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Essential oils and aromatic plants in animal feeding—A European

perspective. A review

Article  in  Flavour and Fragrance Journal · September 2010

DOI: 10.1002/ffj.1967

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Received: 2 November 2009; Accepted: 23 November 2009; Published online in Wiley Online Library: 22 December 2009

(wileyonlinelibrary.com) DOI 10.1002/ffj.1967

Essential oils and aromatic plants in animal

feeding – a European perspective. A review.†,#
C. Franz,a* K. H. C. Baserb and W. Windischc
ABSTRACT: The last two decades have seen a substantial increase in the use of aromatic herbs and essential oils as feed addi-
tives in animal nutrition. One of the main reasons for this trend is to substitute antibiotic growth promoters, which have been
completely banned as feed additives in the European Union since 2006 because they are suspected of contributing substan-
tially to increasing resistance among human pathogens. Recent investigations have shown significant antimicrobial effects of
several essential oils and essential oil compounds against enteropathogenic organisms in farm animals. Porcine proliferative
enteropathy caused by specific Escherichia coli strains could be controlled by in-feed application of carvacrol-rich essential
oils, and the effect of some essential oil components against Clostridium perfringens and necrotic enteritis was confirmed in
poultry. In ruminants, an improvement of the digestion was observed, resulting in reduced methanogenesis and nitrogen
excretion. In addition, the antioxidative activity of aromatic plants and essential oil compounds contributes to the stability
and palatability of animal feed and has, moreover, resulted in an improved shelf-life and quality of animal products, due to
reduced oxidation. The ‘growth-promoting effect’ of essential oils (feed conversion rate, daily weight gain, etc.) is not as
evident, since a large number of publications are (commercial) product-driven, lacking data on the starting material.
Nonetheless, the overall efficacy of essential oils and aromatic herbs, especially their non-nutritive value with impact on the
health status and benefit of animals and humans (via the food chain), is encouraging further research and development in
this field. Copyright © 2009 John Wiley & Sons, Ltd.

Keywords: essential oils; animal feeding; growth-promoting effects; antimicrobial activity; antioxidative activity

Introduction growth promotion, which have now been prohibited to be used

in EU member states since the beginning of 2006. In the USA
Many essential oil plants have been used throughout history in there is until now less legislative regulation but a reduction of
ethnoveterinary practice and animal health management. This is antibiotic use has been achieved by other mechanisms, and
still valid for the majority of developing countries, but also for lobbies led by the American Medical Association exerted pres-
East and South East Asia.[1] The most common uses were in sure to eliminate the inappropriate use of antibiotics in agricul-
Europe, e.g. the use of pine oils against ectoparasites and for ture and especially in food-producing animals.[3,5] Based on the
wound disinfection, camomile and yarrow to treat inflammations strong European regulations and the increasing movements in
or anise, fennel and caraway fruits to prevent gastrointestinal the USA, a worldwide ban of antibiotic growth promoters seems
problems, especially colic and flatulence. Tropical and subtropi- likely on the horizon,[8] although this is probably not the World
cal spices, oleoresins and essential oils have also been mentioned Health Organization (WHO) position.
in the historical European veterinary literature since the eight-
eenth century.[2] Some of the most commonly used species in
traditional European animal healthcare are listed in Table 1.
Following the development in Western medicine in the course
of the last century, the use of plants, extracts and essential oils
* Correspondence to: C. Franz, University of Veterinary Medicine Vienna,
has been replaced by synthetic chemicals in mainstream animal
Department of Farm Animals and Veterinary Public Health, Institute for
healthcare. Public awareness of the potential health risks and Applied Botany and Pharmacognosy, Veterinaerplatz 1, A-1210 Vienna,
environmental problems caused by the excessive use of in-feed Austria. E-mail: [email protected]
antibiotics, growth hormones and some synthetic pharmaceuti-
†
cals, combined with trends towards more natural approaches to This article is part of the Special Issue of Flavour and Fragrance Journal enti-
tled ‘Aromatic Plants, Spices and Volatiles in Food and Beverages’, edited by
food production, has, however, changed attitudes.[3–5] In-feed Ana Cristina Figueiredo and M. Graça Miguel
antibiotics have been used in subtherapeutic dosages for growth
promotion and prophylaxis against enteric pathogens in large- #
Authors would like to dedicate this paper to their colleague and friend, Prof.
scale livestock production for the last almost 50 years. Since the Dr. Heinz Schilcher, who is celebrating his 80th birthday (Zaumberg, Germany)
1990s it has become obvious that their continuing use as a
University of Veterinary Medicine Vienna, Department of Farm Animals and
performance enhancers in animals contributed to a growing Veterinary Public Health, Institute for Applied Botany and Pharmacognosy,
resistance among human pathogens and commensal micro- Vienna, Austria
organisms.[6] Due to human health and safety concerns, the
b
European Union (EU) reacted strongly with regulations affecting Anadolu University, Faculty of Pharmacy, Department of Pharmacognosy,
26470 Eskisehir, Turkey
the feed additives market: by the end of 1998 all but four antibi-
otic growth promoters had been banned, and Regulation (EC) c
BOKU Vienna, Institute of Animal Nutrition, Products & Nutrition Physiology,
1831/2003[7] completed the phasing-out of antibiotics used for
327

A-1190 Vienna, Austria

Flavour Fragr. J. 2010, 25, 327–340 Copyright © 2009 John Wiley & Sons, Ltd.
 C. Franz et al.

