Skip to main content

Advertisement

Essential oil and aromatic plants as feed additives in non-ruminant nutrition: a review

Abstract

This paper summarizes the current knowledge regarding the possible modes of action and nutritional factors involved in the use of essential oils (EOs) for swine and poultry. EOs have recently attracted increased interest as feed additives to be fed to swine and poultry, possibly replacing the use of antibiotic growth promoters which have been prohibited in the European Union since 2006. In general, EOs enhance the production of digestive secretions and nutrient absorption, reduce pathogenic stress in the gut, exert antioxidant properties and reinforce the animal’s immune status, which help to explain the enhanced performance observed in swine and poultry. However, the mechanisms involved in causing this growth promotion are far from being elucidated, since data on the complex gut ecosystem, gut function, in vivo oxidative status and immune system are still lacking. In addition, limited information is available regarding the interaction between EOs and feed ingredients or other feed additives (especially pro- or prebiotics and organic acids). This knowledge may help feed formulators to better utilize EOs when they formulate diets for poultry and swine.

Introduction

Antibiotics fed at sub-therapeutic levels have been widely utilized in the swine and poultry industries to improve growth rate and efficiency of feed utilization, as well as reduce morbidity and mortality [1]. However, many countries have restricted or even banned (i.e. the European Union) the use of antibiotics as feed additives due to increased concerns regarding the transmission and the proliferation of resistant bacteria via the food chain. The restriction on the use of antibiotics as feed additives has driven nutritionists and feed manufacturers to develop alternatives such as organic acids, feed enzymes, and pro- or pre-biotics. These substances are well established in animal nutrition. In contrast, plant extracts, especially EOs, are a new class of feed additives and knowledge regarding their modes of action and aspects of application are still rather rudimentary [2].

In recent years, EOs have attracted increased attention from the swine and poultry industries. However, they are not simple compounds, rather a mixture of various compounds (mainly terpenes and terpene derivatives) [3], which are concentrated hydrophobic liquids containing volatile aromatic compounds obtained from plants [4]. In terms of biological activity and effects, each individual chemical constituent has its own characteristic properties. This means that EOs are of a complex character with rather diverse effects. Furthermore, factors such as species, ecological factors and climatic conditions, harvest time, part of plant used and method of isolation all affect the chemical composition of EOs [4]. This variability complicates the assessment and application of EOs. The purpose of this paper is to provide an overview of the published data on the general applications of EOs in swine and poultry and discuss possible modes of action based on an in vivo model.

Performance response generated by EOs

Numerous studies have documented the benefits of EOs on the performance of swine and poultry. Franz et al. [5] reviewed 8 reports with piglets and Windisch et al. [2] reviewed 11 reports with poultry. They reported that the average improvement in weight gain, feed intake and feed conversion induced by EOs were 2.0, 0.9 and 3.0% for piglets and 0.5, −1.6 and −2.6% for poultry, respectively. We collected data missed in the 2 reviews, as well as recently published data. For piglets, the improvement in performance was on average 10 and 3% while in poultry the improvement in performance was 3 and 3% for weight gain and feed conversion, respectively (Table 1). The different results for the two species are possibly caused by the different digestive physiology, the origin of the EOs or herb species, the quantity added to the feed and the environmental conditions used in the trial.

Table 1 Effects of essential oils and aromatic plants on the performance of swine and poultry

Another important consideration is the stability of EOs during feed processing. Maenner et al. [15] reported a considerable loss of activity of EOs when a pelleting temperature of 58°C was applied. These figures are smaller compared with conventional in-feed antibiotics, where advantages of 16.9% in weight gain (piglets) are reported in the literature [1]. However, in a recent feeding trial, Li et al. [19] compared the performance of piglets fed an unsupplemented control diet with that of piglets fed a diet supplemented with antibiotics or a combination of thymol and cinnamaldehye (Table 2). Weight gain, feed conversion and fecal consistency of pigs fed EOs was essentially equal to that of pigs fed antibiotics.

Table 2 Effect of dietary essential oil and antibiotics on the performance and fecal consistency of weanling pigs 1

Aromatic herbs and EOs are often claimed to improve the flavor and palatability of feed, thus increasing voluntary feed intake resulting in improved weight gain. However, in a choice feed experiment conducted in growing pigs by Schöne et al. [12], the classification of fennel and caraway oils as flavor additives or as ‘appetite promoters’ in diets for pigs was questioned. Unfortunately, only 12 castrated male pigs (28 ± 1 kg) were used with 3 treatments and only a 4 day trial duration, which is weak due to the low level of replication and short feeding period used. Pigs may need a few days to adapt to the special flavor of EOs. Further studies are expected in this field to justify the assumption that herbs, spices and their extracts improve feed intake in pigs.

