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Phytochemicals in Human Milk and Their Potential Antioxidative Protection

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Diets contain secondary plant metabolites commonly referred to as phytochemicals. Many of them are believed to impact human health through various mechanisms, including protection against oxidative stress and inflammation, and decreased risks of developing chronic diseases. For mothers and other people, phytochemical intake occurs through the consumption of foods such as fruits, vegetables, and grains. Research has shown that some these phytochemicals are present in the mother's milk and can contribute to its oxidative stability. For infants, human milk (HM) represents the primary and preferred source of nutrition because it is a complete food. Studies have reported that the benefit provided by HM goes beyond basic nutrition. It can, for example, reduce oxidative stress in infants, thereby reducing the risk of lung and intestinal diseases in infants. This paper summarizes the phytochemicals present in HM and their potential contribution to infant health.
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antioxidants
Review
Phytochemicals in Human Milk and Their Potential
Antioxidative Protection
Apollinaire Tsopmo 1,2 ID
1
Food Science and Nutrition Program, Department of Chemistry, Carleton University, 1125 Colonel By Drive,
Ottawa, ON K1S 5B6, Canada; apollinaire_tsopmo@carleton.ca; Tel.: +1-613-520-2600 (ext. 3122)
2Institute of Biochemistry, Carleton University, 1125 Colonel By Drive, Ottawa, ON K1S 5B6, Canada
Received: 22 December 2017; Accepted: 17 February 2018; Published: 22 February 2018
Abstract:
Diets contain secondary plant metabolites commonly referred to as phytochemicals.
Many of them are believed to impact human health through various mechanisms, including protection
against oxidative stress and inflammation, and decreased risks of developing chronic diseases.
For mothers and other people, phytochemical intake occurs through the consumption of foods such as
fruits, vegetables, and grains. Research has shown that some these phytochemicals are present in the
mother’s milk and can contribute to its oxidative stability. For infants, human milk (HM) represents
the primary and preferred source of nutrition because it is a complete food. Studies have reported
that the benefit provided by HM goes beyond basic nutrition. It can, for example, reduce oxidative
stress in infants, thereby reducing the risk of lung and intestinal diseases in infants. This paper
summarizes the phytochemicals present in HM and their potential contribution to infant health.
Keywords: oxidative stress; human milk; infant; phytochemicals
1. Introduction
Plant secondary metabolites, often referred to as phytochemicals, are believed to play an
important role in human health. Benefits include the protection against oxidative stress, inflammation;
and reduction in risks factors of chronic conditions, such as heart diseases, cancer, diabetes,
and neurodegenerative disorders [
1
,
2
]. Oxidative stress is present in all of these ailments and antioxidant
phytochemicals have been widely investigated in the adult population for their roles in quenching
or reducing excess oxidants, thereby restoring the redox balance. For newborns, human milk (HM)
represents the primary and preferred source of nutrition and there are data in the literature showing
that the benefits of HM go beyond basic nutrition [3].
Human milk from well-nourished mothers is believed to meet the nutrient requirements of
infants for up to six months because its composition is dynamic and varies with the mother’s diet
and time postpartum. The dynamic changes in the composition of HM with time of lactation is to
match the changing needs of growing infants. Proteins in HM are sources of nitrogen, amino acids
and peptides for the newborn. Proteins, specifically those from the whey fraction are also involved
in the development of the immune system, while lactoferrin from the casein group contributes to
non-immunologic defence [
4
]. HM proteins can also serve as a source of antioxidant peptides [
5
,
6
].
As well, glutamate, present in HM, can act as a major oxidative fuel for enterocytes and promote
gastrointestinal barrier function [
7
]. Oligosaccharides and polysaccharides in HM can inhibit the
adhesion of bacteria to the surface of epithelial cells or promote the development of bifidus flora,
thereby contributing to the prevention of infectious diseases in the newborn [
8
,
9
]. Oligosaccharides can
also decrease the likelihood of injury to the retina and the lung in premature infants with respiratory
distress syndrome [
10
,
11
]. HM lipids contain a considerable amount of long chain polyunsaturated
fatty acids, which are precursors of prostaglandin-like prostacyclins that can improve ventricular
Antioxidants 2018,7, 32; doi:10.3390/antiox7020032 www.mdpi.com/journal/antioxidants
Antioxidants 2018,7, 32 2 of 10
function in infants [
12
]. These fatty acids are also essential components of membrane-rich tissues,
such as the brain and the retina photoreceptor membrane [
13
]. HM provides bioactive agents that
include antimicrobial (e.g., immuloglobulins), anti-inflammatory (e.g., lactoferrin) and bioactive
peptides. In addition, there are data demonstrating that breastfeeding promotes the development of
the infant immune system and this might confer long-term health outcomes [
14
]. However, the benefit
of HM goes beyond that of proteins, oligosaccharides and lipids because phytochemicals from mothers’
diets are transferred to their milk. Several of the phytochemicals in HM have antioxidant activities
that may help the infant cope with oxidative stress. The aim of this review is to describe antioxidant
phytochemicals present in the mother’s milk and their potential contribution to redox balance in infants.
