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Department of Pediatrics, University of Iowa, Iowa City, IA and * Department of Preventive Medicine and Community Health, University of Texas Medical Branch, Galveston, TX
2To whom correspondence should be addressed. E-mail: samfomon{at}aol.com.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • iron loss • iron requirements • stable isotopes • adolescents
Recommendations regarding the required iron intake should be based on knowledge about the amount of iron that must be absorbed to maintain iron adequacy. In the normal adult, the requirement for absorbed iron is equal to the amount of iron lost from the body. In the growing individual, the requirement for absorbed iron consists not only of iron needed to replace inevitable losses but also iron needed for growth. In this communication, we present data on the inevitable loss of iron by male and female adolescents after the peak of the adolescent growth spurt. We also present our estimates of the requirement for absorbed iron by adolescents during the same period of adolescence.
Iron is inevitably lost from the gastrointestinal tract, from the skin, and in urine and other bodily secretions. Gastrointestinal loss includes the iron of desquamated gastrointestinal lining cells and of secretions, including bile. Dermal loss includes iron in secretions, predominantly sweat, and in desquamated dermal cells. Urinary loss is trivial.
In adults, when an administered iron isotope has had sufficient time to equilibrate with total body iron, the fractional disappearance of the isotope from the circulation (where it is present almost entirely in the form of isotopically labeled hemoglobin) is the same as the fractional loss of iron from the body. Green et al. (1
) measured the disappearance of circulating isotope over long periods of time (years) and were able to estimate the loss of iron by the adult male to be 
1 mg/d.
In the growing individual, the determination of inevitable iron loss is more complicated. Apparent disappearance of an isotope from the circulation is not only the result of loss of isotope (and iron) from the body, but also the result of expansion of the total body iron pool in which the isotope is distributed. Thus, in the present study of adolescents, we were unable to assume, as did Green et al. (1
), that once the label had been distributed throughout total body iron, fractional disappearance of circulating isotope is the same as fractional loss of total body iron. However, an alternate approach was available. We could calculate total body isotope from isotopic enrichment of circulating iron and estimates of total body iron. From determinations of enrichment of circulating iron at two times after the administered isotope had equilibrated with total body iron, we could calculate the fractional loss of isotope from the body. Because the fractional loss of total iron would be the same as the fractional loss of isotope, we could estimate loss of iron from the body (fractional isotope loss times mean total body iron over the interval). We contend that we can make satisfactory estimates of total body iron and that the assumptions required for this approach are sufficiently robust to lead to an acceptable estimate of inevitable iron loss.
The opportunity to determine isotopic enrichment of circulating iron arose as a consequence of studies of iron absorption that we conducted with preadolescent children from 1986 to 1990. In these studies we used the stable isotope, 58Fe, as a label [(2
,3
) and unpublished data]. In some of these subjects, we were able to obtain additional blood samples on two occasions several years apart and analyses of these samples permitted determination of inevitable iron loss.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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Subjects.
The subjects whose data are reported in this communication had received 58Fe orally as participants in one or more of four studies. One study was designed to examine the usefulness of 58Fe in determining the availability of nonheme iron from meals (2
); the second study (unpublished) was designed to determine the absorption of heme iron from meals; the third and fourth studies were designed to determine whether there is a gender-related difference in erythrocyte incorporation of 58Fe (3
). At the time of 58Fe administration, the children ranged from 7.2 to 11.3 y of age (Table 1
), were believed to be healthy and were preadolescent, i.e., Tanner stage 1 (4
). A baseline blood sample was obtained before 58Fe administration, and additional blood samples were obtained subsequently, including a sample obtained 14 d after 58Fe administration. Of the subjects who participated in these studies, we were able to obtain two blood samples (after the 14-d sample) from 10 males and 13 females.
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Throughout this presentation, "Time 1" refers to the time at which blood sample 1 was obtained, i.e., the blood sample obtained 2 wk after isotope administration. (The corresponding anthropometric measurements were made on the day of isotope administration.) Time 2 is the time at which blood sample 2 was obtained (1.56–3.84 y after obtaining blood sample 1); and Time 3 is the time at which the final sample of blood (blood sample 3) was obtained (3.29–4.43 y after Time 2). The interval between Time 1 and Time 2 is referred to as Interval 2 and that between Time 2 and Time 3 is referred to as Interval 3.
