Is camel milk lactoferrin effective against COVID-19?

Abstract

Lactoferrin is one of the glycoproteins from the transferrin family which binds Fe3+ ion. Lactoferrin is found in mammalian milk but the camel milk has greater quantity of lactoferrinin compared with other livestock species. Lactoferrin strengthens the immune system by protecting the host cells against bacterial and viral infections and inflammations. Activation, proliferation and regulation of the phagocytic action of immune cells are also facilitated by the lactoferrin. The antiviral actions of lactoferrin are against both DNA and RNA viruses and it inhibits viral adhesion and entry into cells and binds viral particles. Generally, camel milk lactoferrin may directly interact with viral molecules or with the viral receptor (heparan sulfate) on the cellular surfaces to prevent the virus attachment and infection. The boosting host immune system by nutritional supplements such as lactoferrin may work against SARS-CoV-2 entry and infection into the host cells. Because of the homology in genetic sequence and receptor binding domain between SARS-CoV and SARS-CoV-2, lactoferrin may inhibit the SARS-CoV-2 invasion in the same way to SARS-CoV, via binding to heparan sulfate and prevent the viral infections and epidemic. Keeping in view this fact that lactoferrin can modulate immune responses to viral infections; it may reduce severe infections. Milk lactoferrin (in particular camel milk with the highest amount of lactoferrin) as powder or tablets may be a novel promising candidate and preventative treatment for more severe cases of COVID-19. However, it needs more studies on the unique medicinal effects of camel milk lactoferrin to verify its efficacy on COVID-19 prevention and treatment.

Full text

World Journal of Pharmaceutical Sciences
ISSN (Print): 2321-3310; ISSN (Online): 2321-3086
Available online at: http://www.wjpsonline.org/
Review Article
Address for Correspondence: Tahereh Mohammadabadi, Faculty of Animal Science and
Food Technology, Agricultural Sciences and Natural Resources University of Khuzestan, Iran;
mail: mohammadabadi@asnrukh.ac.ir; t.mohammadabadi.t@gmail.com
How to Cite this Article: Tahereh Mohammadabadi and Tanveer Hussain. Is Camel milk
lactoferrin effective against COVID-19?. World J Pharm Sci 2021; 9(2): 91-97.
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© 2013-21 World J Pharm Sci
Is camel milk lactoferrin effective against COVID-19?
Tahereh Mohammadabadi1* and Tanveer Hussain2
1Faculty of Animal Science and Food Technology, Agricultural Sciences and Natural
Resources University of Khuzestan, Iran
2Department of Molecular Biology, Virtual University of Pakistan, Lahore, Pakistan
Received: 25-12-2020 / Revised Accepted: 21-01-2021 / Published: 24-01-2021
ABSTRACT
Lactoferrin is one of the glycoproteins from the transferrin family which binds Fe3+ ion.
Lactoferrin is found in mammalian milk but the camel milk has greater quantity of
lactoferrinin compared with other livestock species. Lactoferrin strengthens the immune
system by protecting the host cells against bacterial and viral infections and inflammations.
Activation, proliferation and regulation of the phagocytic action of immune cells are also
facilitated by the lactoferrin. The antiviral actions of lactoferrin are against both DNA and
RNA viruses and it inhibits viral adhesion and entry into cells and binds viral particles.
Generally, camel milk lactoferrin may directly interact with viral molecules or with the viral
receptor (heparan sulfate) on the cellular surfaces to prevent the virus attachment and
infection. The boosting host immune system by nutritional supplements such as lactoferrin
may work against SARS-CoV-2 entry and infection into the host cells. Because of the
homology in genetic sequence and receptor binding domain between SARS-CoV and SARS-
CoV-2, lactoferrin may inhibit the SARS-CoV-2 invasion in the same way to SARS-CoV, via
binding to heparan sulfate and prevent the viral infections and epidemic. Keeping in view this
fact that lactoferrin can modulate immune responses to viral infections; it may reduce severe
infections. Milk lactoferrin (in particular camel milk with the highest amount of lactoferrin)
as powder or tablets may be a novel promising candidate and preventative treatment for more
severe cases of COVID-19. However, it needs more studies on the unique medicinal effects
of camel milk lactoferrin to verify its efficacy on COVID-19 prevention and treatment.
Keywords: Camel milk, Lactoferrin, COVID-19, Anti-viral
INTRODUCTION

