Central Journal of Human Nutrition & Food Science

Cite this article: Sazawal S, Black RE, Dhingra P, Jalla S, Krebs N, et al. (2013) Zinc Supplementation does not Affect the Breast Milk Zinc Concentration of Lactating Women Belonging to Low Socioeconomic Population. J Hum Nutr Food Sci 1(2): 1014.

*Corresponding authorSunil Sazawal, Department of International Health, Johns Hopkins Bloomberg School of Public Health, 615, North Wolfe Street, Baltimore, MD 21205-2103, USA, Tel: 1-443-538-0624; Fax: 1-410-955-2029; E-mail: ssazawal@jhsph.edu

Submitted: 13 September 2013

Accepted: 07 October 2013

Published: 09 October 2013

Copyright© 2013 Sazawal et al.

OPEN ACCESS

Research Article

Zinc Supplementation does not Affect the Breast Milk Zinc Concentration of Lactating Women Belonging to Low Socioeconomic PopulationSunil Sazawal1,2, Robert E. Black1, Pratibha Dhingra2, Sanju Jalla3, Nancy Krebs3, Pooja Malik1, Usha Dhingra1 and Maharaj K. Bhan4

1Department of International Health, Bloomberg School of Public Health, Johns Hopkins University, USA 2Center for Micronutrient Research, Department of Biochemistry, Annamalai University, India3Section of Nutrition, Department of Pediatrics, University of Colorado Health Sciences Center, USA4Department of Biotechnology, Block-2, 7th Floor C.G.O. Complex, Lodi Road, India

INTRODUCTIONIn the last decade there has been a progressive increase in

understanding of the occurrence of zinc deficiency in infants and preschool children and its impact on morbidity, growth and mortality [1,2]. Zinc deficiency may occur early in life, especially among low birth weight infants. Joint WHO/IAEA collaborative study reports that zinc body storages are not extensive, and it should be taken in adequate quantities for optimal growth and development [3]. Reports confirmed positive effects of zinc supplements via improvements in growth, reductions in morbidity and mortality in the first year of life, in low birth weight infants or breast fed infants who are not growing normally [4,5]. Breast milk zinc is an important source of bio-available zinc for infants,

however, the zinc concentration in breast milk declines at a faster rate than other minerals, with increasing postpartum duration of breastfeeding [6,7]. Studies of breast milk zinc concentrations in developed countries have yielded inconsistent results in relation to the impact of zinc supplementation in lactating mothers. This may be due to high dietary zinc intakes and normal zinc nutriture of women in these settings [8-11]. Krebs et al. [12] reported that a mean threshold intake of 13 mg/d dietary zinc during lactation appears to be necessary to ensure that milk zinc concentrations are adequate. Thus, zinc supplementation in the maternal diet could potentially influence the breast milk composition [13]. This might offer an ideal route to provide additional zinc to the infant during the first 6 months of life in populations with low

Abstract

Background: Zinc concentrations of breast milk among lactating women are less affected through zinc supplementation in developed countries, but may potentially affect lactating women with suboptimal zinc status from developing countries.

Objective: In a randomized, double-blind trial, to evaluate the effect of zinc supplementation on breast milk zinc concentrations of lactating women with suboptimal zinc status.

Methods: Lactating women 0-2 mo and 4-6 mo postpartum were randomly allocated to receive either multivitamins plus zinc (40mg) daily in 2 divided doses (n=50, 0-2 mo; n=51, 4-6 mo) or same supplement without zinc (n=61, 0-2 mo; n=50, 4-6 mo) for 1 month. A mid-feeding 10ml breast milk sample was collected at base- and end-line.

Results: Following zinc supplementation, change in breast milk zinc concentrations (mmol/L) between the zinc plus multivitamins group (ZMV) and multivitamin group (MV) of lactating women both at 0-2 months (ZMV: -18.9 ± 28.2, MV: -22.1 ± 16.1) and 4-6 months postpartum (ZMV: -2.2 ± 6.6, MV: -0.6 ± 9.5) was similar. Among 0-2 months postpartum women with a low baseline breast milk zinc concentration, zinc supplementation showed a non-significant rate of decline in breast milk zinc concentration (ZMV: 1.4 ± 19.5, MV: 9.7 ± 8.5, p<0.059), while in 4-6 months postpartum women, differences were not significant.

