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Iron Absorption during Recovery from Malnutrition

Instituto de Nutricion Humana, Hospital Civil "Dr. Juan I. Menchaca," Universidad de Guadalajara, Guadalajara, Jalisco, MEXICO (E.V.G., I.S.T.)
Department of Pediatrics University of Iowa, Iowa City, Iowa (S.E.N., E.E.Z., R.R.R., S.J.F.)
BioChemAnalysis Corporation, Chicago, Illinois (M.J.)

Address reprint requests to: Samuel J. Fomon, MD, Department of Pediatrics, University of Iowa Hospitals and Clinics, 200 Hawkins Drive, Iowa City, Iowa 52242. E-mail: samfomon{at}aol.com

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Objective: In infants and children recovering from severe malnutrition, iron deficiency is common, and the ability to absorb iron during such recovery is uncertain. The objective of this study was to determine iron absorption during recovery from malnutrition.

Methods: During the later stages of recovery from malnutrition, erythrocyte incorporation of orally administered ⁵⁸Fe was determined as a surrogate for iron absorption. Based on four indices, subjects were classified as iron-sufficient, iron-deficient or indeterminate.

Results: Of the 25 subjects, 9 were classified as iron sufficient, 5 as indeterminate and 11 as iron deficient; all but 5 had evidence of inflammation or infection. Geometric mean erythrocyte incorporation of ⁵⁸Fe was 32.0% of the dose in the iron-deficient subjects, which was not significantly different (p = 0.073) than the 13.1% in the iron-sufficient subjects. Incorporation of ⁵⁸Fe by the iron-sufficient subjects did not differ significantly from that by normal subjects in the same age range. Surprisingly, we found no correlation of erythrocyte incorporation of ⁵⁸Fe and reticulocyte count.

Conclusions: Even in the presence of infection or inflammation, iron absorption by children during a late stage of recovery from malnutrition is not impaired.

Key words: iron absorption, malnutrition, iron status

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Iron deficiency with or without anemia is common in infants and children during recovery from severe malnutrition. As a cause of the iron deficiency, Massa et al. [1] suggested that a transitory abnormality in iron absorption may be present in infantile malnutrition, a suggestion based on the increase in ⁵⁹Fe in serum after oral administration of the isotope. However, iron absorption has been found to be unaffected in protein depleted rats [2], and an earlier study of iron absorption by iron-deficient malnourished subjects had failed to provide evidence of decreased iron absorption [3].

Our study was undertaken to provide further data on absorption of iron by malnourished subjects. It was a collaborative effort between a group of investigators working with malnourished infants and small children in Guadalajara, Mexico, and colleagues in Iowa City, Iowa, involved in studies of erythrocyte incorporation of ⁵⁸Fe by normal infants and children. In normal and iron-deficient adults, 80% to 90% of the absorbed isotope is promptly incorporated into erythrocytes [4,5]. The data of Lynch et al. [3] indicated that in malnourished, iron-deficient infants and small children a high percentage of absorbed iron is also promptly incorporated into erythrocytes. Therefore, we used erythrocyte incorporation of ingested ⁵⁸Fe as a surrogate for iron absorption in young subjects recovering from malnutrition.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Study Design
Subjects less than three years of age with birth weights of 2.5 kg or more and z-scores for body weight for age less than -1.8 were considered candidates for study. With few exceptions, they were studied after initial treatment for gastroenteritis or bronchopneumonia. Each iron absorption study consisted of oral administration of an accurately known amount of ⁵⁸Fe. Blood was obtained by heel stick just before and 14 days after ⁵⁸Fe administration, and, from the ⁵⁸Fe enrichment of the erythrocytes, the extent of erythrocyte incorporation of the administered isotope was determined and expressed as percent of the ⁵⁸Fe dose. Data on erythrocyte incorporation of iron were compared with data from normal infants and children and were examined in relation to anthropometric indices, iron nutritional status and evidence of inflammation. Indicators of iron nutritional status were determined on both blood specimens, and the average of the two values was used for classification of iron nutritional status.