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Lactoferrin (LF) is a glycoprotein from bovine milk
which binds iron and has the ability to reversibly
chelate with two Fe3+ ions. This iron withholding
ability of LF is very high, thus it inhibits the
microbial growth and reactive oxygen species
formation.1 The LF is found in high quantity in
milk and colostrum.1,2 After isolation from bovine
milk, LF was also detected and isolated from milk
of camel, sheep and goat.3 Moreover, lactoferrin is
also produced in considerable amounts by
neutrophils about 15g/106 neutrophils1 and mucosal
epithelial cells in cows, goats, horses, rodents and
humans.4Lactoferrin has some physiological
activities which include iron absorption and
regulation in the intestine, protection against
microbial infections, anti-inflammatory, anti-
proliferative and immuno-modulator properties.2
Regarding these important functions, lactoferrin is
regarded as a nutraceutical supplement.
Camel milk has many protective proteins and
enzymes having anti-microbial and immunological
properties against bacterial and viral infections.
These include the immunoglobulins, lactoferrin,
lysozyme, lactoperoxidase, peptidoglycan
recognition protein, vitamins C and
oligosaccharides which work against microbial
infections.5 But most of the anti-microbial and anti-
viral action of camel milk is because of lactoferrin
and immunoglobulins.6 The studies revealed that
the concentration of lactoferrin in bovine milk
ranges from 0.02-0.35 mg/mL.7Lactoferrin content
in camel’s milk is shown to be higher when
compared with the milk from bovine and ranges
from 0.7-2.1 mg/mL.8Lactoferrin has
immunomodulatory functions by binding to
microbial particles or cell receptors and inhibit the
infections.9 Also, it can bind receptors that SARS-
CoV and human coronavirus NL63 use for entry
into the host cells.10 Information on the potential of
camel milk lactoferrin against the COVID-19 is
rarely reported. Therefore, the focus of the current
review is exploring the antiviral effects of camel
milk lactoferrin against COVID-19.
What is lactoferrin?
Lactoferrin glycoprotein is the part of the
transferrin family. The polypeptide chain of
lactoferrin contains 600-700 amino acid residues.2
In addition to Fe2+ or Fe3+, lactoferrin also binds
Mn2+, Cu2+ and Zn2+.1 Protein structure of
lactoferrin is composed of α-helix and β-sheets
which further divided into N- and C- lobe that are
connected by a peptide (334–343 amino acids in
human lactoferrin).
Both the lobes of lactoferrin packed together due to
hydrophobic connections in this molecule. Also,
both lobes of lactoferrin, are highly homologous
(about 33–41%)1 and further divided into two
domains (Figure 1). The iron sites of lobes and
amino acid sequences are highly conserved and
they have a high identity with transferrin. Even
ligands for Fe3+ are the same in both lobes.11 Two
types of lactoferrin exist including apo-LF that do
not bind iron and holo-LF which binds with iron or
Fe3+ and resistance to proteolysis of holo-LF is
highest.12 The iron withholding capacity of
lactoferrin cause to anti-microbial activity and
immuno-modulation properties. Moreover, without
iron binding ability, lactoferrin interact with
bacteria and viruses and inhibits their attachment to
cell surface receptors. Regarding the most studies,
no significant difference was observed in the anti-
viral activity of iron-binding and non-iron binding
forms of lactoferrin.13
Camel milk as important source of lactoferrin
According to studies, human milk showed the
highest concentration of lactoferrin (1.7 mg/mL),
while the lowest concentration is found in donkey
milk (0.07 mg/mL).7 In human colostrum, the
amount of lactoferrin ranges from 5.3±1.9 mg/mL
and after the one month of lactation, this amount
reaches 1 mg/mL.14 The concentration of
lactoferrin in cow’s milk is lower as compared to
human milk and ranges from 0.83mg/mL for
colostrum and 0.09mg/mL for normal milk.15
Higher levels of lactoferrin are observed in camel
milk when compared to other mammals. Alhaji et
al 2020 reported that the amount of lactoferrin in
camel milk is 10 times greater as compared to
cow’s milk lactoferrin (2.48 mg/mL versus 0.07-
0.28 mg/mL, respectively). A high amount of
citrate in the milk reduces the inhibitory effects of
lactoferrin due to citrate ions and lactoferrin
compete for binding Fe. Since camel milk contains
less citrate than cows' milk, so the amount of
lactoferrin in the milk of camel is greater.5
The reason for these variations of lactoferrin in the
camel milk is related to milk yield, lactation period,
feeds, samples, breeds, and analysis methods7.
El – Agamy 2006 reported lactoferrin content of
camel and bovine colostrum was highest on the
first day, but colostrum from a camel in the second
day (after parturition) was around 5.1 mg/mL
compared to bovine colostrum which was 0.5
mg/mL.
The overview of some lactoferrin actions
The effects of milk lactoferrin on immune
responses
Lactoferrin boosts the immune response and
protects host cells against bacterial and viral
infections.13 Also, it has a key role in the host
defense against inflammation.16 However, the anti-
microbial effects of lactoferrin on the cell surface