Conclusion: Zinc supplementation only affected a subgroup with low breast milk zinc concentrations in early lactation. Breast milk zinc concentrations seem to be maintained by active transport, unaffected by zinc supplementation in a population of low zinc intake.

Keywords•Zinc supplementation•Multivitamin•Lactation•Breast milk zinc concentrations

Central

Sazawal et al. (2013)Email: ssazawal@jhsph.edu

J Hum Nutr Food Sci 1(2): 1014 (2013) 2/6

dietary intake of zinc. We conducted a double-blind randomized controlled trial to evaluate if zinc supplementation could affect breast milk zinc concentrations of lactating women, with suboptimal zinc status in a developing country.

METHODS

Study participants

In the peri-urban New Delhi, during April 1994 and July 1994, 212 women, who were breastfeeding either 0-2 months old or 4-6 months old infants, who were likely to stay in the area for the next 1 month, not suffering from any chronic systemic illness or severe anemia, not requiring vitamin or micronutrient prescription, and providing consent to participate, were enrolled. The design of the trial is described in (Figure 1). The study was approved by the Committee for Human Research review at the All India Institute of Medical Sciences.

Enrollment and randomization

Two separate lists using randomization with permuted blocks of fixed length of 10 were drawn, one for lactating women 0-2 months postpartum and the other for women 4-6 months postpartum. These lists provided one of 8 letter codes against each serial number. Four letter codes belonged to each treatment group and the supplement bottles were labeled with 8 letter codes. Enrolled lactating women in two strata i.e. 0-2 months (n=111) and 4-6 months (n=101) postpartum were given a serial number which was used to allocate them to receive either multivitamins plus 40 mg zinc/day as zinc gluconate or an identical control supplement (multivitamins without zinc). The allocation code against each serial number was available to the pharmacy assistant who checked allocation code of the women, and then labeled the bottle with her name and identification information. In the field, the supplement was identified by name and identification of women and not by code. Neither participant

nor investigator or field team had any knowledge regarding the treatment group. The actual allocation code of 8 letters was with the Sandoz India Ltd (Mumbai, India) and statistician in Baltimore.

For the baseline assessment, a nutritionist visited women at home, where the purpose of the study was explained and verbal consent obtained. Once the women were enrolled, the information regarding the date of delivery, frequency of consumption of foods especially rich in zinc, feeding information of the child was gathered and a mid-feeding 10 ml breast milk sample was collected.

Each woman was given an enrollment number corresponding to the serial number allocated, one bottle containing 250 ml supplement was given to be kept at home and replaced after 12 days. Enrolled women were visited by the field assistant daily and were given the supplement once each day in the morning; the second measured dose was left for the women to take in the evening. A daily record of the consumption of previous day’s zinc supplement was maintained. At the end of the 30 days of supplementation, the study nutritionist again visited the women to obtain a second breast milk sample. During the daily visitation, the occurrences of vomiting, diarrhea, rash, or any stomach discomfort (gastric irritation) were recorded.

At baseline on a random sub-sample of 20 women, dietary intake was assessed using 24-h dietary recall method [14]. The intake of energy and zinc was calculated by using the Nutritive Value of Indian Foods [15].

Power estimation

We estimated sample size ([β] - 0.9, [α] - 0.05 two sided) to detect a shift in distribution of breast milk zinc concentrations with overlap of 10% to baseline values. This amounted to a difference of 30% in 0-2 month postpartum and 25% in 4-6 month postpartum lactating women in their breast milk zinc levels with one month zinc supplementation. Given the actual values and participants, the study had a power of 80% in 0-2 month strata and 85% in 4-6 month strata for targeted reductions.

