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Food Control 19 (2008) 9951001

www.elsevier.com/locate/foodcont

Studies on the antimicrobial activities of extracts from Eupatorium

lindleyanum DC against food spoilage and food-borne pathogens
Li-Lian Ji
a

a,b,*
,

Yu-Ming Luo a, Gui-Long yan

Jiangsu Key Lab for CLDM and Department of Biology, Huaiyin Teachers College, Huaian, Jiangsu 223300, PR China
b
Institute of Functional Biomolecules, Nanjing University, Nanjing 210093, PR China
Received 21 May 2007; received in revised form 12 October 2007; accepted 23 October 2007

Abstract
Antimicrobial activity of extracts from Eupatorium lindleyanum DC (EEL), a traditional Chinese medicine, was screened against eight
selected food spoilage and food-borne pathogens. The EEL was observed to show eective antimicrobial eects with a remarkable dose
response relationship and broad antimicrobial spectrum on all test Gram-positive bacteria and Gram-negative species. Acid environment
or medium helps enhance the antimicrobial activity. The activity remains rather stable under conventional food sterilization conditions
and normal shelving temperature. The EEL obtained by water decoction exhibited the maximum inhibitory eect on test strains with its
MIC (minimum inhibitory concentration) and/or MBC (minimum bactericidal concentration) value of 0.40.8 mg ml 1. When the EEL
was used in commercial orange juice at a concentration of 0.4 mg ml 1, a similar antimicrobial eect to potassium sorbate at the level of
0.2 mg ml 1 was observed. In conclusion, in addition to use as a functional food ingredient, the EEL may be selected as an inhibitor to
preserve food products where a natural preservative is desired.
 2007 Elsevier Ltd. All rights reserved.
Keywords: Extracts from Eupatorium lindleyanum DC (EEL); Antimicrobial activities; Food spoilage and food-borne pathogens

1. Introduction
Eupatorium lindleyanum DC, a traditional Chinese herb
belongs to Trifoliolatum markino, contains such pharmacological active ingredients as volatile oil, avonoids and
alkaloids, coumarins, sesquiterpenes and esters. The
extracts of the herb obtained by ethanol and ester produce
salient anti-histamine eect. Hundred percentage decoction
of the herb facilitates to inhibit inuenza, a-Streptococcus,
Staphylococcus aureus and catarrh (Xu, Shan, & Wang,
1998; Yan, Qin, Duan, & Tian, 2003). The herb can relieve
fever and remove toxic substances, arrest cough, dispel
phlegm, and reduce blood pressure, promote urination as
well as subside swelling. It is mainly applied for the
*
Corresponding author. Address: Jiangsu Key Lab for CLDM and
Department of Biology, Huaiyin Teachers College, Huaian, Jiangsu
223300, PR China. Tel.: +86 51783526005; fax: +86 51783526020.
E-mail addresses: jll2663@sina.com, jll2863@vip.sina.com (L.-L. Ji).

0956-7135/$ - see front matter  2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2007.10.007

treatment of chronic bronchitis, tracheobronchitis, hypertension, cold and fever, cough with sputum, headache, tonsillitis, bacillary dysentery, etc. (Xia, Wang, Wei, & Lin,
2004).
Up to now, studies on E. lindleyanum DC have been rare
both in China and other countries. Although there have
been some simple researches on its pharmacology and
components, how to develop it into an additive for
health-care food and natural food has not yet drawn
enough attentions. E. lindleyanum DC has been widely
planted in Xuyi town, Huanan city, Jiangsu province. In
order to fully tap the natural resources, it is imperative to
put the comprehensive utilization and process of E. lindleyanum DC on the agenda. Therefore, in this paper, we
focus on the studies on the antimicrobial activities of
extracts from E. lindleyanum DC (EEL) against general
food spoilage and food-borne pathogens so that new food
preservatives can be explored and developed on the basis of
the EEL.