Table 1. Most commonly used herbs and essential oils in traditional animal health
care and livestock production in Austria and neighbouring countries

Latin name Common name Parts/products used

Achillea millefolium s.l. Yarrow Infusion
Arnica montana Arnica Extract
Boswellia sacra Frankincense Resin
Carum carvi Caraway Seed, essential oil
Citrus sp. Citrus oil Essential oil
Curcuma longa Curcuma Rhizome
Foeniculum vulgare Fennel Seed
Matricaria recutita Camomile Infusion, essential oil
Mentha sp. Mint Infusion, essential oil
Pimpinella anisum Aniseed Seed, essential oil
Pinus sp. Turpentine Essential oil, (oleo)resin
Salvia officinalis Sage Infusion, essential oil
Syzygium aromaticum Cloves Buds, essential oil
Zingiber officinale Ginger Rhizome
Modified after Zitterl-Eglseer et al.[2]

The second reason behind the regulations concerning feed mixtures rather than as single compounds, hence resistance is
additives, especially the ban of antibiotics and hormones, is a less likely to become a problem than with single synthetic
response to consumer pressures to eliminate all xenobiotic compounds. The number of papers published on the use of
agents from food-producing animals and their respective food essential oils, and especially those containing the phenolic
chains. Proposed alternatives to in-feed antibiotics are extremely compounds carvacrol and thymol, has increased dramatically
diverse and include organic acids, pre- and probiotics and espe- over recent years, the majority reporting, however, on produc-
cially herbs and herbal products, e.g. as essential oils. tion parameters (feed uptake, feed conversion, weight gain)
With regard to horses and pet animals, essential oils are fre- only. Comparatively little information is given about their mode
quently applied not only in the field of feed additives but also in of action, metabolism or generally on their science-based func-
hygiene and medical treatments. For this reason one has legally tionality, because many reports deal with the results of commer-
to distinguish between drugs (pharmaceuticals), healthcare and cial products, avoiding statements on pharmacological effects or
hygiene products and feed additives with regard to the enhanced health claims.
performance of animals (Figure 1). Problems of species-specific Generally speaking, feed additives are used with healthy
differences, (in)compatibilities, doping and medical applications animals not only for nutritional purposes but also for additional
are, however, not the topic of this review. On the other hand, functionality on a permanent basis (possibly throughout the
products to be applied to food-producing animals are, at least in entire production period of the respective species), in contrast to
Europe, much more strongly regulated than feed additives and veterinary drugs, used just to treat health problems under the
drugs for pet animals, since the latter are not part of the human control of a veterinarian and applied for a limited period only
food chain and have no environmental impact on arable land. (Table 2).
In an ambiguous position in this respect are horses, as they can Feed additives are defined by Regulation EC 1831/2003[7] as
be sports animals and/or slaughter equines. substances or preparations, other than feed material or premix-
tures, which are intentionally added to feed or water in order to:

General Aspects • Favourably affect the characteristics of the feed, e.g. as flavour-
Herbal products are currently used by the feed industry largely ings or antioxidants.
as sensory additives, flavouring and appetizing substances. • Affect the characteristics of animal products regarding micro-
Although the understanding of their mode of action is a prere- bial load, shelf-life or taste.
quisite for their optimal application in terms of efficacy, a full • Affect the environmental consequences of especially large-
understanding of these aspects in animals has not yet been scale livestock production, e.g. by reduction of ammonia
achieved. For example, aromatic compounds and essential oils excretion or methane production.
act along the animal digestive tract to improve appetite and • Favourably influence animal production, performance or
modulate the bacterial flora, and are able to induce a number of welfare by affecting the gastrointestinal flora and the digesti-
other benefits.[9] The antimicrobial properties of essential oils and bility of feeding stuffs.
extracts can be dose-dependently bacteriostatic and/or bacteri- • Have a coccidiostatic or histomonostatic effect.
cidal. In addition, several investigations have shown their antioxi-
dative effect, their effects on digestive physiology and digestion
at weaning[10] and on the microbiology of the gut,[11] or have been
Growth-Promoting Effects and Palatability
performed in order to implement test models in poultry.[12] One Many aromatic herbs and essential oils are used for improving
advantage of essential oils is that they occur in nature as complex the flavour and palatability of feed or to affect other parameters
328

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Essential oils and aromatic plants in animal feeding – a European perspective

Farmer: Veterinarian:

Feed Additives / Supplements Medicinal Products

Regulation (EC) 1831/2003 Guideline 2004/28/EU (Community Codex
Regulation (EC) 429/2008 Veterinary Drugs)
Directives (EC) 2491/2001, Directive (EC) 726/2004 (Human- & Veterinary
834/2007 and 889/2008 Medicinal Products)
Directives (EC) 2491/2001, 1834/2007
and 889/2008 (Organic Production)

Food-producing Animals
Dir. (EC) 2377/90 (MRL- Values) Horses and Companion Animals
Dir. (EC) 2491/2001, 834/2007
and 889/2008 (Organic Production)
Figure 1. EC regulations[7] concerning feed, feed additives and veterinary drugs and their significance for farm and pet animals

Table 2. Principles of use of feed additives vs. veterinary drugs

Feed additives Veterinary drugs

User/applicant Farmer, feed producer Veterinarian only
Animals Healthy animals Sick animals
Aim of use Improve productivity Restore health
Duration of use Permanently Temporarily
Safety No safety risk accepted, Risk–benefit analysis,
severe safety check waiting periods before
before authorization consumption of products

in livestock production (see the Community Register of Feed results are due to the type and origin of the essential oil or herb
Additives for a full list of authorized additives). Numerous feeding species, the quantity added to the feed and the environmental
trials have been performed with such additives, but most of the conditions of the trial. Investigations under practical conditions
results are reduced to the growth-promoting parameters: feed of large-scale animal production have shown better responses to
intake, weight gain and feed conversion rate (Tables 3, 6). the treatment[13,17] than more recent studies under controlled
In pigs, the improvement of performance was on average 2% experimental conditions with a higher level of hygiene[18] (Tables
increase in weight gain and 3% in feed conversion efficacy, 4, 5). Whilst in large-scale piggeries with 250–500 mg oregano
ranging from −5% to +9% for weight gain (with one extraordi- oil/kg feed improvements on zootechnical parameters of up to
nary exception: Kyriakis et al.[13] reported 23% improvement) and 20% and a heavy decrease in mortality of weaners[13] and piglets[17]
from +4 to −10% in feed conversion rate. These figures are com- could be obtained, no significant differences were observed in
parable to the potential of ‘conventional’ growth promoters (anti- an experimental station between control and the addition
biotics, organic acids, probiotics), where advantages of roughly of either antibiotics or several essential oils.[18] Richter and
4% are to be found in the respective literature.[14–16] The different Löscher[19] stated in 2002 that antibiotic growth promoters also
329

Flavour Fragr. J. 2010, 25, 327–340 Copyright © 2010 John Wiley & Sons, Ltd. View this article online at wileyonlinelibrary.com
 C. Franz et al.