Intervention

The supplement was a liquid preparation manufactured by Sandoz India Ltd (Mumbai, India). Each 10 ml of the supplement contained vitamin A (480 µg), thiamine (1.2 mg), riboflavin (1.0 mg), pyridoxine (1.0 mg), cholecalciferol (5.0 µg), alpha tocopherol (6.0 mg) and niacinamide (20 mg). The treatment preparation in addition contained zinc as zinc gluconate (20 mg of elemental zinc per 10 ml). Women were given 10 ml of the preparation twice daily for 30 days. The dose received was equivalent to 40 mg zinc/day. The supplements were identical in taste, color and packaging.

Method for breast milk sample collection and processing

A standard procedure was used for collection of breast milk samples for zinc analysis [16]. The nipple and areola of the enrolled women and the hands of the collector were washed and rinsed with double distilled water. Milk was manually expressed from each breast directly into the zinc-free polypropylene vials

Analyzed(n=50)

Zinc plus multivitamins Group (ZMV)

(n=50)

Lactating women in 0-2 month/4-6 month post partum identified and enrolled in

peri-urban area, SangamVihar, New Delhi, India

4-6 month postpartum

Inclusion criteria:Stay in study area for 1 monthNo chronic systemic illness or severe anemiaConsent to participate

Multivitamins Group(MV)(n=61)

0-2 month postpartum

Randomizationn

Zinc plus multivitamins Group (ZMV)

(n= 51)

Multivitamins Group(MV)

(n= 50)

Analyzed(n=61)

Analyzed(n=51)

Analyzed(n=50)

Randomization

Figure 1 Trial profile.

Central

Sazawal et al. (2013)Email: ssazawal@jhsph.edu

J Hum Nutr Food Sci 1(2): 1014 (2013) 3/6

(about 10-15 ml) midway through the feeding. Tubes containing the milk sample were then immediately put on ice. On reaching the field office laboratory, they were stored at –200C until thawed for analysis. Zinc concentrations in breast milk were analyzed at Pediatric Nutrition Laboratory, University of Colorado Health Sciences Center, Denver, USA. For analysis, 2 x 150 µl aliquots of breast milk were transferred to small circular quartz dishes for overnight ashing in a low temperature asher (LFE Corp, Waltham MA). The ashed samples were dissolved with 150 µl of 0.1 N HCL. A 100 µl aliquot of the dissolved ash was diluted with 500 µl of 6% n-butanol in 0.1 N HCL. The samples were analyzed by flame atomic absorption spectrophotometry with a modified Perkin-Elmer 503 fitted with deuterium arc background correction and AS-3 auto sampling system (Perkin Elmer Corp, Norwalk, CT). Standards were also made up in 6% n-butanol in 0.1 N HCL. All milk samples were analyzed twice, and the mean zinc concentration was calculated. The zinc analysis was repeated in the samples in which the concentration of the 2 measurements deviated 5% from the mean. The CV between the runs was 7.5%. For checking the accuracy and precision of the analytical method, control samples were analyzed. To ensure quality control, after every 10 samples (for each sample, readings were taken in duplicate), one reading of the control sample was taken.

Statistical analysis

Statistical analyses were performed using SPSSPC + (version 18), P <0.05 was considered significant for all analyses. Means and standard deviations of breast milk zinc concentrations and paired differences between baseline and post-supplementation were estimated. Change in breast milk zinc concentrations between baseline and post-supplementation was compared between the zinc and the control groups using a paired ‘t’ test. An analysis was performed separately with each stratum and as there were no differences, the data were pooled to perform the overall analysis. Breast milk zinc concentration for each monthly interval was compared using a student’s t-test/ chi square test for trend. The baseline zinc concentration and post-supplementation zinc concentrations in the MV group were used to develop curves for the zinc concentration by stage of the lactation in the population. Multiple linear regression analysis was also carried out to investigate the effects of the intervention with baseline breast milk concentrations and/or days/time periods postpartum as covariates.

