Botanical alternatives to antibiotics for use in organic poultry production1

Sandra Diaz-Sanchez, Doris DSouza, Debrabrata Biswas, and Irene Hanning,2

Department of Food Science and Technology, University of Tennessee 2605 River Dr. Knoxville, TN. 37996; and

Department of Animal and Avian Sciences, University of Maryland, College Park MD 20742

ABSTRACT The development of antibiotic resistant are not permitted to use antibiotics. Thus, both conven-
pathogens has resulted from the use of sub-therapeutic tional and organic poultry production need alternative
concentrations of antibiotics delivered in poultry feed. methods to improve growth and performance of poul-
Furthermore, there are a number of consumer concerns try. Herbs, spices, and various other plant extracts are
regarding the use of antibiotics in food animals includ- being evaluated as alternatives to antibiotics and some
ing residue contamination of poultry products and an- do have growth promoting effects, antimicrobial prop-
tibiotic resistant bacterial pathogens. These issues have erties, and other health-related benefits. This review
resulted in recommendations to reduce the use of an- aims to provide an overview of herbs, spices, and plant
tibiotics as growth promoters in livestock in the United extracts, currently defined as phytobiotics as potential
States. Unlike conventional production, organic systems feed additives.
Key words: botanicals, phytobiotics, extracts, essential oils, poultry, Salmonella, Campylobacter
2015 Poultry Science 94:14191430
http://dx.doi.org/10.3382/ps/pev014

INTRODUCTION ments as alternatives to prevent diseases and improve

bird performance. Many studies are evaluating the
With the European Union ban of antibiotics as use of botanicals that have been used traditionally in
growth promoters (AGP) in animal feed, on Jan- humans as feed additives. Most of the beneficial effects
uary 1, 2006 (EC regulation No. 1831/20031 ) (see: attributed to plants and plant extracts are related to
http://eur-lex.europa.eu/LexUriServ.do?uri=OJ:2003: health properties that include stimulating endogenous
268:0029:0043:EN:PDF.), alternative methods are digestive enzymes and antioxidants (Lee et al., 2004b).
being evaluated to improve the performance of agri- Compared with synthetic antibiotics or inorganic
cultural livestock, especially in swine and poultry chemicals, plant-derived products are natural, less toxic
production (Windisch et al., 2008). In some countries, than antibiotics, and typically residue free. Many are
including the United States, where the use of AGP is certified as Generally Recognized As Safe (GRAS) by
still permitted, the increased risk of antibiotic resistant the Food and Drug Administration (FDA) and there-
pathogens and consumers concerns about antibiotic fore, make them ideal candidates to use as feed ad-
residues have resulted in the implementation of some ditives in organic poultry production (Wang et al.,
recommendations to reduce AGP use in livestock 1998). Although the term phytobiotic comprises a
(Institute of Medicine, 1980, 1989; a Council for wide range of substances with respect to biological
Agricultural Science and Technology report 1981; origin, formulation, chemical description and purity,
Committee on Drug Use in Food Animals; Dibner they can be classified into four groups (Windisch and
and Richards, 2005). For organic poultry production, Kroismayr, 2006): 1) herbs (products from flowering,
United States Department of Agriculture (USDA) non-woody and non-persistent plants); 2) botanicals
organic regulations do not allow the use of antibiotics (entire or processed parts of a plant, e.g., roots, leaves,
in animals raised in these rearing systems to prevent bark); 3) essential oils (EOs) (hydrodistilled extracts of
diseases and or as growth promoters. For this reason, volatile plant compounds); and 4) oleoresins (extracts
organic poultry producers need non-antibiotic treat- based on non-aqueous solvents).
Several growth and health promoting properties have
C 2015 Poultry Science Association Inc.
been attributed to phytobiotics usage in poultry. These
Received August 11, 2014. benefits are derived by improving gut health includ-
Accepted November 10, 2014. ing increasing digestibility (Mitsch et al., 2004; Krois-
1
Presented as part of the Symposium: Organic Poultry Production mayr et al., 2008), modifying digestive secretions, and
with Natural Feed Supplements as Antimicrobials at the Poultry Sci-
ence Associations annual meeting Corpus Christi, Texas, July 14 to sustaining and improving gut histology (Williams and
17, 2014. Losa, 2001; Kreydiyyeh et al., 2003; Jamroz et al.,
2
Corresponding author: ihanning@utk.edu 2003). Furthermore, some phytobiotics stabilize the