The application of EOs and aromatic plants in grower-finisher pigs seems unsuccessful. Janz et al. [21] and Yan et al. [22] failed to observe any improvement in performance generated by EOs or aromatic plants in finisher pigs. However, supplementation of EOs in sow diets, especially in lactation sow diets, has been attracting increasing interest. Miller et al. [36] reported that supplementation with 2 g/kg of a blend of EOs (Biomin P. E. P.), from 10 days prior to the estimated farrowing date through to weaning, improved the early lactation feed intake of sows, decreased sow weight loss during the first week of lactation and enhanced piglet body weight at weaning. In a study involving 2100 sows, Allan and Bilkei [37] reported that sows fed diets containing 1 g/kg oregano had higher voluntary feed intake, lower annual mortality rate (4.0 vs. 6.9%), reduced sow culling rate during lactation (8 vs. 14%), increased farrowing rate (77.0 vs. 69.9%), increased number of live born piglets per litter (10.49 vs. 9.95) and decreased stillbirth rate (0.91 vs. 0.81). Similar benefits generated by the feeding of EOs to sows have been reported by other authors [38-40].

Regulation of gut microflora

EOs and aromatic plants are well known to exert antibacterial, antifungal and antiviral activity in in vitro experiments [2]. It is generally accepted that EOs are slightly more active against gram-positive than gram-negative bacteria [41,42]. The EO showed dose-dependent effects on cell integrity, as measured using propidium iodide, of Gram-positive bacteria. However, growth inhibition of Gram-negative bacteria, in contrast, occurred mostly without cell integrity loss [43]. Comparable in vivo studies also found inhibiting effects against pathogens such as C. perfringens, E. coli or Eimeria species (Table 3). The controlled pathogen load also contributed to healthy microbial metabolites, improved intestinal integrity and protection against enteric disease [44-47].

Table 3 Effects of essential oils and aromatic plants on the microflora in swine and poultry

Attention should also be paid to the potential negative effects induced by EOs on healthy intestinal bacteria. Horošová et al. [53] reported that oregano EO exhibited a strong bactericidal effect against Lactobacilli isolated from fecal samples of chickens fed diets with oregano. In a vivo anti-bacteria study, Thapa et al. [43] found that the beneficial commensal Faecalibacterium prausnitzii was sensitive to EO at similar or even lower concentrations than the pathogens. In addition, Cross et al. [28] and Muhl and Liebert [48] reported that EOs had no effect on the microbial population and composition in the digestive tract or fecal excretions of broilers and pigs.

In a review, Brenes and Roura [41] contended that minor components are critical to the bacteriostatic activity of EOs and may have synergistic effects. For example, carvacrol and thymol, the two structurally similar major components of oregano essential oil, were found to give an additive effect when tested against S. aureus and P. aeruginosa [57]. Cymene, a biological precursor of carvacrol, was found to have a higher preference for liposomal membranes, thereby causing more expansion. By this mechanism cymene probably enables carvacrol to be more easily transported into the cell so that a synergistic effect is achieved when the two are used together [58]. However, the major components of EOs obtained from conifers were reported to be more bacteriostatic than the crude essential oil of fir and pine, but were less active or had similar activity as the EO of spruce for L. monocytogenes 4 b and ½ c [40,59,60]. Therefore, it is likely that the other components, or combinations of the different major components, have double-edged effects (negative or positive) on the antimicrobial activity of the EOs from fir and pine. These studies indicate that there is still much work to do in order to develop a blend of EOs with better antimicrobial properties.

Impact on nutrient absorption and gut morphology

EOs have been documented to improve nutrient digestibility in swine [15,19,21,61] and poultry [25,62]. The improvement in nutrient absorption may be partly explained by increased secretions of saliva, bile and enhanced enzyme activity [56,63-65]. However, Muhl and Liebert [66] did not observe improved nutrient digestibility and enhanced pancreatic and duodenal activity of trypsin and amylase in weaned piglets fed diets containing a phytogenic product having carvacrol, thymol and tannins as key constituents. The inconsistent results in apparent digestibility may be caused by endogenous loss resulting from a stimulated secretion of mucus induced by plant extracts [67].

The improved nutrient absorption may allow appropriate modifications to diet nutrient density. In a randomized complete block design, Zeng et al. [20] investigated the acceptance of commercial EOs in low energy density weaned pig diets with wheat and extruded full-fat soybean as the major ingredients. The piglets could freely choose between a standard energy density diet (DE = 3,400 kcal/kg) or a low energy density diet (DE = 3,250 kcal/kg) with 0 or 0.25 g/kg EOs (4.5% cinnamaldehyde and 13.5% thymol). EO supplementation significantly increased weight gain and improved the apparent digestibility of dry matter, crude protein and energy compared with pigs fed the low energy density control diet. Supplementation of EOs to a low-energy pig diet has beneficial effects and leads to similar performance compared with a standard energy density diet (Table 4).

