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563
P-ISSN: 2304-3075; E-ISSN: 2305-4360
International Journal of Veterinary Science
www.ijvets.com; editor@ijvets.com
Research Article
DOI: 10.37422/IJVS/20.070
Toxic Elements in Dried Milk and Evaluation of their Dietary Intake in Infant
Formula
Aml S Ibrahim*, Saad MF and Nagah M Hafiz
Cairo University, Faculty of Veterinary Medicine, Department of Food Hygiene & Control, Giza, Egypt
*Corresponding author: amola201391@gmail.com.
Article History: 20-097
Received: April 10, 2020
Revised: July 04, 2020
Accepted: July 11, 2020
ABSTRACT
Infant’s feeding patterns are important for development and growth; therefore babies are very sensitive to toxic
elements, mainly through their food, so in the present study, the concentrations and daily intake of some Toxic
Elements (TEs); Lead (Pb), Arsenic (As), Cadmium (Cd), Mercury (Hg) and Aluminum (Al) were measured in
different and random 60 dried infant foods {30 infant formula (0-6 months) and 30 milk-cereal based infant formula
(6 months)} which obtained from various supermarkets and pharmacies. The analysis was done using Inductive
Coupled Plasma - Mass Spectrometer (ICP-MS). It could be determined the lead, arsenic, cadmium, mercury and
aluminum by mean values of 0.424±0.006, 0.205±0.003, 0.014±0.0001, 0.298±0.007 and 0.464±0.029 mg/kg in the
examined infant milk formula samples and a ranged minimum to maximum concentrations of 0.114-0.177, 0.155-
0.293, 0.014-0.015, 0.282-0.310 and 0.287-0.437mg/kg, respectively in the examined milk-cereal based infant
formula. Present study indicates that, the greater level of contamination of examined infant formula samples with
toxic elements (lead and mercury) surpasses the maximum limit and Provisional Tolerable Daily Intake (PTDI) of
these elements. Mercury is over PTDI (0.0005 mg/kg bwt/day) in all milk-cereal based infant formula samples, also
arsenic in all examined samples of this type of formula was exceed the maximum limit (0.05 mg/kg) of Indian
standard. This investigation shows such types of infant formula need more amendment to set limit of more toxic
metals for this sensitive group of population.
Key words: Infant formula; Toxic elements; Milk-cereal based infant formula; Spectrometer.
INTRODUCTION
The World Health Organization (WHO) suggested
that; breast milk feeding is the most natural and best
source for nutrition of infants. However, when it is not
enough and/or possible in some cases, mightily available
infant formulas provide a proper substitute (Mehrnia and
Bashti, 2014; WHO, 2015). Although the importance of
infant milk formula and complementary feeding as a
source of nutrition for infants, these are the main root of
toxic elements that pose health risks to children (Kazi et
al., 2010; Pandelova et al., 2012).
Infants are the most sensitive population group to the
harmful effects of toxic metals due to the significant
increased absorption of these metals through the digestive
tract than adults, an inadequate developed detoxification
method, rapid metabolic processes, and higher food intake
relative to their body weight (Pandelova et al., 2012).
Heavy metals presence in infant food may be referred
to many factors such as; contamination of the original
milk, that attributable to consumption of dairy animals to
contaminated feed and water or exposure to massive
environmental pollution, species diversity also during
manufacture and packaging (Abdelkhalek et al., 2015).
The high content of toxic elements as (Lead, Arsenic and
Cadmium), in some baby foods may be due to the food
additives or other ingredients, especially rice and
vegetable (Kazi et al., 2010). Toxic elements could bio-
accumulate in vital organs even in low concentrations as
due to renal immaturity of children (<12 months); hinders
their elimination. These elements get their way in the
body through skin, inhalation and ingestion; mostly a high
concentration couldn’t excrete from infants' body and
accumulated in various organs, results in gathering of
these elements in the body causing critical disorders such
as infertility, neurological, thyroid and autism disorder or
even death (Ozbolat and Tuli, 2016).
