a deficiency in its transport. For this reason, we have considered a serum ferritin concentration of 20 n g / m l to indicate deficiency in iron stores. All groups of sportswomen in this study had mean ferritin concentrations over 20 n g / m l . The lowest values were those of
NUVIALA ET AL.
the karatekas and the handball and basketball players, whereas the runners had higher concentrations that were very similar to those of the control group. However, it should be taken into account that 11 of the 25 runners regularly took iron supplements, which clearly affected the serum ferritin concentration. The majority of studies performed on long distance runners show ferritin values lower than those found in our runners (3,5,7,13,14,20,25). Durstine et al. (8) report a concentration of ferritin in elite runners similar to that of those in the present study, pointing out that 50% of them took iron supplements. Finally, Weight et al. (29) found a mean ferritin figure in their runners of 45.2 n g / m l , which is clearly higher than that of all the sportswomen included in the present series. The levels of haptoglobin were significantly lower in the handball and basketball players and in the runners with respect to the control group, which corresponds to sports with repeated floor-foot impact. This finding is similar to that reported by Haymes and Spillman (13) in long distance runners, presenting, moreover, lower levels than those found in sprinters and particularly in the control group. Clement and Asmundson (3), also referring to long distance runners, report a mean concentration of haptoglobin of 95.0 m g / d l , which is far higher than that of the runners in this study. The high value of haptoglobin found in the karatekas, similar to that of the control group, is surprising, although it might be explained because they practised the " k a t a " discipline, in which no physical contact is produced, as opposite to the " k u m i t e " discipline in which there is contact. The elevated prevalence of inadequate iron intake, both in the control group (89.0%) and in the sportswomen (63%), contrasts with the scarcity of manifest cases of anemia. This is in agreement with the conclusions of Weight et al. (29). Among the sportswomen, the greater number of cases found in the basketball players stands out because they were the ones who had the highest mean intake of total iron and heme iron and the lowest percentage of prevalence of inadequate intake (40%). At the same time, it is surprising that two of the basketball players with manifest anemia had mean iron intakes higher than that of the recommended minimums (18.2 and 17.3 rag/day), whereas the rest of the anemic females, both those of the control group and the sportswomen, did not reach this minimum. Recent studies performed at the level of the serum transferrin receptor and of the iron responsive element binding protein (IRE-BP) may possibly explain, in the near future, some of the unknown factors concerning the absorption of iron at the intestinal level (1). In conclusion, it may be said that the karatekas and the handball and basketball players studied had lower levels of ferritin than the control group, although their iron intake was higher, whereas the middle and long distance runners showed higher values of ferritin, which may be explained in some cases by intake of iron supplements. The organic iron stores in the sportswomen do not seem to depend exclusively on iron intake and its bioavailability, but also the intimate mechanisms of intestinal iron aborption and the different causes of additional iron loss must be considered. Among the sportswomen studied, it was the group of basketball players who had the greatest total iron and heme iron intakes; moreover, they were the only ones who covered the minimum requirements established by the U.S. RDA. ACKNOWLEDGEMENTS This study has been financed by a grant from the Sanitary Research Fund of the Spanish National Health Service (FIS; Exp. 92/0598).
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453
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