Table 4 Effects of dietary essential oil on the performance, fecal consistency and nutrient digestibility of weaned pigs 1

Decreased numbers of pathogenic bacteria in the gut may improve the ability of epithelial cells to regenerated villus and thus enhance intestinal absorptive capacity [68]. It is reasonable to expect such an effect by EOs due to their well-documented inhibitory effects against pathogens. However, the literature is equivocal regarding the use of EOs as feed additives in relation to gut morphology. There are reports that show increased, unchanged as well as reduced villus length and crypt depth in the jejunum and colon for broilers and piglets fed EOs [6,10,19,20,52,69]. Considering the different reactions in gut morphology, Windusch et al. [70] hypothesized that one aspect of the phytogenic action of EOs seems to be irritation of intestinal tissues leading to reduced intestinal surface. In contrast, beneficial effects on gut health (i.e. reduced pathogen pressure) could favor increased villus length and gut surface. Consequently, the overall impact of EOs on gut morphology seems to depend on the balance between tissue irritation and beneficial effects on intestinal hygiene.

Immune status

The gastrointestinal tract’s immune system is often referred to as gut-associated lymphoid tissue (GALT), which possesses the largest mass of lymphoid tissue and plays an important role in antigen defense in the human body [71]. In the results presented by Kroismayr et al. [72], using the techniques of quantitative real time-PCR and gut tissue morphology, EO and avilamycin significantly decreased the expression of the transcriptional factor NFκB, the apoptotic marker TNFα and the size of Peyer’s patches in the intestine of weaned piglets, as well as the proliferation marker cyclin D1 in the colon, mesenteric lymph nodes and spleen. Reduced numbers of intraepithelial lymphocytes in the jejunum and reduced B lymphocytes in mesenteric lymph nodes were also observed by Manzanilla et al. [10,69] and Nofrairas et al. [11]. This might serve as direct evidence for a lower need for immune defense activity in the gut due to the antimicrobial action of EOs. The relieved intestinal immune defense stress may partly contribute to nutrient allocation towards growth rather than immune defense.

Investigations conducted under practical conditions of large-scale animal production have shown better responses to EO treatment than more recent studies conducted under controlled experimental conditions with a higher level of hygiene [5]. This might be explained by a lower pathogen pressure in the intestine and an improved immune status. Supplementing EOs has been reported to improve the immune status of piglets after weaning, as indicated by an increase in lymphocyte proliferation rate, phagocytosis rate, as well as in IgG, IgA, IgM, C3 and C4 serum levels [16,19,20]. Walter et al. [73] reported that pigs fed a diet with 3 g/kg oregano (60 g carvacrol and 55 g thymol per kilogram) had higher proportions of CD4:CD8, MHC class II antigens, and non-T/non-B cells in peripheral blood lymphocytes compared with pigs fed a control diet.

The bioactive substances are quickly absorbed after oral, pulmonary, or dermal administration and most are metabolized and either eliminated by the kidneys in the form of glucuronide or exhaled as CO2 [74]. The absorbed component might initiate an immune response indicated by changes in blood immunological parameters while the unabsorbed component may contribute to relief from intestinal immune defense stress. However, the precise mechanisms through which EOs function are not clear and further investigations are necessary.

Anti-oxidative effects

Stability is very important to minced meat during further processing or after cooking, or as surface treatments for whole cuts prior to storage. In order to prolong the storage stability of foods, synthetic antioxidants are used for industrial processing. Nevertheless, the use of some of the common synthetic antioxidants such as butylated hydroxytoluene (BHT) and butylated hydroxyanisole (BHA) has come into question due to their suspected carcinogenic potential as evidenced by toxicologists [75]. In addition, a general consumer rejection of synthetic food additives has been observed in recent times. For these reasons, there is an increasing interest in studies involving natural additives for use as potential antioxidants.

Herbs of the Labiatae family, particularly rosemary, oregano and sage, have been extensively studied for their antioxidant activity [41]. The potential of dietary EOs and aromatic plants to improve the oxidative stability of meat obtained from broilers, hens or turkeys, has been demonstrated in a series of studies [76-83]. However, Simitzis et al. [84] and Janz et al. [21] reported that dietary oregano EO failed to improve the lipid oxidation status of pork. This may be explained by the different fatty acid composition in the meat of poultry and swine. Although poultry meat contains a low lipid content, its relative concentration of polyunsaturated fatty acids is higher (60 vs 17%, of total fat content) than pork [21,85]. Thus, poultry meat is particularly susceptible to oxidative deterioration, which might contribute to a robust response on the lipid oxidation status of poultry meat that was generated by dietary EOs supplementation.

Beside benefits on meat quality, EOs or plant extracts are also reported to improve redox balance in different organs [55,86], and attenuate oxidative injury induced by different physiological stressors [87-89]. Table 5 shows the results of an experiment where different concentrations of ginger root powder and its EOs were fed to broilers raised under heat stress conditions [33]. Broilers which received 150 mg/kg ginger EO had increased total superoxide dismutase (TSOD) activity and decreased malondialdehyde (MDA) concentrations in the liver compared with a control group. Dietary supplementation of vitamin E, ginger root powder or its EO, increased total antioxidant capacity (TAC) and decreased MDA concentrations in serum compared with a control group.