Table 3. Effect of aromatic herbs and essential oils as feed additives on the performance in piglets

Feed additive Dietary Treatment effects (% difference to untreated control) References

dose Feed Body Daily Feed
(g/kg) intake weight weight gain conversion rate*
Essential oils
Caraway 0.1 −9/−2 −/0 −7/− −3/−2 Schöne et al.[20.21]
Cinnamon 0.1 +5 +2 +3 Gollnisch et al.[18]
Cinnamon 0.1 −5 0 −5 Wald et al.[22]
Clove (5 ml) −5 0 −5 Tartrakoon et al.[23]
Clove 0.1 +1 0 +3 Gollnisch et al.[18]
Clove 0.1 +3 +7 −4 Wald et al.[22]
Essential oil blend 0.04 +4 +6 −2 Kroismayr et al.[24]
Essential oil blend 0.1 +3 0 +3 Gollnisch et al.[18]
Fennel 0.1 +3/+3 −/+6 +4/− −2/−3 Schöne et al.[20,21]
Lemongrass (5 ml) −3 +2 −5 Tartrakoon et al.[23]
Lemongrass 0.1 −2 +2 −4 Wald et al.[22]
Oregano 0.1 +3 +2 0 Gollnisch et al.[18]
Oregano 0.1 0 +5 −5 Wald et al.[22]
Oregano 0.5 −3 +7 −9 Günther and Bossow[25]
Oregano 0.5 +12 +23 −9 Kyriakis et al.[13]
Peppermint (5 ml) −4 −3 −2 Tartrakoon et al.[23]
Peppermint 0.1 −9 −3 −7 Wald et al.[22]
Pimento 0.1 −8 −4 −5 Wald et al.[22]
Herbs and spices
Coriander 2.0 +4 +7 −3 Schuhmacher et al.[26]
Garlic 1.0 −7/+5 +2/+1 −8/+4 Schuhmacher et al.[26]
Oregano 2.0 −1/+4 +9/+5 −10/0 Schuhmacher et al.[26]
Sage 2.0 +3 +7 −4 Schuhmacher et al.[26]
Thyme 2.0 +4 +6 −3 Schuhmacher et al.[26]
Thyme 1.0 −1 +1 −1 −4 Hagmüller et al.[27]
Thyme 5.0 −1 −2 −1 +4 Hagmüller et al.[27]
Yarrow 2.0 +1 +4 −4 Schuhmacher et al.[26]
* Feed conversion rate: kg feed/kg body weight gain.

Table 4. Control of porcine proliferative enteropathy (PE) by in-feed application of

Origanum essential oils[17]

Parameter Control Oregano oil

250 g/t 500 g/t
Average daily gain (g) 573 653 687
Feed conversion rate 3.04 2.74 2.66
Diarrhoea score 2.88 2.16 1.81
Mortality (%) 25.0 13.0 10.0
Observation period, days 25–161.

Table 5. Effect of some essential oils on the performance of rearing piglets in comparison to a standard antibiotic[18]

Additive Group 1 Group 2 Group 3 Group 4 Group 5

None Avilamycin Oregano oil Clove oil Cinnamon oil
Average daily gain (g/day) 398 437 407 392 407
Feed intake (g/day) 596 636 614 602 625
Feed conversion rate (kg/kg) 1.50 1.46 1.51 1.54 1.54
330

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Essential oils and aromatic plants in animal feeding – a European perspective

Table 6. Effect of aromatic herbs and essential oils as feed additives on the performance in poultry

Animals/feed Dietary Treatment effects (% difference to untreated control) References

additives dose Feed Body Daily Feed
(g/kg) intake weight weight gain conversion rate
BROILERS
Essential oils
Anis 0.15 −1 +1 −1 Mayland-Quellhorst[29]
Carvacrol 0.2 +2 +2 −1 Lee et al.[30]
Cinnamaldehyde 0.1 −2 −3 0 Lee et al.[30]
Cinnamon 0.1 −4 −3 −1 Wald[31]
Clove leaf 0.1 −3 −4 +1 Wald[31]
Lemongrass 0.1 +1 −1 +2 Wald31]
Oregano 0.15/0.3 −6/−3 −2/+1 −4/−2 Basmacioglu et al.[32]
Oregano 0.1/1.0 −1/+3 +8/+6 −9/−3 Halle et al.[33]
Oregano 0.1 −2 −1 −1 Wald[31]
Peppermint 0.1 −3 −2 −1 Wald[31]
Rosemary 0.15/0.3 0/−2 −1/+1 −1/−4 Basmacioglu et al.[32]
Thymol 0.1/0.2 +1/−5 +1/−3 −1/−3 Lee et al.[30]
Essential oil blend 0.024/0.048 −4/−5 0/0 −4/−6 Cabuk et al.[34]
Essential oil blend 0.075/0.15 −7/−7 −3/−1 −4/−1 Basmacioglu et al.[32]
Essential oil blend 0.036/0.048 +3/+2 −8/−8 −5/−4 Alcicek et al.[36]
Essential oil blend 0.024/0.048 −2/0 0/+14 −2/−12 Alcicek et al.[35]
Essential oil blend 1.0 −7 −3 −4 Halle et al.[37]
Essential oil blend +2 0 +2 Westendarp et al.[38]
Aromatic herbs
Garlic 1.0 −5 −5 0 Sarica et al.[39]
Oregano 5.0 +5 +7 −2 Florou-Paneri et al.[40]
Thyme 1.0 +1 +2 −1 Sarica et al.[39]
Thyme 1.0/10 0/−1 −3/−5 −2/−4 +3/+6 Haselmeyer[41]
Hops 0.25 +2 +5 +4 −3 Cornelison et al.[42]
TURKEYS
Aromatic herbs
Oregano 1.25 −5 +2 Bampidis et al.[43]
Oregano 2.5 −6 +1 Bampidis et al.[43]