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L.-L. Ji et al. / Food Control 19 (2008) 9951001

2. Materials and methods

2.1. Preparation of EELs
First, the E. lindleyanum DC from Xuyi, Jiangsu province was dried at 5060 C until 6% water was left, and
then it was ground into powder about 40 meshes. Second,
aliquots of 100 g of powder was added individually to
800 ml of the solvents ethyl acetate, 75% (v/v) ethanol
and methanol and reuxed at 60 C for 10 h. The individual extracts were ltered (Whatman No. 1 paper) and the
ltered liquors and residues retained. The residues were
reuxed again with the same solvents to obtain recovery
liquors. The individual liquors were combined and evaporated in vacuum and the dried extracts weighed to obtain
EELs. Another 100 g dry powder was placed into water
(w/v, 1/8) and boiled at 100 C for 30 min to obtain decoction. The decoction was ltered, condensed in vacuum,
dried and weighed to obtain another EEL (water decoction). Aliquots of 50% (w/v) solution of the EELs was
made in sterile water, to which 0.1% Tween 80 can be
added to enhance the solubility of the EELs (Hsieh,
2000; Mall, Chen, & Hsieh, 2002).

(0.2 mg ml 1, for positive control) and Tween 80

(0.1 mg ml 1, for negative control) for 10 min, and then
dried in vacuum. Finally, three plates for each bacterium
were made and six pieces of the lter paper were put on
each plate. After each plate was cultured at 37 C for
48 h, the inhibition zone was then observed and the diameter of the inhibition zone (not including the diameter of
the paper discs) was determined (Hsieh, 2000; Mall et al.,
2002).
The afore-mentioned double-layer culture media were
adjusted by using 0.1 N HCl solution to pH values 3.5,
4.5, 5.5 and 6.5, and their antimicrobial activity was measured to compare the eects of dierent pH values on the
antimicrobial activity of the EELs.
Each of the EELs was treated in dierent food sterilization conditions and its antimicrobial activity was then measured by the afore-mentioned agar diusion method so that
the eects of heat processing of foods on their antimicrobial activity could be observed.
Each of the EELs was stored at temperatures of 5, 15, 25
and 35 C for 12 weeks before its antimicrobial activity was
measured by the same methods as above so that the eects
of dierent storage temperatures on the antimicrobial
activity of the EELs could be studied.

2.2. Test microorganisms and their culture

2.4. Determination of the MIC and MBC of EELs
Eight common bacterial strains of food spoilage and
food-borne pathogens were selected, which included
Gram-positive species, S. aureus (1128), Bacillus subtilis
(4023), Bacillus cereus (1349) and Enterococcus faecium
(29212), and Gram-negative species, Escherichia coli
(3208), Salmonella typhimurium (994), Proteus vulgaris
(845) and Pseudomonas uorescens provided by China
Pharmaceutical University. After two generations of these
test bacteria were activated by Luria broth (LB, provided
by ShangHai Shunbo Biotech. Co., Ltd.) at 37 C before
plating on neutral plate count agar (PCA), a stock suspension of each bacterial culture of 108 cfu ml 1 was prepared
in sterile water and kept in 4 C for 24 h (Jose, Jose, & Herminia, 2001; Kim, Wei, & Marshall, 1995; Sechi, Lezcano,
& Nunez, 2001).
2.3. Determination of antimicrobial activity of EELs
The agar diusion method and double-layer plate
(Whatman No. 1 lter paper) were used to determine the
diameter of inhibition zone of the test bacteria. The bottom
and upper culture medium of PCA containing 1.5% agar,
respectively, were prepared. First, a layer of the bottom
culture medium (about 10 ml) on the plate was spread to
wait for coagulation. Secondly, the molten and cooled agar
of upper culture medium (10 ml) at 45 C was mixed with
the test bacteria before instantly pouring on the bottom
layer of medium, in which the nal bacterial count was
105 cfu ml 1. Next, the autoclaved and dried lter paper
discs (6 mm in diameter) were immersed, respectively, in
the solutions of EELs (0.4 mg ml 1), the sodium benzoate

