International Journal of Food Science and Technology 2016, 51, 581587 581

Original article
Effect of Mentha spicata L. and Mentha aquatica L. essential oils
on the microbiological properties of fermented dairy product,
kashk

Leila Golestan,1* Laleh Seyedyousefi,1 Hami Kaboosi2 & Hamed Safari1

1 Department of Food Science, Ayatollah Amoli Branch, Islamic Azad University, Amol, P.O. Box 678, Iran
2 Department of Microbiology, Ayatollah Amoli Branch, Islamic Azad University, Amol, P.O. Box 678, Iran

(Received 2 June 2015; Accepted in revised form 20 October 2015)

Summary The antibacterial activity of Mentha spicata and Mentha aquatica essential oils (EO) was tested against
Staphylococcus aureus, Lactobacillus reuteri, Bifidobacterium animalis and Clostridium perfringens using
agar well and disc diusion techniques. Results showed that M. spicata EO had the highest inhibition
activity against the studied microorganisms. Then, the antibacterial activity of both EO at 1500 and
2500 ppm was examined in industrial liquid kashk during the storage at 4 C for 20 days. Both EO
reduced the S. aureus viable count below 5 log CFU g 1 after 4 days; however, the population of C.
perfringens, L. reuteri and B. animalis decreased <1 log CFU g 1 during the storage time. The least dete-
riorative eect on the lactic acid bacteria was related to M. aquatica. As revealed by organoleptic studies,
kashk samples containing M. aquatica EO at 1500 and 2500 ppm were the most preferred samples.
Keywords Dairy products, essential oil, kashk, microbiological properties, mint.

from microbial contamination and propagation in

Introduction
In recent years, the consumption of acid-fermented
dairy products has increased considerably because of
their signicant therapeutic and nutritional characteris-
tics (Shiroodi et al., 2012). Dierent kind of acidied
dairy products, such as yogurt, labneh (concentrated
yogurt), ker, soy milk, butter-milk, whey drinks and
dried yogurt, like kashk are widely consumed all over
the world (Roesch et al., 2004). In this context, kashk
is a popular and traditional fermented Iranian dairy
product prepared traditionally in dried form and pro-
duced industrially in liquid form. The dried form is a
concentrated yogurt-type product manufactured with
dehydration of homemade yogurt by sun-drying
(Ogbaei & Prakash, 2008; Shiroodi et al., 2012). As
source of high quality proteins and high calcium con-
tent, kashk is considered as a nutritious food adjunct
and can be recommended for application in diets of
children, pregnant and lactating women (Soltani &
G uzeler, 2013).
Controlling food-borne pathogenic bacteria and
ensuring the safety of food products are the most
important issues for food processors. They also have
the risk of economic loss because of spoilage resulting
*Correspondent: E-mail: l.golestan@iauamol.ac.ir
improperly storing (Oshima et al., 2014). On the other
hand, an increasing number of consumers prefer mini-
mally processed foods and the food industry shows
interest for new food preservation techniques to
replace the old ones like chemical preservatives due to
the evidence of toxicity of synthetic antimicrobials
(Asensio et al., 2014). To answer this demand, signi-
cant interest has been focused on natural preservatives
like plant essential oil (EO) as an alternative to syn-
thetic materials (Abdollahi et al., 2014).
Among these, mints (Mentha spp.), those belonging
to the family Lamiaceaeare, are well-known as aro-
matic and medicinal herbs. They contain biologically
active constituents, are used in traditional medicines
(Tsai et al., 2013), and are famous all over the world
for their EO. The aromatic leaves of mint have been
traditionally utilising fresh and dried as avouring or
spices in dierent foods. Their EO are also used to a-
vour foods, in dental and oral products like tooth-
paste, in fragrances, cosmetics, confectionary, chewing
gum and pharmaceutical industries (Dhi et al., 2011).
Recently, Mentha spicata and Mentha aquatica have
become a subject of scientic interest in view of other
potential applications of their EO and extracts, for the
most part, as antimicrobial and antioxidant agents. In
this regard, several studies have reported the