1419
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 1420 DIAZ-SANCHEZ ET AL.

microbiome, which reduces microbial toxins (Windisch More than 3,000 essential oils are known, 300 of
et al., 2008; Peric et al., 2010; Steiner, 2006). This, in which are commercially important and used in pharma-
turn, reduces inflammation and; therefore, protein pro- ceutical, agronomic, food, sanitary, and cosmetic and
duction can be allocated to growth as opposed to pro- perfume industries as effective alternatives or comple-
duction of immune modulators (Steiner, 2006; Krois- ments to synthetic compounds (Bakkali et al., 2008).
mayr et al., 2008). Recently, the food industry and animal producers have
The positive effect of phytobiotics is mainly linked increased their interest in the use of EOs, not only
to the plant constituents including terpenoids (mono- for their antioxidative and anti-inflammatory proper-
and sesquiterpenes, steroids) phenolics (tannins), glyco- ties, but also for their antimicrobial, coccidiostatic, an-
sides, alkaloids (present as alcohols, alheydes, ketones, tihelmintic, and anti-viral effects (Cuppett and Hall,
esters, ethers, and lactones) flavonoids, and glucosino- 1998; Hirasa and Takemasa, 1998; Nakatani, 2000;
late (Wenk, 2006). For this reason, many herbs and Halliwell et al., 1995; Craig, 1999; Burt, 2004; Rhodes
spices can be added to food with the benefit of enhanc- et al., 2006; Wei and Shibamoto, 2007). Multiple
ing organoleptic properties (Wenk, 2006). oils, including carvacrol (CAR), thymol (THY),
obtained from oregano (Origanum glandulosum) or
MECHANISMS OF ACTION OF eugenol (EUG) obtained from the oil cloves (Eugenia
BOTANICALS caryophillis), are reported to inhibit many pathogenic
bacteria (Applegate et al., 2010; Dorman and Deans,
In general, botanicals, also termed as phytobiotics, 2000; Kollanoor et al., 2010; Si et al., 2006). In view of
contain primary and secondary plant compounds. The these studies, oils also are being evaluated to improve
primary compounds are considered as the principal nu- the microbiological quality of food when used as addi-
trients (protein, fat, and carbohydrates), whereas the tives.
secondary are described as EOs, bitterns, colorants, and EOs are gaining more interest in conventional and
phenolic compounds. Although the precise mechanisms organic poultry nutrition, primarily focusing on the im-
of antimicrobial action of phytobiotics are not eluci- provement of gut functions. The positive effects in the
dated yet, some mechanisms suggested to be responsi- digestive tract include stabilizing the microflora, which
ble for their beneficial properties include: 1) disruption improves nutrient utilization and absorption. EOs im-
of the cellular membrane of pathogens; 2) modification prove nutrient utilization and absorption by increasing
of the surface of the cells affecting to the hydrophobicity the activity of digestive enzymes including trypsin and
and, therefore, their virulence capacity; 3) stimulating amylase (Lee et al., 2003; Jang et al., 2004). Addition-
the immune system, specifically activation of lympho- ally, active components increase intestinal secretions of
cytes, macrophages, and NK cells; 4) protecting intesti- mucus, which prevents the adhesion of pathogens (Jam-
nal mucosa from bacterial pathogens colonization; and roz et al., 2006).
5) promoting the growth of beneficial bacteria such as
Lactobacilli and Bifidobacteria (Vidanarachchi et al.,
2005; Windisch and Kroismayr, 2007).
BOTANICAL PROPERTIES
Among phytobiotics, essential oils have gained more Antimicrobial Properties
attention due to their attributed antimicrobial and
growth promoter properties. Essential oils are com- In order to accomplish the beneficial effects associ-
pounds obtained by distillation or solvent extraction ated with the AGPs in poultry production, it is neces-
from aromatic plants, herbs, or spices (Yang et al., sary to understand the mechanism of action involved in
2009). Many EOs contain multiple active components improving performance and their antimicrobial activ-
and these components are primarily used to protect ity. Most of the beneficial effects of AGPs are linked to
the plants from damage caused by insects and bacte- the reduced incidence of subclinical infections (George
ria. Each component may have a different mechanism et al., 1982; Snyder and Wostmann, 1987; Brennan
of action and these components can work synergisti- et al., 2003). Furthermore, stability of the microbial
cally (Senatore, 1996; Russo et al., 1998). Thus, the ecology by AGPs has been reported to alleviate prob-
mechanism of action of EOs is based on its chemical lems associated with microbial production of toxins in-
composition. As an example, analogous molecules in- cluding the thinning of the intestinal wall, suppression
cluding thymol and carvacrol can exert similar antimi- of inflammation, and the reduction of bioamines and
crobial effects, but the mechanism of action differs due toxins produced by bacteria (Feighner and Daskevicz,
to differences in the location of the hydroxyl group. 1987; Knarreborg et al., 2004).
Similarly, limonene and p-cymene vary in the alkyl Studies using in vitro methods have demonstrated
group location and, thus, the antimicrobial efficiency antimicrobial activity that some plants and plant
(Dorman and Deans, 2000). It is difficult to predict extracts have against pathogenic bacteria including
the efficacy of the EOs, because the active components oregano (carvacrol), thyme (thymol), clove (eugenol),
present in the EOs can vary depending on the method of mustard (allysothiocyanate), cinnamon (cinnamalde-
extraction, geographical origin, plant genotype, the har- hyde), and garlic (allicin) (Table 1; Kollanoor et al.,
vesting season, and length of storage (Cosentino et al., 2010, 2012). Yet, most of the microstatic and microbi-
1999; Dorman and Deans, 2000; Wenk, 2006).
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Table 1. Examples of phytobiotics used as feed additives and their antimicrobial effect.