MIC and MBC of the EELs were determined by the

method of broth dilution. Aliquots of 5 ml of LB media
was placed into tubes before the EEL solution was added
to the tubes to the nal concentration of 50 mg ml 1. Next,
the concentration of the EELs was adjusted ranging from
12.8, 6.4, 3.2, 1.6, 0.8, 0.4, 0.2 to 0.1 mg ml 1 by adding different volumes of the LB media. All above samples were
autoclaved at 121 C and cooling before the test bacteria
suspension was added into to the inoculum size of
106 cfu ml 1 and then incubated at 37 C for 24 h. Another
diluted solution without adding any bacterium was prepared as control sample. The turbidity of all samples was
determined at 540 nm. The determination was based on
the same turbidity of the two subjects of the same concentration, i.e., the minimum inhibitory concentration at
which no bacteria grew in the culture media was dened
as MIC.
After the MICs were determined, the samples showing
no increases in turbidity were streaked on appropriate agar
plates to check bacterial survival and the MBC was determined as the lowest concentration at which the test samples
killed the bacteria.
2.5. Eects of the EEL on the growth curve of the test
bacteria
The LB media were prepared in which the concentration
of the EEL was 0.8, 0.4 and 0.2 mg ml 1, respectively, and
the concentration of potassium sorbate was 0.1, 0.2 and
0.4 mg ml 1, respectively. After wet treating at 121 C

L.-L. Ji et al. / Food Control 19 (2008) 9951001

and cooling, the bacteria (with concentration of

106 cfu ml 1) were added into the LB culture media and
cultivated at 37 C for 30 h for the determination of the
colonies every 5 h by plating on PCA so that the growth
curve of the each test bacteria was obtained.
2.6. Antimicrobial activity of the EEL in orange juice
Fresh orange juice (without any additive) bought from
market was selected for the experiment in which an attempt
was made to test whether the EEL can be applied as natural preservative in food. The EEL of 0.4 and 0.8 mg ml 1
was, respectively, added into the juice after sterilization
with UHT and cooling, then inoculated (102 cfu ml 1) with
afore-mentioned eight bacteria. The juice without the EEL
was used as negative control group while the one with
0.2 mg ml 1 potassium sorbate was used as positive control
group. All the juice was cultured at 30 C and the total viable count was determined every 24 h (Mall et al., 2002).
2.7. Statistic analysis
Statistical calculation was made by the SAS GLM statistical software package (SAS Institute, 1992). Data indexed
by the same letter are statistically not signicantly dierent
from each other (p < 0.05).
3. Results
3.1. Extract of active component from E. lindleyanum DC
As shown in Table 1, the recovery rate reaches up to
optimum by 75% ethanol extractant, amounting to
17.6 g/(100 g dried). Water decoction proves the second
best extractant, which provides 15.3 g/(100 g dried) extract,
methanol provides 11.3 g/(100 g dried) extract, while only
5.0 g/(100 g dried) extract can be obtained by ethyl acetate,
which is hereby considered as the most ineective extractant. Seventy-ve percentage ethanol extractant characteristic of strong permeability exerts marked eects of solubility
and extraction on the eective water and fat soluble components such as volatile oil, avones, saponins, alkaloids,
coumarins, sesquiterpenes and esters, hence an ideal
extractant.

Table 1
Yields of EELs (g/100 g dry sample)
Solvent

Sample code

Yielda

Water
75% Ethanol
Methanol
Ethylacetate

EEL-1
EEL-2
EEL-3
EEL-4

15.3 1.3A
17.6 2.0A
11.3 1.2B
5.0 0.6C

The values were means standard deviation of three replicate experiments. The mean values with dierent letters were signicantly dierent
from one another (p < 0.05) according to Duncan new multiple range test.