Anthropometry and Tanner staging.
At the time of isotope administration and at Time 2 and Time 3, measurements of weight and height were made by standard anthropometric procedures (5
), weight to the nearest 100 g and height to the nearest 0.1 cm. At Time 1 and Time 2, pubertal development was assessed as described by Tanner (4
). All subjects were Tanner stage 1 at Time 1 and all were Tanner stage 2 or higher at Time 2.
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Blood sampling and analysis |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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7 mL) was obtained by antecubital venipuncture and placed in heparinized tubes. Hemoglobin (Hb)3 was determined by Coulter Counter, model M430 (Coulter Electronics, Hialeah, FL) soon after blood collection. Plasma was separated from cells by centrifugation and both plasma and packed cells were stored at -20°C until the time of analysis. Plasma was analyzed for ferritin concentration by immunoradiometric assay, using the Quantimune kit (BIO-RAD Laboratories, Hercules, CA). Isotopic analysis.
Blood samples 1 and 2 were analyzed at BioChem Analysis, Chicago, IL. The analyses were carried out by inductively coupled plasma mass spectrometry (ICP/MS), using an Elan 250 ICP/MS System (Sciex, Thornhill, Canada). The method has been described in detail and the precision is believed to be 0.35% relative SD (rsd) (6
). Blood sample 3 was analyzed in the laboratory of one of the authors (R.E.S.) using a Finnigan Sola ICP/MS (Finnigan MAT, Hemel, Hempstead, UK). The method has been described in detail (7
). The internal precision for the 58Fe/57Fe isotope ratio at or near natural abundance was between 0.15 and 0.40 (mean 0.24) % rsd (8
).
Although the two laboratories performed isotope ratio analyses with comparable precision, we cannot rule out bias. Circumstances did not permit the performance of direct comparisons between the two laboratories. Because each laboratory corrected for the mass bias observed for natural abundance of 58Fe during each instrumental run, bias is likely to be small. If we assume, for example, that analyses of blood sample 2 gave results 5% greater than would have been obtained by the laboratory that analyzed blood sample 3, enrichment of blood sample 2 would have been overestimated (relative to blood sample 3) by 5%. Consequently, the rate of iron loss would have been overestimated by 5%. The effect would have been that iron loss by males would have been estimated at 0.735 mg/d rather than 0.700 mg/d, and iron loss of females would have been estimated at 0.882 mg/d rather than 0.840 mg/d. Given the variance of the estimates (0.32 mg/d and 0.38 mg/d, respectively), the possible error introduced by such a bias is unlikely to be a major factor.
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Calculations |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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Total body iron (TFe) at any age consists of "active" iron and iron in storage (Festor). Active iron consists of Hb iron, myoglobin iron and the iron of various enzymes and of iron transport proteins. In this communication we have, for simplicity, classified the iron compartments as Fecirc (entirely in the form of Hb, thus ignoring the minor contribution of circulating iron-containing enzymes and iron transport proteins), Fenca (iron in myoglobin, in noncirculating iron-containing enzymes and iron associated with noncirculating iron transport proteins) and Festor. In the adolescent, Festor is present primarily in ferritin but also in small amounts in hemosiderin. The estimation of Fecirc is presented below. On the basis of the usual relation in the adult between Fecirc and Fenca (9
), we assumed that the quantity of Fenca in the normal adolescent is 20% of Fecirc.
For reasons to be discussed, in adolescent subjects with plasma ferritin (PF) 
10 µg/L, we based our calculations of Festor on the assumption that 1 µg/L PF equals 109 µg of Festor/kg body, as calculated from the data of Skikne et al. (10
) for adult subjects. PF values < 10 µg/L were considered to indicate zero iron stores. We calculated TFe as the sum of the three identified components, i.e., Fecirc, Fenca and Festor.
Total body isotope.
The quantity of 58Fe label in the body (T58Fe) was calculated as follows:
 | (1) |
where total 58Fe (T58Fe) is expressed in mg, TFe is the quantity of total body iron at time t expressed in mg, 2.119 is the natural abundance (atom %) of 57Fe, IRt is the determined 58Fe/57Fe isotope ratio at time t after dosing, IR0 is the determined 58Fe/57Fe ratio at baseline, 57.933 is the molar mass of 58Fe, and 55.845 is the molar mass of natural iron. Throughout the presentation, reference to 58Fe applies to administered 58Fe label, excluding naturally present 58Fe.