2. Phytochemicals in Human Milk
Polyphenols are one of the largest groups of phytochemicals present in crops. Thousands of
phenolic structures have been identified, of which about half belong to the class of flavonoids. This class
is further sub-divided into flavones, isoflavones, flavanones, catechins and anthocyanins. Polyphenols
have been studies in various systems (
in vitro
and
in vivo
) and they possess biological activities,
such as anti-inflammatory and antioxidant activities. In addition, they can regulate the activity
of many enzymes [
15
,
16
]. These activities are associated with the promotion of vascular health,
cognitive function, redox balance, hormonal balance, or neuronal function [
15
,
17
]. One of the most
common biological functions of polyphenols is their ability to act as antioxidants, thereby potentially
protecting adults against oxidative stress and inflammation, while, at the same time, decreasing the
risk of developing chronic and degenerative diseases (e.g., macular degeneration, cancer, obesity,
diabetes) [
18
,
19
]. Oxidative stress is also present in infants and is associated with respiratory and
intestinal diseases [20,21].
2.1. Flavonoids in Human Milk
Secondary metabolites are classified into classes including polyphenols, of which flavonoids
constitute the largest sub-group. Structures of some flavonoids identified in the mother’s milk are
presented in Figure 1and their concentrations in Table 1. A study conducted by Song et al. [
18
] detected
seven flavonoids—epicatechin, epicatechin gallate, epigallocatechin gallate, naringenin, kaempferol,
hesperetin, and quercetin—in milk of mothers who gave birth to full term babies. Mean concentrations
at one week postpartum varied from 15.7 nmol/L for kaempferol to 1118.8 nmol/L for epigallocatechin
gallate. An ingestion of roasted soybeans (20 g, equivalent to 37 mg isoflavones) resulted in mean total
isoflavone concentrations of about 0.2
µ
mol/L in breast milk, with the main constituents being daidzein
and genistein [
22
]. In the work of Khymenets et al. [
23
], the consumption of dark chocolate led to the
identification of epicatechin and its metabolites 12 h after ingestion in the HM of mothers obtained at
6 months postpartum. The metabolites were sulfates and glucuronates of epicatechin, metoxy-catechin,
and
γ
-valerolactone [
23
]. In nursing mothers who consumed a soy beverage containing 55 mg of
total isoflavones for 2–4 days, isoflavone contents of their milk increased from 5.1 to 70.7 nmol/L,
while amounts in the urine of their infants went from 29.8 to 111.6 nmol/mg creatinine [
24
]. In addition,
the mean isoflavone concentration in the plasma of these infants was 19.7 nmol/L. Data from this
research is an indication that isoflavones are available in infants and can potentially protect them from
oxidative stress because they are known antioxidant molecules. In a related study, nursing women
who received 250 mL of soy drink with an isoflavone content of 12 mg for 6 days had 12 nmol of
isoflavone/L in their milks [
25
]. Compared to the study of Franke et al. [
24
], 12 nmol of isoflavone/L
of HM seems small but this is because the two soy drinks had different amounts of isoflavone (12 mg
vs. 55 mg). In another study, breastfeeding women received meals that provided 1 mg of quercetin/kg
bodyweight. In milks collected after 12 h, its mean concentration was 68
±
8 nmol/L and represented
about a 1.7-fold increase relative to values before and at 48 h after the supplementation [26].
Antioxidants 2018,7, 32 3 of 10
Antioxidants 2018, 7, x FOR PEER REVIEW 3 of 10
Figure 1. Chemical structures of polyphenols detected in human milk.