Table 5 Effect of ginger herb and its essential oil on antioxidant parameters and malondialdehyde in the erythrocytes, serum and liver of broilers raised under heat stress 1

The efficacy of EOs

There is limited information concerning the interaction between EOs and nutritional factors (such as nutrient level, type of basal diet, as well as synergistic or antagonistic effects with other feed additives). Jamroz et al. [67] investigated the influence of diet type (corn vs. wheat and barley) on the ability of plant extracts (100 mg/kg containing 5% carvacrol, 3% cinnamaldehyde and 2% of capsicum oleoresinon) to modify morphological and histochemical characteristics of the stomach and jenunal walls in chickens. Their results showed significantly more jenunal wall villi in chickens fed the maize diet supplemented with plant extracts.

The incorporation of carvacrol, cinnamaldehyde, and capsicum oleoresin promotes positive and negative changes in digestive function, intestinal epithelium, microbial ecology, and fermentation in weaned pigs depending on the amount of protein included in the diet [69]. In a study conducted to investigate the effects of three doses of individual and combined dietary supplements of specific blends of organic acids and EOs on broiler performance, Bozkurt et al. [90] concluded that a combination of acidifiers and EOs may allow a reduced dosage to be used due to their synergistic effects.

Conclusions

The search for alternatives to antibiotics has generated considerable interest in recent years. The new generation of feed additives includes herbs and essential oils, and their beneficial effects for animal production have been well documented [2].

Although most of the latest research has noted the major components and original sources of EOs in vivo trials, only a few papers have identified the quantity of the principle components present. In addition, Brenes and Roura [41] argued that minor components present are critical to the activity of EOs and may have a synergistic influence. Sometimes the minor components may counteract the exerted effects. Therefore, in the future, the detailed constituents of EOs are needed to be determined in order to assess their different biological effects. In this way, it may be possible to compare different EO products and formulate mixtures that optimize their efficacy.

References

  1. 1.

    Cromwell GL. Why and how antibiotics are used in swine production. Anim Biotechnol. 2002;13:7–27.

  2. 2.

    Windisch W, Schedle K, Plitzner C, Kroismayr A. Use of phytogenic products as feed additives for swine and poultry. J Anim Sci. 2008;86(E. suppl):E140–8.

  3. 3.

    Başer KHC, Demirci F. Chemistry of Essential Oils. In: Flavours and Fragrances: Chemistry, Bioprocessing and Sustainability, edited by Berger RG. New York: Springer; 2007. p. 43–86.

  4. 4.

    Màthé A. Essential oils–biochemistry, production and utilisation. In: Phytogenics in Animal Nutrition, Natural Concepts to Optimize Gut Health and Performance, edited by Steiner T. Nottingham University Press 2009. p 1–18.

  5. 5.

    Franz C, Baser K, Windisch W. Essential oils and aromatic plants in animal feeding–a European perspective. A review Flavour Frag J. 2010;25:327–40.

  6. 6.

    Manzanilla EG, Perez JF, Martin M, Kamel C, Baucells F, Gasa J. Effect of plant extracts and formic acid on the intestinal equilibrium of early-weaned pigs. J Anim Sci. 2004;82:3210–8.

  7. 7.

    Namkung H, Li J, Gong M, Yu H, Cottrill M, de Lange CFM. Impact of feeding blends of organic acids and herbal extracts on growth performance, gut microbiota and digestive function in newly weaned pigs. Can J Anim Sci. 2004;84:697–704.

  8. 8.

    Cho JH, Chen YJ, Min BJ, Kim HJ, Kwon OS, Shon KS, et al. Effects of essential oils supplementation on growth performance. IgG concentration and fecal noxious gas concentration of weaned pigs. Asian-Austrial J Anim Sci. 2006;19:80.

  9. 9.

    Kommera SK, Mateo RD, Neher FJ, Kim SW. Phytobiotics and organic acids as potential alternatives to the use of antibiotics in nursery pig diets. Asian-Austrial J Anim Sci. 2006;19:1784.

  10. 10.

    Manzanilla EG, Nofrarias M, Anguita M, Castillo M, Perez JF, Martin-Orue SM, et al. Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. J Anim Sci. 2006;84:2743–51.

  11. 11.

    Nofrarias M. Effects of spray-dried porcine plasma and plant extracts on intestinal morphology and on leukocyte cell subsets of weaned pigs. J Anim Sci. 2006;84:2735–42.

  12. 12.

    Schöne F, Vetter A, Hartung H, Bergmann H, Biertümpfel A, Richter G, et al. Effects of essential oils from fennel (Foeniculi aetheroleum) and caraway (Carvi aetheroleum) in pigs. J Anim Physiol An N. 2006;90:500–10.

  13. 13.

