Vol.

9 - 1987 Pharmaceutisch Weekblad Scientific Edition 193

review articles
Antimicrobial activities of essential oils

A z976-z986 literature review on possible applications

A.M. JANSSEN,* J.J.C. SCHEFFER*w AND A. BAERHEIM S'VENDSEN*

Introduction efficiency (Table I). Table I indicates that under the

Antimicrobial assays of essential oils are in most conditions given the chance to miss activities in an
cases performed with a specific goal and/or appli- agar overlay technique is low for Escherichia coli,
cation in mind. The experimental set-up should be but quite high for Candida albicans.
made in view of this aim, because the closer the
experimental situation mimicks the practical situ-
ation, the stronger its predictive value. Essential oils Screening for disinfecting or antiseptic properties
have been tested for the following purposes: Disinfection of rooms has been the aim of a
- to screen for antimicrobially active oils or con- classical study; 4 such disinfection is used to lower the
stituents; microbial contamination on surfaces and in the air.
- to screen for disinfecting or antiseptic activities; Essential oils seem advantageous for such purposes
- to screen for food conserving properties; because of their volatility.
- t o study the possible role of essential oils in The oils of wasabi, garlic, ginger and lemon grass,
biological interactions; respectively, were tested on some bacteria for their
- t o study the possible use of essential oils as effects in a closed chamber, s The MIC values,
therapeutic agents. expressed as mg/l, were lower in the vapour phase
than in the medium, which may be caused by a
different distribution or by an activation in the
Screening for antimicrobially active oils or vapour phase.
constituents The oils of peppermint, lavender, wormwood and
The technique that is most often employed is the lemon were effective in reducing the contamination
agar overlay technique, using filter paper discs) 3 of the air with Staphylococci, Streptococci and
This is basically a preliminary test, indicating which Sarcina. 6 In.another study an oil (designated FI) was
oils are interesting for further study. To estimate the active against pathogenic Staphylococci and Strepto-
value of the technique, the percentage of false- oocci when applied as an aerosol in a flight simu-
positive, false-negative and correct predictions lator. 7
should be known. Morris et al. determined the Apart from the results given here, some results
inhibition diameters and minimal inhibitory concen- obtained by the agar overlay technique via the
tration (MIC) values for a large number of aroma vapour phase may also be relevant for the determi-
compounds and essential oils. ~Their results are used nation of disinfecting properties in closed rooms.
in this paper to give an impression of the screening In addition, essential oils have been tested for

Key words
Antibiotics
Antifungal agents
Antisepsis
Disinfectants
Drug screening Janssen AM, Scheffer JJC, Baerheim Svendsen A. Antimicrobial activities
Essential oils of essential oils. A 1976-1986 literature review on possible applications.
Food preservatives Pharm Weekbl [Sci] 1987;9:193-7.

*Division of Pharmacognosy, Abstract

Center for Bio-Pharmaceutical The testing of essential oils for antimicrobial activities is reviewed with
Sciences, State University of respect to various possible applications. Consideration is given to the
Leiden, Gorlaeus Laboratories, screening for antimicrobially active oils or constituents, for disinfecting or
P.O. Box 9502, 2300 RA Leiden, antiseptic properties and for food conserving properties. The role of
the Netherlands. essential oils in biological interactions and their potential as therapeutic
w agents are also discussed.
I94 Vol. 9 - 1987 Pharmaceutisch Weekblad Scientific Edition