compensated for lack of hygiene only when the weight gain was (0.06% and 0.6% of each herb, respectively), corresponding to
improved by 10% and the feed conversion rate by 6% in com- 20 and 200 mg essential oil/kg feed, respectively. There was a
parison to control. significant preference for standard feed without herbs, and
Aromatic herbs and essential oils are often claimed to improve within the treated feeds there was a clear tendency to preference
the flavour and palatability of feed, thus enhancing zootechnical for thyme compared with oregano. This might be due to the
performance. Indeed, there are some reports of higher feed fact that oregano in general has a ‘stronger’ flavour and taste.
intake of piglets through flavouring additives. However, a rise in A statement on performance was, however, not possible,
feed intake is commonly observed with growth-promoting feed since the animals were not forced to ingest a specific additive.
additives and primarily reflects the higher consumption capacity Overall, no better palatability was achieved by adding these
of larger grown animals compared to untreated controls, but not herbs.
necessarily a specific enhancement of voluntary feed consump- In poultry, most studies have shown no significant change in
tion due to improved palatability. Very few experimental assess- feed intake caused by herbal or essential oil additives, although
ments of feed acceptance, preference and palatability affected growth was often enhanced and the feed conversion rate
by flavouring additives have been reported so far, indicating improved (Table 6). Since poultry are known to adjust feed intake
reduction of voluntary feed intake in piglets through increasing according to energy demand, the feed conversion rate is there-
amounts of fennel and caraway oils[21] and thyme and oregano fore a better parameter of the effects of growth promoters.
herbs,[28] respectively. Published results are, however, contradictory. In one experiment,
In a randomized block design, Ungerhofer[44] investigated where broilers were fed with 200 mg/kg feed-stuff carvacrol or
the acceptance of thyme and oregano herbs as feed additives thymol, carvacrol lowered the feed intake, weight gain and feed
in pigs. The animals could freely choose between standard feed conversion rate, whereas thymol showed no effect.[30] Addition of
without herbs, two concentrations of the single herbs (approxi- oregano herb in quantities of 2–20 g/kg feed or of oregano oil
mately 0.12% and 1.2%, respectively) or mixtures of both herbs (100–1000 mg/kg feed) resulted, in contrast, in all cases in better
331

Flavour Fragr. J. 2010, 25, 327–340 Copyright © 2010 John Wiley & Sons, Ltd. View this article online at wileyonlinelibrary.com
 C. Franz et al.

performance of broiler chicks.[45] Another trial made by this

research group[38] using carvacrol, p-cymene and γ-terpinene as
pure substances in approximately 50 (carvacrol) or 25 (terpinene,
p-cymene) mg/kg showed no significant effects. Haselmeyer[41]
studied the effect of thymol in four concentrations from 0.1% to
1.0% as feed additive in broilers. No significant difference in per-
formance was observed over the whole growing period (35 days).
Turkeys fed with 1.25–3.75 g/kg dried oregano leaves showed, in
contrast, a clearly improved feed conversion rate.[43] Adding
60 ppm carvacrol-rich thyme oil to the diet of quails resulted in
significantly higher body weight gain and better feed efficiency
as well as decreased abdominal fat weight.[46] Finally, the addition
of 250 mg/kg hops to the diet of broilers resulted in significant
improvements in feed conversion and feed efficiency at all ages,
and also improved the body weight when compared to the nega- Figure 2. Gastric emptying of piglets retarded by essential oils[50]
tive control[42].
Many more positive results on animal performance are compounds together with capsaicin to piglets and reported an
reported with herbal or essential oil mixtures and especially com- increased gastric retention time of ingested feed (Figure 2),
mercial products. From a scientific point of view many of these resulting in better nutrient absorption and favouring intestinal
reports are difficult to assess, since detailed information on the stability against digestive disorders. Thus, there is evidence that
formulation used and on the phytochemical and sensorial quality essential oils and aromatic compounds may favourably affect
is missing. This is also often true for published reports on feeding gut functions.
trials. However, even if there are some uncertainties associated Essential oils used as feed additives for broilers were shown to
with the reporting of studies, there is sufficient evidence that enhance the activities of trypsin, of amylase in tissue homoge-
herbs and essential oils are able to improve zootechnical per- nates of the pancreas, as well as the jejunal chyme content.[30,51]
formance in piglets and poultry. A mixture of carvacrol, cinnamaldehyde and capsaicin also stimu-
As regards ruminants, very little is known about the effect lated the intestinal secretion of mucus: Jamroz et al.[52] stated that
on feed intake and palatability of aromatic plants or volatile the increased release of large amounts of mucus and the creation
compounds.[3,5] Estell et al.[47] reported that terpene volatiles of a thick layer of mucus on the glandular stomach and jejunum
could affect feed intake in sheep, which is quite important wall in chicks fed with the above mixture could be responsible
when grazing in Mediterranean pastures. Better knowledge of for the reduced adherence of pathogens (E. coli, Clostridium
specific chemical interactions with feed intake would be useful perfringens and others) to the gut epithelium.
for altering feeding management. In addition, the potential of This confirms – as already known from human nutritional
essential oils as manipulators of rumen metabolism is of high physiology[53] and phytopharmacology[54] – that the mode of
significance. action of spices and essential oils on gut function arises at least
partly from an irritation of the epithelial tissues, leading to higher
secretions of mucus and enzymes.
Impact on Gut and Intestine Functions Remarkably little has been published on the effects of essen-
The primary mode of action of growth promoting feed additives tial oils and aromatic plants on rumen metabolism. Broudiscou
appears to arise from stabilizing feed hygiene and from benefi- et al.[55] observed in vitro that Lavandula officinalis promoted the
cially affecting the ecosystem of gastrointestinal microflora by extent of rumen fermentation and that Salvia officinalis had a
controlling potential pathogens. This applies especially to those possible inhibitory effect on methane production. Some essen-
critical phases of the animals’ development where a higher sus- tial oils have been reported to inhibit enzyme activity,[56] e.g.
ceptibility to digestive disorders may be present, e.g. the weaning thymol is a strong deaminase inhibitor.[57] Cardozo et al.[58] found,
phase of piglets, the early life span of poultry or restocking at furthermore, that higher doses of cinnamaldehyde decreased
young bull fattening. ruminal L-lactate concentration.
Improved intestinal health favoured by feed additives may An interesting in vitro investigation was performed by Busquet
mean that animals are less exposed to microbial toxins or other et al.,[59] who incubated selected essential oils (e.g. oregano, cin-
undesired metabolites, e.g. ammonia and biogenic amines. namon and clove bud oil) and isolated compounds (carvacrol,
Consequently, additives such as aromatic herbs or volatile oils carvone, cinnamaldehyde and eugenol) for 24 h in diluted ruminal
may relieve the animals from having to mount an enhanced fluid with a 50:50 forage:concentrate diet. At 3.0 g/l the oils and
immune defence during critical situations, increasing the intesti- compounds resulted in an up to 50% reduction in ammonia con-
nal availability of essential nutrients for absorption and, thus, centration. Since the rumen is a complex bioreactor, it is of note
assisting the animal to grow better within its genetic potential. that some essential oil compounds can withstand 24 h exposure
A large number of aromatic plants, spices and essential oils are to rumen fluid in a rumen simulation technique apparatus
known for digestive or carminative activity. This is due to the (RUSITEC) but others, such as neral, geranial, linalool or thujone,
stimulation of digestive secretions, e.g. saliva, bile, mucus, as were metabolized (Figure 3).[60] This might be due to the interac-
well as enhanced enzyme activity being a core mode of benefi- tion with the rumen flora as well as acidity and could have an
cial nutritional action.[48] Rats additionally fed anise oil reacted impact on the ammonia and methane production of ruminants.
with a pronounced nutrient absorption, especially that of glucose More knowledge about the effects of essential oils on rumen
in the small intestine.[49] Manzanilla et al.[50] fed a combination of function would be useful, particularly on enzymes associated
essential oils with carvacrol and cinnamaldehyde as the main with proteolysis and deamination. Such activities of essential
332