997

3.2. Antimicrobial activity of EELs

Through agar diusion and double-layer plate methods,
the diameter of the inhibition zone ranges from 1621 mm
(not including the diameter of the paper discs) suggests
strong antimicrobial activity, 1115 mm indicates moderate antimicrobial activity and the diameter less than
10 mm shows weak antimicrobial activity. As shown in
Table 2, all EELs display antimicrobial activity and broad
antimicrobial spectrum. The antimicrobial activity of water
decoction and 75% ethanol extract is better than that of the
extracts obtained by methanol and ethyl acetate. Such bacteria as S. aureus, B. subtilis, B. cereus, E. coli, E. faecium,
and S. typhimurium are rather susceptible to the EEL by
water decoction while P. vulgaris and Pseudomonas aeruginosa display strong resistance. In general, the EELs have
a little stronger inhibitory eect on the G+ bacteria than on
the G bacteria.
Fig. 1 shows that heat treatment conditions have little
eect on the EEL by water decoction. The sample heated
at 100 C for 15 min or 30 min has better antibacterial
action than the one unheated. The reason is likely that
the EEL concentration in sample rises because the solvent
vaporizes when the sample is heated unsealed. Its antimicrobial activity decreases a little at ultrahigh temperature
of 121 C. Thus, the sound heat endurance of the EEL
prospects well for food preservatives.
Fig. 2 indicates that as the acidity (the initial pH value is
6) of the EEL by water decoction rises, its antagonism to
the test bacteria becomes reinforced. As the pH value of
the sample reaches 3.5 or 4.5, its antagonism rises 20%
on average. Therefore, the EEL are applicable in acid conditions and agreeable with acid products.

Table 2
Inhibitory zone of EELs on test bacteria
Strains

Diameter of inhibitory zone (mm)a

EPL-1b

EPL-2b

EPL-3b

EPL-4b

Positive
controlc

Gram-positive
S. aureus
B. subtilis
B. cereus
E. faecium

17
16
15
13

b
b
b
b

20
21
20
17

c
c
c
c

15
15
14
13

b
b
b
b

15
16
15
13

b
b
b
b

21
20
20
18

c
c
c
c

Gram-negative
E. coli
S. typhimurium
P. vulgaris
P. uorescens

15
14
12
11

b
b
b
b

19
16
13
13

c
b
b
b

13
12
10
10

b
b
b
b

15b
12 b
10 b
11 b

19
19
17
17

c
c
c
c

The diameter (mm) was the mean of the three independent experiments
(not including the 6 mm diameter of the paper disk). The values with
dierent letters in the same line were signicantly dierent from the values
for zone diameters with superscript a and from one another (p < 0.05)
according to Duncan new multiple range test.
b
The concentration was 0.4 mg ml 1. EEL-1, EPL-2, EEL-3 and EEL-4
indicated the EEL obtained by 75% ethanol, water decoction, methanol
and ethylacetate, respectively.
c
The concentration of potassium sorbate was 0.2 mg ml 1.

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L.-L. Ji et al. / Food Control 19 (2008) 9951001

Fig. 3. Eect of shelving temperature on antimicrobial activity of the EEL

to Escherichia coli. Values were the means of the three independent
experiments (p < 0.05).
Fig. 1. Eect of heat treatment on antimicrobial activity of the EEL
obtained by water decoction. Values were the means of the three
independent experiments. Within each bacterium, values were not
statistically dierent (p < 0.05).

Table 3
MICs and MBCs of EELs to test strains
Strain

Fig. 2. Eect of pH on antimicrobial activity of the EEL. Values were the

means of the three independent experiments. Within each bacterium,
values are not statistically dierent (p < 0.05). The EEL tested was by
water decoction.

Fig. 3 indicates when the EEL by water decoction is

reserved in open environment at 525 C for 12 weeks, its
antibacterial activity undergoes little change and lowers a
little at 15 or 25 C. However, when it is reserved open at
35 C for a long period of time, its antibacterial activity
reduces by 20% on average, yet still capable of inhibiting
the growth of the bacteria. Obviously, the EEL can be utilized as an additive with fairly good stability for food
reserved in normal temperature.
3.3. The MICs and MBCs of EELs
Table 3 shows the MICs and MBCs of EELs. All EELs
display certain antibacterial and bactericidal property. In