doi:10.1111/ijfs.13014
2016 Institute of Food Science and Technology
582 Effect of mint essential oil on kashk L. Golestan et al.
antimicrobial eects of the mints EO in food systems
(Burt, 2004; Kanatt et al., 2008; Karag ozl
u et al.,
2011). Also, the addition of the plant extracts to dairy
products like milk (Cava-Roda et al., 2010), cheese
(Asensio et al., 2014; Mahmoudi et al., 2014), yoghurt
(Evrendilek & Balasubramaniam, 2011; Mahmoudi
et al., 2013), labaneh, ayran and doogh (Simsek et al.,
2007) have been reported successfully in some studies.
Nevertheless, the ecacy of plant extracts and EOs in
controlling the quality of the industrial liquid kashk
has not been studied.
As a fermented dairy product, kashk can be a suit-
able substrate for probiotic bacteria. Also, the
presence of coagulas-positive staphylococcus, sulphite-
reductase clostridiums, fungi and yeasts must be under
control in quality control plans (ISIR 2406).
Thus, the present study aimed to evaluate the
antimicrobial eects of EOs from (M. spicata L.
(spearmint) and M. aquatica L. (water mint), on
Lactobacillus reuteri, Bifidobacterium animalis subsp.
Lactis, Staphylococcus aureus, Clostridium perfringens,
in industrial liquid kashk as well as determining their
eect on the sensory properties of the product.
Materials and methods
Plant sample preparation
Fresh herbal plants were purchased from a local mar-
ket, Amol city, Iran and identied by specialists in
Mazandaran Agriculture and Natural Resource
Research Institute, Sari, Iran as spearmint and water
mint. Then, the leaves of the plants were washed,
shade dried and grinded into powder. The prepared
powder was kept in tight dark containers protected
completely from light.
Essential oils extraction
The dried aerial parts of mint samples (100 g) were
separately subjected to the hydrodistillation for 2.5 h
at 100 C, using a clevenger-type apparatus. The
extraction was performed according to the method rec-
ommended by the European Pharmacopoeia (Mah-
moudi et al., 2014) to produce oils from each mint
species. The obtained oils were collected separately as
the pure EOs and stored in dark containers at 4 C
until tested and analysed.
GC-MS analysis of essential oils
The gas chromatography analysis of the two EOs were
carried out using a Shimadzu QP 5050 Gas Chro-
matograph-Mass Spectrometer (Tacoma, Washington,
UT, USA) with a MDN-5S fused silica column
(30 m 9 0.32 mm, lm thickness 0.25 lm). The initial
International Journal of Food Science and Technology 2016
temperature was set at 50 C and temperature ramp
5 C min 1, 240300 C min 1 (holding for 3 min)
and injector temperature at 290 C. The helium was
carrier gas and the split ratio was 0.8 mL min 1. All
results were quantied by a built-in, data-handling
programme provided by the manufacturer of the gas
chromatograph.
Microbial strain preparation and storage
Lyophilised stock culture of S. aureus (ATCC 9144),
L. reuteri (ATCC 23272) and B. animalis subsp. lactis
(PTCC 1736, DSM 10140), C. perfringens (ATCC
13124) were obtained from Persian Type Culture Col-
lection (IROST, Tehran, Iran). The cultures were
transferred to 10 mL of brain and heart infusion
(BHI) broth and were grown in a shaker incubator at
37 C for 24 h. A second transfer of 0.1 mL of cul-
tures into 10 mL of BHI broth was grown in a shaker
incubator at 37 C for 24 h to the end of the exponen-
tial phase of growth. Subsequently, these appropriately
diluted cultures were used for the inoculation of the
agar plates and industrial liquid kashk in order to
obtain target inoculums.
Disc diffusion assay
Antibacterial properties of mint EOs were studied
using the agar diusion method as recommended by
CLSI (2006). Propylene glycol was used for the dilu-
tion of the EOs. Sterile lter paper discs (Whatman,
6 mm diameter; Sigma-Aldrich Chemical Co, St Louis,
MO, USA) were dipped in the spearmint and water
mint EOs at dierent dilutions, including pure, 1/2, 1/
4, 1/8, 1/20 and 1/40 and then dried. The discs were
applied to the surface of agar plates of Mueller
Hinton (Scharlau Chemie, Barcelona, Spain) agar
(with 2.5 cm distance between the edge of the discs on
a plate), that were previously seeded by 0.1 mL of
inoculum containing approximately 108 CFU mL 1 of
the indicator bacteria. Next, the plates of the bacteria
were incubated at 37 C for 24 h, for L. reuteri,
B. animalis subsp. Lactis and C. perfringens in anaero-
bic container. After incubation, microbial growth was
observed, and the degree of inhibition was expressed
as follows: totally inhibited, +++; partially inhibited,
++; slightly inhibited, +; no inhibition, . Experiments
were carried out in triplicate (Kalemba & Kunicka,
2003; Abdollahzadeh et al., 2014).
Inoculation of kashk samples and storage
Inoculation and storage of the kashk samples were
done as explained by Evrendilek & Balasubramaniam
(2011). Kashk samples (10 g) were inoculated with dif-
ferent microorganisms L. reuteri, B. animalis subsp.
2016 Institute of Food Science and Technology
 Effect of mint essential oil on kashk L. Golestan et al. 583