2.2. Carotenoids
The other abundant class of phytochemicals in human milk is the carotenoids (Figure 2, Table
1). Dietary supplementation of lactating mothers with antioxidant rich foods has an influence on how
much is present in milk and therefore, the exposure of infants to these molecules. In the study
conducted by Haftel et al. [27], women took 15 mg β-carotene or 15 mg of lycopene, in the form of
carrot puree or mashed tomato, per day. The two carotenoid molecules were detected in HM and
their concentrations increased with time to reach maximum values after two or four days, depending
on the individual. Lycopene levels rose to a maximum of 130%, and β-carotene to a maximum of
200%, relative to baseline values [27]. In a related work, seven carotenoids were detected in HM
collected one to thirteen weeks postpartum from free living mothers (i.e., no diet intervention).
Amongst them, β-carotene (164.3–88.0 nmol/L), lutein (121.2–56.4 nmol/L) and lycopene (119.9–49.5
nmol/L) were the most abundant [18]. The concentrations of others were α-cryptoxanthin (30.6–13.5
nmol/L), β-cryptoxanthin (57.4–24.8 nmol/L), and zeaxanthin (46.3–21.4 nmol/L). The amount of each
carotenoid decreased from week 1 to week 13 [18]. The variation in the concentration of each of the
carotenoid molecules was most likely due to the oxidative status of the mother or to the amount in
their diet, although the study did not collect information on the participants’ diets. In another study,
pregnant women received daily, 6 g of Chlorella, a single-cell green algae rich in carotenoids, from
16–20 weeks of gestation until the day of delivery [28]. There were significant increases of 1.7, 2.6 and
2.7-fold in β-carotene, lutein and zeaxanthin, respectively in HM of the experimental group,
compared to the control group, at 0–6 days postpartum. A recent study quantified carotenoids in
donors’ and lactating mothers’ milk and found that concentrations of α-carotene, β-carotene,
lycopene and β-cryptoxanthin were 1.9 to 5.7-fold lower in the donors’ milk samples [29]. Lower
contents of carotenoids in donor milk could be due to the pasteurization of milk necessary to prevent
microbial growth and ensure its safety [30], but storage might contribute to the reduction as well.
Donor milk is an effective alternative source of nutrition, specifically for preterm infants, when the
mother’s own milk is not available. Information on whether the amount of antioxidant
phytochemicals present in donors milk has an effect on oxidative stress related outcomes in the
preterm infant is not available. Phytochemicals (e.g., flavonoids and carotenoids) have antioxidant
properties and their presence in diets might protect pregnant women and their fetuses against
oxidative stress induced during pregnancy. The protection can continue after birth because some of
the phytochemicals have been detected not only in HM, but also in biological fluids (e.g., blood and
urine) [31]. In fact, there are direct correlations between concentrations of HM lutein with its daily
Figure 1. Chemical structures of polyphenols detected in human milk.
2.2. Carotenoids
The other abundant class of phytochemicals in human milk is the carotenoids (Figure 2, Table 1).
Dietary supplementation of lactating mothers with antioxidant rich foods has an influence on how
much is present in milk and therefore, the exposure of infants to these molecules. In the study conducted
by Haftel et al. [
27
], women took 15 mg
β
-carotene or 15 mg of lycopene, in the form of carrot puree or
mashed tomato, per day. The two carotenoid molecules were detected in HM and their concentrations
increased with time to reach maximum values after two or four days, depending on the individual.