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93
area due to preventing the adhesion and
proliferation of microbes and destroying the
membrane of microorganisms.13Immuno-
modulatory effects of lactoferrin are based on
interfering with infectious particles for adhesion to
the receptors on the host cells9 and complex with
lipopolysaccharide (LPS) and neutralizing it
connection with to TLR416. Lactoferrin regulates
cytokines production, chemokines, ROS (reactive
oxygen species) and peroxides.17Lactoferrin is
involved in activation, differentiation, and
proliferation of immune cells and further regulate
the modulation of lytic activity and motility of
immune cells.18-19
It has been proved that the anti-inflammatory
activity of lactoferrin is due to the prevention of
pro-inflammatory cytokines such as interferon-
gamma, tumor necrosis factor-alpha and
interleukins 1, 2 and 6. Lactoferrin strengthens the
recruitment of neutrophils and leukocytes, induces
phagocytosis, stimulates migration and cell
activation,2 affects the expression of immune
effectors (cytokines and chemokines) thus control
inflammation and immunity.20
Milk lactoferrin as anti-viral supplement
The lactoferrin antiviral activity is against many
viruses including enveloped and naked viruses,
respiratory syncytial virus, herpes simplex viruses,
rotavirus and HIVs.1Lactoferrin as an innate
immunity agent against mucosal infections on the
cell surfaces; inhibits the attachment and entry of
the virus into host cells, blocks the interaction of
viruses with heparan sulfate receptors, binds to
virus particles and prevents their localization in the
nucleus. The cationic nature of LF may be
responsible for binding with viral particles thus
inhibits viral invasion to the cells and avoiding the
infection.15Lactoferrin is shown to inhibit the
viruses in the early phase and also prevent viral
replication in the host cell.21 Also the antiviral
functions of lactoferrin through avoiding the
viruses’ entry more than stimulation of the immune
cells.22 According to the studies, bovine and human
LF had no significant differences in the antiviral
effects1 and they prevent viral entry inside the host
by blocking receptors or connecting to viruses in
the early phase.13 But some studies proved that
bovine milk lactoferrin has greater antiviral effects
than human milk lactoferrin.23Lactoferrin has been
considered the most active anti-viral protein in the
milk when compared to b-lactoglobulin and a-
lactalbumin.2
Seganti et al 2004 reported lactoferrin inhibits
human respiratory syncytial virus more than human
milk lactoferrin.24 Also, human lactoferrin
neutralizes simplex virus-1 and prevents the
intracellular spread of viruses.1 Strong activity of
lactoferrin against human immunodeficiency virus
(HIV) was due to inhibition of viral replication in
the host cells. Both apo and holo-lactoferrin have
antiviral action against HIV, but the apo form may
show more inhibitory than holo-lactoferrin.25
Lactoferrin blocks the internalization of some
viruses into the host cell, as poliovirus type 1,
herpes simplex virus types I and II and
cytomegalovirus. In the case of HCV and rotavirus,
lactoferrin showed to inhibit the replication of the
virus in the host rather than preventing virus entry.
The high lactoferrin of camel milk is a primary
drug against HCV infection.26 Out of many
hypotheses the one important is that lactoferrin
blocks viral receptor of heparin sulphate and
inhibits infection.
Lactoferrin effect on respiratory viruses
Bovine milk lactoferrin inhibited cell apoptosis by
interfering in the caspase 3 function; also it blocked
the entry of ribonucleoproteins in the H3N2
influenza A virus.1 According to the studies,
lactoferrin inhibited RSV absorption and growth by
blocking the internalization of viruses into the host
cell but the antiviral activity of lactoferrin will be
decreased after processing.2
Lactoferrin control IL-8 secretion from cells that
induced by RSV and hindered RSV uptake and
infectivity.27 Sano et al 2005 revealed that the
lactoferrin directly interacted with F protein for
penetration of RSV and occupied sites of protein
for attachment of viruses.27Lactoferrin has also
showed antiviral effects against human para
influenza virus type 2 infections by preventing
virus adsorption to the cells surface and limiting
viral replication and infection.28 Administration of
lactoferrin by 100-1000mg per day in humans
reduced the incidences of colds like symptoms.29
Anti-viral activity of camel milk lactoferrin
The behavior of lactoferrin from camel milk is
different and unique compared to lactoferrin
present in the milk of other mammals but the
inhibition way of lactoferrin from camel’s milk is
similar to bovine milk lactoferrin.26
Redwan & Tabll, 2007 reported that lactoferrin of
camel milk has anti-viral activity and inhibits the
virus entry into the cells.30 The camel milk
lactoferrin stops HCV entry and replication in
infected HepG2 cells two-times higher than
lactoferrin of human, bovine, and sheep milk.31
Generally, camel milk lactoferrin may directly
interact with viral molecules or receptors (heparan
sulfate) on the cell surface and prevent the virus
attachment to the host cells and hinder infection.26
The virucidal mechanism of camel milk lactoferrin
depends on its alpha-helical structure and cationic