lactis, C. perfringens cultures at the level of 105 Results and discussion

106 CFU mL 1. To evaluate the eect of the mint EO,
they were added at the concentrations of 1500 and Chemical composition
2500 ppm (based on liquid kashk) to the inoculated
kashk samples. Inoculated samples without the EOs Major chemical composition of the EOs extracted from
were also prepared as control. All the samples were M. spicata and M. aquatica is summarised in Tables 1
stored at 4 C and the microbial counts were deter- and 2, respectively. Seventy-one and forty-nine com-
mined at days 0, 4, 8, 12, 16 and 20 as explained in pounds were identied in the EO of M. spicata and
the following. M. aquatica, respectively (not shown). As the results of
GC-MS analysis showed, M. spicata mainly contained
D-limonene (17.35%), a-phellandrene (5.93%), 4-terpi-
Microbiological analysis of kashk samples
nenol (7.16%), borneol (8.69%), carvone (25.23%) and
Staphylococcus aureus caryophyllene (10.13%). On the other hand, b-pinene
Baird parker agar with egg yolk tellurite emulsion was (5.26%), DL-limonene (5.79%), 1,8-cineole (17.92%),
used (Himedia, Maharashtra, India) to count S. aureus menthofurane (15.16%) and viridiotol (6.25%) were
in the kashk samples during the storage period. The the major components of M. aquatica L.
plates were incubated at 37 C for 72 h and then the
black colonies were counted (ISO 6888-1:1999). Table 1 Major chemical composition of spearmint (Mentha spicata)
essential oil
Clostridium perfringens
Compound name Percentage (%)
SPS agar medium (Sulte Polymyxin Sulfadiazine
Agar; Merck, Darmstadt, Germany) was used for the Pinene 1.20
enumeration of C. perfringens in the samples. The Camphene 3.50
plates of the bacteria were incubated in an anaerobic D-Limonene 17.35
jar at 37 C for 72 h and then the colonies were a-Phellandrene 5.93
counted (ISO 7937: 2004). Isoterpinolene 3.86
a-Terpinene 2.86
4-Terpinenol 7.16
Lactobacillus reuteri, Bifidobacterium animalis
Menthone 4.12
Changes in the population of the probiotic bacteria
Menthol 2.89
were studied by counting L. reuteri and B. animalis in Borneol 8.69
the kashk samples during the storage. Bidobacterium Carvone 25.23
agar (Merck) and MRS agar (Merck) were used to Carvacrol 6.32
count L. reuteri and B. animalis in the kashk samples b-Bourbonene 3.56
during the storage period. The plates of the bacteria b-Elmene 1.36
were incubated in an anaerobic jar at 37 C for 72 h Caryophyllene 10.13
and then the colonies were counted. Virirdiflorene 1.36