Lycopene levels rose to a maximum of 130%, and
β
-carotene to a maximum of 200%, relative to
baseline values [
27
]. In a related work, seven carotenoids were detected in HM collected one to thirteen
weeks postpartum from free living mothers (i.e., no diet intervention). Amongst them,
β
-carotene
(164.3–88.0 nmol/L), lutein (121.2–56.4 nmol/L) and lycopene (119.9–49.5 nmol/L) were the most
abundant [
18
]. The concentrations of others were
α
-cryptoxanthin (30.6–13.5 nmol/L),
β
-cryptoxanthin
(57.4–24.8 nmol/L), and zeaxanthin (46.3–21.4 nmol/L). The amount of each carotenoid decreased
from week 1 to week 13 [
18
]. The variation in the concentration of each of the carotenoid molecules
was most likely due to the oxidative status of the mother or to the amount in their diet, although the
study did not collect information on the participants’ diets. In another study, pregnant women received
daily, 6 g of Chlorella, a single-cell green algae rich in carotenoids, from 16–20 weeks of gestation
until the day of delivery [
28
]. There were significant increases of 1.7, 2.6 and 2.7-fold in
β
-carotene,
lutein and zeaxanthin, respectively in HM of the experimental group, compared to the control group,
at 0–6 days postpartum. A recent study quantified carotenoids in donors’ and lactating mothers’ milk
and found that concentrations of
α
-carotene,
β
-carotene, lycopene and
β
-cryptoxanthin were 1.9 to
5.7-fold lower in the donors’ milk samples [
29
]. Lower contents of carotenoids in donor milk could
be due to the pasteurization of milk necessary to prevent microbial growth and ensure its safety [
30
],
but storage might contribute to the reduction as well. Donor milk is an effective alternative source of
nutrition, specifically for preterm infants, when the mother’s own milk is not available. Information on
whether the amount of antioxidant phytochemicals present in donors’ milk has an effect on oxidative
stress related outcomes in the preterm infant is not available. Phytochemicals (e.g., flavonoids and
carotenoids) have antioxidant properties and their presence in diets might protect pregnant women
and their fetuses against oxidative stress induced during pregnancy. The protection can continue after
birth because some of the phytochemicals have been detected not only in HM, but also in biological
fluids (e.g., blood and urine) [
31
]. In fact, there are direct correlations between concentrations of HM
Antioxidants 2018,7, 32 4 of 10
lutein with its daily intake and this has led to the recommendation by some institutions to increase fruit
and vegetable intakes throughout the duration of pregnancy and lactation [32].
Antioxidants 2018, 7, x FOR PEER REVIEW 4 of 10
intake and this has led to the recommendation by some institutions to increase fruit and vegetable
intakes throughout the duration of pregnancy and lactation [32].
Figure 2. Chemical structures of carotenoids detected in human milk.
Table 1. Concentrations of phytochemicals found in human milk.
Compound
Concentration
(nmol/L)
Information on Mothers and Milk
Epicatechin
63.7828.5
Free living mothers, milk at 1, 4 and 13 week [18]
Epicatechin gallate
55.7–645.6
Epigallocatechin gallate
215.1–2364.7
Naringenin
64.1–722.0
Kaempferol
7.8–71.4
Hesperetin
74.8–1603.1
Quercetin
32.5–108.6
Free living mothers, milk at 1, 4 and 13 week [18]
68 ± 8.44
Diet with 1 mg quercetin/kg of body weight [26]
Lutein
56.4–121.2
Free living mothers, milk analyzed at 1, 4 and 13 weeks [18]
497–824
Chlorella supplementation, 6 months from gestational week 16–20
until delivery [28]
280 ± 22
Free living mothers. Milk collected at day 3 [32]
Zeaxanthin
46.321.4
Free living mothers, milk at 1, 4 and 13 weeks [18]
33.2±17.2
Healthy women. Milk collected at days 2–6 [33]
α-Cryptoxanthin
13.5–30.6
Free living mothers, milk at 1, 4 and 13 weeks [18]
β-Cryptoxanthin
24.8–57.4
Free living mothers, milk at 1–14 weeks [18,34]
α-Carotene
23.2–59.0
Free living mothers, milk at 1, 4 and 13 weeks [18]
β-Carotene
88.0–164.3
Free living mothers, milk at 114 weeks [18,34]
75–400
Supplementation, 30 mg β-carotene/d for 28 days [35]
275–484 Chlorella supplementation 6 months, from gestational week 1620
until day of delivery [28]
Lycopene
119.9–49.5
Free living mothers, milk analyzed at 1, 4 and 13 weeks [18,34]
86–244
Chlorella supplementation for 6 months, from gestational week 16
20 until day of delivery. Milk collected at 1–6 days [28]
Isoflavones
70.7 ± 19.2
Soy beverage with 55 mg isoflavones daily for 24 days [24]
12.0
Soy drink, 12 mg isoflavones daily for 6 days [25]
Epicat-Gluc-4 *
0.0–36.4
Free living mothers, milk collected at 130 days [23]
Epicat-Sulf-3 *
0.0–14.5
MetEpicat-Sulf-3 *
0.0–23.7
Figure 2. Chemical structures of carotenoids detected in human milk.
Table 1. Concentrations of phytochemicals found in human milk.