    Yan L, Meng QW, Kim IH. The effect of an herb extract mixture on growth performance, nutrient digestibility, blood characteristics and fecal noxious gas content in growing pigs. Livest Sci. 2011;141:143–7.

  14. 14.

    Huang Y, Yoo JS, Kim HJ, Wang Y, Chen YJ, Cho JH, et al. Effects of dietary supplementation with blended essential oils on growth performance, nutrient digestibility, blood profiles and fecal characteristics in weanling pigs. Asian-Austral J Anim Sci. 2010;23:607–13.

  15. 15.

    Maenner K, Vahjen W, Simon O. Studies on the effects of essential-oil-based feed additives on performance, ileal nutrient digestibility, and selected bacterial groups in the gastrointestinal tract of piglets. J Anim Sci. 2011;89:2106–12.

  16. 16.

    Li SY, Ru YJ, Liu M, Xu B, Péron A, Shi XG. The effect of essential oils on performance, immunity and gut microbial population in weaner pigs. Livest Sci. 2012;145:119–23.

  17. 17.

    Zhang S, Jung JH, Kim HS, Kim BY, Kim IH. Influences of phytoncide supplementation on growth performance, nutrient digestibility, blood profiles, diarrhea scores and fecal microflora shedding in weaning pigs. Asian-Austral J Anim Sci. 2012;25:1309–15.

  18. 18.

    Huang CW, Lee TT, Shih YC, Yu B. Effects of dietary supplementation of Chinese medicinal herbs on polymorphonuclear neutrophil immune activity and small intestinal morphology in weanling pigs. J Anim Physiol An N. 2012;96:285–94.

  19. 19.

    Li PF, Piao XS, Ru YJ, Han X, Xue LF, Zhang HY. Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health. Asian-Australas J Anim Sci. 2012;25:1617–26.

  20. 20.

    Zeng ZK, Xu X, Zhang Q, Li P, Zhao PF, Li QY, et al. Effects of essential oil supplementation of a Low-Energy diet on performance, intestinal morphology and microflora, immune properties and antioxidant activities in weaned pigs. Anim Sci J. 2014. doi:10.1111/asj.12277 (Published online).

  21. 21.

    Janz JAM, Morel PCH, Wilkinson BHP, Purchas RW. Preliminary investigation of the effects of low-level dietary inclusion of fragrant essential oils and oleoresins on pig performance and pork quality. Meat Sci. 2007;75:350–5.

  22. 22.

    Yan L, Wang JP, Kim HJ, Meng QW, Ao X, Hong SM, et al. Influence of essential oil supplementation and diets with different nutrient densities on growth performance, nutrient digestibility, blood characteristics, meat quality and fecal noxious gas content in grower–finisher pigs. Livest Sci. 2010;128:115–22.

  23. 23.

    Jang IS, Ko YH, Kang SY, Lee CY. Effect of a commercial essential oil on growth performance, digestive enzyme activity and intestinal microflora population in broiler chickens. Anim Feed Sci Tech. 2007;134:304–15.

  24. 24.

    Isabel B, Santos Y. Effects of dietary organic acids and essential oils on growth performance and carcass characteristics of broiler chickens. J Appl Poult Res. 2009;18:472–6.

  25. 25.

    Basmacioglu Malayoglu H, Baysal S, Misirlioglu Z, Polat M, Yilmaz H, Turan N. Effects of oregano essential oil with or without feed enzymes on growth performance, digestive enzyme, nutrient digestibility, lipid metabolism and immune response of broilers fed on wheat-soybean meal diets. Brit Poult Sci. 2010;51:67–80.

  26. 26.

    Kirkpinar F, Unlu HB, Ozdemir G. Effects of oregano and garlic essential oils on performance, carcase, organ and blood characteristics and intestinal microflora of broilers. Livest Sci. 2011;137:219–25.

  27. 27.

    Amerah AM, Peron A, Zaefarian F, Ravindran V. Influence of whole wheat inclusion and a blend of essential oils on the performance, nutrient utilisation, digestive tract development and ileal microbiota profile of broiler chickens. Brit Poult Sci. 2011;52:124–32.

  28. 28.

    Cross DE, Mcdevitt RM, Hillman K, Acamovic T. The effect of herbs and their associated essential oils on performance, dietary digestibility and gut microflora in chickens from 7 to 28 days of age. Brit Poult Sci. 2007;48:496–506.

  29. 29.

    Roofchaee A, Irani M, Ebrahimzadeh MA, Akbari MR. Effect of dietary oregano (Origanum vulgare L.) essential oil on growth performance, cecal microflora and serum antioxidant activity of broiler chickens. Afr J Biotechnol. 2011;10:6177–83.

  30. 30.

    Hong JC, Steiner T, Aufy A, Lien TF. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livest Sci. 2012;144:253–62.

  31. 31.

    Alali WQ, Hofacre CL, Mathis GF, Faltys G. Effect of essential oil compound on shedding and colonization of Salmonella enterica serovar Heidelberg in broilers. Poult Sci. 2013;92:836–41.