Subjects
A cohort of 25 subjects was studied. With the exception of two subjects at or near three years of age (Subjects 1 and 19), subjects ranged in age from 6 to 27 months at the time of isotope administration (Table 1) All of the subjects were believed by the parents to have been born at term, and birth weights reported by the parents for 18 of the 25 subjects ranged from 2.5 kg to 4.0 kg. Subjects 5, 7 and 14 had previously been treated in the hospital, were being followed as outpatients and were admitted specifically for the ⁵⁸Fe study. Subject 15 was referred by another department, was not acutely ill and was admitted for the ⁵⁸Fe study. The other subjects were studied after 9 to 76 days of hospitalization (only one subject more than 55 days). At the time of admission and subsequently when studied for erythrocyte incorporation (see RESULTS), the subjects were underweight and stunted as indicated by z-scores for weight and length. Z-scores of weight-for-length were also low.

Classification with Respect to Iron Nutritional Status
Despite other evidence indicating the presence of iron deficiency in quite a number of the subjects, the great majority of plasma ferritin concentrations were in or above the range encountered in normal subjects of similar age. The highest values (11 of 48 plasma ferritin values were more than 100 µg/L) were presumably a reflection of inflammation, except for Subject 6, who was six months old, had received a transfusion of packed erythrocytes and oral iron treatment. All but 9 of the 49 ESR values were greater than 13 mm/hour, the value considered to be the upper limit of normal [6]. ESR values were not significantly correlated with indices of iron nutritional status.

Because evidence of inflammation was present in so many of the subjects and because inflammation is associated with increase in plasma ferritin concentration, we classified each subject with respect to iron nutritional status on the basis of four relevant indices of iron nutritional status. If none or only one of the indices was abnormal, the subject was classified as iron-sufficient; if two indices were abnormal, the subject was classified as indeterminate (i.e., of uncertain iron nutritional status), and if three or four of the indices were abnormal, the subject was classified as iron-deficient. All four indices were abnormal in seven of the eleven iron-deficient subjects.

The indices with their cutoff values were as follows:

• (1) Plasma ferritin concentration less than 12 µg/L or less than 50 µg/L if the ESR was more than 13 mm/hour. An upper cutoff value of 50 µg/L in the presence of inflammation has been suggested by Galan et al. [7].
  
• (2) Erythrocyte protoporphyrin content greater than 80 µg/dL of erythrocytes [8].
  
• (3) Iron saturation of transferrin less than 12% [8].
  
• (4) Hemoglobin concentration less than 110 g/L.
  

Refeeding Program
With the exceptions already noted (Subjects 5, 7, 14 and 15), the refeeding program was similar for all of the subjects. Feeding of a milk-based infant formula was begun immediately after admission to the hospital or, when considered necessary, after intravenously administered rehydration therapy. The energy density of a 67 kcal/dL formula was increased to 80 kcal/dL by the addition of corn syrup and fed by continuous infusion by an infusion pump and nasogastric tube. Feeding volumes were gradually increased so that by the 6th day of hospitalization an energy intake of 200 kcal · kg^-1 · d^-1 and a protein intake of 4 g · kg^-1 · d^-1 were achieved. Thereafter, the same formula (80 kcal/dL) was fed ad libitum by bottle. Infants older than 12 months of age were also fed hospital-prepared gruels made from fruits, vegetables and cereals.

Anthropometric Measurements
Body weight and recumbent length were measured by trained examiners using standard methods [9]. Age appropriate z-scores for weight, length and weight-for-length were calculated on the basis of NCHS reference data [10].

Administration of ⁵⁸Fe
Elemental iron enriched with ⁵⁸Fe (84.58 atom% ⁵⁸Fe) was obtained from Oak Ridge National Laboratory (Oak Ridge, TN) and was prepared in the form of ferrous sulfate as previously described [11]. A precisely weighed amount of ⁵⁸Fe solution was added to 5 mL of a 50 g/L glucose solution containing 10 mg of ascorbic acid, 1.1 mg of ⁵⁸Fe and 1.3 mg total iron. This solution was delivered directly into the back of the oral cavity by syringe in a small volume to decrease the likelihood of regurgitation. For the next hour, during which no feeding was given, the subjects were observed closely for the possibility of regurgitation.