Sensory evaluation Table 2 Major chemical composition of water mint (Mentha aquat-
ica) essential oil
The sensory evaluation of the samples was done using
a 5-point hedonic acceptance test. A twelve-member Compound name Percentage (%)
trained panel consisting of the scientic sta of the
a-Pinene 2.72
Department of Food Science, Islamic Azad University
b-Pinene 5.26
of Amol, performed the sensory evaluation. Each pan- b-Myrcene 1.02
elist was asked to evaluate the kashk samples by rating DL-Limonene 5.79
them using a 5-point scale where 5 = extremely like 1,8-Cineole 17.92
and 1 = extremely dislike for the taste (Mahmoudi Menthofurane 15.16
et al., 2014). Terpinen-4-ol 1.85
DL-Menthone 1.01
Bicycloheptane 1.07
Statistical analysis b-Elemene 1.05
One-way ANOVA was used and mean comparison was Caryophyllene 11.82
a-Caryophallene 1.32
performed by Duncans new multiple range test. Statis-
D-Cadinene 1.01
tical analysis was prepared using the SPSS statistical Viridiflotol 6.25
software (release 16.0) for Windows (SPSS Inc., Chi- a-Cadinole 2.25
cago, IL, USA). All data are presented as mean  SD.

2016 Institute of Food Science and Technology International Journal of Food Science and Technology 2016
584 Effect of mint essential oil on kashk L. Golestan et al.

Boukhebti et al. (2011) detected 57 compounds in study. The EO of M. spicata was found to be more
the leaf EO of M. spicata. The major component sepa- active compared with the M. aquatic EO. Both EOs
rated in their study was carvone (59.40%), other com- were considerably more active at higher concentrations
ponents present in appreciable contents were limonene against the studied microbial strains. Staphylococcus
(6.12%) and 1,8-cineol, germacrene-D (04.66%). In aureus and C. perfringens were recognised as the most
arer et al., 2011;
other studies (Sokovic et al., 2009; S sensitive microorganism against both EO with higher
Govindarajan et al., 2012), carvone was also reported vulnerability to M. spicata oil. Interestingly, the probi-
as the major constituent. Sokovic & Van Griensven otic bacteria L. reuteri and B. animalis were the least
(2006) also reported that carvone (49.52%), menthone sensitive microorganisms to both EOs. This result was
(21.92%), limonene (5.77) and 1,8-cineole (3.06%) in agreement with those reported with S arer et al.
were the major components recognised in the EO of (2011) who studied the antimicrobial activities of
M. spicata from Montenegro. M. spicata oil against four bacteria and two yeasts. In
Some studies also reported chemical composition of a disc diusion assay, their results showed that the oil
M. aquatica from other regions in the world. For of M. spicata had strong activity against S. aureus.
example, the major constituents of EO of Iranian Boukhebti et al. (2011) reported that the EO of
M. aquatica were 1,8-cineole (27.2%), menthofuran M. spicata has a dose-dependent activity against nine
(23.2%), b-caryophyllene (12.8%) and limonene bacteria susceptible species. Similarly, Dhi et al.
(5.2%), as reported by Morteza-Semnania et al. (2011) showed that M. aquatica EO was active against
(2006). Jerkovic & Mastelic (2001) found that the Staphylococcus, Escherichia coli and Bacillus, but it did
major compounds in M. aquatica from southern Croa- not show an inhibitory eect against Candida. This oil
tia is menthofuran followed by 1,8-cineole and E-car- had inhibitory or germicidal eect depending on the
yophyllene which supports our results. However, some type of microorganisms. Getahun et al. (2008) showed
dierences observed between the composition of the that Ethiopian M. aquatica EO had a considerable
EO from M. spicata and M. aquatica in the present activity against the Gram-positive bacteria. Kac aniov
a
study with other reviewed studies could be related to et al. (2014) studied antibacterial activity of fteen EO
many factors including genotype, environment (Fahlen against Clostridium genus. They found good activity of
et al., 1997), agronomic conditions such as harvesting Mentha piperita EO against Clostridium genus and the
date, and culture density (Dhi et al., 2011). best antibacterial activity of the EO was observed
against C. butyricum.
These dierences observed in the antimicrobial activ-
Antimicrobial activity by disc diffusion assay
ity of two mints EOs could be due to the dierences in
The antimicrobial activity of the EO of M. spicata and the chemical composition of the oils. The antimicrobial
M. aquatica against the four studied bacteria is pre- activity of spearmint (M. spicata) has been suggested to
sented in Table 3. The EO of both mint species be mainly related to carvone and 1,8-cineole, as showed
showed weak to excellent antimicrobial activities in Table 1 (Hussain et al., 2010; Boukhebti et al., 2011;
against all the microorganisms tested in the present arer et al., 2011). Moreover, Bader et al. (2003)
S
demonstrated that carvone exhibited better antimicro-
Table 3 Antimicrobial properties of the essential oils determined by bial activity than the entire M. spicata EO. On the
disc diusion method
other hand, the biological activity of water mint
Oil dilution (M. aquatica) EO has been suggested to correlate with
its richness in oxygenated monoterpenes like menthofu-
Essential oil Microorganism Pure 1/2 1/4 1/8 1/20 1/40 rane, as showed in Table 2 (Dhi et al., 2011). An
important mechanism for antimicrobial activity of EO
Spearmint Staphylococcus +++ +++ ++ + + +
aureus
and their components is related to their hydrophobicity.
Lactobacillus ++ ++ ++ + + + That characteristic enables them to partition the lipids
reuteri of the bacterial cell membrane and mitochondria, dis-
Bifidobacterium ++ ++ + + + + turbing the cell structures and rendering them more
animalis permeable (Burt, 2004).
Clostridium +++ + + + + +
perfringens
Water mint S. aureus ++ ++ + + + + Antimicrobial activity of essential oils in kashk during
L. reuteri + + + + + + storage
B. animalis ++ ++ + + + +
Changes in the population of S. aureus in the kashk
C. perfringens ++ + + + + +
samples containing 1500 and 2500 ppm of M. spicata
: No inhibited; +: slightly inhibited; ++: partially inhibited; +++: totally and M. aquatica during 20 days of storage at 4 C are
inhibited. shown in Fig. 1. The initial numbers of S. aureus in