Compound Concentration (nmol/L) Information on Mothers and Milk
Epicatechin 63.7–828.5
Free living mothers, milk at 1, 4 and 13 week [18]
Epicatechin gallate 55.7–645.6
Epigallocatechin gallate 215.1–2364.7
Naringenin 64.1–722.0
Kaempferol 7.8–71.4
Hesperetin 74.8–1603.1
Quercetin 32.5–108.6 Free living mothers, milk at 1, 4 and 13 week [18]
68 ±8.44 Diet with 1 mg quercetin/kg of body weight [26]
Lutein
56.4–121.2 Free living mothers, milk analyzed at 1, 4 and 13 weeks [18]
497–824 Chlorella supplementation, 6 months from gestational week
16–20 until delivery [28]
280 ±22 Free living mothers. Milk collected at day 3 [32]
Zeaxanthin 46.3–21.4 Free living mothers, milk at 1, 4 and 13 weeks [18]
33.2±17.2 Healthy women. Milk collected at days 2–6 [33]
α-Cryptoxanthin 13.5–30.6 Free living mothers, milk at 1, 4 and 13 weeks [18]
β-Cryptoxanthin 24.8–57.4 Free living mothers, milk at 1–14 weeks [18,34]
α-Carotene 23.2–59.0 Free living mothers, milk at 1, 4 and 13 weeks [18]
β-Carotene
88.0–164.3 Free living mothers, milk at 1–14 weeks [18,34]
75–400 Supplementation, 30 mg β-carotene/d for 28 days [35]
275–484 Chlorella supplementation 6 months, from gestational week
16–20 until day of delivery [28]
Lycopene
119.9–49.5 Free living mothers, milk analyzed at 1, 4 and 13 weeks [18,34]
86–244
Chlorella supplementation for 6 months, from gestational week
16–20 until day of delivery. Milk collected at 1–6 days [28]
Isoflavones 70.7 ±19.2 Soy beverage with 55 mg isoflavones daily for 2–4 days [24]
12.0 Soy drink, 12 mg isoflavones daily for 6 days [25]
Antioxidants 2018,7, 32 5 of 10
Table 1. Cont.
Compound Concentration (nmol/L) Information on Mothers and Milk
Epicat-Gluc-4 * 0.0–36.4
Free living mothers, milk collected at 1–30 days [23]
Epicat-Sulf-3 * 0.0–14.5
MetEpicat-Sulf-3 * 0.0–23.7
Caffeine ** 0.06–0.77
Milk of habitual coffee and chocolate mothers [34]
Theobromine 0.08–0.50 **
Paraxanthine 0.15–1.68 **
Theophylline 0.10–0.66 **
* Epicatechin metabolites; ** Concentrations expressed as µg/mL.
2.3. Other Phytochemicals
Three garlic acid metabolites, known as allyl methyl sulfide, allyl methyl sulfoxide and allyl
methyl sulfone, were detected in breast milk 2.5 h after the consumption of garlic [
36
]. Allyl methyl
sulfide affected the odor of milk but showed antioxidant activity, characterized by its ability to reduce
the rate of oxidation of cumene [37]. Both odor and antioxidant characteristics of allyl methyl sulfide
are due to the presence of sulfur. Caffeine and its catabolic products, theobromine, and xanthine,
are key molecules in tea and coffee. Their concentrations and those of related molecules, theophylline
and paraxanthine, in HM were determined to vary from 0.06 to 0.77
µ
g/mL [
38
]. Caffeine, theobromine
and xanthine have been found in model systems to quench hydroxyl radicals, thereby preventing
oxidative DNA breakage induced by this radical species [
39
]. Meanwhile, the effects of caffeine and
its congeners at concentrations detected in HM on the biochemistry of HM or on newborn outcomes
are unknown.
3. Oxidative Stress in Infants
The higher production of oxygen-derived metabolites, collectively known as reactive oxygen
species (ROS) in aerobic organisms, compared to the concentration of available antioxidant molecules
and enzymes is termed oxidative stress. The presence of excess ROS is an important mediator of
cell and tissue damage [
20
,
40
]. Biological molecules susceptible to oxidation include lipids, proteins,
and nucleotides [
41
,
42
]. In general, organisms prevent oxidative damage by maintaining a critical
oxidation–reduction balance, but this is not always the case in the presence of diseases, external stimuli,
improper nutrition or exposure to a hyperoxic environment, as encountered at birth. Data exist to
show that the transition from an intrauterine to an extrauterine life is characterized by physiological
and metabolic changes due, in part, to an increase in the availability of oxygen and a high level of free
iron that can enhance the production of highly toxic hydroxyl radicals through the Fenton reaction [
40
].