Feed additive Inclusion Rate Antimicrobial effect Reference

Capsaicin 18 ppm Reduction of S. enteritidis in ceca (Tellez et al., 1993)
Capsaicin 150 to 300 ppm Reduction of E. coli and C. perfringens (Jamroz et al., 2003)
Cinnamic aldehyde
Thyme oil 1 g/kg Reduction of coliform counts (Cross et al., 2003)
3 g/kg
5 g/kg
Blend A 100 ppm Reduction of C. perfringens colonization in the gut (Mitsch et al., 2004)
CRINApoultry
R Eugenol
Blend B + Curcumin
Thymol/Carvacrol Piperin
XTRACT TM : 100 mg/Kg Reduction of E. coli (Jamroz et al., 2005)
Carvacrol Light reduction of Cl. perfringens
Trans-cinnamaldehyde
Capsaicin
Capsaicin 5 ppm Prophylactic effect against S. enteritidis (Orndorff et al., 2005)
Oleoresin 20 ppm
Extracts from: Increase lactic acid bacteria (Vidanarachchi et al., 2006)
Cabbage tree 5g/kg Reduction of C. perfringens in ileum and ceca
Golden wattle tree 10g/Kg
Seaweed
Thyme Herbs at 10g/kg No effect on the intestinal microflora populations (Cross et al., 2007)
Oregano EOs at 1g/kg
Marjoram
Rosemary
Yarrow
CRINA R poultry 25mg/Kg Reduce coliforms in ileum and ceca (Jang et al., 2007)
50mg/Kg
Capsaicin (Chili pepper) 36 ppm Reduce S. enteritidis organ colonization (Vicente et al., 2007)
Hops (lupulone) 62.5 ppm Inhibition of C. perfringens in the gut (Siragusa et al., 2008)
125 ppm
250 ppm
Biomin P.E.P 125 poultry 125g/tn Notable reduction of E. coli in ceca (Peric et al., 2010)
Thymol 15 g/tn Reduction of E. coli and Clostridium (Tiihonen et al., 2010)
Cinnamaldehyde 5 g/tn Increase Bifidobacterium and Lactobacillus
Thymol 150 to 200g/tn Control necrotic enteritis (Timbermont et al., 2010)
Cinnamaldehyde 150g/tn (C. perfringens)
Eucalyptus EO
Green Tea extract 0.1g/kg Decrease caecal coliform bacteria (Erener et al., 2011)
0.2g/kg
Grape Pomace Concent (GPC) 60g/kg GSE increase Lactobacillus in ileum (Viveros et al., 2011)
Grape Seed Extract (GSE) 7.2g/kg GPC/GSE increase E. coli, Lactobacillus,
Enterococcus and Clostridium in ceca
Enviva EO 101 100g/tn Combined with xylanase reduced S. Heidelberg in ceca (Amerah et al., 2012)
Pennyroyal 0.025% Reduce E. coli (Erhan et al., 2012)
0.50% Increase lactic acid bacteria
Trans-cinnamaldehyde 0.75% Reduction of Salmonella colonization in cecum (Kollanoor-Johny et al., 2012)
Eugenol 1%
Carvacrol 0.05% Reduction of S. Heidelberg in the crop (Alali et al., 2013)
Thymol
Eucalyptol
Lemon
Capsicum oleoresin 4mg/kg Protective immunity against Necrotic Enteritis (C. (Hyen Lee et al., 2013)
perfringens)
Turmeric oleoresin
Trans-cinnamaldehyde 500 mg/kg Reduction of Br. intermedia in the ceca (Verlinden et al., 2013)
Thymol 0.25% Reduction of Campylobacter in ceca contents (Ali et al., 2014)
Carvacrol 0.5%
1%
2%
Thymol+Carvacrol 0.5%
Ground Yerba Mate 0.5% No reduction of S. Enteritidis in caecum (Gonzalez-Gil et al., 2014)
1%