  32. 32.

    Khattak F, Ronchi A, Castelli P, Sparks N. Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poult Sci. 2014;93:132–7.

  33. 33.

    Habibi R, Sadeghi G, Karimi A. Effect of different concentrations of ginger root powder and its essential oil on growth performance, serum metabolites and antioxidant status in broiler chicks under heat stress. Brit Poult Sci. 2014;55:228–37.

  34. 34.

    Aguilar CAL, Lima KRDS, Manno MC, Maia JGS, Fernandes Neto DL, Tavares FB, et al. Rosewood ( Aniba rosaeodora Ducke) oil in broiler chickens diet. Revista Brasileira de Saude e Producao Animal 2014, 15.

  35. 35.

    Giannenas I, Papaneophytou CP, Tsalie E, Pappas I, Triantafillou E, Tontis D, et al. Dietary supplementation of benzoic acid and essential oil compounds affects buffering capacity of the feeds, performance of turkey poults and their antioxidant status, pH in the digestive tract, intestinal microbiota and morphology. Asian-Austral J Anim Sci. 2014;27:225–36.

  36. 36.

    Miller JA, Laurenz JC, Rounsavall JW, Burdick NC, Neher FJ. Enhancing feed intake by the sow during lactation using BIOMIN® PEP. In Phytogenics in Animal Nutrition: Natural Concepts To Optimize Gut Health and Performance, edited by Steiner T. Nottingham University Press 2009. p 87–96.

  37. 37.

    Allan P, Bilkei G. Oregano improves reproductive performance of sows. Theriogenology. 2005;63:716–21.

  38. 38.

    Khajarern J, Khajarern S. The efficacy of origanum essential oils in sow feed. Int Pig Topics. 2002;17:17.

  39. 39.

    Kis RK, Bilkei G. Effect of a phytogenic feed additive on weaning-to-estrus interval and farrowing rate in sows. J Swine Health Prod. 2003;11:296–9.

  40. 40.

    Cabrera R, Jordan N, Wilson M, Hedges J, Knott J, Fent R, et al. Oregano Essential Oil in Sow Diets Improves Sows and Piglet Performance, Paper read at American Association of Swine Veterinarians. 2008. internet: http://www.aasp.org/cdrom/ (accessed 02.03.2009).

  41. 41.

    Brenes A, Roura E. Essential oils in poultry nutrition: main effects and modes of action. Anim Feed Sci Tech. 2010;158:1–14.

  42. 42.

    Burt S. Essential oils: Their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol. 2004;94:223–53.

  43. 43.

    Thapa D, Losa R, Zweifel B, Wallace RJ. Sensitivity of pathogenic and commensal bacteria from the human colon to essential oils. Microbiology. 2012;158:2870–7.

  44. 44.

    Placha I, Chrastinova L, Laukova A, Cobanova K, Takacova J, Strompfova V, et al. Effect of thyme oil on small intestine integrity and antioxidant status, phagocytic activity and gastrointestinal microbiota in rabbits. 2013;61:197–208.

  45. 45.

    Tiihonen K, Kettunen H, Bento MH, Saarinen M, Lahtinen S, Ouwehand AC, et al. The effect of feeding essential oils on broiler performance and gut microbiota. Br Poult Sci. 2010;51:381–92.

  46. 46.

    Oviedo-Rondón EO, Hume ME, Hernández C, Clemente-Hernández S. Intestinal microbial ecology of broilers vaccinated and challenged with mixed Eimeria species, and supplemented with essential oil blends. Poult Sci. 2006;85:854–60.

  47. 47.

    Baker J, Brown K, Rajendiran E, Yip A, Decoffe D, Dai C, et al. Medicinal Lavender Modulates the Enteric Microbiota to Protect Against Citrobacter Rodentium-Induced Colitis. 2012. p. G825–36.

  48. 48.

    Muhl A, Liebert F. Growth and parameters of microflora in intestinal and faecal samples of piglets due to application of a phytogenic feed additive. J Anim Physiol An N. 2007;91:411–8.

  49. 49.

    Giannenas I, Florou-Paneri P, Papazahariadou M, Christaki E, Botsoglou NA, Spais AB. Effect of dietary supplementation with oregano essential oil on performance of broilers after experimental infection with Eimeria tenella. Arch Anim Nutr. 2003;57:99–106.

  50. 50.

    Waldenstedt L. Effect of vaccination against coccidiosis in combination with an antibacterial oregano (Origanum vulgare) compound in organic broiler production. Acta Agr Scand A-An. 2003;53:101–9.

  51. 51.

    Mitsch P, Zitterl-Eglseer K, Köhler B, Gabler C, Losa R, Zimpernik I. The effect of two different blends of essential oil components on the proliferation of Clostridium perfringens in the intestines of broiler chickens. Poult Sci. 2004;83:669–75.

  52. 52.