Laboratory Methods
Using a disposable spring-loaded device (Tenderfoot, International Technidyne Corp., Edison, N.J.), blood samples were obtained by heel stick. Hemoglobin concentration was determined by the cyan-methemoglobin method (catalog number 368555 Boehringer Mannheim Diagnostics, Indianapolis, IN). Blood was analyzed for erythrocyte protoporphyrin by the method of Piomelli [12]. Plasma was analyzed for concentration of ferritin by radioimmunoassay using the Micromedic Ferritin RIA Kit (Micromedic Systems, Inc., Horsham, PA), for concentration of iron with the Ferrochem II Analyzer (ESA, Inc., Bedford, MA) and concentration of transferrin as described by Borum et al. [13]. Based on an atomic weight of iron of 56, molecular weight of transferrin of 74,000, and two iron-binding sites for transferrin, total iron binding capacity was calculated as transferrin concentration (µg) x 0.00151, and iron saturation of transferrin (%) was calculated as plasma iron concentration (µg) divided by total iron-binding capacity x 100. Erythrocyte sedimentation rate (ESR) was determined by a micromodification of the method of Wintrobe [14]. Blood smears stained with brilliant cresyl blue were counted for reticulocytes with the aid of a Miller Disc (American Optical Company, Buffalo, NY). Four slides were counted and each value therefore represented 2000 erythrocytes.

Calculations
The ⁵⁸Fe/⁵⁷Fe ratio in erythrocytes was determined by inductively coupled plasma mass spectrometry (ICP/MS) using the Elan 250 ICP/MS system as described by Janghorbani et al. [11]. As described previously [15–17], the quantity of administered ⁵⁸Fe incorporated into erythrocytes (⁵⁸Fe*_inc) at a specified time t after administration of the dose was calculated as follows:

where ⁵⁸Fe*_inc is expressed in mg, MIR^t_58/57 is the determined ⁵⁸Fe/⁵⁷Fe ratio at time t, MIR⁰_58/57 is the determined baseline ratio, Fe_circ is the quantity of total circulating iron (mg) at time t and 0.00322 is the natural abundance (weight fraction) of ⁵⁸Fe. The quantity of total circulating iron was estimated as follows:

where BV is blood volume in liters (assumed to be 0.065 L/kg body weight), Hb is hemoglobin concentration in g/L and 3.47 is the concentration of iron in hemoglobin (mg/g). In the remainder of this communication the term "⁵⁸Fe" will refer to the administered isotope.

Statistical Analysis
Unless specifically noted, values for plasma ferritin, plasma iron, percent saturation of transferrin, erythrocyte protoporphyrin content and erythrocyte incorporation of ⁵⁸Fe were transformed by natural logarithms before statistical analyses. Descriptive, associative, and comparative statistics were performed using SAS version 6.12 (SAS Institute, Cary NC). Linear relationships were determined by Pearson correlations and regression analyses. Comparisons of iron deficient versus iron sufficient and of malnourished versus normal subjects were analyzed using general linear models procedures with and without covariate adjustment for log ferritin. Least significant squares comparisons of least-square means were performed for variables with a significant F-test for grouping factor.

Ethical considerations
The study protocol was reviewed and approved by the institutional review board of the University of Guadalajara and by the University of Iowa Committee on Research Involving Human Subjects. The study procedures were explained to one or both parents and written consent was obtained.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
Weight, length and weight-for-length (Table 1) indicated that the subjects were underweight and stunted (mean weight z-score -3.06, SD 0.74; mean length z-score -3.25, SD 1.48) and underweight for length (mean weight-for-length z-score -1.45, SD 1.11). The severity of underweight did not appear to be age related, as indicated by the lack of significant correlation of the weight z-score and age, but the correlation for weight-for-length z-score and age was significant (r=-0.49, p=0.013).

The entries in Table 1 for indices of iron status and for ESR are the averages of two determinations, one obtained at the time of ⁵⁸Fe administration and the other 14 days later. The two values were significantly correlated with correlation coefficients ranging from 0.55 to 0.92, with the exception of plasma iron, for which the correlation coefficient was not statistically significant (r=0.38).

That iron deficiency and severity of anemia were inversely related to age is evident from the inverse correlation with age of hemoglobin (r=-0.58, p=0.002), log plasma ferritin concentration (r=-0.61, p=0.001) and log percent saturation of transferrin (r=-0.58, p=0.003), and the positive relation with age of log erythrocyte protoporphyrin content (r=0.41, p=0.04) and log percent erythrocyte incorporation of ⁵⁸Fe (r=0.52, p=0.008).