The quantity of circulating iron was estimated as follows:
 | (2) |
where Hb is hemoglobin concentration (g/L), 3.47 is the concentration of iron in Hb (mg/g) and BV is blood volume (L) calculated for each subject from weight in kg and height in cm, using the gender-specific regression equations of Linderkamp et al. (11
) for subjects < 15 y old, and the gender-specific regression equations of Nadler et al. (12
) for subjects 15 y old.
Loss of total body iron.
The fractional loss per year of T58Fe during Interval 3 was calculated as the difference in T58Fe between Time 2 and Time 3 divided by the mean amount of T58Fe divided by the elapsed time from Time 2 to Time 3. The TFeloss (mg/y, mg/d) during Interval 3 was calculated from the mean total body iron (TFemean) during the interval multiplied by the fractional loss of 58Fe.
Statistical methods.
Data were analyzed using SAS version 6.12 (SAS Institute, Cary NC). Age effects were assessed on a gender-specific basis using repeated-measures ANOVA, equivalent to paired t tests. Gender differences were assessed by F-test from ANOVA. Differences were considered significant at the 
level of 0.05. Although sample size was fixed and limited for this retrospective study, age and gender differences of 1.25 SD could be detected with a power of 0.80.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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Individual data concerning various subject characteristics are presented for the 10 male and 13 female subjects at Times 1, 2 and 3 (Table 1)
; summary data for age at Times 1, 2 and 3, elapsed time during Intervals 2 and 3, and gains in weight and height during Intervals 2 and 3 are also presented (Table 2
). Iron and 58Fe data and calculations in various body compartments are included in Tables 3
, 4
and 5
.
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). The laboratory performing the analyses of blood sample 3 routinely performed repeated analyses of unenriched (baseline) material throughout the day. The precision of analyses varied somewhat from day to day, and only samples whose enrichment was > 3X%rsd above baseline for the day were reported as being enriched.
Males.
The slightly lesser gains in height during Interval 3 than during Interval 2 suggested that the majority of the males were beyond the peak of the adolescent growth spurt during Interval 3. As was to be anticipated, Hb was greater at Time 3 than at Time 2 (P < 0.001) (Table 1)
. PF data indicated that, with the exception of Subject 44 at time 3, iron nutritional status was adequate throughout the study. The elevated PF-values for Subjects 30 and 42 at Time 3 were assumed to be caused by acute reactions; therefore, for the purpose of calculating storage iron, these values were replaced by the value 24 µg/L, i.e., the mean value for the remaining eight subjects. At time 3, mean 58Fe enrichment of Fecirc was 3.59% (range 1.58–6.99%).
Total body iron is presented as the sum of iron in the three iron compartments: Fecirc, Fenca and Festor (Table 3)
. Because of complete mixing of the isotope with TFe during Interval 3, fractional total 58Fe loss was the same as the fractional loss of TFe. Fractional iron loss was 9.70%/y. Quantitative loss (fractional loss times TFe) was 255 mg/y [0.70 mg/d; 95% confidence interval (CI) 0.47–0.93 mg/d].
Females.
The considerably lesser gains in height during Interval 3 than during interval 2 indicated that most of the females were beyond the peak of the adolescent growth spurt during Interval 3. Hb remained within normal limits throughout the study (Table 1)
. Plasma ferritin concentrations indicated adequate iron nutritional status at Time 1. Only Subject 31 (PF 9 µg/L) appeared to be iron deficient at Time 2. The geometric mean for PF decreased from 19.6 µg/L at Time 2 to 15.0 µg/L at Time 3 (P = 0.28). At Time 3, three subjects (#16, 31, 52) were iron deficient and Subject 45 (PF 11 µg/L) had low Festor. Mean TFeloss by the three iron-deficient subjects (#16, 31 and 52) and the subject (#45) with PF of 11 µg/L was not significantly greater than that by the other female subjects (P = 0.40). At Time 3, mean 58Fe enrichment of Fecirc was 3.55% (range 0.98–9.62%).
