pISSN 2287-3732   eISSN 2287-3740
Open Access, Quarterly
    Clin Nutr Res. 2016 Jan;5(1):15-25. English.
    Published online Jan 29, 2016.
    https://doi.org/10.7762/cnr.2016.5.1.15
    © 2016 The Korean Society of Clinical Nutrition
    Original Article

    Association of Maternal Diet With Zinc, Copper, and Iron Concentrations in Transitional Human Milk Produced by Korean Mothers

    Yun Kyung Choi,1 Ji-Myung Kim,2 Ji-Eun Lee,3 Mi Sook Cho,1,4 Bong Soo Kang,5 Hyeon Choi,6 and Yuri Kim1,4
      • 1Department of Clinical Nutrition, The Graduate School of Clinical Health Sciences, Ewha Womans University, Seoul 03760, Korea.
      • 2Food and Nutrition Major, Division of Food Science and Culinary Arts, Shinhan University, Uijeongbu 11644, Korea.
      • 3Department of Physical Education, College of Education, Chung-Ang University, Seoul 06974, Korea.
      • 4Department of Nutritional Sciences and Food Management, Ewha Womans University, Seoul 03760, Korea.
      • 5U2 Bio Co. Ltd., 68, Seoul 05755, Korea.
      • 6Inuri Medical Group, Seoul 03037, Korea.
    • Corresponding author: Yuri Kim. Address Department of Nutritional Science and Food Management, Ewha Womans University, 52 Ewhayeodae-gil, Seodaemun-gu, Seoul 03760, Korea. Tel +82-2-3277-4485, Fax +82-2-3277-2862, Email: yuri.kim@ewha.ac.kr
    Received January 14, 2016; Revised January 19, 2016; Accepted January 20, 2016.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    The aims of this study were to evaluate zinc, copper, and iron concentrations in the transitory milk of Korean lactating mothers and to investigate the relationship between these concentrations and maternal diet. Human milk samples were collected between 5 and 15 days postpartum from 96 healthy, lactating mothers in postpartum care centers in Seoul, Korea. Dietary intake during lactation was determined based on a 3-day dietary record. The mean zinc, copper, and iron concentrations in the human milk samples collected were 3.88 ± 1.74 mg/L, 0.69 ± 0.25 mg/L, and 5.85 ± 8.53 mg/L, respectively. The mothers who consumed alcoholic beverages during pregnancy had tended to have lower concentrations of zinc and copper, as well as significantly lower concentrations of iron, in their milk (p < 0.047). In contrast, the mothers who took daily supplements had much higher iron concentrations in their milk (p = 0.002). Dietary intakes of zinc, copper, and iron during lactation did not affect the concentrations of zinc, copper, and iron in the milk samples analyzed. Intakes of vitamin C, selenium, and iodine were associated with the concentration of copper in the milk samples analyzed, and consumption of food categorized as 'meat and meat products' was positively associated with the concentration of zinc. Consumption of rice was the top contributor to the concentrations of all three minerals. In conclusion, associations between maternal diet and nutrient concentrations in transitory human milk can provide useful information, particularly in regard to infant growth.

    Keywords
    Human transitional milk; Zinc; Copper; Iron; Dietary intake

    Introduction

    Human milk is considered to provide an infant with all the essential nutrients needed in the early stages of life following birth [1]. Correspondingly, the World Health Organization recommends that breastfeeding should constitute the exclusive source of nutrition for infants up to at least 6 months of age [2]. Therefore, investigations of human milk content and the factors affecting human milk composition are important for improving the growth and development of breastfeeding infants and for establishing nutritional requirements for lactating mothers.

    Minerals are essential nutrients for the growth and development of healthy tissues for both adults and infants [3]. The concentrations of most minerals in human milk remain fairly constant during lactation, except for zinc, copper, and iron. The latter three minerals have their highest concentrations immediately after delivery, and then these concentrations decrease over several months thereafter [4, 5, 6]. For infants with deficiencies in these trace elements, adverse effects on growth, motor development, cell-mediated immunity, and skeletal development have been observed [7].

    Zinc is essential for cellular metabolic processes, immunity, neurological function and sexual development. Zinc also plays a fundamental role in growth and development [8]. Copper has an important role in the growth and formation of bone and in the nervous system [9], while iron is a component of hemoglobin in the blood and has an essential role in biological oxidation [10]. Copper and iron affect the absorption of zinc by competing with each other, thereby demonstrating how the excessive intake of one essential element may compromise the intake and status of another.