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Essential oils and aromatic plants in animal feeding – a European perspective

oils/compounds could limit rumen ammonia concentrations and One mode of action of essential oil compounds as antimicrobi-
consequently lead to more efficient utilization of dietary nitro- als is the rapid depletion of the intracellular ATP pool through the
gen.[3] The use of essential oils to manipulate ruminant digestion reduction of ATP synthesis and simultaneously increased hydro-
is, however, to date under-exploited.[5] lysis. The reduction of the transmembrane electric potential
being the driving force of ATP synthesis enhances the proton
permeability of the membrane. The leakage of ions, e.g. potas-
Antimicrobial Activity sium and phosphate, out of the cell indicates membrane damage,
The antimicrobial activity of essential oils and essential oil com- resulting in disturbances of the osmotic pressure of the cells.[67–69]
pounds, whether bacteriostatic or bactericidal, or against other Furthermore, changes in the fatty acid compositions of bacterial
food-borne pathogens such as fungi and protozoa, is well docu- cell membranes have been observed at sublethal doses of several
mented.[61–64] Most active in this respect are the phenolic com- essential oil compounds.[70]
pounds carvacrol, thymol and eugenol, but also other substances, Other effects are shown by substances such as carvacrol,
such as phenylpropane, limonene, geraniol or citronellal.[65,66] which prevents the synthesis of flagellin, causing bacterial/cells
to be aflagellate and therefore non-motile. Such cells are signifi-
cantly less able to adhere to epithelial cells, which renders poten-
100 tially pathogenic strains of bacteria non-infective,[71] a mechanism
80
similar to that known from galacturonic acids in the diet.[72]
Recovery %

In vitro antimicrobial activities have been measured with a

60
number of essential oils and single compounds, mainly against
40
the enteropathogenic strains Escherichia coli, Salmonella spp. or
20 Clostridium perfringens. Using either the broth microdilution
0 method or the agar diffusion test, essential oils with a higher
a-Pinene
b-Pinene
Myrcene
Limonene
Cineol
Fenchone
Linalool
Thujone
Fenchyl alcohol
Camphor
Menthone
Menthofurane
Menthol
Citronellol
Nerol
Geraniol
Piperitone
Thymol
Carvacrol

percentage of phenolic compounds showed the strongest inhibi-

tory capacity in terms of minimum inhibitory concentration
(MIC).[73–75] Differences in activity have been observed, however,
between plant species and plant parts on the one hand and the
sensitivity of species and strains of the microorganisms on
Figure 3. Recovery rate of essential oil compounds after 24 h the other (Figures 4, 5).[66] This is due to the varying chemical
incubation with ruminal fluid[60] composition of the plant materials (chemotype, morpho- and

60

50
Zone Diameter of Inhibition [mm]

40

B.cereus*
30 E. coli
S. typhimurium
S. aureus*
Y. enterolitica
20

10

0
FL 1 LV 1 FL 2 LV 2 FL 3 LV 3
O. x intercedens O.onites O.vulgare

Figure 4. Antibacterial activity of Origanum spp. FL, flower oil; LV, essential oil from leaves[66]
333

Flavour Fragr. J. 2010, 25, 327–340 Copyright © 2010 John Wiley & Sons, Ltd. View this article online at wileyonlinelibrary.com
 C. Franz et al.

30.0

25.0
Zone Diameter of Inhibition [mm]

20.0

15.0

10.0

5.0

0.0 10

11

12

13

15

16

17

18

19

20

21
1

Sage Oil Samples

Figure 5. Antibacterial activity of sage (Salvia officinalis) essential oils on Escherichia coli (each column represents one individual plant/clone)[66]

Table 7. Minimum inhibitory concentration (MIC) of several essential oils and some compounds on selected microorganisms
(in μl/ml)[65,66,76]

Escherichia Salmonella Staphylococcus Listeria Bacillus

coli typhimurium aureus monocytogenes cereus
Rosemary 4.5–10.0 >20.0 0.4–10.0 0.2 0.2
Sage 3.5–5 10–20 0.75–10 0.2
Oregano 0.5–1.2 1.2 0.5–1.2
Thyme 0.4–1.2 0.45–20 0.2–2.5 0.2–0.5
Clove 0.4–2.5 >20.0 0.4–2.5 0.3
Lemongrass 0.6 2.5 0.6
Limonene 0.70
Carvacrol 0.1–5.0 0.2–0.25 0.2–0.45 0.4–0.5 0.25
Thymol 0.10–0.45 0.06 0.17–0.25 0.20–0.45 0.35–0.45
Geraniol 0.15 0.35 1.25 0.35
Eugenol 0.55 0.75 0.55 0.30

ontogenetic variation), which is often neglected in microbiologi- and equilibrium of the intestinal flora could be achieved by such
cal or animal studies. From Figure 4 it is evident that several treatments. Kroismayr et al.[24] found, in a piglet study, that adding
pathogens respond differently to various Origanum spp. and oils 40 mg/kg of a mixture of carvacrol, thymol, anethol and limonene
from different plant parts. Figure 5 shows the plant-to-plant vari- to the diet reduced E. coli colony counts at the end of the ileum,
ation in activity against E. coli of sage (Salvia officinalis) essential and as a consequence smaller amounts of toxic biogenic amines,
oils, both caused by phytochemical polymorphism. The in vitro e.g. cadaverine and scatol, were found in the gut lumen resulting
active levels exceeded in general the dietary doses accepted by from microbial degradation (Figures 6, 7). The fact that Hagmüller
animals (Table 7), which results in few studies available so far et al.[27] failed to measure differences in the number of E. coli in
demonstrating the efficacy of essential oil(s) (compounds) fecal samples from pigs treated with thyme might be due to a
against specific pathogens in vivo. Killing the intestinal flora, on sublethal dose leaving the bacteria alive but with reduced viabil-
the other hand, as happens with broad-spectrum antibiotics, is ity. On the other hand, some studies with poultry showed a clear
undesirable, but a stabilization of the microecology in the gut reduction of Clostridium perfringens in the jejunum and caecum
334