MIC and MBCa mg ml

EPL-1b

EPL-2b

Gram-positive
S. aureus
B. subtilis
B. cereus
E. faecium

0.4
0.8
0.8
1.6

a
b
b
c

0.4
0.4
0.4
0.4

Gram-negative
E. coli
S. typhimurium
P. vulgaris
P. uorescens

0.8
0.8
1.6
1.6

b
b
c
c

0.4
0.4
0.8
0.8

EPL-3b

EPL-4b

Positive
control

a
a
a
a

0.8
0.8
0.8
1.6

b
b
b
c

0.4
0.8
0.8
0.8

a
b
b
b

0.20.4
0.20.4
0.20.4
0.20.4

a
a
b
b

0.8
0.8
>1.6
>1.6

b
b
c
c

0.8
0.8
>1.6
>1.6

b
b
c
c

0.20.4 a
0.20.4 a
0.4 a
0.4 a

a
a
a
a

a
The values were the means of the average of three samples. The values
with dierent letters in the same line were signicantly dierent from one
another (p < 0.05) according to Duncan new multiple range test.
b
EEL-1, EEL-2, EEL-3 and EEL-4 indicated the EEL with the solvent
of obtained by 75% ethanol, water decoction, methanol and ethylacetate,
respectively.

general, the MICs and MBCs of the EELs aecting all test
bacteria range from 0.4 mg ml 1 to 1.6 mg ml 1. The values of the EEL by water decoction reach 0.8 mg ml 1
against P. vulgaris, and P. aeruginosa and 0.4 mg ml 1
against other test bacteria to exhibits the best antibacterial
and bactericidal property. S. aureus is most susceptible to
the EELs while P. vulgaris and P. aeruginosa are least susceptible to the EELs, which, consequently corresponds
with the results shown in Table 2. Table 3 also shows that,
other conditions being equal, the MBC and MIC of the
EEL aecting each of the test bacteria are identical, indicating that the EEL inhibits the growth and propagation
of the test bacteria by killing them. However, the antagonism of the EELs obtained by the methanol and ethyl acetate to P. vulgaris and P. uorescens is an exception with
MIC of 1.6 mg ml 1, at which evidently, P. vulgaris, and
P. uorescens are not disinfected. As a result, dosage of

L.-L. Ji et al. / Food Control 19 (2008) 9951001

0.4 mg ml 1 is the optimum concentration for most common food spoilage and food-borne pathogens.
3.4. Eect of the EEL on the growth curve of the test
bacteria
The growth curve of the test bacteria under the inuence
of the EEL by water decoction further demonstrates its

log cfu ml-1

log cfu ml-1

antagonizing eect on food spoilage and food-borne pathogens. In general, the antibacterial action shown in Fig. 4
corresponds with the afore-mentioned conclusion, i.e., the
EEL exhibits varied inhibiting eects on the growth of
the test bacteria, showing a remarkable doseresponse relationship. Its antagonizing eect at the concentration of
0.4 mg ml 1 is more powerful than that of 0.2 mg ml 1
potassium sorbate to all test bacteria except for E. faecium

7
6
5

6
5
4

4
3

3
0

10

15

20

25

30

Incubation time (h)

9

15

20

25

30

25

30

25

30

25

30

6
5
4

6
5
4

3
0

10

15

20

25

30

Incubation time (h)

10

Incubation time (h)

log cfu ml-1

log cfu ml-1

999

10

15

20

Incubation time (h)

log cfu ml-1

log cfu ml-1

8
7
6
5
4

7
6
5
4
3

3
0

10

15

20

25

30

Incubation time (h)

9
8

15

20

9
8

log cfu ml-1

log cfu ml-1

10

Incubation time (h)

7
6
5
4

7
6
5
4
3

3
0

10

15

20

Incubation time (h)

25

30

10

15

20

Incubation time (h)

Fig. 4. Growth curves of test bacteria. (a) Staphylococcus aureus, (b) Bacillus subtilis, (c) Bacillus cereus, (d) Enterococcus faecium, (e) Escherichia coli,
(f) Salmonella typhimurium, (g) Proteus vulgaris and (h) Pseudomonas uorescens: () the EEL 0.2 mg ml 1, (j) the EEL 0.4 mg ml 1, (d) the EEL
0.8 mg ml 1, (m) potassium sorbate 0.1 mg ml 1, (h) potassium sorbate 0.2 mg ml 1 and (s) potassium sorbate 0.4 mg ml 1.