    Studies of maternal diet in relation to concentrations of zinc, copper, and iron in human milk have produced mixed results. For example, in one study [4], no relationship between the iron and zinc content of the human milk and maternal nutritional status was observed, while another study [11] also reported the absence of relationship between maternal intake of zinc and zinc concentration in human milk. However, Arnaud and Favier [12] reported that the concentration of copper in human milk is related to a mother's body mass index (BMI). A study by Leotsinidis et al. [13] further revealed that dietary habits play a role in determining mineral levels in human milk, while smoking affected copper levels. Similarly, both diet and environment have been shown to strongly influence zinc distribution [14].

    Transitory milk is secreted between 5 and 15 days after delivery [15]. During this period, the nutritional components and immune substances vary in human milk. Several researchers have reported that changes in trace elements concentrations, particularly zinc, copper, and iron in human milk can vary according to a mother's diet and its characteristics [12, 14]. However, many studies have focused on examining the components of colostrum and mature milk, while data regarding the concentrations of zinc, copper, and iron in transitory human milk and in relation to maternal diet and environmental factors are limited. Therefore, the aim of the present study was to investigate whether maternal diet and other environmental factors during lactation affect the concentrations of zinc, copper, and iron in transitory human milk, thereby providing useful information for promoting healthy infant growth and development.

    Materials and Methods

    Study subjects

    Ninety-six women who gave birth to healthy full-term babies between 10 June 2013 and 27 January 2014 agreed to participate in this study. All of the women were staying at postpartum care centers in Seoul and Gyeonggi province in South Korea and were in good health, they did not have any known diseases (e.g., hypertension, gestational diabetes, etc), and they provided informed written consent. Convenience sampling was conducted between 5 and 15 days postpartum. This was approved by the Institutional Review Board (IRB) of Ewha Womans University (IRB no: 2013-51-18).

    Each participant in this study was interviewed by a trained dietician. Information on general characteristics, including age, height, present weight, BMI, and weight gain during pregnancy, supplementation, and smoking and drinking status, was collected for each mother. For the newborn infants, age, gender, and birth weight were recorded.

    Dietary intake assessment

    All subjects submitted a 3-day dietary record for dietary assessment that was performed within two weeks of their interview. Each participant was instructed on how to complete the dietary record and was asked to record details regarding the quantity and types of foods they consumed. Food models were used to represent the amount of foods consumed. Dietary intake data were assessed with the Computer Aided Nutritional Analysis Program software (CANPro, version 4.0, The Korean Nutrition Society, Seoul, Korea 2011). Following the assessment of each mother's dietary intake, 28-nutrient and 16-food group classifications during lactation were identified. Each daily nutrient intake profile was compared with the estimated average requirements recommended by the 2010 Korean Dietary Reference Intakes 2010 (KDRIs 2010, the Korean Nutrition Society, Seoul, Korea).

    Breast milk collection

    Human milk samples (20-50 mL) were collected from 96 healthy lactating mothers between 5 and 15 days after they gave birth. The samples were obtained with an electronic breast pump and were collected into polyethylene bottles. The samples were sealed, placed on ice, then transported to our laboratory to be stored at -20℃ until use.

    Sample assessment

    The contents of each milk sample were analyzed by spectrophotometry. Briefly, nitric acid (HNO3) was added to 1 mL of each milk sample. After each sample underwent digestion under pressure, the samples were quantitatively transferred to clean polyethylene tubes and were diluted in 10 mL of high purity water. Copper and zinc content were analyzed by using an inductively coupled plasma mass spectrometer (NEXION 350D, Perkin Elmer, Waltham, MA, USA). To analyze the iron concentration of each sample, samples were centrifuged at 690 x g for 20 min and then the aqueous phase was collected. Iron concentrations were determined with an automated biochemical analyzer (BS-2000M, Mindary, Shenzhen, China). The detection limits, defined as three standard deviations for the blank, were 0.15 µg/L for copper, 39 µg/L for iron, and 11 µg/L for zinc. The accuracy of these analyses were checked by various methods and a reference material (BCR, Geel, Belgium) was included for each test.