regarding their spectrum of activity, potency, and ap- in the chicken intestinal tract remains a large chal-
plications are in debate (Delaquis et al., 2002). lenge. The target of many phytobiotic studies has been
Among the foodborne pathogens that can be trans- to reduce zoonotic pathogens (Table 2), but the in-
mitted through the consumption of poultry prod- formation available about the effects and the phys-
ucts, Salmonella enterica and Campylobacter jejuni iological impact of these active compounds on ani-
are the most common infectious agents (Heres et al., mal performance is still scarce. It is obvious that,
2004; White et al., 1997). Reducing the colonization although these compounds may be active against
of poultry by Salmonella Enteritidis and C. jejuni pathogens, they would not be acceptable if production
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Table 2. Examples of studies evaluating any effect on performance after including phytobiotics to the feed of chickens.

Feed additive Inclusion Rate Performance effect Reference

Oregano EO 50 to 100 mg/Kg No effect on growth (Botsoglou et al., 2002)
Japanese Green tea 1.0%
2.5% Decrease BW and FI with higher dose (Kaneko et al., 2001)
5.0%
Japanese Green tea 0.5%
0.75% Decrease BW and FI with higher dose
1.0% Improve FCR (Biswas and Wakita, 2001)
1.5%
Carvacrol 300 mg/Kg Improvement of daily gain by 8.1%
Improvement in FCR by 7.7% (Jamroz and Kamel, 2002)
Thyme EO 1g/kg
3g/kg Reduction of FI and WG with high (Cross et al., 2003)
inclusion levels
5g/kg
Thymol (thy) 100 ppm (Thy)
Cinnamaldehyde (cn) 100 ppm (Cn) No improvement in performance (Lee et al., 2003)
CRINA R
poultry 50 ppm (CRINA)
Herbromix TM 36 mg/kg Improve BWG by 2.060 to 2.063 (Alcicek et al., 2004)
48mg/kg Improve FCR by 1.96 to 1.97
Chinese herbal formula (mix of 14 herbs) 0.25g/kg
0.5g/kg Improve growth performance from 7 to (Guo et al., 2004)
21 days (age)
1g/kg
2g/kg
EO extract :
Oregano
Cinnamon 200 ppm No improvement in performance (Hernandez et al., 2004)
Pepper
Labiatae extract :
Sage 5,000 ppm
Thyme
Rosemary
Grape Seed Extract (GSE) 2g/kg
5g/kg At up to 10g/kg reduced FI (Hughes et al., 2005)
Concentrate of Tannins 10g/kg No reduction on FE
30g/kg
Capsaicin 100 mg/kg Improvement of BW by 1 to 2% (Jamroz et al., 2005)
Cinnamaldehyde
Carvacrol
Nor-SpiceR
Thyme 1g/kg No significant effect on BW, FI, and (Sarica et al., 2005)
FCR
Nor-Spice S Garlic 1g/kg
RepaXol TM 100 to 150gr/tn At 150gr/tn improved FCR (Zhang et al., 2005)
Avigro TM 0.5gr/tn
Blend EOs:
Oregano oil 24mg/kg
Laurel leaf oil 48 mg/kg No significant effect on BW (Cabuk et al., 2006)
Sage leaf oil
Myrtle leaf oil
Fennel seed oil
Citrus peel oil
Hops (Humulus iupulus) 0.5 lbs/tn Improve BW by 2.837 Kg (Cornelison et al., 2006)
1.0 lbs/tn Improve FCR by 1.669
1.5 lbs/tn
2.0 lbs/tn