Monitoring of these toxic elements in infant milk
formula is of great health significance to save infants from
their acute & chronic toxicity. Appropriate good
manufacturing practice and fulfilment of Hazard Analysis
and Critical Control Points (HACCP) system are wanted
for the maximum safety manufacture (Kazi et al., 2010;
Burrell and Exley, 2010; Hafiz et al., 2016). We aim in
Cite This Article as: Ibrahim AS, Saad MF and Hafiz NM, 2020. Toxic elements in dried milk and evaluation of their
dietary intake in infant formula. Int J Vet Sci, 9(4): 563-567. www.ijvets.com (©2020 IJVS. All rights reserved).
Int J Vet Sci, 2020, 9(4): 563-567.
564
this study to define the potential health hazards of toxic
elements (Pb, Cd, As, Hg and Al) in infant formula and
and milk-cereal based infant formula as a source of these
metals for Egyptian infants by determination their level
and comparing it with permissible limits available in
Egyptian standards and several international standards,
also we aim to evaluate the intake risk on the basis of the
FAO/WHO recommendations; when infants depend on
their feeding on these formula and/or milk cereal foods.
MATERIALS AND METHODS
Collection of samples
A total of sixty random samples {30 each of infant
formula (0-6-month age) and milk-cereal based infant
formula (6-month age)} were obtained from various retail
shops, supermarkets and pharmacies located at Giza and
Cairo Governorate, Egypt. All samples were keeping in
their packages to be examined in the laboratory and were
still valid for consumption. All samples were coded and
stored at the same conditions like their sources till
analysis.
Sample preparation according to (AOAC, 2012)
Into each microwave digestion vessel; a homogenized
sample (typically 1g) was weighed and only 0.5ml of
deionized water was added to low the nitrous fumes
resulting from the matrix digestion in the digestion vessel.
Then 8ml of concentrated HNO3 (Sigma-Aldrich,
Germany) (shaking well) and 2 ml of H2O2 30% (Sigma-
Aldrich, Germany) were added. The vessels were capped
securely and hold into the High-pressure microwave oven
(Milestone, Italy) according to the manual instructions.
Samples were digested at power of 1800 watt to reach a
minimum temperature of 200°C for a minimum time of 15
min, left at the same temperature for other 15min, and
then allowed withdrawing for <80°C. After the heating
cycle has been completed, the vessels allowed cooling
down in water bath for 30min and then vessels were
opened carefully. The residual contents of each vessel
were poured into an acid-cleaned 50ml volumetric flask
and the dilution was done by deionized water to a final
volume of 20ml. The samples were stored in
polypropylene tubes until be measured by ICP-MS.
Analysis of samples
After complete digestion; all samples were analyzed
for their metal contents; lead (Pb), arsenic (As), cadmium
(Cd), mercury (Hg) and aluminum (Al) by Inductive
Coupled Plasma-Mass Spectrometer (ICP-MS) Method
“Perkin-Elmer model optima 2000DV, Waltham, USA” at
the trace elements analytical laboratory, Regional Center
for Food and Feed (RCFF), Agriculture Research Center,
Giza, Egypt.
Calculation of the Estimated Daily Intake
Estimated Daily Intakes (EDI) of these toxic metals
was calculated using the following equation:
EDI = C × D / BW
Express the mean EDI of toxic elements in mg/kg
bwt/day, C: concentration of metals obtained from
samples, D: concentration of daily intake of powder infant
formula (g/day) and BW: average Body Weight.
Average daily consumed infant formula powder from
feeding dosages recommended by label instructions and
growth charts at 6-month-old were 135g/day, while the
average body weights of infants were 7.5kg and only
100g/day for milk-cereal based infant formula (Mehrnia
and Bashti, 2014; Sipahi et al., 2014). PTWI (Provisional
Tolerable Weekly Intake) values were divided by 7 to
calculate the Provisional Tolerable Daily Intake (PTDI)
(Sipahi et al., 2014), while EWI (Estimated Weekly
Intake) calculated by multiplying EDI by 7. We
comparing the EDI and EWI with PTDI and PTWI set by
(JECFA, 2018).