Erythrocyte Incorporation of ⁵⁸Fe
Erythrocyte incorporation of ⁵⁸Fe was significantly correlated (r=-0.53, p=0.007) with plasma ferritin concentration (Fig. 1). Geometric mean erythrocyte incorporation of ⁵⁸Fe was 13.1% of the dose by the iron-sufficient subjects and 32.0% of the dose by the iron-deficient subjects. The difference was borderline significant (p=0.073). We have no explanation for the extremely high value for erythrocyte incorporation of ⁵⁸Fe (88.7% of the dose) by iron-sufficient Subject 7. Three published reports concerning normal infants and young children were available for comparison with the data on erythrocyte incorporation of ⁵⁸Fe by the iron-sufficient malnourished subjects. Combined data from two studies (29 infants 165 to 215 days of age) reported by Fomon et al. [18,19] gave a geometric mean ⁵⁸Fe erythrocyte incorporation of 14.4% of the dose, a value that did not differ significantly from that of the iron-sufficient malnourished subjects (p=0.77). Neither did the values for ten infants 12 to 15 months of age studied by Abrams et al. [20] (10.6% of intake) differ from those of the iron-sufficient subjects.

View larger version (10K): [in this window] [in a new window]   Fig. 1 Erythrocyte incorporation of 58Fe in relation to plasma ferritin concentration of infants and children during recovery from malnutrition. Each symbol indicates the incorporation of 58Fe as percent of the dose in one subject with the iron nutritional status of the subject as follows: = iron-sufficient, x = indeterminate iron status, • = iron-deficient.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
We studied 25 underweight and stunted infants and young children, during recovery from malnutrition, most of them after initial treatment for gastroenteritis or bronchopneumonia, and none during the acute stage of malnutrition associated with circulatory disturbances [21]. Many were iron-deficient and, as judged by ESR values, all but four had evidence of infection or inflammation, conditions known to be associated with elevated values for plasma ferritin concentration and erythrocyte protoporphyrin content and for decrease in the iron saturation of transferrin [8].

The finding that a number of the plasma ferritin concentrations were quite high (11 of 48 determinations more than 100 µg/L) is perhaps not surprising because even in presumably normal subjects in the age range of the malnourished subjects, concentrations greater than 100 µg/L are sometimes found [22–24], and six of the seven subjects with values greater than 100 µg/L had evidence of infection or inflammation. The finding of lesser concordance in malnourished than in normal subjects with respect to the relation of plasma ferritin concentrations obtained in the same subject at an interval of 14 days suggests an instability of the values in the malnourished subjects. We do not know whether this instability is related to inflammation or to other factors.

That plasma ferritin concentrations were in the normal range for most of the iron-deficient malnourished subjects may not be entirely the effect of inflammation. Despite the high reliability of low concentrations of ferritin in plasma or serum as an indicator of iron deficiency, concentrations in the normal range in iron deficiency are not uncommon [7,8,25–27]. This perhaps explains the failure of Wickramasinghe et al. [28] to demonstrate a correlation between stainable iron in the marrow and plasma ferritin concentration.

Despite the general elevation of the plasma ferritin values, there was evidence that plasma ferritin concentration was related to iron nutritional status. Thus, erythrocyte incorporation of ⁵⁸Fe was inversely correlated with plasma ferritin concentration (Fig. 1) and log plasma ferritin was inversely correlated with log erythrocyte protoporphyrin and positively correlated with log percent saturation of transferrin.