The quantity of Festor in females was low at Times 2 and 3 and, at Time 3 was less, although not significantly less (P = 0.28) than that of males (Table 3)
. The increase in Fecirc during Interval 3 was considerably less (P < 0.001) for females than for males (Table 5
), reflecting both the slower growth of females and the lesser increase in Hb. Consequently, the increase in TFe was less (P < 0.001) in females. Fractional iron loss was 14.60%/y. Quantitative loss during Interval 3 (Table 5)
was 306 mg/y (0.84 mg/d; 95% CI 0.60–1.07 mg/d).
Adolescent requirement for absorbed iron
In growing individuals, the requirement for absorbed iron consists not only of iron needed to replace inevitable losses, but also of iron needed for growth. Iron needed for growth (Fegrow) was calculated as the sum of the increases in Fecirc, Fenca and Festor from Time 2 to Time 3 (Table 5)
. We estimated Fecirc, Fenca and Festor as already described. The calculated iron requirement for growth during Interval 3 was 280 mg/y (0.77 mg/d) for males and 113 mg/y (0.31 mg/d) for females. Because rate of growth is a major factor in determining the need for active iron during Interval 3, the greater increase in weight and height by males than by females (Table 2)
explains their greater need for iron for growth. In males Fegrow was greater than TFeloss, whereas in females Fegrow was considerably less than TFeloss (Table 5)
.
We estimated the requirement for absorbed iron by adolescents after the peak of the adolescent growth spurt by adding the TFeloss to Fegrow (Table 5)
. For males, the requirement for absorbed iron is 535 mg/y (1.47 mg/d) and for females, 419 mg/y (1.15 mg/d). The difference between genders was significant (P = 0.024).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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,3
) and unpublished data], we administered the least abundant stable isotope of iron, 58Fe, and obtained, in addition to a baseline sample, a sample of blood for isotope ratio determinations 2 wk after isotope administration. Two additional blood samples were obtained subsequently and analyzed for Hb, PF and the 58Fe/57Fe isotope ratio. Blood sample 2 was obtained (at time 2) no sooner than 1.56 y after blood sample 1, and blood sample 3 (at Time 3) no sooner than 3.29 y after blood sample 2. Because Green et al. (1
) provided evidence that in normal adult males, complete distribution of an administered iron isotope throughout TFe occurs by 11 mo after administration, we believe that in our study equilibration of the administered 58Fe with TFe was complete by Time 2.
In growing individuals in whom an isotope has equilibrated throughout the body iron pool, isotopic enrichment of Fecirc and TFe decline over time because of expansion of the TFe. This decline is in addition to the decline caused by fractional iron loss from the body and replacement by unenriched iron. Therefore, it was necessary to calculate inevitable iron loss differently than did Green et al. (1
). From the determined enrichment of Fecirc and the estimated TFe at Time 2 and Time 3, we calculated total body 58Fe at both times and, from the difference, calculated fractional loss of T58Fe. Mean TFe times fractional loss of T58Fe yielded TFeloss. Calculated TFeloss by female adolescents after the peak of the adolescent growth spurt (306 mg/y, 0.84 mg/d) was greater than that by males (255 mg/y, 0.70 mg/d), explained mainly by loss of iron during menstruation.
We have more confidence in the generalizability of our estimate of inevitable loss of iron by males than by females because, in the absence of data on usual menstrual loss of iron by adolescent females after the peak of the adolescent growth spurt, we cannot judge whether the iron loss by the 13 females in our study reflects such loss by the relevant general population.
Inevitable iron loss by adolescent males in our study may be compared with the inevitable loss reported by Green et al. (1
) from their study of adult males. Excluding two groups with iron overload, mean TFeloss (mg/d) by three groups was as follows: Caucasian subjects in Seattle, WA, 0.95; mestizos in Venezuela, 0.90; Indians in Durban, South Africa, 1.02. Loss of iron by the male adults studied by Green et al. (1
) was greater than the mean of 0.70 mg/d by the adolescent males in our study, and the difference was significant with respect to the Caucasian subjects (P < 0.05) and the Durban Indians (P < 0.05) but not the Venezuelan mestizos. Because Green et al. (1
) did not specify body weights, we have assumed a mean weight of 70 kg for the male Caucasian subjects to make a rough comparison of inevitable iron loss by this group with that of our adolescent males. Inevitable iron loss was 0.014 mg/(kg · d) by the adult males, a value not greater (P = 0.15) than the 0.012 mg/(kg · d) by the adolescent males. Thus, TFeloss/kg body of the adolescent males in our study was not shown to be significantly different from that by male adults.