RepaXol TM 100 g/tn Improve BW by 2,665 g (Lippens et al., 2006)
Improve FCR by 1.574
Thyme Herbs at 10g/kg Thyme oil and yarrow herb had (Cross et al., 2007)
positive effect on BW, FCR, AFC, AG
Oregano EOs at 1g/kg Feed intake decrease by 10%
Marjoram
Rosemary
Yarrow
Blend EOs:
Oregano 200 ppm Improve FCR and BW (Garcia et al., 2007)
Cinnamon
Pepper 200 ppm
Grape Pomace 5g/kg No effect on growth performance (Goni et al., 2007)
15g/kg
30g/kg
CRINApoultry
R 25 mg/kg No effect on BW/total gain (Jang et al., 2007)
50 mg/kg
Thyme 100 ppm Improve BW and FCR (Al-Kassie, 2009)

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Table 2. Continued.

Feed additive Inclusion Rate Performance effect Reference

Cinnamon 200ppm Improve BW and FCR (Al-Kassie, 2009)
Grape Seed Extract (GSE) 0.6g kg1 No effects on growth performance (Brenes and Roura, 2010)
1.8g kg1
3.6g kg1
Moringa olefeira leaf 5% Performance decrease at inclusion (Olugbemi et al., 2010)
levels above 5%
10%
Biomin P.E.P 125 poultry 125g/tn BW improvement (Peric et al., 2010)
2210 253 gr
Thymol (Thy) 15gr/tn (thy) Increase BW by 4 to 5% (Tiihonen et al., 2010)
Cinnamaldehyde (Cn) 5 gr/tn (cn)
Green Tea extract 0.1g/kg Increase BW and FE (Erener et al., 2011)
0.2g/kg
Ginger 250 g/100kg No effects on performance (Mohammed and Yusuf, 2011)
500g/100kg
750g/100kg
Grape Pomace Con (GPC) 60g/kg GSE decreased weight gain (Viveros et al., 2011)
Grape Seed Extract (GSE) 7.2g/kg
Rosemary leaf 5.7; 8.6; 11.5g/kg Rosemary EOs improve LWG and FE (Yesilbag et al., 2011)
Rosemary EOs 100; 150; 200mg/kg
Thyme extract 0.2% No significant effect on BW/FCR (Pourmahmoud et al., 2013)
0.4%
0.6%
Enviva EO 101 100 g/tn Improve BW by 1,924 gr (Amerah et al., 2012)
Improve FCR by 1.90
Moringa oleifera leaf 25% Improve feed intake (Gadzimarayi et al., 2012)
50% At higher inclusion levels decrease final
weight/WG
75%
100%
Rosemary EO 50 to 100mg/kg Improved BW and FE (Mathlouthi et al., 2012)
Oregano EO 50 to 100 mg/kg
EO mixture 1,000 mg/kg
Copaiba EO 0.30 mL kg1 Decrease on performance at high (Aguilar et al., 2013)
inclusion levels
0.45 mL kg1
0.60 mL kg1
Grape Seed Extract (GSE) 0.025g/kg Reduction in BW gain up to 2.5g/kg (Chamorro et al., 2013)
0.25g/kg
2.5g/kg
5g/kg
Thymol+Carvacrol 60 mg/kg Increase ADG (g) by 71.4% (Hashemipour et al., 2013)
100 mg/kg Increase G:F (g/Kg) by 601
200 mg/kg
Tecnaroma Herbal Mix PL 100 g/tn Improve BW by 3.418 to 3.427 Kg (Khattack et al., 2014)
200 g/tn Improve F:G ratio by 1.64 to 1.68
300 g/tn
400 g/tn
500 g/tn
Marjoram leaf 0.5% Improve LBW, BWG, FCR, and FI (Ali, 2014)
1.0%
1.5%
BW = Body Weight; FCR = Feed Conversion Ratio; AFC = Average Feed Conversion; AG = Average gain; FE = Feed
efficiency; LWG = Live weight gain; ADG = Average daily gain; G:F = Weight gain/Feed conversion; FI = Feed Intake.