their disinfecting and/or antiseptic properties flavus and its aflatoxin production, whereas the
when applied to surfaces. Morris et al. studied the ef- other spices tested had only an effect on the
ficiency of a 'hand-degerming' composition which production of the toxins.~9 Interesting was the obser-
contained some essential oils and aroma chemicals vation that high amounts of some spices caused an
found most active in a screening) However, com- activation of the growth of the fungus. 19 Various
pared to a synthetic preparation the activity was spices were tested for their effect on toxigenic fungi
low. by Hitokoto et al.13 Most spices inhibited the pro-
Good clinical results were obtained for the oil of duction of mycotoxins to some extent, while only
Satureja montana (winter savory), a The oil reduced clove, star-anise and allspice inhibited fungal growth
the endocanalar contamination with some relevant completely. Extracts of some spices were also effec-
bacteria as well "as the symptoms of caries (fourth tive against Vibrio parahaemolyticus, 2~ an organism
degree) in seven out of eight patients. This seems to that can cause foodborne poisoning outbreaks.
be the only case where antimicrobial activity has Because the activity of essential oils on the growth
been linked with an amelioration of clinical signs. of toxigenic fungi can be considered as a very
Eugenol and clove oil have been used for many interesting effect, a number of studies on the
years in dentistry, especially in fillings. However, inhibition of fungal growth as well as on production
side effects such as contact dermatitis 9 and severe of toxins are summarized in Table n. In one study
burning of the oral mucosa ~~ have been reported. cinnamon oil, cinnamic acid and eugenol influenced
The antimicrobial effect of caraway oil was similar to the growth of several toxin-producing fungi in bread
that of eugenol, but the observed toxic effects (acute dough in concentrations of 0.0I-0.I%. 14-Remark-
and chronic) were milder, n able was the observation that the higher concen-
trations within this interval inhibited the fungi,
whereas the lower concentrations stimulated their
Screening for food conserving properties growth. Generally it is observed that whenever the
Spices have been popular since ancient times also growth of a toxigenic fungus is inhibited, the same is
for their food conserving properties. Several studies true for the production of mycotoxins.~5 2223
indicate that the essential oils present play an Some studies have concentrated only on the
important role.~2~6 However, an antimicrobial effect growth-inhibiting properties of essential oils on
of a spice is not always wholly due to the volatile toxigenic fungi. For example, the oils of bay,
components present. For example, rosemary extract cinnamon bark, cinnamon leaves, cloves, pimento
containing no volatiles, was active against Staphylo- berries, pimento leaves and thyme, respectively,
coccus aureus, a micro-organism that is associated inhibited mycelial growth of twenty toxigenic and
with food poisoning) 7 In the case of black pepper non-toxigenic fungi completely at concentrations of
part of the activity against Aspergillus parasiticus I00o and 50o ppm. 24 Another paper mentioned that
could be attributed to the content of piperine) 2 Mentha arvensis (mint) and Mentha x piperita (pep-
Some examples of the activity of spices will be given permint) essential oils inhibited the growth of Asper-
below. gillus flavus (toxigenic) and Aspergillus niger at a
Clove and cinnamon were shown to have a lower concentration of I. 1%.25
bacterial contamination on their surface than pep- Another interesting activity of essential oils is that
per, nutmeg mace and cardamom) s This could be on food-spoilage micro-organisms. Japanese investi-
correlated with the inhibition diameters obtained for gators found essential oils and their constituents to
the essential oils and for chloroform extracts of these be effective in retarding the growth o f several
spices when Aspergillus parasiticus is used as the test fungi. 26Perillaldehyde and several other essential oil
organism. Furthermore, in the presence of extracts constituents showed an interesting positive inter-
of clove and cinnamon neither growth of the men- action with sodium chloride, 27 mixtures of sodium
tioned fungus nor production of aflatoxins was chlorid~ and acetic acid, 28 and sodium chloride
observed. This was in contrast With extracts of the combined with ethanol and acetic acid ,29when tested
three other spices. on airborne fungi. The addition of perilla leaves,
In another study clove was found to be quite Japanese pepper, laurel and cherry to a Japanese
effective in inhibiting the growth of Aspergillus bean paste containing I0% sodium chloride was very

