Review Article: Development of Probiotic Candidate in Combination with Essential Oils from Medicinal Plant and Their Effect on Enteric Pathogens: A Review

Abstract

Medicinal plants and probiotics both have very high potential in terms of their antimicrobial activity against antibiotic-resistant enteric pathogens. The probiotics being enteric microorganism do not have any parasitic effect on human beings. They have been an integral part of daily food for centuries. They have been shown to have health beneficiary properties. The probiotics retard the growth of the microorganisms, while essential oil kills them. Combining the effect of medicinal plant extract and probiotics may be a new approach due to their complementary antimicrobial effects and practically no side effects. The synergistic effect of the essential oil and probiotics will be necessarily higher than using them alone as health product.

Full text

Hindawi Publishing Corporation
Gastroenterology Research and Practice
Volume 2012, Article ID 457150, 6pages
doi:10.1155/2012/457150
Review Article
Development of Probiotic Candidate in Combination with
Essential Oils from Medicinal Plant and Their Effect on Enteric
Pathogens: A Review
Shipradeep,1Sourish Karmakar,1Rashmi Sahay Khare,2Sumedha Ojha,1
Kanika Kundu,2and Subir Kundu1
1School of Biochemical Engineering, Indian Institute of Technology, Banaras Hindu University, Varanasi 221005, India
2Chemistry Section, MMV, Banaras Hindu University, Varanasi 221005, India
Correspondence should be addressed to Subir Kundu, skundu.bce@itbhu.ac.in
Received 17 March 2012; Revised 4 May 2012; Accepted 12 May 2012
Academic Editor: Antonio Gasbarrini
Copyright © 2012 Shipradeep et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Medicinal plants and probiotics both have very high potential in terms of their antimicrobial activity against antibiotic-resistant
enteric pathogens. The probiotics being enteric microorganism do not have any parasitic effect on human beings. They have been
an integral part of daily food for centuries. They have been shown to have health beneficiary properties. The probiotics retard the
growth of the microorganisms, while essential oil kills them. Combining the effect of medicinal plant extract and probiotics may
be a new approach due to their complementary antimicrobial effects and practically no side effects. The synergistic effect of the
essential oil and probiotics will be necessarily higher than using them alone as health product.
1. Introduction
The plants have been used in Ayurvedic medicines from
ancient times. The extracts from these plants have shown
potent antimicrobial effect. Recently, much work has been
done on extraction of chemicals responsible for the antimi-
crobial effect from these plant species. It has been reported
that the essential oils extracted from these plants have potent
activity against microorganisms [1]. However, the studies
have shown that these essential oils have very high MIC
(minimal inhibitory concentration) against beneficial enteric
bacteria known as probiotics [2,3].
Probiotic is the term as per WHO definition denotes
“live microbial feed supplement which beneficially affects the
host animal by improving its intestinal microbial balance.”
As the definition clearly indicates, most of the intestinal
bacteria have an important role to play in the digestive
system. Earlier, probiotics were given to animals to improve
their health, but later much research has been put in
the development of the probiotics for human health. The
major probiotics that are taken in the diets belongs to the
genera of Lactobacilli and Bifidobacteria [4]. Apart from
that, the gut flora predominately has obligate anaerobes that
include Bifidobacteria, Clostridia, Eubacteria, Fusobacteria,
Peptococci, Peptostreptococci,andBacteroides.Onlyabout1%
of these bacteria are facultative anaerobes belonging to the
genera of Lactobacilli, Escherichia coli, Klebsiella, Streptococ-
cus, Staphylococcus,andBacilli. In the case of newborns,
food habits play a major role in the development of enteric
flora. The breastfed babies normally have abundance of
Bifidobacteria, while the others have complex microflora
in their enteric system. Bifidobacterium sp. can be isolated
mostly from the feces of infant milk feed baby. However,
in the case of infants fed on normal formula based food
products the gut flora is found to be rich in Enterobacteria,
Lactobacilli, Bacteroides, Clostridia,andStreptococci. These
gut flora help to digest the milk-based food and offer the
primary line of defense against the pathogenic bacteria.
The infants have weak but developing immune system [5].
These enteric bacteria help the infantile immune system to
fight against pathogenic enteric bacteria by lowering the pH
of the gut, rendering it unsuitable for pathogenic bacteria
to survive [6]. Even the medical practitioners recommend
probiotics-based supplement to both patients suffering from