Evidence supporting the assumption that after sufficient time, an iron isotope in the circulation becomes completely distributed through the body iron pool was provided by study of an individual who had been given 55Fe 36 mo previously (14
). This subject underwent repeated phlebotomy until anemia developed. Specific 55Fe activity of the blood obtained by phlebotomy remained constant until iron stores were exhausted, demonstrating that equilibrium among circulating iron, noncirculating active iron and storage iron had been established.
It is necessary to examine the two assumptions on which the calculation of TFe depends: 1) in iron-sufficient adolescents, the relationship between Fecirc and Fenca was similar to the relationship in adults and remained constant during the period of study; and 2) 1 µg/L of PF is equivalent to 109 µg storage iron/kg body, as calculated from the data of Skikne et al. (10
). The assumption that Fenca is 20% of Fecirc rests entirely on analogy with the relationship in adults (9
). However, Fenca is a relatively small percentage of TFe and, therefore, if the Fenca were 18 or 22% rather than 20% that of Fecirc, the change in calculated TFe would not be greatly affected.
The relationship between PF and Festor has been determined in adults by studies in which PF was related to the quantity of iron removed by successive phlebotomy and corrected for the quantity of iron assumed to have been absorbed over the time of the study. The results indicate that 1 µg/L of PF is equivalent to 8–10 mg of Festor (15
). Finch et al. (15
) suggested that for children and small adolescents, it would be better to consider 1 µg/L of PF equivalent to 120 µg/kg of Festor. This relation is quite similar to that determined by Walters et al. (16
), i.e., 1 µg/L PF reflects Festor of 8 mg, which corresponds to 114 µg/kg for a 70-kg adult. As calculated from the data of Skikne et al. (10
), we have assumed that 1 µg/L of PF reflects Festor of 109 µg/kg. Until data are available on the relationship between PF and Festor in adolescents, we contend that adult values per unit of body weight are likely to give a reasonable estimate for adolescents.
Calculations of Fenca and Festorare based on analogy with what has been established over many years for the adult with the use of radioisotopes, and there are few data available to indicate how body iron compartments in the adult relate to those of infants, children or adolescents. This is an important area for further study.
The requirement for absorbed iron is greater for males than for females, indicating that the menstrual loss of iron by females is not sufficient to override the considerably greater iron needs for growth by males. We believe that the requirement for absorbed iron estimated from data obtained from our study of 10 males is likely to be reasonably representative of that of adolescent males after the peak of the adolescent growth spurt. As already indicated, we have less confidence in the generalizability of our estimate of the requirement for absorbed iron by females.
Our estimate of the requirement for absorbed iron by adolescent males after the peak of the growth spurt (1.47 mg/d) is 50% greater than the 1 mg/d (1
) requirement for adult males. Nevertheless, in the United States, iron deficiency is not common in adolescent males. In the 1976–1980 National Health and Nutrition Examination Survey (NHANES II) iron deficiency with or without anemia was < 1% for 14- to 19-y-old males and only slightly greater than that for adult males (17
). In the subsequent survey from 1988 to 1994 (NHANES III), iron deficiency was 1% for 12- to 15-y-old males and < 1% for 16- to 19-y-old males (18
). Iron deficiency with anemia was < 1% in both age groups.
It seems likely that nearly all adolescent males are able to absorb 1.5 mg/d of iron from their usual diet. On the basis of data from the U.S. Total Diet Study for the years 1991–1996, Egan et al. (19
) reported mean iron intake of 14.8 mg/d by 14- to 16-y-old males. For the years 1982–1986, the respective values were 17.4 and 15.9 mg/d (20
). The percentage of nonheme iron absorption is inversely related to the size of iron stores (21
–23
) and mean iron stores by the adolescent males in our study were estimated to be 108 mg at Time 2 and 161 mg at Time 3; these are considerably less than the 700 mg of adult males (16
). Although the relation of PF to the percentage absorption of iron is well established for adults (22
,24
), no data are available on whether the relation of iron stores to iron absorption or the relation of PF to iron absorption is the same for adults and adolescents.