Newborns, specifically those who are premature, cannot efficiently deal with oxygen at relatively high
concentrations compared with the intrauterine environment because antioxidant enzymes mature
during late stage gestation and also, because of inadequate transfer of antioxidants, like vitamins E, C,
β-carotene, and ubiquinone, across the placenta [43].
The evaluation of oxidative stress in newborns is based on the quantification of antioxidant
molecules, enzyme activities or markers of lipids and proteins, or DNA damage. For example,
malondialdehyde (MDA), a marker of lipid peroxidation and 8-hydroxy-2
0
-deoxyguanosine, a maker of
DNA damage, is higher in the cord blood of preterm low birth weight infants [
44
]. Higher concentrations
of protein carbonyls were reported in neonatal lungs of subjects with bronchopulmonary dysplasia [
45
],
while in infants treated with supplemental oxygen, ortho-tyrosine, a marker of protein oxidation,
increased with increasing inspired oxygen [
46
]. Perinatal hypoxia increased the oxidation of lipids in
cord blood and also decreased the concentration of the intracellular antioxidant peptide, glutathione [
47
].
Oxidative stress in newborns has been linked to several conditions. Some of these are chronic
lung diseases or bronchopulmonary dysplasia, a condition that usually occurs in preterm infants
Antioxidants 2018,7, 32 6 of 10
receiving respiratory support with mechanical ventilation or prolonged oxygen supplementation [
48
].
Other oxidative stress-associated conditions are necrotizing enterocolitis, an inflammation of the
small intestine and bowel surface, with infiltration of epithelial cells by bacteria; and retinopathy
of prematurity, a type of oxygen-induced damage to blood vessels in the retina that are undergoing
neovascularization [49,50].
There are several strategies for reducing oxidative stress in newborns including supplementation
with enzymatic or non-enzymatic antioxidants [
51
]. Meanwhile, human milk seems to provide better
antioxidant protection in early life due, in part, to its ability to scavenge free radicals compared to
formulas [
52
]. This might be due to the presence of the antioxidant enzymes—glutathione peroxidase,
catalase, and superoxide dismutase—present in HM but not in formula [
53
], which, in addition to their
antioxidant effects in the gut, may pass through the porous neonatal intestine early in infancy [
52
].
In addition to enzymes, vitamins E and C, and possibly phytochemicals can contribute to the protection
provided by HM.
4. Antioxidant Phytochemicals in Human Milk and Redox Balance in Infants
Secondary plant metabolites, and specifically those with antioxidant and anti-inflammatory
properties, play an important role in human health. Human milk (HM) is the optimal food for
newborns and is, in many cases, the only source of nutrition for up to six months. The presence of
plant antioxidant molecules in HM, like polyphenols and carotenoids, indicates that they might have
a role in newborn health outcomes. There are several reviews on the contribution of polyphenols in
the management of oxidative stress and related conditions in the adult population [
17
,
54
] but not in
infants. The effect of the consumption of dietary polyphenols through HM on the health of infants
is not entirely understood because only a few studies have attempted to determine the availability
of polyphenols in HM of lactating mothers and their potential accessibility to HM-fed infants [
23
].
The effect can be studied by analyzing phytochemicals in HM and how they affect milk stability or by
quantifying the amount of these molecules in infant bio-fluids and relating this to health outcomes in
which oxidative stress plays a role. The total concentration of polyphenols in HM, collected three days
after parturition, inversely correlated with malondialdehyde, a genotoxic product of lipid peroxidation,
indicating an increase stability of milk from mothers with high intake of vegetables that are rich in
antioxidant phytochemicals [
55
]. A recent study found that the carotenoid content of HM samples
decreased with an increasing lactation period but, for flavonoids, there was only minimal or, in certain
cases, no change in content with the stage of lactation [
18
]. How this affects the oxidative stability of
HM is unknown because it was not part of that study. Other works have been conducted to determine
the antioxidant potential of HM collected at various stages of lactation and the information was recently
reviewed [
56
]. Although, in one of the studies, total antioxidant capacity of HM was correlated with
α
-tocopherol concentration [
57
], none of the studies looked at the oxidative stability of milk with
regard to the content of their antioxidant phytochemicals.