performance were decreased. In chickens, the primary retention of the antimicrobial is essential for efficacy
colonization site of Salmonella Enteritidis and C. je- (Arsi et al., 2014).
juni is the cecum, which can result in horizontal trans- Because there are several active compounds present
mission, contamination off egg-shells with feces, and in the EOs, elucidating the mechanisms of antimicrobial
carcass contamination during processing (Stern, 2008; activity can be difficult (Skandamis et al., 2001; Carson
Gantois et al., 2009). Because the cecum is at the pos- et al., 2002). One antimicrobial property is attributed to
terior end of the gastrointestinal tract, the phytobi- the hydrophobic nature of EOs, which disrupts the bac-
otics must retain their activity during transit through teria cell membrane (Sikkema et al., 1994). Other non-
the entire gastrointestinal system. Some studies con- phenolic components including functional groups and
clude that the antimicrobial property is either reduced aromaticity have been demonstrated to have antimi-
or eliminated while moving through the gastrointesti- crobial activity (Farag et al., 1989; Bowles and Miller,
nal tract (Kohlert et al., 2002; Meunier et al., 2006). 1993). Kollanoor et al. (2012) reported that Salmonella
Given the location of Salmonella and Campylobacter, motility and invasion of avian intestinal epithelial cells
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were substantially inhibited by trans-cinnamaldehyde ucts because they lose the desirable color, odor, and
and eugenol. Evaluation of gene expression revealed flavor and shorten shelf-life (Botsoglou et al., 1997;
that motility and invasion genes, motA, flhC, hilA, Maraschiello et al., 1998). The antioxidant effect of EOs
hilD, and invF, were significantly downregulated. is attributed to their redox properties, chemical struc-
EOs tend to be more effective against gram-positive ture, and mainly to the presence of phenolic groups
than gram-negative bacteria (Burt, 2004). The phe- (Brenes and Roura, 2010). Studies testing the effec-
nolic compounds present in the EOs cannot pene- tiveness of certain aromatic plants such as rosemary,
trate the lipopolysaccharide wall of gram-negative cells oregano, sage, (Economou et al., 1991) and spices in-
(Ratledge and Wilkinson, 1988). But the outer mem- cluding cinnamon (Kamel, 1999) can retard the pro-
brane of gram-negative bacteria is not totally imper- cess of lipid peroxidation in oils and fatty acids. The
meable and hydrophobic molecules can pass through high content of polyunsaturated fatty acids in pre-
pores. EOs extracted from basil, sage, hyssop, rose- cooked and ready-to-eat poultry products make it par-
mary, oregano, and marjoram have demonstrated a ticularly susceptible to oxidative deterioration (Igene
wide antibacterial spectrum against most gram-positive and Pearson, 1979). Herbs including rosemary (Lopez-
and gram-negative bacteria evaluated in vitro (Burt, Bote et al., 1998), tea catechins (Tang et al., 2000),
2004; De Martino et al., 2009). In addition, multiple in and EOs have been reported to stabilize raw and pre-
vivo experiments have reported antimicrobial activity cooked chicken meat during refrigeration storage (Bot-
of phytobiotics as feed additives (Table 1). Cross and soglou et al., 2003, 2004; Young et al., 2003; Mirshekar
co-workers (2007) observed a decrease of cecal coliform et al., 2009). Poultry nutritionists are also interested
populations in birds treated with thyme oil after a col- in the antioxidant properties of certain plants and EOs
isepticemia infection, suggesting a protective effect af- that might improve meat quality. Grape seed and grape
ter administration of the oil. Nevertheless, the suscepti- pomace concentrate have been suggested as promising