    Statistical analysis

    Statistical analyses were performed using the SAS statistic software package, version 9.3 (SAS Institute, Cary, NC, USA). For continuous data, mean ± standard deviation was calculated. Categorical data were reported as the number and percentage being occupied. Normal probability plots and the Kolmogorov–Smirnov test were used to determine whether the variable followed a normal distribution. Differences between two groups were compared with an independent t-test. When the variables did not exhibit a normal distribution, the variables were subjected to the Wilcoxon's-rank sum test to compare two groups. To analyze the association between continuous variables, Pearson's correlation test was used for data with a normal distribution, while Spearman's rank correlation method was used for data that were not normally distributed. The correlation analysis for dietary intake was adjusted for age, weight, alcohol drinking history, and supplementation during pregnancy. Association between the food items consumed and zinc, copper, and iron concentrations in the human milk samples analyzed were identified with multiple regression models. A stepwise forward selection procedure was used where independent variables and confounders were added to the model according to their significance. For all of the analyses performed, a p-value less than 0.05 was considered statistically significant.

    Results

    General characteristics of the subjects

    The general characteristics of the mothers and their babies that were examined are presented in Table 1. The mean age of the mothers was 31.8 ± 3.9 years, their mean height was 162.0 ± 4.8 cm, and their mean weight was 60.6 ± 8.2 kg. The mean BMI for the mothers was 23.1 ± 2.8 kg/m2. The mothers gained an average of 13.4 ± 5.3 kg during pregnancy and 82.3% took nutritional supplements during pregnancy. None of the mothers smoked during their pregnancy, although 11.5% of the lactating mothers reported a history of smoking before their pregnancy and 88.5% had no history of smoking. Only 14.6% of the lactating mothers consumed alcoholic beverages during pregnancy. Of the babies born, 52.1% were male and the average birth weight was 3.2 ± 0.4 kg. The average age of babies was 11.2 ± 2.8 days.

    Table 1
    General characteristics of the subjects and their baby (n = 96)

    Zinc, copper, and iron concentrations in the human transitional milk and their concentrations according to alcohol drinking and mineral supplement intake

    The concentrations of zinc, copper, and iron that were detected in the human milk samples analyzed are listed in Table 2. The mean concentrations were 3.88 ± 1.74 mg/L (range: 0.80 – 10.00 mg/L), 0.69 ± 0.25 mg/L (range: 0.08 – 1.50 mg/L), and 5.85 ± 8.53 mg/L (range: 0.05 –34.00 mg/L), respectively.

    Table 2
    Analysis of zinc, copper, and iron levels in transitional human milk and comparison with reported studies

    The concentrations of these three minerals in the human milk samples examined according to alcohol and supplement intake of each mother are presented in Table 3. The mothers who consumed alcoholic beverages during pregnancy tended to have lower concentrations of zinc and copper in their milk, as well as a significantly lower concentration of iron (p = 0.047). In contrast, the iron concentration in the milk samples obtained from the mothers who took daily supplements was significantly higher than in the milk samples from the mothers who did not take daily supplements (p = 0.002).

    Table 3
    Zinc, copper, and iron concentrations in human transitional milk according to alcohol drinking and mineral supplement intake

    Daily nutrient intakes during lactation and concentration of zinc, copper, and iron in human milk

    Table 4 presents the daily nutrient intake data during lactation and the correlation of these data with zinc, copper, and iron concentrations that were detected in the milk samples. The average energy intake for the mothers was 2092.0 ± 314.7 kcal, and their average daily intake of iron, zinc, and copper were 23.6 ± 15.5 mg, 12.5 ± 2.2 mg, and 1.8 ± 1.9 mg, respectively. These amounts of mineral intakes were sufficient to meet KDRIs 2010. While zinc concentrations in the milk samples had no relationship with any particular nutrient intakes during lactation, copper concentrations in the milk samples were positively associated with the consumption of vitamin C (R = 0.236, p = 0.022) and selenium (R = 0.232, p = 0.025), and were inversely associated with iodine intake (R = -0.267, p = 0.013). In addition, iron concentrations in the milk samples significantly correlated with the maternal daily intake of fat (R = 0.215, p = 0.038).