Statistical analysis according to (SPSS version 25)
The analysis of variance (ANOVA) test was
conducted to test the possible significance (P≤0.05)
among mean values of heavy metals concentrations using
Fishers Least Significance Difference (LSD).
RESULTS
As showing in Table 1, all the examined infant milk
formula samples were contaminated with all measured
metals; lead, cadmium, aluminium, arsenic and mercury in
a ranged minimum to maximum concentrations of 0.384-
0.480, 0.014-0.015, 0.296-0.761, 0.174-0.233 and 0.236-
0.345mg/kg, respectively, while the mean values for milk-
cereal based infant formula samples were 0.145±0.004,
0.014±0.0001, 0.352±0.009, 0.214±0.008 and
0.296±0.014mg/kg, respectively as illustrated in (Table 2).
Table 1: Toxic metals levels in the examined infant milk
formula samples (n=30)
Metal
Positive samples
Min.
Max.
Mean±SEM
(mg/kg)
No.
%
Pb
30
100.00
0.384
0.480
0.424±0.006a
Cd
30
100.00
0.014
0.015
0.014±0.0001b
Al
30
100.00
0.296
0.761
0.464±0.029a
As
30
100.00
0.174
0.233
0.205±0.003a
Hg
30
100.00
0.236
0.345
0.298±0.007a
n=number of examined samples. a and b: significance
difference, P<0.05; No.: Number of positive samples.
Table 2: Toxic metals levels in the examined milk-cereal based
infant formula samples (n=30)
Metal
Positive samples
Min.
Max.
Mean±SEM
(mg/kg)
No.
%
Pb
30
100.00
0.114
0.177
0.145±0.004a
Cd
30
100.00
0.014
0.015
0.014±0.0001b
Al
30
100.00
0.287
0.437
0.352±0.009a
As
30
100.00
0.155
0.293
0.214±0.008a
Hg
30
100.00
0.282
0.310
0.296±0.014a
n=number of examined samples. a and b: significance
difference, P<0.05; No.: Number of positive samples.
With evaluation the degree of acceptability for infant
milk formula (Table 3), all samples weren’t acceptable for
(Pb, Cd and Al) according to each available standard. In
(Table 4); Estimated Daily Intake (EDI) of infant milk
formula was tolerable for all measurable metals (Cd, Al
and As) with values 0.0003, 0.008 and 0.004mg/kg
bwt/day, respectively except lead (0.008mg/kg bwt/day)
and mercury (0.005mg/kg bwt/day).
Int J Vet Sci, 2020, 9(4): 563-567.
565
Table 3: Degree of acceptability of the examined infant formula samples based on available standards (n=30)
Metal
Standard
Pb
Cd
Al
ML
No.
%
ML
No.
%
ML
No.
%
Egyptian Standards (ES: 7136 / 2010)
0.02
0
0.00
NA
----
-----
NA
-----
-----
JECFA (2018)
0.01
0
0.00
NA
----
-----
NA
-----
-----
European Commission (EC) (1881/2006)
0.05
0
0.00
0.01
0
0.00
NA
-----
-----
FSANZ* (2.9.1/ 2017)
0.02
0
0.00
0.01
0
0.00
0.2
0.00
0.00
n=number of examined samples; No.: Number of acceptable samples; ML=Maximum Limit (mg/kg); NA=Not Available; *FSANZ:
Food Standards Australia New Zealand.
Table 4: Comparison of Estimated daily/weekly intake and provisional tolerable daily/weekly intake of toxic elements of infant
formula samples according to The Joint Food Agriculture Organization (FAO)/World Health Organization (WHO), 2018 (n=30)
Daily/Weekly intake (mg/kg)
Metal
PTWI
PTDI
EWI
EDI
Acceptable samples
Unacceptable samples
No.