1000

L.-L. Ji et al. / Food Control 19 (2008) 9951001

10
9

log cfu g-1

8
7
6
5
4
3
2
0

Storage time (days)

Fig. 5. Eect of the EEL on spoilage bacteria of orange juice. (s) The
control, () the EPL (0.4 mg ml 1), (j) the EEL (0.8 mg ml 1) and (m)
potassium sorbate (0.2 mg ml 1).

and S. typhimurium. On the whole, the antimicrobial activity of 0.8 mg ml 1 EEL is better than that of 0.4 mg ml 1
potassium sorbate but to the exception of P. vulgaris,
and P. uorescens. Finally, what needs to be stressed is that
either 0.8 mg ml 1 EEL or 0.4 mg ml 1 potassium sorbate
exerts complete antibacterial eect on the test bacteria
except to P. vulgaris, and P. uorescens.
3.5. Preservative ecacy of the EEL in orange juice
Add the EEL obtained by water decoction into fresh
orange juice so as to determine its preservative eect on
beverages. As shown in Fig. 5, it produces eective antimicrobial eect. During 24 h, the growth of the test bacteria
in the culture of the orange juice where 0.4 mg ml 1 and
0.8 mg ml 1 EEL are added is completely inhibited. After
48 h, the control group shows rapidly growing bacteria
and gives o foul odor while the condition in the sample
containing 0.4 mg ml 1 and 0.8 mg ml 1 EEL is on the
contrary. The inhibitory rate against the orange juice spoilage bacteria of 0.4 mg ml 1 EEL is equivalent to that of
0.2 mg ml 1 potassium sorbate. The bacteria growth rate
of the sample with 0.8 mg ml 1 EEL remains rather low
during the whole test period. Moreover, there was no one
to feel any changes in taste, color and texture of the juice
added with the EEL among 500 consumers selected randomly from a local street on one Sunday. Obviously, the
EEL can be readily utilized as natural preservative in fruit
juice.

The method of microbial growth inhibition most appropriate to food is the use of food preservatives. An ideal
food preservative must be inexpensive, corrosion-free,
low in toxicity, and have good antimicrobial activity. The
inhibitors available for practical use today are mainly
chemical preservations. However, the safety problems with
chemical preservatives are receiving growing attention, and
natural preservatives for foods have high potential for the
food industry (Li & Yi, 2003; Xie, Zhong, Xu, & She,
2001).
Many extracts from medicine plant have been known to
possess antimicrobial eects and used for the purpose of
food preservation and medicinal purposes (Cowan, 1999;
Lee, Chang, & Su, 2007; Ros & Recio, 2005; Shelef,
Naglik, & Bogen, 1980; Smith, Stewart, & Fyte, 1998;
Tassou, Koutsoumanis, & Nychas, 2000; Valero &
Salmeroj, 2003; Zaika, 1988). In this study, the EEL
obtained by water decoction displays eective antimicrobial eects against food spoilage and food-borne pathogens
and broad antimicrobial spectrum. Its eective antimicrobial concentration is 0.4 mg ml 1 and its antimicrobial
eect is tantamount to that of 0.2 mg ml 1 potassium
sorbate. Acid environment or medium helps enhance the
antimicrobial activity of the EEL. Therefore, the EEL are
readily applicable for acid or medium acid food. Its antimicrobial activity remains rather stable under conventional food sterilization condition and normal shelving
temperature.
It has been reported in some literatures that such materials as avonoids (e.g., quercetin, hypersoide, jaceosidin,
kaempferol), ternary compounds (e.g., taraxasterol palmitate, b-taraxasterol), sesquiterpenes (e.g., eeupalinolide A
and eupalinolide B) and volatile oil can be obtained from
E. lindleyanum DC. These active ingredients produce varied pharmacological eects such as disinfection, antiinammation, anti-neoplasm, immunoregulation, liver
and damage protection, blood glucose decrease (Kazuo,
Yoshihisa, & Mitsumasa, 1979; Xu et al., 1998; Yan
et al., 2003). The application of the extracts of E. lindleyanum DC in food industry not only facilitates antimicrobial
and antimicrobial activities, but also contributes to such
pharmacological activities as food antioxidation, healthcare as well as food nutrients (Wang, Xiao, Xiao, & Lin,
2002). Therefore, it is a natural food additive with considerable market prospect.

4. Discussion

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