RESULTSWe contacted and enrolled 212 women, who were either

in the period 0-2 months (n-111) or 4-6 months (n-101) postpartum periods; none of the subjects declined participation during the course of the study. In both the strata, women were randomly allocated to receive either ZMV or MV supplementation for a month. The two intervention groups in both strata were comparable for baseline characteristics in terms of age, breastfeeding status, duration of lactation (percentage of women in 0-30 d postpartum for the 0-2 mo postpartum group and percentage of women in 120-150 d postpartum for the 4-6 mo postpartum group), the number of children less than 5 years of age (Table 1) and baseline breast milk zinc concentrations (Table 2). These women had a comparable high frequency of low zinc intake foods (Table 1). The reported dietary intake of zinc in 0-2

mo postpartum varied between 1-6.5 mg/d with a mean of 4.5 mg/d and in 4-6 mo postpartum it varied between 4-6 mg/d with a mean of 5.5 mg/d. Intake of dietary zinc among this population is far below the recommended dietary allowances for lactating women [18] and the reported results from the US studies [12,19] (Figure 2).

There was a marked decline in the breast milk zinc concentrations from baseline to end of study in both the groups (ZMV: paired diff –10.5 ± 21.9 µmol/ L, p<0.001; MV: paired diff –12.4 ± 17.2 µmol/ L, p<0.001), but this difference was not statistically significant between the two groups (ZMV and MV, p=0.47). When the paired difference in breast milk zinc concentrations between the two groups (ZMV and MV) was evaluated by postpartum duration i.e. 0-2 months and 4-6 months postpartum, no significant differences were observed (Table 2).

In order to explore if the effect of zinc was related to baseline breast milk zinc concentrations, women were categorized into two groups according to the baseline breast milk zinc concentration. The threshold concentration was set at 45 µmol/L for 0-2 months (≤50th percentile) and 15.5 mol/L for 4-6 months (≤50th percentile). At 0-2 months, the decline of the breast milk zinc concentration among women with low baseline levels was more in the MV group (-9.7 ± 8.5 µmol/L) as compared to ZMV group (-1.4 ± 19.5 µmol/L, p<0.059) which was of borderline significance. At 4-6 months, there was no statistical difference in the decline of zinc concentration by the baseline zinc concentration in both the groups (Table 3).

Evaluated by stage of lactation, the decline of breast milk zinc concentration among 4-60 days postpartum group was slightly greater, though non-significant, in the MV group than the ZMV group. For the women in the 121-180 days postpartum group, the decline was greater in the ZMV group but none of these

Characteristics0-2 month

postpartum4-6 month postpartum

ZMV MV ZMV MV

Women, n 50 61 51 50

Age of women, y 24.8 ± 5.3 24.6 ± 4.3 24.3 ± 4.4 25.8 ± 3.7

Duration of lactation, % 60.0b 63.9b 60.8c 48.0c

Exclusive breastfeeding, % 12.0 18.0 7.8 2.0

Partial breastfeeding, % 88.0 82.0 92.2 98.0

Height of women, cm 149.2 ± 5.1 151.1 ± 4.9 149.5 ± 6.7 149.5 ± 5.0

More than 3 children <5 years of age, %

16.0 11.5 15.7 16.0

Cumulative no. of times food eaten/month

Very rich in zincd 27.9 30.5 28.3 25.4

Rich in zincd 19.7 22.8 11.8 14.2

Poor in zincd 89.9 99.4 90.1 89.9

Very Poor in zincd 121.8 127.5 134 127.1

Table 1: Baseline Comparison of Participants in the Studya.

a Values are mean ± SD or percentb % of women in 0-30 days postpartumc % of women in 120-150 days postpartum d Reference [17]

Central

Sazawal et al. (2013)Email: ssazawal@jhsph.edu

J Hum Nutr Food Sci 1(2): 1014 (2013) 4/6

Krebs et al, USA [12]

Karra et al,USA [18]

Study Sample

Lactation RDA

Study Sample

Dietary Zinc Intake (mg/d)

Mon

ths o

f Lac

tatio

n

4-6

mo

0-2

mo

2466

181266

24186

Figure 2 Dietary zinc intake among lactating Indian population compared to studies from US and the RDA for Zinc in lactating Woman.