%
No
%
Pb
0.025*
0.004
0.05
0.008
0
0.00
30
100.00
Cd
0.006
0.0009
0.002
0.0003
30
100.00
0
0.00
Al
2.00
0.29
0.05
0.008
30
100.00
0
0.00
As
NA
NA
0.03
0.004
-
-
-
-
Hg
0.004
0.0005
0.04
0.005
0
0.00
30
100.00
n=number of examined samples; No.: Number of acceptable or unacceptable samples; PTWI=Provisional Tolerable Weekly Intake;
PTDI=Provisional Tolerable Daily Intake; EWI=Estimated Weekly Intake; EDI=Estimated Daily Intake; NA=Not Available;
*=Withdrawn at the 73rd meeting (2010), JECFA (The Joint FAO/WHO Expert Committee on Food Additives).
Table 5: Degree of acceptability of the examined milk-cereal based infant formula sample based on available standards (n=30)
Metal
Standard
Pb
Cd
As
ML
No.
%
ML
No.
%
ML
No.
%
Egyptian Standards (ES: 7136 / 2010)
0.2
30
100.00
0.2
30
100.00
1*
30
100.00
JECFA (2018)
0.2
30
100.00
0.1
30
100.00
NA
-----
-----
European Commission (EC) (1881/2006)
0.05
0
0.00
0.04
30
100.00
NA
-----
-----
n=No of examined samples; No.: Number of acceptable samples; ML=Maximum limit; NA=Not available; * Egyptian Standards (ES:
3284/2005).
Table 6: Comparison of Estimated daily/weekly intake and provisional tolerable daily/weekly intake of toxic elements of examined
milk-cereal based infant formula samples, JECFA: 2018 (n=30)
Daily/Weekly intake (mg/kg)
Metal
PTWI
PTDI
EWI
EDI
Acceptable samples
Unacceptable samples
No.
%
No.
%
Pb
0.025*
0.004
0.014
0.002
30
100.00
0
0.00
Cd
0.006
0.0009
0.0013
0.0002
30
100.00
0
0.00
Al
2.00
0.29
0.03
0.005
30
100.00
0
0.00
As
NA
NA
0.02
0.003
-
-
-
-
Hg
0.004
0.0005
0.03
0.004
0
0.00
30
100.00
n=number of examined samples; No.: Number of acceptable or unacceptable samples; PTWI=Provisional Tolerable Weekly Intake;
PTDI=Provisional Tolerable Daily Intake; EWI=Estimated Weekly Intake; EDI=Estimated Daily Intake; NA=Not Available;
*=Withdrawn at the 73rd meeting (2010), JECFA (The Joint FAO/WHO Expert Committee on Food Additives).
In Table 5, all examined milk-cereal based infant
formula samples was acceptable for Pb, Cd and As
according to each available standard except for lead
concentration which not agreeable (unacceptable) to
(European Commission, 2006). The EDI for milk-cereal
based infant formula samples was not tolerable for
mercury (0.005mg/kg bwt/day) only; as showed in (Table
6), while other metals (Pb, Cd, Al and As) have
acceptable EDI 0.002, 0.0002, 0.005 and 0.003mg/kg
bwt/day, respectively. All data of EDI and Estimated
Weekly Intake (EWI) were judging according to (JECFA,
2018).
DISCUSSION
The majority of metals exist in baby foods naturally
or due to incorrect human actions, such as storage,
processing, agriculture & industrial activities, increased
municipal waste water, formula preparation with low
quality water and improper handling by mothers (Joseph
et al., 2011). Arsenic, Lead, Mercury, and Cadmium
classified as 1st, 2nd, 3rd, and 4th, respectively in a priority
list the “Top 20 Hazardous Substances” in 2001; which
complied by the Agency for Toxic Substances and
Disease Registry (ATSDR) in collaboration with the U.S.
Environmental Protection Agency (Cruz et al., 2009).
Lead
The analytical data for infant milk formula samples in
Table 1, were lower than (Pandelova et al., 2012). In
Table 2, lead concentration of milk-cereal based infant
formula samples was below than findings of (Pandelova et
al., 2012; Sipahi et al., 2014). This unforeseen high Pb
level in examined baby formula samples could be due to
contamination during food processing of various
ingredients (Kazi et al., 2010). Lead is one of the most
vigorous neurotoxin that has irrevocable effect on infant
nervous system development, lead to less learning abilities
with negative effects on the intelligence and showing
toxicity in children even at minimum levels of exposure,
due to its high possible absorption especially in this group
of population (US Environmental Protection Agency, 2003).