Carotenoids are known for their antioxidant properties and this can enhance the immune system
and visual acuity because of their accumulation in the eye. The deposition of lutein and zeaxanthin,
for example, in the human retina occurs early in life [
58
], and their content in HM may then be
critical to the development of the infant visual acuity. The macular pigment optical density in the
retina of healthy full term infants significantly correlated with concentrations of zeaxanthin in their
serum samples (r= 0.68) and in their mother’s serum (r= 0.59) [
58
]. Additionally, the same work
reported mother–infant correlations for total serum carotenoids and skin carotenoids, indicating further
potential contribution of this group of phytochemicals to infant development. The retina is exposed
to an intense energy source from lens focused light that generates free radicals [
59
]; the presence of
carotenoids in the eye can consequently improve infant visual acuity while also preventing oxidative
stress. Lactating mothers with low intakes of carotenoids might possibly expose their infants to less
protection from oxidative stress. Fruits and vegetables are recommended throughout the duration
of pregnancy and lactation to maintain sufficient amounts of carotenoids [
28
] and possibly, to better
Antioxidants 2018,7, 32 7 of 10
protect infants. In a study by Perrone et al. [
60
], newborns received lutein at 12 h and 36 h after birth.
The quantification of hydroperoxides, a maker of lipid oxidation in the cord blood, at 48 h of life in
infants, showed a significant reduction in oxidative stress in the lutein group compared to the control
group [
60
]. This is an indication of a decrease oxidation of lipids in infants due to the antioxidant nature
of lutein. In a related work, a combination of lycopene, lutein, and
β
-carotene given to preterm infants
decreased C-reactive protein in plasma and improved rod photoreceptor sensitivity [
61
]. A possible
mechanism for this could be through an antioxidant mechanism that prevented oxidative damage to
the photoreceptor.
The exposure of infants to the flavonoid, quercetin, through HM was estimated to be 0.01 mg/day
based on the assumption that they consumed 900 mL/day of milk, equivalent to about 45 nmol
quercetin/L [
26
,
62
]. In a related work, mothers who consumed 20–25 mg of isoflavones daily might
have exposed their breastmilk fed infants to 0.005–0.01 mg/day of this group of polyphenols [
63
].
The contribution of flavonoids to the reduction of oxidative stress in infants is not clear, although
genistein, daidzein and glycitein were detected in the urine of 4 to 6 month old infants fed soy
products [
64
]. An increase of 14-fold in isoflavone content was found in the milk of lactating mothers
who consumed soy products, concomitantly with an increase of 4-fold in the urine of their babies [
24
].
The presence of flavonoids in biological fluids of infants is an indication that they might help them
cope with oxidative stress, although evidence is needed from future studies.
5. Conclusions
Carotenoids found in human milk may play a role in its oxidative stability and in infant redox
balance, inflammatory status and visual acuity. The minimum concentrations needed to provide
protective effects are not available. This is due, at least in part, to the limited number of studies that
have correlated carotenoid contents in human milk to a specific infant health outcome. The contribution
of flavonoids, the other main group of antioxidant phytochemicals in human milk, to infant oxidative
status is even less clear. Despite this, the recommendation to consume more fruits and vegetables
during both pregnancy and lactation is a key component of dietary guidelines to boost phytochemicals
and protect mothers and infants from oxidative damage and related diseases.
Acknowledgments:
This work was carried out with the support of the National Science and Engineering Research
Council of Canada Discovery Grant No: 371908.
Conflicts of Interest: The author declares that there are no conflicts of interest.
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2018 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
... With regard to bioactive compounds, the antioxidant content of breast milk has been the subject of a number of studies, confirming the presence of different components that have been reported to modulate the effects of oxidative stress [4][5][6][7][8][9][10]. Birth represents a significant oxidative challenge because it involves the transition from the relatively hypoxic intrauterine conditions to the oxygen-rich extrauterine environment. ...
... It has been widely reported that breast milk has a powerful and essential antioxidant composition, which is related to the combination of both exogenous and endogenous molecules including, among others, enzymes, vitamins, protein components and derivatives, oligoelements, carotenoids, and polypohenols [7,17]. Mastitis is associated with inflammatory processes and innate immune cell recruitment and activation, which in turn results in the release of proinflammatory cytokines [43]. ...
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... When considering that colostrum has a high nutritional, immunological and protective contribution to the intestinal microbiome, it is fundamental that it be offered to the neonate 23 . The pertinent literature points out that skin-to-skin contact and breastfeeding in the first hour of life favor not only its offer, but also prolonged EBF and, above all, the motherchild bond. ...
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