TABLE I
Screening efficiency of the inhibition diameters determined by Morris et al. ~using the agar overlay technique as compared
with MIC values obtained by the dilution method. Positive results: d > 9.5 mm; MIC <~5o0 ppm
Test organism False-positive (%) False-negative (%) Correct (%)
Escherichia coli 40 2 58
Staphylococcus aureus 26 I2 62
Candida albicans 20.5 I9. 5 60
Vol. 9- I987 Pharmaceutisch Weekblad Scienttfic Edition I95
TABLE II
It is also interesting that essential oils and some of
Summary of studies concerning the effect of essential oils
and their constituents on both the growth of toxigenic fungi their constituents reduced the microbial contami-
and the production of mycotoxins nation of tablets containing pancreatin. Solutions of
cinnamic alcohol (2%) and cinnamic acid (2%) were
Oil/constituent Fungus Mycotoxin Reference more effective than those of cinnamaldehyde (2%),
studied* productiont clove oil (2%), eugenol (2%) and cinnamic acid
(t%). 4~
Anethol 2,3,4 + I3
Bitter orange oil I + 23
Cinnamaldehyde I -.I- 2I Possible role of essential oils in biological
Cinnamic acid 1,3,4 "[- 14
Cinnamon oil I + I5,2I interactions
Cinnamon oil x,3,4 + I4 Because it is not known why plants produce
Clove oil i -I- 2I volatile compounds, one can speculate on their
Eucalyptus oil I - 15 possible role in the interactions between plants and
Eugenol I + 2I other organisms. A plant producing an essential oil
Eugenol 2,3, 4 + 13 with an activity against pathogens might well benefit
Eugenol 1,3,4 + 14 from it. Tomato varieties covered with glands and
Ginger oil x + 15 producing volatiles in high amounts were less sus-
Lime oil x + 23 ceptible to fungal infections than other varieties.
d-Limonene I + 23
Nutmeg oil I -- 23 This led to studies on the produced volatiles. 4243 In
Orange oil i + 23 one species (Lycopersicum hirsutum) 2-tridecanone
Pepper oil I + I2 was found in such a quantity that it might play a role
Rosemary oil I Jr- 15 with respect to the mentioned activity.
Sandalwood oil I - x5 The defence system of tomato plants exerted by
Thymol I -'}- I5,22 their volatiles was tested with Botrytis cinerea as test
Thymol 2,3,4 + I3 fungus. The volatiles seem to act on the differen-
tiation of the vegetative and reproductive structures
* I : Aspergillusparasiticus; 2: Aspergillusflavus; 3: Asper- of the fungus leading to less or non-infectious hyphae
gillus ochraceus; 4: Aspergillus versicolor.
t +: inhibiting effect; - : no effect. and conidia. ~ The volatile.off from the glandular
hairs of Solanum tuberosum cultivars consisted to a
effective inpreventing growth of fungi as compared large extent of oxygen-containing compounds which
to a blank." might be responsible for an antifungal activity. 45
Conner and Beuchat tested 3 2 essential oils by the The monoterpenes of the Douglas fir were studied
agar overlay technique for their effect on several for their effect on several bacteria and a yeast. 46 All
yeasts that are known to cause food spoilage. The main constituents of the essential oil (a-pinene,
oils of allspice, cinnamon, clove, garlic, onion, camphene, limonene and isobornyl acetate) in-
oregano, savory and thyme were most active) ~ hibited Bacillus thuringiensis to some extent. Subse-
Results obtained by the 'poisoned food technique' quently it was shown that larvae of the Douglas fir
may also predict food conserving properties. The oil tussock moth (Orygia pseudotsugata) fed on food
of Cedrus deodara was effective in reducing the containing (t-pinene, could tolerate higher numbers
fungal contamination on the surface of fruits of of spores of Bacillus thuringiensis. So the volatiles
Coriandrum sativum (coriander) and Foeniculum present in the needles of the Douglas fir may be
vulgate (fennel) during their storage in polythene important to maintain the sterility of the gut of these
bagsfl 32 Several oils were found effective against larvae.
phytopathogens which cause deterioration in Citrus In tobacco leaves, biosynthesis of sesquiterpenes
fruits.32 In some cases an effect was seen in vivofl can be induced by Pseudomonas solanacearum and
Studies on the change in antimicrobial activity of an by some other factors; ~ some of the induced com-
oil during storage,3~ 35after heat treatment or auto- pounds showed activities against Pseudomonas sola-
claving, 3"1-35"37 or after exposure to UV irradiation 38 nacearum or Pseudomonas syringae pv. tabaci.
are important with respect to practical appli- Sesquite_rpenes are claimed to play a role as phyto-