    Jamroz D, Wiliczkiewicz A, Wertelecki T, Orda J, Skorupińska J. Use of active substances of plant origin in chicken diets based on maize and locally grown cereals. Brit Poult Sci. 2005;46:485–93.

  53. 53.

    Horošová K, Bujňáková D, Kmeť V. Effect of oregano essential oil on chicken lactobacilli andE. Coli Folia Microbiol. 2006;51:278–80.

  54. 54.

    Rahimi S, Zadeh ZT, Torshizi M, Omidbaigi R, Rokni H. Effect of the three herbal extracts on growth performance, immune system, blood factors and intestinal selected bacterial population in broiler chickens. J Agr Sci Tech-Iran. 2011;13:527–39.

  55. 55.

    Placha I, Takacova J, Ryzner M, Cobanova K, Laukova A, Strompfova V, et al. Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. Brit Poult Sci. 2014;55:105–14.

  56. 56.

    Jang IS, Ko YH, Yang HY, Ha JS, Kim JY, Kim JY, et al. Influence of essential oil components on growth performance and the functional activity of the pancreas and small intestine in broiler chickens. Asian-Austrial J Anim Sci. 2004;17:394–400.

  57. 57.

    Lambert R, Skandamis PN, Coote PJ, Nychas GJ. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol. 2001;91:453–62.

  58. 58.

    Ultee A, Bennik M, Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microb. 2002;68:1561–8.

  59. 59.

    Mourey A, Canillac N. Anti-Listeria monocytogenes activity of essential oils components of conifers. Food Control. 2002;13:289–92.

  60. 60.

    Canillac N, Mourey A. Antibacterial activity of the essential oil of Picea excelsa on Listeria, Staphylococcus aureus and coliform bacteria. Food Microbiol. 2001;18:261–8.

  61. 61.

    Ahmed ST, Hossain ME, Kim GM, Hwang JA, Ji H, Yang CJ. Effects of resveratrol and essential oils on growth performance, immunity, digestibility and fecal microbial shedding in challenged piglets. Asian-Austral J Anim Sci. 2013;26:683–90.

  62. 62.

    Emami NK, Samie A, Rahmani HR, Ruiz-Feria CA. The effect of peppermint essential oil and fructooligosaccharides, as alternatives to virginiamycin, on growth performance, digestibility, gut morphology and immune response of male broilers. Anim Feed Sci Tech. 2012;175:57–64.

  63. 63.

    Lee K, Everts H, Kappert HJ, Frehner M, Losa R, Beynen AC. Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. Brit Poult Sci. 2003;44:450–7.

  64. 64.

    Platel K, Srinivasan K. Influence of dietary spices and their active principles on pancreatic digestive enzymes in albino rats. Food Nahrung. 2000;44:42–6.

  65. 65.

    Platel K, Srinivasan K. Stimulatory influence of select spices on bile secretion in rats. Nutr Res. 2000;20:1493–503.

  66. 66.

    Muhl A, Liebert F. No impact of a phytogenic feed additive on digestion and unspecific immune reaction in piglets. J Anim Physiol An N. 2007;91:426–31.

  67. 67.

    Jamroz D, Wertelecki T, Houszka M, Kamel C. Influence of diet type on the inclusion of plant origin active substances on morphological and histochemical characteristics of the stomach and jejunum walls in chicken. J Anim Physiol An N. 2006;90:255–68.

  68. 68.

    Mourão JL, Pinheiro V, Alves A, Guedes CM, Pinto L, Saavedra MJ, et al. Effect of mannan oligosaccharides on the performance, intestinal morphology and cecal fermentation of fattening rabbits. Anim Feed Sci Tech. 2006;126:107–20.

  69. 69.

    Manzanilla EG, Pérez JF, Martín M, Blandón JC, Baucells F, Kamel C, et al. Dietary protein modifies effect of plant extracts in the intestinal ecosystem of the pig at weaning. J Anim Sci. 2009;87:2029–37.

  70. 70.

    Windisch W, Rohrer E, Schedle K. Phytogenic feed additives to young piglets and poultry: Mechanisms and application. In Phytogenics in Animal Nutrition: Natural Concepts To Optimize Gut Health and Performance, edited by Steiner T. Nottingham University Press. 2009. p19–39.

  71. 71.

    Salminen S, Bouley C, Boutron M, Cummings JH, Franck A, Gibson GR, et al. Functional food science and gastrointestinal physiology and function. Brit J Nutr. 1998;80:S147–71.

  72. 72.

    Kroismayr A, Sehm J, Pfaffl MW, Schedle K, Plitzner C, Windisch W. Effects of avilamycin and essential oils on mRNA expression of apoptotic and inflammatory markers and gut morphology of piglets. Czech J Anim Sci. 2008;53:377–87.

  73. 73.

    Walter BM, Bilkei G. Immunostimulatory effect of dietary oregano etheric oils on lymphocytes from growth-retarded, low-weight growing-finishing pigs and productivity. Tijdschr Diergeneeskd. 2004;129:178–81.