International Journal of Food Science and Technology 2016 2016 Institute of Food Science and Technology

the control was 4.89 log CFU mL 1 which reduced
down to 4.22 in the sample containing 2500 ppm of
M. spicata EO. After storage for 4 days, the number
of survived cells in the samples treated with M. spicata
and M. aquatica in both concentrations signicantly
reduced to 0.58 log CFU mL 1, whereas in the con-
trol it reached 4.42 log CFU mL 1 (P < 0.05). After
that, the number of bacteria reduced gradually in both
the control and the mints EO containing samples until
the end of storage period. It reached to 3.66 and
0.13 log CFU mL 1 for the control and 2500 ppm
spearmint sample, respectively. These results were in
good agreement with high sensitivity of S. aureus to
both EO observed in the disc diusion assay (Table 3)
which can be mainly related to the phenolic com-
pounds like carvone and 1,8-cineole characterised by
GC-MS in both EOs (Tables 1 and 2). Evrendilek &
Balasubramaniam (2011) also reported that the addi-
tion of mint (M. piperita) EO concentrations at 0.05
and 0.1 mL per 100 mL 1 reduced the initial popula-
tions of Listeria monocytogenes by 0.25 and
0.55 log CFU mL 1, respectively.
Changes in the population of C. perfringens in the
kashk samples containing 1500 and 2500 ppm of
M. spicata and M. aquatica during 20 days of storage
at 4 C are shown in Fig. 2. The initial population of
C. perfringens in the control was 4.59 log CFU mL 1
which reduced down to 4.30 log CFU mL 1 in the sam-
ple containing 2500 ppm of M. spicata EO. Although
both EO could reduce the initial number of C. perfrin-
gens, the reduction was <1 log in the all samples during
the storage period. This shows the resistance of C. per-
fringens against the EO in kashk. The observed reduc-
tion could be due to the intrinsic low pH in the kashk
(<4.2). The lowest count of the bacteria was observed in
the samples treated with 2500 ppm of M. spicata EO
Figure 1 Eect of spearmint (Mentha spicata) and water mint
(Mentha aquatica) essential oils on industrial kashk samples inocu-
lated with Staphylococcus aureus.
2016 Institute of Food Science and Technology
Effect of mint essential oil on kashk L. Golestan et al. 585
during the storage period (P < 0.05). In the disc diu-
sion assay, Clostridium was sensitive to the pure EOs,
especially M. spicata. This was in agreement with those
observed by Kacaniova et al. (2014) who reported good
activity of M. piperita EO against Clostridium genus.
However, Simsek et al. (2007) reported that the inhibi-
tory eects of spiced mint (M. spicata), thyme (Thymus
vulgaris) and garlic (Allium sativum) on E. coli O157:H7
were similar to the control samples in Ayran.
The eects of M. spicata and M. aquatica EOs at
1500 and 2500 ppm on two probiotic bacteria L. reuteri
and B. animalis in the inoculated kashk samples are
presented in Fig. 3a and b. As can be seen, the initial
counts of both probiotic bacteria was reduced by the
addition of M. spicata (0.34 and 0.38 log CFU mL 1
for L. reuteri and B. animalis, respectively) and
M. aquatica (0.20 log CFU mL 1) EOs. Moreover, the
population of L. reuteri showed a slight decrease in all
the treatments during the storage period, except the
sample containing 2500 ppm of M. spicata EOs that
showed a signicant dierence with the control from
day 4 until the end of the storage period. Furthermore,
the population of B. animalis in all the samples
decreased <1 log CFU g 1 during the storage period.
Nevertheless, the sample containing both EOs showed a
signicant dierence with the control from day 8 until