    Table 4
    Correlations between daily nutrient intakes during lactation and zinc, copper and iron concentrations in human milk (n = 96)

    Food intakes by groups and zinc, copper, and iron concentrations in human milk

    Table 5 lists the daily food intake profiles during lactation for the present study, as well as their correlation with zinc, copper, and iron concentrations in the milk samples analyzed. The intake data were divided into 15 categories, and were also classified into an animal-based group and a plant-based group. Among the former group, 'meat and meat products' was found to positively correlate with zinc concentrations in the milk samples. The other food groups, except 'beverage' was shown no significant correlation with the concentrations of zinc, copper, and iron.

    Table 5
    Correlations between food intakes by groups during lactation and zinc, copper and iron concentrations in human milk (n = 96)

    The cumulative percent contribution and cumulative R2 of the top 20 food items that affected zinc, copper, and iron concentrations are presented in Table 6. For this analysis, the dietary intake of the mothers was used to determine the priority and cumulative R2 of each related food item. Rice was the top contributor to the intake of all three minerals. For zinc, beef, followed by pork and dried seaweed were key food items. However, after considering between-person variability, soy bean sauce, wheat flour, and raw seaweed were the top three food items that contributed to zinc concentrations. In contrast, higher levels of both copper and iron were associated with the intake of lemon, bread with jam, and fly fish caviar.

    Table 6
    Cumulative %contribution and cumulative R2 of top 20 for zinc, copper, and iron intakes

    Discussion

    Transitory milk shares some of the characteristics of colostrum, and then milk production is rapidly increased to support the nutritional and developmental requirements of a growing infant [15]. Zinc, copper, and iron concentrations are higher in colostrum and transitory milk compared with mature milk, and this corresponds with the greater need of newborn infants for larger amounts of these minerals and the low volume of milk intake early in their life [16].

    In Table 2, zinc, copper, and iron concentrations in transitional human milk samples that were analyzed in previously reported studies are listed. Zinc (3.88 mg/L) and copper concentrations (0.69 mg/L) in the lactating participants of the present study are within the range previously reported. Regarding zinc, the mean concentrations from the present study were similar or slightly lower than that reported in other studies conducted in Germany [17] (2.06 mg/L), Korea [18, 19] (2.92 mg/L, 3.94 mg/L), and Greece [13] (2.99 mg/L). Conversely, zinc concentrations in the transitory milk of lactating mothers in France were 5.03 mg/L, and this is higher than the concentration determined in the present study [12]. Regarding mean copper concentrations in human milk, various values have been reported worldwide for similar stages of lactation. However, the mean concentration of copper determined in the present study did not markedly differ from those reported in other studies, particularly the values reported by studies conducted in France (0.61 mg/L) [20], Korea (0.63 mg/L) [18], and Canada (0.73 mg/L) [21]. However, the copper concentrations reported by studies conducted in the United States (0.59–1.33 mg/L) [22] and Turkey (0.10–3.60 mg/L) [23] are higher than that of the present study. These differences may be due to geographical and nutritional influences associated with these populations [22]. In contrast with the zinc and copper concentrations, the mean iron concentrations reported in the present study tended to be higher than the values previously reported in other studies. However, iron concentrations in the milk samples of the present study did not exhibit a normal distribution, and this could account for the difference in results. Iron supplementation up to comparatively high levels is common in many affluent countries during pregnancy, and often continues into the lactation period [13]. Thus, a wide deviation in milk iron concentrations is possibly due to iron supplementation. Several studies have also mentioned that these differences may be explained by geographical and nutritional influences [22, 23, 24], as well as differences in sampling procedures [25].

    Among the trace elements present in human milk, only iron was significantly associated with some of the general characteristics of the participants examined. For example, a higher concentration of iron was detected in the milk sample that was obtained from mothers who gained less weight during pregnancy, who did not consume alcoholic beverages during pregnancy, and who took daily supplements. Numerous studies have studied the effects of mineral supplements on the concentrations of trace elements in human milk, and most have reported that maternal supplements do not affect the concentrations of trace minerals in human milk [26, 27]. For example, Mello-Neto et al. [27] found no difference in iron concentrations in the human milk produced by women who took daily supplements during pregnancy and the lactating period versus those that did not. In another study, the effect of maternal zinc supplements was very weak and was only apparent in woman who had taken zinc supplements for long periods of time [28]. In the present study, an association between daily iron supplementation and iron concentration in the milk samples analyzed was observed. In Korea, iron supplementation is recommended to minimize the harmful effects of iron-deficiency-based anemia during pregnancy, based on the assumption that long-term iron supplementation during pregnancy and lactation influences the iron concentrations in human milk. A potential detrimental aspect of iron supplementation is the risk of inhibiting the absorption of other micronutrients, including copper and zinc [29, 30, 31, 32, 33, 34]. Iron metabolism involves both zinc and copper, and this mainly mediated via divalent metal transporter 1 [35, 36, 37, 38] and human copper transporter [38]. It has been reported that women receiving iron supplements can have zinc malabsorption [32]. However, in the present study, iron supplementation did not appear to influence the levels of copper and zinc in transitional human milk.