Int J Vet Sci, 2020, 9(4): 563-567.
566
As shown in Table 3, the lead content of all examined
infant milk formula samples were over permissible limit
of Egyptian and other international standards.
Consequence to high concentration of Pb in infant
formula shows high level of daily intake 0.008 mg/kg
bw/day compared with PTDI (0.004 mg/kg) which was
withdrawn at the 73rd meeting of (JECFA, 2010), due to
estimate that previous PTDI is related to reduce children’s
Intelligence Quotient (IQ) and increase blood pressure in
adults. So this PTDI was concluded to be no longer health
protective (Table 4). Only according to EC standard (0.05
mg/kg); the lead concentration of milk-cereal based infant
formula samples was 100% unacceptable, but acceptable
by 100% for all other comparing standards with low and
agreeable EDI as shown in Tables 5 and 6.
Cadmium
Cadmium toxicity results in kidney failure, renal
stone formation, neurological effects, disturbance in Ca+2
metabolism, liver disorders, prostate cancer and fetal
death (Zaidan et al., 2013; Sipahi et al., 2014).
As shown in Tables 1 and 2, there was a significant
difference (P<0.05) between concentrations of cadmium
and other toxic elements in all the examined infant
formula samples. In Table 1, the cadmium level of infant
milk formula samples was elevated than data obtained
through (Pandelova et al., 2012; Chekri et al., 2019). The
results of milk-cereal based infant formula samples
presented in Table 2 were lower than that reported via
(Chekri et al., 2019). Permissible limit of cadmium in all
type of infant formula need more attention as not
mentioned in Egyptian or JECFA standards, as in this
study all of examined infant milk formula samples were
exceed permissible limit (0.01mg/kg) of EC and FSANZ
standards along with passable EDI 0.0003mg/kg bwt/day
as revealed in Tables 3 and 4. Cadmium content of all
thirty milk-cereal based infant formula samples was
acceptable for all mentioned standards (Table 5), with
tolerable EDI 0.0002mg/kg bwt/day as mentioned in
Table 6.
Aluminium (Al)
This element reported to contaminate baby dried
foods and infant formula through equipment used in both
processing and storing of bulk products or prepared for
selling using Al packaging material (Burrell and Exley,
2010). Because of newborns undeveloped renal system
and intestinal barriers, high level of Al would collect in
their thyroid gland, brain and vital organs causing sever
renal and nervous disorders as Alzheimer’s disease
(Sipahi et al., 2014; Ahmed et al., 2016).
The data presented in Table 1 in infant formula
samples were higher than results obtained by (Chekri et
al., 2019), but decreased than findings reported by (Sipahi
et al., 2014). Milk-cereal based infant formula
contaminated with high Al level (Table 2) and was lower
than results reported by (Chekri et al., 2019). All
examined infant formula samples were more than
maximum limit of FSANZ standard (0.2mg/kg). No more
standards mention limit of aluminium for infant formula
or even for milk-cereal based infant formula and this need
more study due to high content of aluminium in examined
baby food samples (Table 3).
In Tables 4 and 6, aluminium EDI of infant milk
formula was (0.008mg/kg bwt/day), but was lower intake
(0.005mg/kg bwt/day) for milk-cereal based infant
formula samples. These results were similar to (Burrell
and Exley, 2010), and below than PTDI which set by
(JECFA, 2018) (0.29mg/kg bwt/day); so that we need
more study as well as determination of its risk in baby
foods. Bishop et al., 1997; mentioned that parenteral
exposure of preterm infants to 0.055 mg Al/kg bwt/day,
which is a level of aluminium that is possible with regular
feeding of infant formulas for particular duration resulted
in neurodevelopmental effects at 18 months.
Many of researchers have debated inadequacy of
emitted acceptable recommended standards for human
exposure to aluminium especially newborn children.