cations. alexins. ~ In a recent review concerning phytoalexins
Elkhouly and Tawil showed that to% (wt/vol) and stress metabolites in the sapwood of trees, some
emulsions of fixed oil to which rosemary, caraway essential oil constituents were mentioned, like
and cinnamon oil, respectively, were added, were [3-phellandrene, methyleugenol, 7-hydroxycalamen-
very effective in killing a small inoculum of Escher- ene and 7-hydroxycadalenal. 49
ichia coli. 394oThe efficiency decreased by increasing The monoterpenes from Artemisia tridentata (big
the amount of fixed oil, which shows again the sagebrush) showed an effect on the bacteria in the
influence of the medium. The essential oils enhanced rumen of sheep and d e e r J ~51 Such an effect might
the activity of the preservatives chlorhexidine and affect the digestability of big sagebrush and thus
phenylmercuric acetate when used in emulsions. affect the food choice of the mentioned ruminants.
196 Vol. 9 - I987 Pharmaceutisch Weekblad Scientific Edition
Taldykin OE. Use of phytoncidic activity of essential
More recent studies, however, showed that a corre- oils for improving the air in sealed places. Fitonsidy: Rol
lation between the percentage of m o n o t e r p e n e s in Biogeotsenozakh Znach Med Mater Soveshch 8th,
Artemisia tridentata and' its digestability did not 1979:2Ol-3 (via Chemical Abstracts I982;97:9762IS).
exist. 52 8 Pellecuer J, Jacob M, Simeon de Buochberg M, et al.
Essais d'utilisation d'huiles essentielles de plantes aro-
matiques mediterraneennes en odontologie conserva-
Possible use o f essential oils as t h e r a p e u t i c agents trice. Plant Med Phytother I98O;I4:83-98.
Recently some reviews concerning pharmacologi- 9 Wade A, ed. Martindale. The Extra Pharmacopoeia.
cal activities of essential oils have been published. 5~ 27th ed. London: The Pharmaceutical Press, 1977:
lO18.
Some positive clinical experience was gathered on to Lavelle CLB, Proctor DB. Clinical Pathology of the
external application of the oils of fennel, chamomile, Oral Mucosa. San Francisco: Harper & Row, 1978:
peppermint and thyme. 53 25I.
Juniper and sandalwood oil were mentioned to be " Hintz D, Margineanu C, Hodisan V, Popa L. Compara-
used in case of bladder infection. 56 Terpinen-4-ol, tive antimicrobial effect of eugenol and of the volatile oil
and tx- and [3-santalol might be the active compo- of Carum carvi L. Rev Chir Oncol Radiol ORL
nents, respectively. Oftalmol Stomatol Stomatol I98I;28:259-64 (via
Concerning the use of essential oils it can be stated Chemical Abstracts I982;96:2IO5O2y ).
t2 Madhyastha MS, Bhat RV. Aspergillus parasiticus
that there is a lack of recent studies on the thera-
growth and aflatoxin production on black and white
peutic applications of such oils, especially when we pepper and the inhibitory action of their chemical
consider the vast amount of analytical studies on constituents. Appl Environ Microbiol 1984;48:376-9.
essential oils. t3 Hitokoto H, Morozumi S, Wauke T, Sakai S, Kurata H.
Inhibitory effects of spices on growth and toxin pro-
duction of toxigenic fungi. Appl Environ Microbiol
Conclusion I980;39"818-22.
From the large n u m b e r of papers published so far 14 Reiss J. Mycotoxins in foods, x~. Studies on the effect
it is clear that essential oils possess interesting o f the components of cinnamon bark on the growth of
antimicrobial properties which may be useful for molds on bread and formation of mycotoxins. Getreide
Mehl Brot I982;36:5o-3 (via Chemical Abstracts
practical purposes. F u r t h e r m o r e essential oils may
play a role in some biological interactions. H o w e v e r ,
1982;96:14 I325d).
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inadequate. As a rule one can state that the more a production of AspergiUus parasiticus by spice oils. J
test m e t h o d resembles the practical sitiaation, the Food Sci Technol I983 ;20:131-3.
more relevant the results will be. t6 Forstreuter-Kfinstler M, Ahlert B. Hemmung von
In future studies one should pay more attention to Mikroorganismen durch Gewiirzinhaltstoffe. Lebens-
the possible use of essential oils as antimicrobial mittelchem Gerichtl Chem I984;38:143-5.
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spice extractive on growth of microorganisms in meats.
would eliminate many ambiguities that exist as to the
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GB. Microbiological status and antifungal properties of
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