    In previous studies, a correlation between maternal intakes of zinc, copper, and iron and the concentrations of these minerals, in human milk has not been observed [11, 28, 39]. Correspondingly, the results of the present study also did not show a clear correlation between dietary zinc intake of the mother and zinc concentrations in human milk. This may be due to active transport mechanisms involving zinc, copper, and iron in the mammary gland [40, 41, 42, 43]. However, iron concentrations in human milk were positively associated with a mother's dietary intake of fat, cholesterol, and magnesium, which may be due to the consumption of meat and meat products. Numerous studies have also reported that intake of dietary copper does not affect copper concentrations in human milk [44, 45, 46, 47, 48]. However, in the present study, daily intakes of vitamin C, selenium, and iodine were related to copper concentrations in the milk samples. Maru et al. [49] previously reported that differences in copper concentrations in human milk between rural and urban mothers could be attributed to variations in the dietary intake of the mothers.

    A human's requirement for iron and zinc may be more easily met with animal-based, higher-protein meal plans which provide these nutrients in their most bioavailable form. Many studies have investigated the contents of human milk in relation to dietary nutrient intake, although the use of categorized food groups in these studies has been limited. In the present study, zinc concentrations in the milk samples analyzed were found to be positively influenced by the intake of meat and meat products, while fats and oils appeared to be positive factors for zinc. In contrast, dietary intakes appeared to have less effects on copper and iron concentrations in human milk in the present study. Regarding iron concentrations, there were found to be positively associated with the consumption of certain beverages, including drinks containing fruit nectar, shakes, coffee, and soda. It is difficult to explain these observations, and thus, further studies are needed.

    When the major food items that influenced zinc, copper, and iron concentrations in human milk were analyzed by stepwise multiple regression, rice, a staple food of the Korean diet, was the top contributor to all three minerals. For zinc intake, animal-based food items, including beef, pork, eggs, and chicken, were also important contributors. In a similar study [13], zinc levels were found to be associated with the consumption of fruit and rice, while copper levels were appeared to increase following the consumption of fruits and potatoes. Moreover, plant-based food items such as rice, soy milk, cucumber, and red beans were found to have greater effects on copper intake than animal-based food items.

    Conclusion

    In summary, maternal daily intakes of zinc, copper and iron during lactation did not directly affect zinc, copper, and iron concentrations that were detected in the milk samples that were analyzed. However, zinc concentrations were related to the intake of meat and meat products, and copper concentrations correlated with the intake of vitamin C, selenium, and iodine. Furthermore, iron concentrations was found to be more closely associated with the general characteristics of a pregnancy (e.g., drinking during pregnancy and daily supplements during pregnancy) than dietary factors, although food items contributed greatly to iron concentrations in the milk samples than to the zinc and copper concentrations. food items contributed greatly to the concentrations of iron in the milk samples more than to the zinc and copper concentrations. Based on these results, further studies to investigate critical dietary factors that are associated with zinc, copper, and iron concentrations are warranted, with the goal of promoting healthy infant growth and development.

    Notes

    Conflict of interest:The authors declare no conflict of interest.