Lactation stratum

ZMV MV

Women, n 101 111

Overall Baseline 32.9 ± 24.9 38.2 ± 23.9

Paired differenceb -10.5 ± 21.9 -12.4 ± 17.2Women, n 50 61

0-2 months Baseline 49.0 ± 26.2 52.4 ± 22.9

Paired difference -18.9 ± 28.2 -22.1 ± 16.1Women, n 51 50

4-6 months Baseline 17.1 ± 7.3 20.9 9.4

Paired difference -2.25 ± 6.61 -0.63 ± 9.52

Table 2: Effect of Zinc Supplementation on Breast Milk Zinc Concentrations (µmol/L)a.

a Values are mean ± SD unless indicated otherwiseb(Mean±SD) of the paired differences between the breast milk zinc concentrations at baseline and at the end of study

comparisons were significantly different between ZMV and MV groups (Table 4).

Median breast milk zinc concentration at each month of lactation using baseline concentrations of both groups and post-supplementation concentrations of the MV group are presented in Figure 3, in comparison with concentrations reported from Denver [20] and Bangladesh [21]. Zinc concentration declined very rapidly up to 3-4 months postpartum [(µmol/L), 62.8 (1mo), 32.2 (2 mo), 23.1(3 mo), 16.3 (4 mo), 18.3 (5 mo), 18.5 (6 mo), 16.0 (7 mo)], but the decline and concentrations in the study sample were similar to the US and Bangladesh populations.

DISCUSSIONIn a population with low zinc intakes, daily supplementation

with 20 mg zinc twice a day, for one month did not alter the decline in breast milk zinc concentrations as lactation progressed. A small net benefit resulted in terms of zinc delivery to the infants of women having low zinc status/low breast milk zinc concentrations in the early stages of lactation i.e. at 0-2 months postpartum. These results are consistent with cross-sectional and longitudinal trials of lactating women from developed countries [12, 22-25] and a trial reported from the developing country [13]. Among women in the 0-2 month postpartum stratum, with baseline milk zinc concentrations below 45 µmol/L, there appeared to be a decrease in the rate of decline of breast milk zinc concentrations with zinc supplementation. Krebs et al, 1985

[20] in a non-randomized trial of maternal zinc supplementation found a slower rate of decline in milk zinc concentrations, but these results were not confirmed in a randomized intervention study by Krebs et al. [12]. Salmenpera et al. [26] reported an elevation of maternal serum zinc concentration during the first 2 months when zinc was supplemented at 40 mg/d and smaller decline in breast milk zinc concentration by 6 month, though not observed with 20 mg zinc supplementation. In a study by Karra et al. [19] zinc supplementation with 25 mg/day showed a positive correlation with breast milk zinc concentration in American women compared with non-supplemented American and Egyptian women. As the study was not a randomized trial the results could have been confounded by other factors. Animal studies, however, suggest that zinc absorption is increased during lactation with the relative increase in dietary zinc intake [27], but not reflected in breast milk zinc concentration with zinc supplementation. In agreement with previous studies breast milk zinc concentrations are not influenced by maternal dietary zinc intake [12,21,22,28-30]. Lack of effect of supplementation indicated in this study, could unlikely be related to low

Lactation Stratum Breast Milk zinc concentration

0-2 months Baseline zinc <45 µmol/L Baseline zinc ≥45 µmol/L

ZMV MV ZMV MV

Women, n 26 24 24 37

Pre supplemented 27.0 ± 9.4 30.2 ± 10.7 72.8 ± 15.2 66.7 ± 16.1

Post supplemented 25.6 ± 18.4 20.5 ± 9.0 34.9 ± 18.6 36.6 ± 13.5

Difference -1.4 ± 19.5b -9.7±8.5b -37.9 ± 23.7 -30.2 ± 14.7

4-6 months Baseline zinc <15.5 µmol/L Baseline zinc ≥15.5 µmol/L

ZMV MV ZMV MV

Women, n 23 14 28 36

Pre supplemented 10.6± 2.7 9.31± 2.58 22.4 ± 5.4 25.4 ± 6.8

Post supplemented 10.9 ±4.9 11.6 ± 6.73 18.0 ± 7.5 23.6 ± 9.4

Difference 0.31 ± 5.5 2.35 ± 6.4 -4.4 ± 6.8 -1.8 ±10.4

Table 3: Effect of Zinc Supplementation on Breast Milk Zinc Concentration of Lactating Women with Different Baseline Zinc Concentrations at 0-2 months and 4-6 Months Postpartuma.