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Essential oils and aromatic plants in animal feeding – a European perspective

Jejunum
100%
80%
60%

40%
20%
0%
C A B C A B C A B
14 21 30 days

Caecum
100%

80%

60%
Figure 6. Influence of a mixture of essential oil compounds (carvacrol,
thymol, anethol and limonene) as feed additive (40 mg/kg) on bacterial 40%
counts at the end of the ileum of rearing piglets[24] 20%
0%
C A B C A B C A B
14 21 30 days

< log 2 log 2 - log 6 >log 6

Figure 8. Relative frequency of Clostridium perfringens concentrations

in the jejunum and caecum of broilers in the presence of essential oil
compounds used as feed additives.[77] A, Thymol, eugenol, curcumin,
piperin; B, thymol, carvacrol, eugenol, curcumin, piperin; C, control

Essential Oil Components

100
90
80
Figure 7. Reduction of biogenic amines by compounds from essential 70
oils (carvacrol, thymol, anethol and limonene) or an antibiotic 60
Borneol(Sage/Oregano)
AI%

(avilamycin) as feed additives (40 mg/kg) in rearing piglets[24] 50

Thymol(Sage/Oregano)
40 Carvacrol(Sage)
30
20
of broilers fed with a mixture of essential oil components (Figure 10
8).[77,78] The same blend of components as well as oregano oil or 0
25000 3125 390.6 48.83 6.1 0.76 0.09
crude drug was effective against Eimeria spp. infections in broil-
Concentration(ppm)
ers, thus reducing the need for conventional coccidiostats.[79–81]
Some authors argue that essential oils increase the mucus secre- Figure 9. Thiobarbituric acid reactive substances (TBARS) assay for
tion in the intestine, which protects the surface of villi.[52] Two borneol, thymol and carvacrol. AI (%), antioxidative index[66]
further benefits may follow from the addition of essential oils to
animal feed: the reduction of feed microbial load and improve-
ment of the microbial hygiene of the carcass.[82,83] The number of Essential Oil Component
reports in this area is, however, too limited to draw conclusions. 100
90
80
Antioxidative Effect 70 b -Caryophyllene(Oregano/Sage)

60
Many essential oil plants and essential oils are known for their Terpinen-4-ol(Oregano/Sage)
AI%

50
antioxidative properties, based mainly on phenolic compounds in 40 d-3-Carene(Oregano)
the oil (Figure 9) or in other phytochemical fractions. Some non- 30
phenolic substances may also show a considerable antioxidative 20 a -Terpinene(Oregano/Sage)

potential (Figure 10). Such substances contribute to the protec- 10

tion of feed lipids from oxidative damage, partly substituting the 0
25000 3125 390.6 48.83 6.1 0.76 0.09
use of α-tocopheryl acetate and related compounds as feed addi-
Concentration(ppm)
tives or preservatives. Essential oils may also affect lipid metabo-
lism in the animal: a dietary supply of thyme oil or thymol to Figure 10. Thiobarbituric acid reactive substances (TBARS) assay for
ageing rats showed a beneficial effect on the antioxidative β-caryophyllene, terpinen-4-ol, δ-3-carene and α-terpinene.
enzymes superoxide dismutase and glutathione peroxidase, as AI (%), antioxidative index[66]
335

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 C. Franz et al.

9 Results obtained by the EU-funded research and development

8 project SAFEWASTES[93] (2005–2008) demonstrated that residues
7
of several essential oil plants after distillation could find a proper
use in animal feeding as zootechnical additives. Traditionally
CO in fat (ppm)