    References

      1. Bernt KM, Walker WA. Human milk as a carrier of biochemical messages. Acta Paediatr Suppl 1999;88:27–41.
      1. Winiarska-Mieczan A. Cadmium, lead, copper and zinc in breast milk in Poland. Biol Trace Elem Res 2014;157:36–44.
      1. Al-Awadi FM, Srikumar TS. Trace-element status in milk and plasma of Kuwaiti and non-Kuwaiti lactating mothers. Nutrition 2000;16:1069–1073.
      1. Donangelo CM, Trugo NM, Koury JC, Barreto Silva MI, Freitas LA, Feldheim W, Barth C. Iron, zinc, folate and vitamin B12 nutritional status and milk composition of low-income Brazilian mothers. Eur J Clin Nutr 1989;43:253–266.
      1. Nagra SA. Longitudinal study in biochemical composition of human milk during first year of lactation. J Trop Pediatr 1989;35:126–128.
      1. Lamounier JA, Danelluzzi JC, Vannucchi H. Zinc concentrations in human milk during lactation: a 6-month longitudinal study in southern Brazil. J Trop Pediatr 1989;35:31–34.
      1. Rajalakshmi K, Srikantia SG. Copper, zinc, and magnesium content of breast milk of Indian women. Am J Clin Nutr 1980;33:664–669.
      1. Rangan A, Jones A, Samman S. Zinc supplement use and contribution to zinc intake in Australian children. Public Health Nutr 2015;18:589–595.
      1. Tan JC, Burns DL, Jones HR. Severe ataxia, myelopathy, and peripheral neuropathy due to acquired copper deficiency in a patient with history of gastrectomy. JPEN J Parenter Enteral Nutr 2006;30:446–450.
      1. Larkin EC. In: Importance of fetal and neonatal iron: adequacy for normal development of central nervous system. Brain behaviour, and iron in the infant diet. London: Springer-Verlag; 1990. pp. 43-57.
      1. Moser PB, Reynolds RD. Dietary zinc intake and zinc concentrations of plasma, erythrocytes, and breast milk in antepartum and postpartum lactating and nonlactating women: a longitudinal study. Am J Clin Nutr 1983;38:101–108.
      1. Arnaud J, Favier A. Copper, iron, manganese and zinc contents in human colostrum and transitory milk of French women. Sci Total Environ 1995;159:9–15.
      1. Leotsinidis M, Alexopoulos A, Kostopoulou-Farri E. Toxic and essential trace elements in human milk from Greek lactating women: association with dietary habits and other factors. Chemosphere 2005;61:238–247.
      1. Iyengar GV. Reference values for the concentrations of As, Cd, Co, Cr, Cu, Fe, I, Hg, Mn, Mo, Ni, Pb, Se, and Zn in selected human tissues and body fluids. Biol Trace Elem Res 1987;12:263–295.
      1. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am 2013;60:49–74.
      1. Ohtake M, Tamura T. Changes in zinc and copper concentrations in breast milk and blood of Japanese women during lactation. J Nutr Sci Vitaminol (Tokyo) 1993;39:189–200.
      1. Dörner K, Dziadzka S, Höhn A, Sievers E, Oldigs HD, Schulz-Lell G, Schaub J. Longitudinal manganese and copper balances in young infants and preterm infants fed on breast-milk and adapted cow's milk formulas. Br J Nutr 1989;61:559–572.
      1. Lee JS, Lee YN, Kim ES. Study on Zinc and Copper Intakes of Breast-fed Infants. Korean J Nutr 2000;33:857–863.
      1. Kwon MS, Yun IS, Cho MS, Lee HS, Kim WY. Effect of Maternal Factors on the Concentrations of Minerals and Immunological Substance in Breast Milk. Korean J Nutr 2004;37:809–816.
      1. Sann L, Bienvenu F, Lahet C, Bienvenu J, Bethenod M. Comparison of the composition of breast milk from mothers of term and preterm infants. Acta Paediatr Scand 1981;70:115–116.
      1. Mendelson RA, Anderson GH, Bryan MH. Zinc, copper and iron content of milk from mothers of preterm and full-term infants. Early Hum Dev 1982;6:145–151.
      1. Casey CE, Neville MC, Hambidge KM. Studies in human lactation: secretion of zinc, copper, and manganese in human milk. Am J Clin Nutr 1989;49:773–785.