2Gastroenterology Research and Practice
enteric diseases. The most popular probiotics supplements
belong to the genera of Lactobacilli and Bifidobacteria. The
recommended dosage of 109–1010 CFU is considered a
minimum for healthy enteric system [7].
Present review emphasizes on the synergistic antimicro-
bial effect of essential oil of the Lamiaceae family and probi-
otics administered together as flavored fermented milk prod-
ucts. The advantage of using such a combination is its benefi-
cial effect with its antimicrobial property. The probiotics can
help in improving the gut epithelial conditions while essen-
tial oil acts on killing the pathogens present in the human
body.
2. Health Benefits of Probiotics
Probiotics, though recently popular, have been an integral
part of the human diet for centuries. All the civilizations from
ancient times have documented the benefits of curd in the
human diet. The lactose-tolerant people are always advised
to take curd with their diet. The curd is rich in Lactobacillus
sp. and Streptococcus sp. These microorganisms utilize the
lactose present in milk-based food and convert it to lactic
acid [8].Theoccurrenceofflatulenceincarbohydrate-
intolerant individuals is also observed with fatty acid. The
carbohydrates that are not fully digested due to lack of
certain enzymes in human being can also be digested with
probiotics. These carbohydrates are fermented into short-
chain acids such as butyric acid, lactic acid, or acetic acid
[9]. These acids are readily utilized in by human cells for
ATP metabolism providing energy to the individuals. The
lactic acid also helps in protein metabolism by coagulating
the protein chunks from meat inside the intestine [10].
Formation of hydrogen peroxide is also prevented by cata-
lases produced from probiotics preventing protein-caused
rancidity [11–13]. Hydrolysis of sarcoplasmic protein was
also observed with many species of Lactobacillus genus [14–
16]. Coprecipitation of cholesterol with bile salts at lactic
acid-induced lower pH is also observed in in vitro conditions
[17].
Probiotic microorganisms are also found to be involved
in synthesis of vitamins. The probiotics microorganisms are
known to synthesize biotin and vitamin K [18]. Apart from
that, they are also involved in the ions absorption such as
Mg2+,Ca
2+,andFe
3+.
The probiotic microorganisms are also involved in the
enhancement of expression of certain pattern recognition
receptors. Pattern recognition receptors such as TLRs have
active role in wound healing process. The intestinal cells have
high need for these receptors for supporting their process of
proliferation and differentiation, healing the wounds made
due to irregular bowel movement [19]. The short-chain
fatty acid produced from carbohydrate metabolism also
enhances the process of proliferation and differentiation of
gut epithelial cells.
The probiotics have also a major role to play in preven-
tion of allergies in children [5]. However, the connection
of probiotics and immune system regulation is still under
investigation. It has been observed that with allergy-prone
adults and children, the count of Lactobacilli and Bifidobac-
teria is lower. It has been also observed that administration
of probiotic strains during prenatal stage can decrease the
chance of atopic eczema. In addition, the production of pat-
tern recognition receptors, interleukin, and growth factors
from the probiotic microorganisms in gut epithelia also play
an important role in prevention of allergies. Therefore, it
can be inferred that these microorganisms have direct role
in immune system regulation [5]. Apart from that, these
microorganisms also play a role in immune response mod-
ulation. The probiotic microorganisms interact with the gut-
associated lymphoid tissue (GALT) [20]. The probiotics are
involved in cytokine synthesis, that plays an important role in
immune system regulation. However, due to insufficient clin-
ical trial, administration of probiotics in immunosuppressed
individuals is still prohibited.
It has been also observed from both in vitro and in vivo
studies that probiotics may prevent cancer [21]. It has
been found that daily intake of fermented milk products
substantially decrease the concentration of nitroreductases,
azoreductases, and β-glucuronidase in the gut. These micro-
bial enzymes are associated with carcinogen production
in the gut [22]. Lactobacillus casei have also shown an
antigenotoxic effect. It prevents inducible DNA damage in
the tumor target tissues of gastrointestinal tract of rats.
3. Antimicrobial Effect and
Mechanism of Action
Probiotics have a known antimicrobial effect. They are
very potent against pathogens. There are several proposed
mechanisms for the antimicrobial action of the probiotics.
Bacteriocins, organic acids, hydrogen peroxide, diacetyl, and
other inhibitory chemicals are released by the probiotics [23].
All of these chemicals are known for their potent antimi-
crobial effects. Bacteriocins are toxic chemicals released by
the probiotics, that are highly potent against most of the
bacteria. However, the most feasible mode of action seems
to be lowering of pH with release of organic acids such as
lactic acid [24,25]. In the limiting condition of available
substrates inside the intestine, lowering the pH ensures the
survival of acidophilic micro-organisms only. The growth
of the pathogens gets inhibited at acidic conditions, slowing
the metabolic process in them. Lactobacillus strain GG has
been reported to produce inhibitory chemicals, possibly a
microcin, that have high activity against pathogenic microor-
ganisms. It has been found effective against Clostridium spp.,
Bacteriodes spp., Enterobacteriaceae spp., Staphylococcus spp.,
and Pseudomonas spp. in microbiological assays. Lactocidin
released by strains of lactobacillus acidophilus is found active
against Staphylococcus aureus and Pseudomonas aeruginosa
[26]. There has been a study that Lactobacillus acidophilus
LB release chemicals that are effective against both gram
positive and gram negative microorganisms. These chemicals
released in the broth were effective against Staphylococ-
cus aureus,Listeria spp.,Salmonella typhimurium,Shigella
flexneri,E. coli,Klebsiella pneumoniae,Bacillus cereus,Pseu-
domonas aeruginosa,andEnterobacter spp. [27]. However,