6
known in this respect is the use of parsley stalks (a co-product
5 of the production of dried parsley leaves) in dairy cows to
4 enhance milk production. However, care is necessary, since
3 essential oils and other compounds, e.g. phenolic substances,
2 could influence the flavour and taste of the products or even
1
cause an ‘off-flavour’. But the taste and flavour of the animal
product can also be positively affected by herbs and essential
0
Control Sage Mixture Oregano oils. Greber[94] fed fattening pigs a diet containing 0.3–1.2% sage
(Salvia officinalis) leaves and found, with increasing addition of
Figure 11. Influence of herbs as feed additive in fattening of pigs sage, not only some of the monoterpenes (camphene, 1,8-
(1% herbs, 6 months storage) on the shelf-life of bacon. CO, cholesterol cineole and others) in the animal tissue but also an aromatic-
oxide content[89] spicy note in the cooking and frying test. Anyone who has ever
tasted products of the black Corsican ‘Nustrale’ pig knows that
well as on polyunsaturated fatty acid composition in various feed intake in the Mediterranean macchia with many essential oil
tissues. Animals receiving these supplements had higher enzyme plants results in a naturally flavoured tasty meat, ham and bacon
levels and higher concentrations of polyunsaturated fatty acids in (Keyserlingk, pers. commun.). Comparable results are known
phospholipids of the brain than the untreated controls.[84] Oregano from sheep grazing in Mediterranean pastures.[47]
added in doses of 50–100 mg/kg to the diet of chickens exerted an
antioxidant effect in the animal tissues;[85] the pattern of fatty acids
of the abdominal fat of chicken was also altered by oregano oil[31]
Conclusion
and dietary carvacrol lowered plasma triglycerides.[30] In food- The trend over recent decades towards the use of herbal prod-
producing animals such effects are of importance for product ucts in human medicine and as dietary supplements in human
quality: they may improve the dietary value and lead to a better nutrition has also resurrected interest in their use in animal hus-
oxidative stability and longer shelf-life of fat, meat and eggs.[86,87] bandry. Until the 1990s, optimizing the nutritive value of the
Oxidation of meat and membrane phospholipids from broilers fed animal diet has been the main objective of large-scale livestock
with 500 mg/kg diet rosemary and sage extracts was significantly production, driven by quantitative economic reasons only. In the
lower after 9 days refrigerated storage compared to 200 mg/kg meantime, quality aspects and confidence in safe and healthy
α-tocopherol and the control, respectively.[88] The concentration foodstuffs of animal origin are of the utmost significance, as seen
of total cholesterol oxidation products was also reduced, and a by the establishment of the European Food Safety Authority
similar trend was observed in microsomal fraction isolates, in (EFSA) in 2002 and a number of recently issued EU regulations.[7]
which the rate of metmyoglobin/hydrogen peroxide-catalysed In this context, the ‘non-nutritive value’ of food and feed compo-
lipid peroxidation was lower in birds receiving essential oil plants nents, especially secondary plant products with impact on the
than in controls fed on basal diet only. A diet containing 1% Salvia health status of animals and humans (via the food chain). has
officinalis or Origanum vulgare crude herbal drug, either alone or attracted science, since the functionality of these substances was
in a 1:1 mixture, was tested with pigs. Raw belly bacon produced poorly understood. As this has changed, interest in the applica-
from animals fed with only oregano as the additive showed a sig- tion of herbs as feed ingredients and extracts and especially
nificantly improved stability and lower cholesterol oxide content essential oils as feed additives has increased tremendously, and
compared to controls after 34 weeks storage (Figure 11).[89] Sage as not only in organic livestock farming. Due to many well-known
the additive, in contrast, had a much lower impact. characteristics, the functions and effects of essential oils and
The effect of dietary thyme (3% ground herb of Thymus vul- essential oil plants and their value when used in animal hus-
garis as feed additive for laying hens) on the oxidative stability of bandry can be summarized under three headings, as follows:
eggs over 60 days storage in the refrigerator was evaluated by
Botsoglou et al.[86] Thyme feeding reduced the oxidation of liquid 1. Improvement of feed characteristics. Depending on the chemi-
yolk, but a comparative examination of the activity of various cal composition, there is an antimicrobial and proven antioxi-
antioxidants added to yolk suggested that thymol alone could dative effect on feed, especially of essential oils containing
not be responsible for the oxidative resistance of eggs from phenolic compounds, improving the shelf-life. To avoid losses
thyme-fed animals. and reactions with air, and with regard to further activities in
The fact that substances other than the essential oil compo- the animal body, essential oils and aroma compounds should
nents, e.g. rosmarinic acid, carnosol and carnosic acid, are at least be microencapsulated.[95] This also offers the advantage of a
as important as antioxidants was clearly demonstrated by feeding sustained effect. Results on palatability and the stimulation of
experiments with distillation residues on small ruminants. Sheep feed intake are contradictory. In general, the ‘sweeter’ essen-
and goats fed with 10–20% distilled rosemary or thyme in the tial oils taste (to humans), the better is the acceptance and the
diet for several months showed a higher antioxidant stability of more pungent, the more adverse effects have been noticed.
the meat, a higher concentration of polyphenolic antioxidants In any case, a period of adaptation would be helpful, espe-
in the meat, a higher concentration of polyphenolic antioxidants cially in pigs.
in the milk, lower susceptibility of oxidative stress in suckling 2. Improvement of digestion and performance. Well proven is an
goat kids and, finally, an increased content of polyphenols with overall stimulation of the zootechnical performance, espe-
antioxidant capacity in the cheese.[90–92] cially as regards the feed conversion rate. This might be due
336

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Essential oils and aromatic plants in animal feeding – a European perspective

to retarded gastric emptying and stabilization of the intestinal and essential oils, have to follow the safety regulations, i.e. the
microbiota and/or higher enzymatic activity, and therefore product has to be safe to the animal, to the user (farmer, worker),
better absorption of the digestible nutrients. The antimicro- to the consumer and to the environment.[7]
bial activity of essential oils is well demonstrated in vitro but In general, there is sufficient evidence that essential oils and
in only a few cases confirmed in vivo. A beneficial modification aromatic plants can be used as feed materials and additives for
of the ruminal flora has been verified, as has an effect as coc- the benefit of animals, the benefit of the farmer and last, but not
cidiostat and against clostridia in poultry. Another mode of least, the quality of the products. However, there are several
action is described as a slight irritation of the intestine tissues obstacles when evaluating the published results.
followed by pronounced mucus production, preventing the Quite often one can find confusion in the definitions of the
adhesion of enteropathogenic organisms. The overall benefit material used, and many authors are unable to differentiate
of this might be summarized as a favourable effect on the gut between herbs, extracts, (distilled) essential oils, isolated essen-
microbiota with less microbial activity in the small intestine tial oil compounds, synthetic compounds and other aromatic
and consequently less exposure to microbial toxins, reduced (plant) products. Within a single paper the terms may change,
innate immune defence and therefore better digestion. especially between extracts and essential oils, but also in using
3. Improved characteristics of animal products. Of particular the botanical and/or common plant name in the title and feeding
importance is the improved oxidative stability of the carcass, isolated (or synthetic) compounds according to material and
the meat and fat and the egg yolk, caused by several antioxi- methods. Especially when commercial products are used in a
dative compounds in essential oils or the respective plants. feeding experiment, caution is required, since other synthetic
Flavour might be beneficially or detrimentally influenced. substances may be added, adulterating the results.
Particular caution is required for some species, e.g. parsley and In a case where a herb is used as a feed additive, the botanical
caraway causing ‘off flavour’ of milk due to a carry-over of species might be unclear or undefined, especially if only the
some essential oil compounds. common name is used. For instance, there are dozens of species
in the world called ‘oregano’, belonging not only to the 39 species
Less is known about the possible interactions of essential of the genus Origanum, but also to other genera and plant
oils and aroma compounds with other substances, especially families (Table 8), all having more or less the sensorial properties
other feed additives. All feed additives, including aromatic herbs of oregano. In addition, the chemotype and especially the

Table 8. Different species called ‘oregano’ worldwide[96]