The requirement for absorbed iron by the female adolescents in our study was estimated to be 1.15 mg/d, and it is evident from the low PF-values of four subjects at Time 3 (11 µg/L Subject 45; <10 µg/L Subjects 16, 31, 52; Table 1
) that 4 of the 13 female adolescents in our study failed to meet their needs for absorbed iron. U.S. national surveys have documented the prevalence of iron deficiency in adolescent females (17
,18
,25
), with estimates of iron deficiency in 1976–1980 (NHANES II) ranging from 2.7 to 6.1% for those 11–14 y old and from 2.5 to 14.2% for those 15–19 y old (17
). The prevalence of iron deficiency in females from 1988 to 1994 (NHANES III) was reported by Looker et al. (18
) to be 9% for 12- to 15-y-olds (iron-deficiency anemia 2%) and 11% for 16- to 19-y-olds (iron-deficiency anemia 3%).
Iron intakes are 11 mg/d by females 14–16 y old (19
,20
). The mean calculated requirement for growth by the four iron-deficient subjects in our study was not greater than that by the other female subjects. Although we cannot exclude the possibility that menstrual losses by the iron-deficient subjects were substantially greater than those by the other subjects, it seems likely that iron deficiency resulted, at least in part, from low intake of bioavailable iron.
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FOOTNOTES |
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3 Abbreviations used: CI, confidence interval; Fecirc, circulating iron; Fegrow, iron incorporated into newly synthesized tissues; Fenca, noncirculating active iron (i.e., TFe - Fecirc - Festor); Festor, storage iron; Hb, hemoglobin concentration; ICP/MS, inductively coupled plasma/mass spectrometry; IR, 58Fe/57Fe isotope ratio; NHANES, National Health and Nutrition Examination Survey; PF, plasma (or serum) ferritin concentration; rsd, relative standard deviation; TFe, total body iron; TFeloss, total iron loss.
Manuscript received 7 June 2002. Initial review completed 8 July 2002. Revision accepted 21 October 2002.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSBlood sampling and analysisCalculationsRESULTSDISCUSSIONLITERATURE CITED |
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1. Green, R., Charlton, R., Seftel, H., Bothwell, T., Mayet, F., Adams, B., Finch, C. & Layrisse, M. (1968) Body iron excretion in man. A collaborative study. Am. J. Med. 45:336-353.[Medline]
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3. Woodhead, J. C., Drulis, J. M., Nelson, S. E., Janghorbani, M. & Fomon, S. J. (1991) Gender-related differences in iron absorption by preadolescent children. Pediatr. Res. 29:435-439.[Medline]
4. Tanner, J. M. (1962) Growth at Adolescence 2nd ed. 1962:28-39 Blackwell Oxford, UK.
5. Gordon, C. C., Chumlea, W. C. & Roche, A. F. (1991) Stature, recumbent length, and weight. Lohman, T. G. Roche, A. F. Martorell, R. M. eds. Anthropometric Standardization Reference Manual abridged ed. 1991:3-8 Human Kinetics Champaign, IL. .
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18. Looker, A. C., Dallman, P. R., Carroll, M. D, Gunter, E. W. & Johnson, C. L. (1997) Prevalence of iron deficiency in the United States. J. Am. Med. Assoc. 277:973-976.
19. Egan, S. K., Tao, S.S.-H., Pennington, J.A.T. & Bolger, P. M. (2002) US Food and Drug Administration’s Total Diet Study: intake of nutritional and toxic elements, 1991–96. Food Addit. Contam. 19:103-125.[Medline]
20. Pennington, J.A.T., Young, B. E. & Wilson, D. B. (1989) Nutritional elements in U. S. diets results from total diet study, 1982–1986. J. Am. Diet. Assoc. 89:659-664.[Medline]
21. Bothwell, T. H., Charlton, R. W., Cook, J. D. & Finch, C. A. (1979) Iron Metabolism in Man 1979:276 Blackwell Scientific Publications Oxford, UK. .
22. Cook, J. D., Lipschitz, D. A., Miles, L.E.M. & Finch, C. A. (1974) Serum ferritin as a measure of iron stores in normal subjects. Am. J. Clin. Nutr. 27:681-687.[Abstract]
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