It is recognized that in field studies, iron deficiency can best be identified by using several indices of iron-nutritional status [29,30], and we classified each subject with respect to iron nutritional status on the basis of four criteria (see RESULTS). Subjects were classified as iron-sufficient if none or only one criterion was abnormal, as of indeterminate iron nutritional status if two indices were abnormal and as iron-deficient if three or four indices were abnormal. Assuming that an elevated ESR value was an indication of current or recent infection or inflammation, we used a different cutoff value for plasma ferritin concentration in subjects with elevated ESR values than in subjects without elevated ESR values. We made no ESR-related adjustment in the cutoff values for hemoglobin concentration, transferrin saturation or erythrocyte protoporphyrin content because we are unaware of data on the quantitative nature of the effect of infection or inflammation on these indices. Nevertheless, by requiring that three or four of the four indices be abnormal for a subject to be classified as iron-deficient, we believed the identification of iron-deficient subjects to be strongly supported. Erythrocyte incorporation of ⁵⁸Fe was only slightly (p=0.073) greater by subjects we classified as iron-deficient than by those we classified as iron-sufficient. Lynch et al. [3] determined iron absorption by ⁵⁹Fe whole body counting in 10 subjects 6 to 20 months of age. The subjects were iron-deficient, as indicated by lack of stainable iron in the bone marrow, and were studied 34 to 76 days after initiation of treatment for kwashiorkor. Erythrocyte incorporation of ⁵⁹Fe was determined concurrently in six of the subjects. Geometric mean absorption was 35.2% of isotope intake and erythrocyte incorporation was 32.0% of intake. The value for erythrocyte incorporation of the iron isotope was identical to that in our study. The data of Lynch et al. [3] also indicate that, in malnourished iron-deficient subjects, in contradistinction to findings in normal infants [18], erythrocyte incorporation of iron accounts for a high percentage of absorbed iron, thus validating the use of erythrocyte incorporation as a surrogate for iron absorption in this group of subjects.

Our data and those of Lynch et al. [3] do not suggest that iron absorption by iron-deficient subjects is impaired during recovery from malnutrition. In addition, erythrocyte incorporation of ⁵⁸Fe by iron-sufficient subjects recovering from malnutrition did not differ significantly from results with normal subjects in the same age range [18–20].

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 
We conclude that at least for groups of subjects similar to those studied by Lynch et al. [3] and by us, iron absorption is unimpaired during recovery from severe malnutrition.

	ACKNOWLEDGMENTS

 
Supported in part by USPHS grant HD 07578 and by Programa de ayuda a la investigación de Nestlé Nutrition.

Received January 23, 2001. Accepted March 26, 2001.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSION REFERENCES

 