Family Species Commercial name(s) found in literature

Labiatae Calamintha potosina Schaf. oregano de la sierra, oregano, origanum
Coleus amboinicus Lour. (syn. C. aromaticus Benth) oregano, oregano brujo, oregano de Cartagena,
oregano de Espana, oregano Frances
Coleus aromaticus Benth. oregano de Espana, oregano, origanum
Hedeoma floribunda Standl. oregano, origanum
Hedeoma incana Torr. oregano
Hedeoma patens Jones oregano, origanum
Hyptis albida H.B.K. oregano, origanum
Hyptis americana (Aubl.) Urb. (H. gonocephala Gris.) oregano
Hyptis capitata Jacq. oregano, origanum
Hyptis pectinata Poit. oregano, origanum
Hyptis suaveolens (L.) Poit. oregano, oregano cimarron, origanum
Monarda austromontana Epling oregano, origanum
Ocimum basilicum L. oregano, origanum
Origanum compactum Benth. (syn. O. glandulosum Salzm, oregano, origanum
ex Benth.)
Origanum dictamnus L. (Majorana dictamnus L.) oregano, origanum
Origanum elongatum (Bonent) Emberger et Maire oregano, origanum
Origanum floribundum Munby (O. cinereum Noe) oregano, origanum
Origanum grosii Pau et Font Quer ex Letswaart oregano, origanum
Origanum majorana L. oregano
Origanum microphyllum (Benth) Vogel oregano, origanum
Origanum onites L. (syn. O. smyrneum L.) *Turkish oregano, oregano, origanum
Origanum scabrum Boiss et Heldr. (syn. O. pulchrum Boiss oregano, origanum
et Heldr.)
Origanum syriacum L. var. syriacum (syn. O. maru L.) oregano, origanum
Origanum vulgare L. subsp. gracile (Koch) Letswaart (syn. oregano, origanum
O. gracile Koch, O. tyttanthum Gontscharov)
Origanum vulgare subsp. hirtum (Link) Ietswaart (syn. O. *oregano, origanum
hirtum Link)
337

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 C. Franz et al.

Table 8. Continued

Family Species Commercial name(s) found in literature

Origanum vulgare subsp. virens (Hoffmanns et Link) oregano, origanum, oregano verde
letswaart (syn. O. virens Hoffmanns et Link)
Origanum vulgare subsp. viride (Boiss.) Hayek (syn. O. *Greek oregano, oregano, origanum
viride) Halacsy (syn. O. heracleoticum L.)
Origanum vulgare L. subsp. vulgare (syn. Thymus oregano, origanum
origanum (L.) Kuntze)
Origanum vulgare L. oregano, orenga, Oregano de Espana
Poliomintha longiflora Gray oregano
Salvia sp. oregano
Satureja thymbra L. oregano cabruno, oregano, origanum
Thymus capitatus (L.) Hoffmanns et Link (syn. *Spanish oregano, oregano, origanum
Coridothymus capitatus (L.) Rchb.f.)
Verbenaceae Lantana citrosa (Small) Modenke oregano xiu, oregano, origanum
Lantana glandulosissima Hayek oregano xiu, oregano silvestre, oregano,
origanum
Lantana hirsuta Mart. et Gall. oreganillo del monte, oregano, origanum
Lantana involucrata L. oregano, origanum
Lantana purpurea (Jacq.) Benth.& oregano, origanum
Hook. (syn. Lippia purpurea Jacq.) Lantana trifolia L. oregano, origanum
Lantana velutina Mart.&Gal. oregano xiu, oregano, origanum
Lippia myriocephala Schlecht.&Cham. oreganillo
Lippia affinis Schau. oregano
Lippia alba (Mill) N.E. Br. (syn. L. involucrata L.) oregano, origanum
Lippia Berlandieri Schau. oregano
Lippia cordiostegia Benth. oreganillo, oregano montes, oregano, origanum
Lippia formosa T.S.Brandeg. oregano, origanum
Lippia geisseana (R.A.Phil.) Soler. oregano, origanum
Lippia graveolens H.B.K. *Mexican oregano, oregano cimarron, oregano,
origanum
Lippia helleri Britton oregano del pais, oregano, origanum
Lippia micromera Schau. oregano del pais, oregano, origanum
Lippia micromera var. helleri (Britton) Moldenke oregano
Lippia origanoides H.B.K. oregano, origano del pais
Lippia palmeri var. spicata Rose oregano
Lippia palmeri Wats. oregano, origanum
Lippia umbellata Cav. oreganillo, oregano montes, oregano, origanum
Lippia velutina Mart. et Galeotti oregano, origanum
Rubiaceae Borreria sp. oreganos, oregano, origanum
Scrophulariaceae Limnophila stolonifera (Blanco) Merr. oregano, origanum
Apiaceae Eryngium foetidum L. oregano de Cartagena, oregano, origanum
Asteraceae Coleosanthus veronicaefolius H.B.K. oregano del cerro, oregano del monte, oregano
del campo
Eupatorium macrophyllum L. (syn. Hebeclinium oregano, origanum
macrophyllum DC.)
* Species of main economic importance, according to Lawrence and Reynolds.[97]

detailed chemical composition are frequently missing, since this often only general conclusions can be drawn concerning growth
is only voluntary information in reports on feed additives. A parameters and productivity, i.e. feed intake, weight gain and
similar situation is found with (commercial) essential oils – source feed conversion rate. This shows clearly that information on
unknown or at least undeclared, chemotype and/or composition essential oils and aromatic herbs as feed additives is still mainly
not mentioned in the paper. Finally, very often commercial prod- ‘product-driven’ instead of following a scientifically ‘function-
ucts are tested in ‘scientific papers’ where at best the (main) ingre- driven’ approach. Apart from the examples presented and
dients are mentioned only but the exact composition remains discussed here, there is still need for information regarding
undisclosed. absorption, distribution, metabolism and excretion (ADME)
A concise relationship between active principles (substances) and, in general, the mode of action of essential oils and their
and observed effects can only rarely be established; more components in animal nutrition, especially with respect to
338

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Essential oils and aromatic plants in animal feeding – a European perspective

animal health and welfare and the sensory and hygienic charac- 28. M. Jugl-Chizzola, J. Spergser, F. Schilcher, J. Noval, A. Bucher,
teristics of animal products. Nonetheless, the overall efficacy of C. Gabler, W. Hagmueller, K. Zitteri-Eglseer. Berl. Munch. Tierarztl.
Wochenschr. 2005, 118(11–12), 495.
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the quality of animal-derived food seems to be promising. Germany, 2002.
30. K. W. Lee, H. Everts, H. J. Kappert, M. Frehner, R. Losa, A. C. Beynen.
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