Gastroenterology Research and Practice 3
Tab l e 1: MICs of essential oil against known pathogenic microorganisms.
Bacterial strains Coleus aromaticus Shyama tulasi Rama tulasi
Providencia rettgeri ∼4μl/mL ∼3μl/mL ∼2μl/mL
Shigella flexneri ∼1μl/mL ∼5μl/mL ∼5μl/mL
Shigella dysentery ∼3μl/mL — ∼5μl/mL
Vibrio parahaemolyticus ∼2μl/mL ∼5μl/mL ∼5μl/mL
Salmonella enteritis ∼4μl/mL ∼2μl/mL ∼3μl/mL
Salmonella typhi ∼0.5 μl/mL ∼2μl/mL ∼2μl/mL
Vibrio cholerae ∼2μl/mL ∼2μl/mL ∼1μl/mL
the chemical did not have any inhibitory effect on probiotics
strains such as Lactobacillus and Bifidobacterium spp. This
can be explained by the similarity of survival conditions
of both these microorganisms. Some of the strains of
Bifidobacterium spp. have potent activity against Salmonella
typhimurium. However, not all the strains of Bifidobacterium
spp. have the activity against S. typhimurium. All of the pro-
biotics have higher survivability in low pH conditions. These
microorganisms produce acids by breaking the carbohydrate
present in the diet. The properties of acid production and
acid survivability increase their survivability in the toughest
of conditions [28,29]. The adherence property of the
probiotic microorganisms also ensures their longevity in the
human guts [30]. However, the probiotic strains have shown
an effective potential in inhibiting the adhesion of pathogen
such as E. coli and Salmonella enterica in in vitro conditions
[31]. The potential of adhesion inhibition by the probiotics
is credited to the mucin production and competitive binding
to gut epithelial receptor sites. Lactobacillus acidophilus
LA1 has high calcium independent adhesive property that
inhibits the invasion of enteropathogenic bacteria. Mucins
are complex glycoprotein that inhibits the enterobacterial
adhesion by protection of intestinal epithelial cell receptors.
Both MUC2 and MUC3 produced by Lactobacillus spp. are
potent examples of Mucins that have adhesion inhibitory
activity against enteropathogens.
4. Antimicrobial Effects of Essential Oils from
Medicinal Plants
There has been lot of studies in recent year that have
established the antimicrobial effect of essential oils of
medicinal plants such as plants of the Lamiaceae family
[2,3]. The essential oils predominately present in the
leaves of the plant species have a pleasant aroma. They are
commonly used in flavor enhancement in food industries,
as they are safe for human consumption. These essential
oils have been shown to have a bactericidal effect. The
plant species of Lamiaceae family have been proven effective
against Uropathogen [32]. Tab l e 1 shows the MICs of Coleus
aromaticus and Ocimum sanctum (Rama Tulasi and Shayama
Tul a s i) against few known enteric pathogens [32]. The
essential oil from the plants of Carum carvi, Coleus aro-
maticus, Rama Tulasi, Shyama Tulasi, Citrus aurantium var.
amara,foeniculumvulgare dulce, Illicium verum, Lavandula
angustifolia, Mentha arvensis, Mentha x piperita,andTra-
chyspermum copticum have been shown to be effective against
variety of microorganisms. These plants extracts have been
found effective against Bacteroides fragilis, Candida albicans,
Clostridium difficile, Clostridium perfringens, Enterococcus
faecalis, Escherichia coli, Eubacterium limos, Staphylococ-
cus aureus, Klebsiella oxytoca, Proteus vulgaris, Escherichia
coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Proteus
mirabilis,andPeptostreptococcus anaerobius [2]. The MICs
against these microorganisms varies from 0.1 to 3%v/v.
The MICs of the same plant extracts against probiotic
microorganisms such as Bifidobacterium bifidum, Bifidobac-
terium longum, Lactobacillus acidophilus,andLactobacillus
plantarum are much higher in magnitude than the pathogens
[2]. Therefore, if the dosage of essential oil is low, then
it effectively wipes out the pathogens without harming the
beneficial probiotics.
5. Proposal on Synergistic Effect of Probiotics
and Essential Oil from Plants
The essential oils have high MIC values for probiotics,
while it is effective in much lesser concentration against
the pathogens. The above phenomenon makes it possible
that both probiotics and essential oil can be administered
together to cure pathogenic infection in human gut. They
both can be combined to form essential oil-flavored fer-
mented milk products such as flavored curd beverages or
flavored yogurt. Antibiotics coupled with probiotics are
already present in the market, but these medicines mostly
face stiffchallenge from antibiotic-resistant bacteria. Further
frequent use of the antibiotics may lead to the development
of antibiotic resistance in the pathogenic microorganisms
too. Hence, the strategic use of probiotics may be beneficial
to curb the growing phenomenon of antibiotic resistance.
Probiotics have antimicrobial properties associated with the
production of bacteriocin-like chemicals. However, it mostly
arrests the proliferation of the pathogens by lowering the pH
in the gut environment. The pathogens do not normally have
any mechanism against the action of essential oils. Essential
oils are resistant against enzymatic activity of β-lactamase
produced as a countermeasure against β-lactam antibiotics.
The use of probiotics lowers the survivability chances of
pathogen, while the essential oil in lower dosage ensures
their complete killing inside the human digestive tract. The
probiotics may also impart its good benefits discussed earlier.