1. Massa E, MacLean Jr WC, de Romana GL, de Martinez Y, Graham GG: Oral iron absorption in infantile protein-energy malnutrition. J Pediatr 93: 1045–1049, 1978.[Medline]
2. Beard JL, Huebers HA, Finch CA: Protein depletion and iron deficiency in rats. J Nutr 114: 1396–1401, 1984.
3. Lynch SR, Becker D, Seftel H, Bothwell TH, Stevens K, Metz J: Iron absorption in kwashiorkor. Am J Clin Nutr 23: 792–797, 1970.[Abstract/Free Full Text]
4. Larsen L, Milman N: Normal iron absorption determined by means of whole body counting and red cell incorporation of ⁵⁹Fe. Acta Med Scand 198: 271–274, 1975.[Medline]
5. Heinrich HC, Fischer R: Correlation of postabsorptive serum iron increase and erythrocyte-⁵⁹Fe-incorporation with the whole body retention of absorbed ⁵⁹Fe. Klin Wochenschr 60: 1493–1496, 1982.[Medline]
6. Behrman RE, Kliegman RM, Arvin AM (eds): "Nelson Textbook of Pediatrics," 15th ed. Philadelphia, WB Saunders Company, 1042, 1996.
7. Galan P, Etard JF, Borel E, Debenaze C, Hercberg S: Relationship between serum ferritin, erythrocyte protoporphyrin and transferrin saturation in Mauritanian free living children. Internat J Vit Nutr Res 59: 214–218, 1989.
8. Dallman PR, Yip R, Oski FA: Iron deficiency and related nutritional anemias. In Nathan DG and Oski FA (eds): "Hematology of Infancy and Childhood," 4th ed. Philadelphia: WB Saunders Company, 413–450, 1993.
9. Fomon SJ, Nelson SE: Size and growth. In Fomon SJ: "Nutrition of Normal Infants." St. Louis: Mosby-Year Book, 36–84, 1993.
10. Hamill PVV, Drizd TA, Johnson CL, Reed RB, Roche AF, Moore WM: Physical growth: National Center of Health Statistics percentiles. Am J Clin Nutr 32: 607–629, 1979.[Abstract/Free Full Text]
11. Janghorbani M, Ting BTG, Fomon SJ: Erythrocyte incorporation of ingested stable isotope of iron (⁵⁸Fe). Am J Hematol 21: 277–288, 1986.[Medline]
12. Piomelli S: A micromethod for free erythrocyte porphyrins: the FEP test. J Lab Clin Med 81: 932–940, 1973.[Medline]
13. Borum PR, Bennett SG: A simple and inexpensive method for plasma transferrin determination. Nutr Res 5: 937–940, 1985.
14. Wintrobe MM, Landsberg JW: A standardized technique for the blood sedimentation test. Am J Med Sci 189: 102, 1935.
15. Fomon SJ, Janghorbani M, Ting BTG, Ziegler EE, Rogers RR, Nelson SE, Ostedgaard LS, Edwards BB: Erythrocyte incorporation of ingested 58-iron by infants. Pediatr Res 24: 20–24, 1988.[Medline]
16. Fomon SJ, Ziegler EE, Rogers RR, Nelson SE, Edwards BB, Guy DG, Erve JC, Janghorbani M: Iron absorption from infant foods. Pediatr Res 26: 250–254, 1989.[Medline]
17. Fomon SJ, Ziegler EE, Nelson SE: Erythrocyte incorporation of ingested ⁵⁸Fe by 56-day-old breast-fed and formula-fed infants. Pediatr Res 33: 573–576, 1993.[Medline]
18. Fomon SJ, Ziegler EE, Serfass RE, Nelson SE, Rogers RR, Frantz JA: Less than 80% of absorbed iron is promptly incorporated into erythrocytes of infants. J Nutr 130: 45–52, 2000.[Abstract/Free Full Text]
19. Fomon SJ, Serfass RE, Nelson SE, Rogers RR, Frantz JA: Time course of and effect of dietary iron level on iron incorporation into erythrocytes by infants. J Nutr 130: 541–545, 2000.[Abstract/Free Full Text]
20. Abrams SA, O’Brien KO, Wen J, Liang LK, Stuff JE: Absorption by 1-year-old children of an iron supplement given with cow’s milk or juice. Pediatr Res 39: 171–175, 1996.[Medline]
21. Viart P: Hemodynamic changes in severe protein-calorie malnutrition. Am J Clin Nutr 30: 334–348, 1977.[Abstract/Free Full Text]
22. Saarinen UM, Siimes MA: Serum ferritin in assessment of iron nutrition in healthy infants. Acta Paediatr Scand 67: 745–751, 1978.[Medline]
23. Sherriff A, Edmond A, Hawkins N, Golding J, the ALSPAC Children in Focus Study Team: Haemoglobin and ferritin concentrations in children aged 12 and 18 months. Arch Dis Child 80: 153–157, 1999.[Abstract/Free Full Text]
24. Edmond AM, Hawkins N, Pennock C, Golding J, the ALSPAC Children in Focus Team: Haemoglobin and ferritin concentrations in infants at 8 months of age. Arch Dis Child 74: 36–39, 1996.[Abstract]
25. Dallman PR, Reeves JD, Driggers, DA, Lo EYT: Diagnosis of iron deficiency: the limitations of laboratory tests in predicting response to iron treatment in 1-year-old infants. J Pediatr 98: 376–381, 1981.
26. Herschko C, Bar-Or D, Gaziel Y, Naparstek E, Konijn AM, Grossowicz N, Kaufman N, Izak G: Diagnosis of iron deficiency anemia in a rural population of children. Relative usefulness of serum ferritin, red cell protoporphyrin, red cell indices, and transferrin saturation determinations. Am J Clin Nutr 39: 1600–1610, 1981.
27. Madanat F, El-Khateeb M, Tarawaneh M, Hijazi S: Serum ferritin in evaluation of iron status in children. Acta Haematol 71: 111–115, 1984.[Medline]
28. Wickramasinghe SN, Gill DS, Broom GN, Akinyanju 00, Grange A: Limited value of serum ferritin in evaluating iron status in children with protein-energy malnutrition. Scand J Haematol 35: 292–298, 1985.[Medline]
29. Pilch SM, Senti FR (eds): "Assessment of the Iron Nutritional Status of the US Population Based on Data Collected in the Second National Health and Nutrition Examination Survey, 1976–1980." Bethesda, MD: Life Sciences Research Office, FASEB, 1984.
30. Baynes RD, Bothwell TH: Iron deficiency. Annu Rev Nutr 10: 133–148, 1990.[Medline]

This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Garibay, E. V. Articles by Fomon, S. J. Search for Related Content PubMed PubMed Citation Articles by Garibay, E. V. Articles by Fomon, S. J.