      1. Parr RM, DeMaeyer EM, Iyengar VG, Byrne AR, Kirkbright GF, Schöch G, Niinistö L, Pineda O, Vis HL, Hofvander Y, Omololu A. Minor and trace elements in human milk from Guatemala, Hungary, Nigeria, Philippines, Sweden, and Zaire. Results from a WHO/IAEA joint project. Biol Trace Elem Res 1991;29:51–75.
      1. Yoshinaga J, Li JZ, Suzuki T, Karita K, Abe M, Fujii H, Mishina J, Morita M. Trace elements in human transitory milk. Variation caused by biological attributes of mother and infant. Biol Trace Elem Res 1991;31:159–170.
      1. Picciano MF, Guthrie HA. Copper, iron, and zinc contents of mature human milk. Am J Clin Nutr 1976;29:242–254.
      1. Chierici R, Saccomandi D, Vigi V. Dietary supplements for the lactating mother: influence on the trace element content of milk. Acta Paediatr Suppl 1999;88:7–13.
      1. Mello-Neto J, Rondó PH, Oshiiwa M, Morgano MA, Zacari CZ, dos Santos ML. Iron supplementation in pregnancy and breastfeeding and iron, copper and zinc status of lactating women from a human milk bank. J Trop Pediatr 2013;59:140–144.
      1. Lönnerdal B. Effects of maternal dietary intake on human milk composition. J Nutr 1986;116:499–513.
      1. Lönnerdal B. Trace element nutrition of infants--molecular approaches. J Trace Elem Med Biol 2005;19:3–6.
      1. Meadows NJ, Grainger SL, Ruse W, Keeling PW, Thompson RP. Oral iron and the bioavailability of zinc. Br Med J (Clin Res Ed) 1983;287:1013–1014.
      1. Rossander-Hultén L, Brune M, Sandström B, Lönnerdal B, Hallberg L. Competitive inhibition of iron absorption by manganese and zinc in humans. Am J Clin Nutr 1991;54:152–156.
      1. O'Brien KO, Zavaleta N, Caulfield LE, Wen J, Abrams SA. Prenatal iron supplements impair zinc absorption in pregnant Peruvian women. J Nutr 2000;130:2251–2255.
      1. Fischer Walker C, Kordas K, Stoltzfus RJ, Black RE. Interactive effects of iron and zinc on biochemical and functional outcomes in supplementation trials. Am J Clin Nutr 2005;82:5–12.
      1. Domellöf M. Iron requirements, absorption and metabolism in infancy and childhood. Curr Opin Clin Nutr Metab Care 2007;10:329–335.
      1. Umapathy NS, Gnana-Prakasam JP, Martin PM, Mysona B, Dun Y, Smith SB, Ganapathy V, Prasad PD. Cloning and functional characterization of the proton-coupled electrogenic folate transporter and analysis of its expression in retinal cell types. Invest Ophthalmol Vis Sci 2007;48:5299–5305.
      1. Andrews NC. The iron transporter DMT1. Int J Biochem Cell Biol 1999;31:991–994.
      1. Frazer DM, Wilkins SJ, Becker EM, Murphy TL, Vulpe CD, McKie AT, Anderson GJ. A rapid decrease in the expression of DMT1 and Dcytb but not Ireg1 or hephaestin explains the mucosal block phenomenon of iron absorption. Gut 2003;52:340–346.
      1. Lee J, Peña MM, Nose Y, Thiele DJ. Biochemical characterization of the human copper transporter Ctr1. J Biol Chem 2002;277:4380–4387.
      1. Domellöf M, Lönnerdal B, Dewey KG, Cohen RJ, Hernell O. Iron, zinc, and copper concentrations in breast milk are independent of maternal mineral status. Am J Clin Nutr 2004;79:111–115.
      1. Nikniaz L, Mahdavi R, Gargari BP, Gayem Magami SJ, Nikniaz Z. Maternal body mass index, dietary intake and socioeconomic status: differential effects on breast milk zinc, copper and iron content. Health Promot Perspect 2011;1:140–146.
      1. Moser PB, Reynolds RD, Acharya S, Howard MP, Andon MB, Lewis SA. Copper, iron, zinc, and selenium dietary intake and status of Nepalese lactating women and their breast-fed infants. Am J Clin Nutr 1988;47:729–734.
      1. Dhonukshe-Rutten RA, Vossenaar M, West CE, Schumann K, Bulux J, Solomons NW. Day-to-day variations in iron, zinc and copper in breast milk of Guatemalan mothers. J Pediatr Gastroenterol Nutr 2005;40:128–134.
      1. Hannan MA, Faraji B, Tanguma J, Longoria N, Rodriguez RC. Maternal milk concentration of zinc, iron, selenium, and iodine and its relationship to dietary intakes. Biol Trace Elem Res 2009;127:6–15.