a Values are mean ± SD unless indicated otherwiseb P< 0.059

Days Postpartum ZMV MV

Women, n 30 39

4-30 days Baseline

Paired Difference59.2±25.7-26.4±27.9

63.2±19.7-28.1±15.8

Women, n 20 22

31-60 days Baseline

Paired Difference33.7±18.8-7.61±25.2

33.2±13.8-11.5±10.3

Women, n 31 24

121-150 days Baseline

Paired Difference17.5±7.6

- 1.84±7.320.8±10.5

- 0.19±10.4

Women, n 20 26

151-180 days Baseline

Paired Difference 16.3±7.1-2.89±5.5

20.9±8.4- 1.03±8.8

Table 4: Effect of Zinc Supplementation for One Month on Breast Milk Zinc Concentrations (µmol/L) by Stage of Lactation at Enrollmenta.

a Values are mean unless indicated otherwise

Central

Sazawal et al. (2013)Email: ssazawal@jhsph.edu

J Hum Nutr Food Sci 1(2): 1014 (2013) 5/6

bioavailability of zinc supplement, as this source of zinc has shown significant increases in plasma zinc after supplementation in children in our previous studies [31].

Limitations of the present study include; diets of all the subjects were not adequately evaluated, maternal serum zinc concentrations were not analyzed and pre-post concentrations of zinc in breast milk were measured only from the single sample collected i.e. at the beginning and end of the study. The association of maternal zinc status with the breast milk zinc concentrations could not be adequately evaluated.

There have been reports of differences in breast milk zinc concentrations by socio-economic status [32] within a study population and lower concentrations in some populations with lower socio-economic status as compared to western population [33]. Our findings and similar findings from China [34] do not exclude that variations may be related to dietary or non-dietary factors other than zinc intake. In this context our finding of a marginal change in breast milk zinc concentration in women with lower values may have some importance, but needs to be confirmed. In the present study, all the necessary precautions were taken while sampling and handling of breast milk samples, therefore, it is unlikely that this could have affected our results.

However, there is data suggesting that at least in part homeostatic mechanisms in response to lower zinc intakes increase fractional absorption and intestinal conservation of endogenous zinc [34-36] and the increase in absorbed zinc may be substantial relative to the output in milk. Although in the present study, it does not get reflected in breast milk zinc concentration. Breast milk zinc concentrations at different months of lactation being comparable to lactating women in developed countries suggests there is an active transport mechanism regulating the concentration of zinc in breast milk, favoring the baby irrespective of the zinc status of the mother. This mechanism it seems does not allow for extra zinc secretion in milk irrespective of excessive maternal zinc intake. The active transport may be due to excretion of zinc via an active pump mechanism [34,37]. More studies are required to fully understand the mechanisms of zinc secretion in breast milk, implications of this secretion for maternal nutrition and the possibility of enhancing breast milk zinc concentrations.

CONCLUSIONBreast milk zinc, an important source of bio-available zinc for

infants shows a faster rate of decline postpartum. In developed countries, breast milk zinc concentrations have yielded inconsistent results with maternal zinc supplementation; data from less developing countries is lacking. In the present study when we evaluated the effect of zinc supplementation (20 mg daily for 1 month) on breast milk zinc concentrations of lactating women with suboptimal zinc status, it did not alter the decline in breast milk zinc concentrations as the lactation progressed which was very similar to the US and Bangladesh populations. However, it appears that zinc supplementation affected a subgroup of women with low breast milk zinc concentrations in early lactation, 0-2 months postpartum. The results of this study highlight that maternal zinc supplementation during lactation cannot be used to improve the zinc status of the young infant.