Therefore; more need for research to minify Aluminium
levels in infant formula (Redgrove et al., 2019).
Arsenic
The Agency for Toxic Substances and Disease
Registry (ATSDR, 2018) classifies arsenic as number one
on its list that pose the highest potential threat to human
health. Arsenic belongs to a group of carcinogens that has
many chronic effects as several types of cancers, skin
lesions, cardiac disease and neurotoxicity. The first solid
food for babies (4-6 months) is rice cereal that known to
have been contaminated with high quantity of arsenic, as
arsenic exposure in infants is about 3 times than adults
(Carignan et al., 2016).
It is showed in our study that; the tested samples of
infant milk formula were contaminated by arsenic with a
mean value of 0.205±0.003mg/kg (Table 1); which more
than level reported via (Chekri et al., 2019), while in
milk-cereal based baby food concentrations were with a
mean value of 0.214±0.008mg/Kg (Table 2), this similar
to data reported by (Fao et al., 2019), but higher than
results obtained by (Chekri et al., 2019).
Referred to Indian Standard, 2006; all infant formula
samples exceed 0.05mg/kg permissible limit and only
60% over limit of (National Standards on Food Safety of
China, 2010); 0.2mg/kg without any other available
standards. The EDI of arsenic for infant milk formula
samples exhibited in Table 4 was 0.004mg/kg bwt/day
with no available PTDI for total arsenic. In case of
examined milk-cereal based baby food samples referred to
Egyptian standard; all samples were within legal limit, but
exceed limit of Indian Standard, 2006; (0.05mg/kg) with
EDI (0.003mg/kg bwt/day) as presented in Tables 5 and 6.
In 1955, infants arsenic poisoning had taken place in
Japan from milk powder; this resulted in poisoning of
12131 neonate infants and death of 130. The poisoned
infants showed hematopoietic and pancreatic caners and
the only six hundred survivors from the previous disaster
suffered from neurological diseases and mental
retardation effects in their 50 years (Nepalia et al., 2017).
Mercury
All examined infant food samples were polluted with
mercury in high levels with a mean value of
0.298±0.007mg/kg for infant milk formula; these results
are similar to (Cruz et al., 2009), and with a mean value of
0.296±0.014 mg/kg for milk-cereal based infant formula
(Table 1 and 2), these findings were higher than reported
Int J Vet Sci, 2020, 9(4): 563-567.
567
by (Pandelova et al., 2012). Such high contamination
level in infant formula and milk-cereal based infant
formula samples with Hg exceed the PTDI set by JECFA
(0.0005mg/kg bwt/day) as shown in (Table 4 and 6) with
elevated EDI (0.005mg/kg bwt/day) and (0.004mg/kg
bwt/day), respectively. Even though no regulatory limit
for mercury content in any of mentioned standards for
infant formula and milk cereal-based baby food and this
need more attention from Egyptian and international
authorities. Mercury is excreted firstly after 1–3 months in
feces for inorganic Hg and urine for methyl Hg, which is
able to cross the Placenta and Blood-Brain, causing neuro-
toxicity, teratogenicity and brain damage, accordingly
mercury in high amount is considering very harmful for
infants and has serious consequences on brain, kidney,
and lungs (EFSA, 2012).
Conclusion
In our study; infant formula, that especially neonates
(0 - 6 month), are highly polluted with unexpected levels
of lead, arsenic and mercury as well as not neglectable
contamination by cadmium and aluminum; where now the
majority of infants all over the world received this type of
food. The tolerable values have been established by
JECFA for lead and arsenic were withdrawing in 2011
and that mean the tolerable intake values were not
considered secure anymore. As our young children are
with high sensitivity and vulnerability during growth, they
need more attention from authorities. The cereal baby
food standards need to be checked as not all elements
permissible limit was established. Parents are requiring to
be informed about the importance and safety of breast
milk especially first 6 month of baby life. Therefore, the
infant milk-based food industries need a strict periodical
monitoring for levels of potential toxic metals
contamination in order to ensure that their products are
safe for infants.
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