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94
nature. The antiviral effects of lactoferrin from
camel milk have been demonstrated against many
viruses and the mechanism of action behind this
activity is the neutralization of virus particles and
inhibition of their replication.26 According to
studies, the most therapeutic effects of camel milk
are due to lactoferrin and immunoglobulins.32
Connection between camel milk lactoferrin and
COVID-19
The spike protein of SARS-CoV-2 causes the virus
to gain entry into the host cells, so boosting the
immune system will be useful against this virus.
Milk of livestock in particular camel milk contains
various protective proteins and enzymes such as
lactoferrin which have immunological properties
against the bacterial and viral infections park. Milk
lactoferrin has immuno-modulatory properties that
strengthen host immune responses and prevent
infections. Nutritional supplements are useful
against COVID-19, but there are few clinical
trials.33Lactoferrin as an anti-viral factor acts
against viruses such as SARS-CoV.34 Since the
79% of sequences of the SARS-CoV and SARS-
CoV-2 and also receptor-binding domain are
homologous, therefore lactoferrin may inhibit
SARS-CoV-2 invasion in the same manner to
SARS-CoV.35 The incidence of COVID-19 in
infants was mild without ventilation support and
lower respiratory tract infections rarely happened36.
Lactoferrin inhibited virus entry via binding to
heparan sulfate glycosaminoglycan in the cell
surface of human coronaviruses hCOV-NL6310 and
pseudotyped SARS-CoV CoV.35
Although if there is no published researches on
lactoferrin effects on the SARS-CoV-2 entry into
host cells but the interaction of lactoferrin with
heparan cell receptors, which allow attachment on
the cell surface in the primary phase of virus
infections particularly in coronaviruses.37
Lactoferrin prevents accumulation of viruses on the
cell surface and inhibit the contact between the
viruses and host cells and prevent the viral
infection that is observed in the SARS-CoV
epidemic and may be the same for SARSCoV-2. In
some severe COVID-19 cases, mortality happens
not only due to viral infection but also increases in
cytokines and acute phase reactants37 such as
interleukin IL-6, tumor necrosis factor-a (TNFa)
and ferritin cause to mortality.38Lactoferrin showed
50% inhibitory on human coronavirus of pseudo
typed SARS-CoV that is most closely related with
SARS-CoV-2 which causes COVID-19. Milk
lactoferrin is effective for innate response to
infections such as SARS-CoV-2.
Daily administration of 32 mg lactoferrin
(liposomal bovine lactoferrin) for 10 days with zinc
led to 100 % recovery of 75 SARS-CoV-2 positive
patients within 4 – 5 days39.
Conclusion
Milk lactoferrin of livestock can modulate immune
responses to viral infections by binding to virus
particles or receptors and may acts against viral
attacks and reduce the severe infections, so it could
be an adjunct treatment for more severe cases of
COVID-19. Immuno-modulatory, anti-bacterial
and antiviral properties of lactoferrin make it
unique preventative agent against COVID-19. But
it needs more studies to verify dosage and efficacy
of lactoferrin on prevention and treatment of
COVID-19. Therefore, lactoferrin as powder or
tablets can be a novel promising method against
viral infections and application as a drug carrier.
According to this point that camel milk has highest
amount of lactoferrin in comparison with the other
species milks, so antiviral activity may be high as
well; therefore, it will be a precious source of
lactoferrin against the viruses. One important point
is applying the indirect and mild heating for milks
is necessary to save this protein and its anti-viral
properties.
Conflict of interest: The authors declared that
there is no conflict of interest regarding the
publication of this article.
Figure 1: The bovine lactoferrin structure with two lobes and domains. Image is adapted from Baker and Baker,
2005.30

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Figure 2: The inhibitory effect of lactoferrin against Gram-positive and Gram-negative bacteria. Image adapted
from Gonzalez-Chavez et al., 2009.
Figure 3: The inhibitory effects of lactoferrin against viruses. Image adapted from Gonzalez-Chavez et al.,
2009.
Figure 4: Antiviral action of lactoferrin against several viruses. Image adapted from Vanderstate et al 2001.25

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Figure 5: Antiviral mechanisms of lactoferrin. Image adapted from Changet al 2001.39
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