ACKNOWLEDGEMENTSAll the investigators contributed substantially to the design,

implementation of the study and to analysis and writing of the paper. We are grateful to the mothers for their participation, time and co-operation.

FUNDINGThe study is supported in part from the grants of World

Health Organization and Indian Council of Medical Research.

ETHICAL APPROVALThe study was approved by the Committee for Human

Research review at the All India Institute of Medical Sciences. All the procedures were followed according to the ethical standards of the review board.

REFERENCES1. Bhutta ZA, Black RE, Brown KH, Gardner JM, Gore S, Hidayat A, et

al. Prevention of diarrhea and pneumonia by zinc supplementation in children in developing countries: pooled analysis of randomized controlled trials. Zinc Investigators’ Collaborative Group. J Pediatr. 1999; 135: 689-97.

2. Shankar AH, Genton B, Baisor M, Paino J, Tamja S, Adiguma T, et al. The influence of zinc supplementation on morbidity due to Plasmodium falciparum: a randomized trial in preschool children in Papua New Guinea. Am J Trop Med Hyg. 2000; 62: 663-669.

3. World Health Organization (WHO). Report of a Joint WHO/IAEA Collaborative Study. Minor and Trace Elements in Breast Milk. World Health Organization Geneva. 1989 (accessed 10 September 2013).

4. Brown KH, Peerson JM, Rivera J, Allen LH. Effect of supplemental zinc on the growth and serum zinc concentrations of prepubertal children: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2002; 75: 1062-1071.

5. Sazawal S, Black RE, Menon VP, Dinghra P, Caulfield LE, Dhingra U, et al. Zinc supplementation in infants born small for gestational age reduces mortality: a prospective, randomized, controlled trial. Pediatrics. 2001; 108: 1280-1286.

6. Mbofung CM, Atinmo T, Omololu A. Mineral content of colostrum and mature milk of lactating Nigerian women as influenced by stage of lactation. Nutr Rep Int. 1984; 30: 1137-1146.

7. Brown KH, Engle-Stone R, Krebs NF, Peerson JM. Dietary intervention

Time Postpartum (months)0 1 2 3 4 5 6 7

Bre

ast M

ilk Z

inc

(µ m

ol/L

)

0

10

20

30

40

50

60

70

80

90

Krebs et al USA [19]Study SampleSimmer et al Bangladesh [21]

Figure 3 Breast milk zinc concentration (mmol/L) in early 6 months of lactation in three studies.

Central

Sazawal et al. (2013)Email: ssazawal@jhsph.edu

J Hum Nutr Food Sci 1(2): 1014 (2013) 6/6

Sazawal S, Black RE, Dhingra P, Jalla S, Krebs N, et al. (2013) Zinc Supplementation does not Affect the Breast Milk Zinc Concentration of Lactating Women Belonging to Low Socioeconomic Population. J Hum Nutr Food Sci 1(2): 1014.

Cite this article

strategies to enhance zinc nutrition: promotion and support of breastfeeding for infants and young children. Food Nutr Bull. 2009; 30: S144-171.

8. 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.

9. Casey CE, Walravens PA, Hambidge KM. Availability of zinc: loading tests with human milk, cow’s milk, and infant formulas. Pediatrics. 1981; 68: 394-396.

10. Sandström B, Keen CL, Lönnerdal B. An experimental model for studies of zinc bioavailability from milk and infant formulas using extrinsic labeling. Am J Clin Nutr. 1983; 38: 420-428.

11. Krebs NF. Zinc supplementation during lactation. Am J Clin Nutr. 1998; 68: 509S-512S.

12. Krebs NF, Reidinger CJ, Hartley S, Robertson AD, Hambidge KM. Zinc supplementation during lactation: effects on maternal status and milk zinc concentrations. Am J Clin Nutr. 1995; 61: 1030-1036.

13. Khosravi HM, Jalali BA, Eftekhari MH. Effects of dietary zinc supplement during lactation on longitudinal changes in plasma and milk zinc concentration. Pak J Biol Sci. 2007; 10: 1313-1316.