  74. 74.

    Kohlert C, Van Rensen I, März R, Schindler G, Graefe EU, Veit M. Bioavailability and pharmacokinetics of natural volatile terpenes in animals and humans. Planta Med. 2000;66:495–505.

  75. 75.

    Shahidi F. Antioxidants in food and food antioxidants. Food Nahrung. 2000;44:158–63.

  76. 76.

    Marcinčák S, Cabadaj R. Popelka P, šoltýsová L. Antioxidative effect of oregano supplemented to broilers on oxidative stability of poultry meat Slov Vet Res. 2008;45:61–6.

  77. 77.

    Florou-Paneri P, Giannenas I, Christaki E, Govaris A, Botsoglou N. Performance of chickens and oxidative stability of the produced meat as affected by feed supplementation with oregano, vitamin C, vitamin E and their combinations. Arch Geflugelkd. 2006;70:232–40.

  78. 78.

    Giannenas IA, Florou-Paneri P, Botsoglou NA, Christaki E, Spais AB. Effect of supplementing feed with oregano and/or alpha-tocopheryl acetate on growth of broiler chickens and oxidative stability of meat. J Anim Feed Sci. 2005;14:521–35.

  79. 79.

    Botsoglou N, Florou-Paneri P, Botsoglou E, Dotas V, Giannenas I, Koidis A, et al. The effect of feeding rosemary, oregano, saffron and a-tocopheryl acetate on hen performance and oxidative stability of eggs. S Afr J Anim Sci. 2005;35:143–51.

  80. 80.

    Botsoglou NA, Christaki E, Florou-Paneri P, Giannenas I, Papageorgiou G, Spais AB. The effect of a mixture of herbal essential oils or á-tocopheryl acetate on performance parameters and oxidation of body lipid in broilers. S Afr J Anim Sci. 2004;34:52–61.

  81. 81.

    Botsoglou NA, Florou-Paneri P, Christaki E, Fletouris DJ, Spais AB. Effect of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues. Brit Poult Sci. 2002;43:223–30.

  82. 82.

    Govaris A, Botsoglou N, Papageorgiou G, Botsoglou E, Ambrosiadis I. Dietary versus post-mortem use of oregano oil and/or α-tocopherol in turkeys to inhibit development of lipid oxidation in meat during refrigerated storage. Int J Food Sci Nutr. 2004;55:115–23.

  83. 83.

    Papageorgiou G, Botsoglou N, Govaris A, Giannenas I, Iliadis S, Botsoglou E. Effect of dietary oregano oil and α‐tocopheryl acetate supplementation on iron‐induced lipid oxidation of turkey breast, thigh, liver and heart tissues. J Anim Physiol An N. 2003;87:324–35.

  84. 84.

    Simitzis PE, Symeon GK, Charismiadou MA, Bizelis JA, Deligeorgis SG. The effects of dietary oregano oil supplementation on pig meat characteristics. Meat Sci. 2010;84:670–6.

  85. 85.

    Hrdinka C, Zollitsch W, Knaus W, Lettner F. Effects of dietary fatty acid pattern on melting point and composition of adipose tissues and intramuscular fat of broiler carcasses. Poult Sci. 1996;75:208–15.

  86. 86.

    Lu T, Piao XL, Zhang Q, Wang D, Piao XS, Kim SW. Protective effects of Forsythia suspensa extract against oxidative stress induced by diquat in rats. Food Chem Toxicol. 2010;48:764–70.

  87. 87.

    Zeng ZK, Li QY, Piao XS, Liu JD, Zhao PF, Xu X, et al. Forsythia suspensa extract attenuates corticosterone-induced growth inhibition, oxidative injury, and immune depression in broilers. Poult Sci. 2014;93:1–8.

  88. 88.

    Zhang HY, Piao XS, Zhang Q, Li P, Yi JQ, Liu JD, et al. The effects of forsythia suspensa extract and berberine on growth performance, immunity, antioxidant activities, and intestinal microbiota in broilers under high stocking density. Poult Sci. 2013;92:1981–8.

  89. 89.

    Wang L, Piao XL, Kim SW, Piao XS, Shen YB, Lee HS. Effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities in broiler chickens under high ambient temperature. Poult Sci. 2008;87:1287–94.

  90. 90.

    Bozkurt M. Küçükyilmaz K, çatli AU, çinar M, çabuk M. Alçiçek A Effects of administering an essential oil mixture and an organic acid blend separately and combined to diets on broiler performance Arch Geflügelk. 2012;2:81–7.

Download references

Author information

Correspondence to Xiangshu Piao.

Additional information

Authors’ contributions

ZZ carried out the literature review and manuscript writing. SZ, HW and XP participated in literature review. All authors read and approved the final manuscript.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Keywords

  • Antimicrobial
  • Antioxidant
  • Essential oils
  • Feed additives
  • Growth promoter
  • Gut function
  • Immunity