      1. Vaughan LA, Weber CW, Kemberling SR. Longitudinal changes in the mineral content of human milk. Am J Clin Nutr 1979;32:2301–2306.
      1. Vuori E, Mäkinen SM, Kara R, Kuitunen P. The effects of the dietary intakes of copper, iron, manganese, and zinc on the trace element content of human milk. Am J Clin Nutr 1980;33:227–231.
      1. Finley DA, Lönnerdal B, Dewey KG, Grivetti LE. Inorganic constituents of breast milk from vegetarian and nonvegetarian women: relationships with each other and with organic constituents. J Nutr 1985;115:772–781.
      1. Kirksey A, Ernst JA, Roepke JL, Tsai TL. Influence of mineral intake and use of oral contraceptives before pregnancy on the mineral content of human colostrum and of more mature milk. Am J Clin Nutr 1979;32:30–39.
      1. Feeley RM, Eitenmiller RR, Jones JB Jr, Barnhart H. Copper, iron, and zinc contents of human milk at early stages of lactation. Am J Clin Nutr 1983;37:443–448.
      1. Maru M, Birhanu T, Tessema DA. Calcium, magnesium, iron, zinc and copper, compositions of human milk from populations with cereal and 'enset' based diets. Ethiop J Health Sci 2013;23:90–97.
      1. Trugo NM, et al. Concentration and distribution pattern of selected micronutrients in preterm and term milk from urban Brazilian mothers during early lactation. Eur J Clin Nutr 1988;42:497–507.
      1. Friel JK, et al. Elemental composition of human milk from mothers of premature and full-term infants during the first 3 months of lactation. Biol Trace Elem Res 1999;67:225–247.
      1. Tripathi RM, et al. Daily intake of heavy metals by infants through milk and milk products. Sci Total Environ 1999;227:229–235.
      1. Aquilio E, et al. Trace element content in human milk during lactation of preterm newborns. Biol Trace Elem Res 1996;51:63–70.
      1. Perrone L, et al. Interaction of trace elements in a longitudinal study of human milk from full-term and preterm mothers. Biol Trace Elem Res 1994;41:321–330.
      1. Kim ES, Cho KH. Iron, Copper and Zinc Levels in Human Milk and Estimated Intake of the Minerals by Breast-Fed Infants during the Early Lactation. J East Asian Soc Diet Life 2004;14:27–33.
      1. Yang Hye RK, Keum HK, Kime ES. A Study on the Contents of Selenium and Zinc in Human Milk. Korean J Nutr 1995;28:872–879.
      1. Choi MG, et al. A Study on Iron, Zinc and Copper Contents in Human Milk and Trace Element Intakes of Breast-fed Infants. Korean J Nutr 1991;24:442–449.
      1. Atinmo T, Omololu A. Trace element content of breastmilk from mothers of preterm infants in Nigeria. Early Hum Dev 1982;6:309–313.
      1. Wasowicz W, et al. Selenium, zinc, and copper concentrations in the blood and milk of lactating women. Biol Trace Elem Res 2001;79:221–233.
      1. Jirapinyo P, et al. Trace elements in Thai breast milk and infant formulas. J Trop Pediatr 1985;31:157–159.
      1. Turan S, et al. Determination of. Determination of heavy metal contents in human colostrum samples by electrothermal atomic absorption spectrophotometry. J Trop Pediatr 2001;47:81–85.
      1. Lemons JA, et al. Differences in the composition of preterm and term human milk during early lactation. Pediatr Res 1982;16:113–117.
      1. Moran JR, et al. Concentrations and total daily output of micronutrients in breast milk of mothers delivering preterm: a longitudinal study. J Pediatr Gastroenterol Nutr 1983;2:629–634.
    Cited by
    Crossref 15
    Google Scholar 
    PubMed Central 14
    MeSH Terms
    Alcoholic Beverages
    Ascorbic Acid
    Copper*
    Diet Records
    Diet*
    Female
    Humans*
    Infant
    Iodine
    Iron*
    Korea
    Lactation
    Meat
    Milk
    Milk, Human*
    Minerals
    Mothers*
    Postnatal Care
    Postpartum Period
    Pregnancy
    Selenium
    Seoul
    Zinc*
    Metrics
    Share
    Links to
    Tables
    slide
    slide
    slide
    slide
    slide
    slide

    1 / 6

    ORCID IDs
    PERMALINK