14. Thimmayamma, BVS. A handbook of schedules and guidelines in socio-economic and diet surveys. Hyderabad, India: National Institute of Nutrition—Indian Council of Medical Research Press; 1987.

15. Gopalan C, Ramashastri BV, Balasubramanian SC. Nutritive value of Indian foods. Hyderabad, India: National Institute of Nutrition—Indian Council of Medical Research Press; 2010.

16. Meret S, Henkin RI. Simultaneous direct estimation by atomic absorption spectrophotometry of copper and zinc in serum, urine, and cerebrospinal fluid. Clin Chem. 1971; 17: 369-373.

17. King JC, Keen CL. Zinc. In: Shils ME, Shike M, Ross AC, Caballero B, Cousins RJ. Modern Nutrition in Health and Disease. 10 ed. Lippincott Williams & Wilkins 2005; 214-230.

18. Nutrient requirements and recommended dietary allowances for Indians. Report of the Expert Group of the Indian Council of Medical Research; 2010.

19. Karra MV, Kirksey A, Galal O, Bassily NS, Harrison GG, Jerome NW. Zinc, calcium, and magnesium concentrations in milk from American and Egyptian women throughout the first 6 months of lactation. Am J Clin Nutr. 1988; 47: 642-648.

20. Krebs NF, Hambidge KM, Jacobs MA, Rasbach JO. The effects of a dietary zinc supplement during lactation on longitudinal changes in maternal zinc status and milk zinc concentrations. Am J Clin Nutr. 1985; 41: 560-570.

21. Simmer K, Ahmed S, Carlsson L, Thompson RP. Breast milk zinc and copper concentrations in Bangladesh. Br J Nutr. 1990; 63: 91-96.

22. 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.

23. 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.

24. Vaughan LA, Weber CW, Kemberling SR. Longitudinal changes in the mineral content of human milk. Am J Clin Nutr. 1979; 32: 2301-2306.

25. 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.

26. Salmenperä L, Perheentupa J, Näntö V, Siimes MA. Low zinc intake during exclusive breast-feeding does not impair growth. J Pediatr Gastroenterol Nutr. 1994; 18: 361-370.

27. Davies NT, Williams RB. The effect of pregnancy and lactation on the absorption of zinc and lysine by the rat duodenum in situ. Br J Nutr. 1977; 38: 417-423.

28. Moore ME, Moran JR, Greene HL. Zinc supplementation in lactating women: evidence for mammary control of zinc secretion. J Pediatr. 1984; 105: 600-602.

29. Mahdavi R, Nikniaz L, Gayemmagami SJ. Association between zinc, copper, and iron concentrations in breast milk and growth of healthy infants in Tabriz, Iran. Biol Trace Elem Res. 2010; 135: 174-181.

30. 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.

31. Sazawal S, Black RE, Bhan MK, Jalla S, Bhandari N, Sinha A, et al. Zinc supplementation reduces the incidence of persistent diarrhea and dysentery among low socioeconomic children in India. J Nutr. 1996; 126: 443-450.

32. Rajalakshmi K, Srikantia SG. Copper, zinc, and magnesium content of breast milk of Indian women. Am J Clin Nutr. 1980; 33: 664-669.

33. 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.

34. Sian L, Krebs NF, Westcott JE, Fengliang L, Tong L, Miller LV, et al. Zinc homeostasis during lactation in a population with a low zinc intake. Am J Clin Nutr. 2002; 75: 99-103.

35. Fung EB, Ritchie LD, Woodhouse LR, Roehl R, King JC. Zinc absorption in women during pregnancy and lactation: a longitudinal study. Am J Clin Nutr. 1997; 66: 80-88.

36. Donangelo CM, Zapata CL, Woodhouse LR, Shames DM, Mukherjea R, King JC. Zinc absorption and kinetics during pregnancy and lactation in Brazilian women. Am J Clin Nutr. 2005; 82: 118-124.

37. Moser-Veillon PB. Zinc needs and homeostasis during lactation. Analyst. 1995; 120: 895-897.