4Gastroenterology Research and Practice
Tab l e 2: Test of the beverages made with mixing different concentration of essential oil of Coleus aromaticus, Rama tulasi, and Shyama tulasi against common pathogens for 24hrs at 37◦C
(−sign denotes no pathogen; + sign denotes the presence of pathogen).
S. Bacteria Gram Beverage Beverage Beverage Beverage Beverage Beverage Beverage Beverage Beverage
number +ve/−ve123456789
(1) Citrobacter freundii −ve −−−−−−−−−
(2) Proteus mirabilis −ve + + + −−−+−−
(3) Klebsiellal pneumoniae −ve++++++++−
(4) E. coli ATCC 25922 −ve + −−++++−−
(5) Entero. faecalis ATCC 29912 +ve −−−−−−−−−
(6) Salmo. typhi MTCC 3216 −ve −−−−−−++−
(7) Staph. aureus ATCC 25923 +ve + + −++−+−−
(8) Salmonella typhimurium −ve + −−−−−−−−
(9) Salmonella paratyphi −ve + + −+−−++−
(10) Vibrio cholerae −ve −−−−−−−−−
(11) Pseudo. aeru. ATCC 27853 −ve −−−−−−−−−
(12) Proteus vulgaris −ve + + −−−−+−−
(13) Listeria monocytogenes +ve + + −++−+−−
(14) Shigella flexneri −ve −−−+−− ++−
(15) Helicobacter pylori −ve −−−−−−−−−
(16) Strptococcus heamophila +ve + −−−−−−−−

Gastroenterology Research and Practice 5
Apart from that, the fermented milk product will surely
impart benefits in terms of supplying nutrients such as
sugar, water, salt, and acid to the human body. Adding
essential oil will not only give an aromatic flavor to these
fermented milk beverages or products, but also increase their
shelf like considerably by preventing the microbial spoilage.
The product will act as both probiotic health product and
preventive antimicrobial product against enteric pathogens.
In an independent study, beverages A, B, and C were
prepared with probiotic curd (109CFU/ml) [33]withvary-
ing concentration of essential oil of Coleus aromaticus, Rama
Tul a s i and Shyama Tulasi,respectively[1]. The beverages
A1, A2, and A3 were prepared with essential oil of Coleus
aromaticus; beverage B1, B2, and B3 with essential oil of
Shyama Tulasi and beverages C1, C2, and C3 with essential
of Rama Tulasi in varying concentrations of 1, 2, and 3 μl/ml
respectively. These beverages were then grown with common
enteric pathogens in equal concentration, measured by count
of CFU, in nutrient broth for 24 hours in airtight culture
vials at 37◦C to simulate the anaerobic condition prevailing
in the intestine [34]. The individual vial was tested for the
traces of pathogen as seen in Tab l e 2 with −sign indicating
the cidal effect of the beverage against the pathogen (no
growth of the pathogens), while + sign indicated the growth
of the pathogen. The sample beverages were found to be
highly effective in inhibiting the growth of the pathogen. The
shelf life of the beverages was also found to be significantly
higher than normal probiotics [34]. The test results can be
interpreted as the beverage’s capacity for prevention against
enteric pathogens. The use of beverage does not need the
stringent FDA regulations, yet it will impart the benefit of
preventive diseases.
6. Conclusion
Probiotics and essential oils both have a great potential
in terms of their beneficial effect against microbial gut
infection. They also show a synergistic effect that is normally
higher than any known drug due to their complementary
actions. Since most of these medicinal plants are edible, their
extracts as food product do not have any side effects with
low dosage. Therefore, these products may be very beneficial
for human beings. However, much research is needed to be
put into these studies, as drug regulatory authorities still
have strong regulations against usage of plant extracts as
medicines.
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