the end of the storage period (P < 0.05). It has been
widely reported that lactic acid bacteria (LAB) are often
known as the most resistant species of Gram-positive
bacteria against the antimicrobial compounds of herbs
(Lemay et al., 2002). Our results are in agreement with
those obtained for Ziziphoraclinopodioides on Lacto-
bacillus acidophilus activity as bio-yoghurt starter cul-
ture (Sarabi-Jamab & Niazmand, 2009), who reported
that there was no signicant dierence in the viability
of Aacidophilus among the samples containing various
concentration of M. piperita EO, Ziziphora clinopodi-
oides and control (P < 0.05). Singh et al. (2011) also
Figure 2 Eect of spearmint and water mint essential oils on indus-
trial kashk samples inoculated with Clostridium perfringens.
International Journal of Food Science and Technology 2016
586 Effect of mint essential oil on kashk L. Golestan et al.
Figure 3 Eect of spearmint and water mint essential oils on indus-
trial kashk samples inoculated with (a) Lactobacillus reuteri and (b)
Bifidobacterium animalis.
reported that the anise oil and its oleo-resin had no sig-
nicant inuence on the viability of LAB in yogurt dur-
ing storage at 4 C. In contrast, in some papers, it has
been reported that the addition of some EOs could
improve the viability of probiotic bacteria (LAB) in
some dairy products. For example, Mahmoudi et al.
(2010) showed that the survival of Lactobacillus casei in
cheese samples containing 0.03% Mentha longifolia EO
was higher compared with the control at the end of
60 days storage period. According to our observations
and the results reported in the last mentioned paper it
can be concluded that the eect of herbal EO on LAB
in dairy products can be dierent according to the type
of EO, bacteria and dairy product.
Organoleptic properties
The mean acceptability taste scores of the kashk sam-
ples containing dierent concentrations of mint EOs
are presented in Fig. 4. As can been seen, M. spicata
EO at both 1500 and 2500 ppm and M. aquatica EO
at 2500 ppm signicantly aected the taste of the
kashk samples. The control and kashk samples con-
International Journal of Food Science and Technology 2016
Figure 4 Organoleptic properties of kashk samples added with
spearmint and water mint essential oils (SM: spearmint, WM: water
mint essential oils).
taining 1500 ppm of M. aquatica EO were the most
preferred samples (P < 0.05). In general, kashk sam-
ples containing M. aquatica EO at 1500 and 2500 ppm
were acceptable to panelists.
Conclusion
The ability of M. spicata and M. aquatica EOs to con-
trol pathogenic microorganism (S. aureus, C. perfrin-
gens) and their eect on the population of some LAB
(L. reuteri and B. animalis) in industrial liquid kashk
were studied. Results showed that both EOs could
eectively reduce the population of S. aureus, in kashk
samples during the storage period. However, the popu-
lation of C. perfringens, L. reuteri and B. animalis
reduced <1 log CFU g 1 in the samples during the
storage period. Moreover, the lowest LAB count was
observed in the samples treated with 2500 ppm of
M. spicata EO during the storage period. Thus, the
least deteriorative eect on LAB was related to
M. aquatica EO. In conclusion, regarding the results
of sensory evaluation and the good performance of
M. aquatica EO in controlling the pathogenic microor-
ganisms and less eect on LAB in kashk sample, it
can be used in industrial liquid kashk. Further studies
are required to determine the impacts of the EOs on
the physicochemical properties of dairy products.
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