bility of each bacteria species is different and also strain additives due to their antioxidant effects as free radi-
dependent. De Martino and co-workers (2009) reported cal scavengers (Viveros et al., 2011; Chamorro et al.,
different susceptibilities of two Bacillus cereus strains 2013). However, some of these botanicals can affect the
against the same EOs. Outtara and co-workers (1997) sensory quality of the meat.
reported that treatment time was a factor as gram-
negative cells died after 48 hours while gram-positive
cells died within 24 hours.
The beneficial properties of the metabolites present Sensory Properties
in the plants and EOs are well documented. In chicken
nutrition, it has been demonstrated that some phy- Palatability of phytobiotics is an important factor to
tobiotics select for beneficial bacterial growth leading consider. Some herbs and spices have a positive influ-
to enhanced digestion of nutrients, improving body ence on feed intake due to increased palatability and,
weight and weight gain (Jamroz et al., 2003; Hernandez thus, improve the growth rate (Brenes and Roura, 2010;
et al., 2004; Lee et al., 2004b,c). Viveros and co-workers Lee at al., 2004b,c). However, some phytobiotics have
(2011) suggested the potential role of grape-derived a negative effect on total feed intake due to the strong
products including grape seed extract as a feed ad- flavors (Windisch et al., 2008; Gonzalez-Gil et al. 2014).
ditive due to the ability of the products to favor the Regarding consumption, the smell of phytobiotics is
growth of specific groups of beneficial bacteria. Using the first step. When oronasal stimulation occurs, the
new molecular techniques, this same study reported an GI starts to prepare for food reception including the in-
increase of bacteria diversity and Lactobacillus popula- crease of digestive secretions, favoring gut motility and
tions when grape seed extract was included at 7.2 g/kg the protection of the intestinal epithelium (Katschinski,
in the chicken diet. Yerba Mate extracts supported and 2000; Teff, 2000; Hiraoka et al., 2003; Akiba et al., 2002;
increased the growth of Lactobacillus and Pediococcus Platel and Srinivasan, 2004). But the sensitivity of the
and were antimicrobial against Salmonella and Campy- somatosensing system is different between species. In
lobacter (Gonzalez-Gil et al. 2014). poultry production the study of the effect of flavors has
not received as much attention, because the response
to flavors is less notable when compared to other an-
Antioxidant Properties imals like pigs (Moran, 1982). Studies in pigs showed
the negative response to some EOs including capsaicin,
Lipid metabolism and hypocholesterolemic effects cinnamaldehyde, carvacrol, or formic acid as they evoke
have also been reported. Qureshi et al. (1988) reported feed refusal when added to food (Green, 1989; Bikker
the role of limonene in cholesterol synthesis. Similarly et al., 2003; Eissemann and van Heugten, 2007). Cross
other authors reported that thymol, carvacrol, and and co-workers (2003) observed a feed intake reduc-
-ionone have a regulatory effect of non-sterol prod- tion during the first two weeks of age when thymol oil
ucts (Case et al., 1995; Elson, 1996). Lipid oxidation was added to the feed, suggesting that young chickens
occurs during meat processing, cooking, and refriger- may be more sensitive to flavor and odor characteris-
ated storage, which affects the quality of food prod- tics. Similarly, Ali (2014) reported suppression on feed
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intake in chicks when marjoram leaves were added to when using different types, concentration, or combina-
the diet. tions of plant extracts (Botsoglou et al., 2002; Cross
et al., 2003; Lee et al., 2003; Hernandez et al., 2004;
Sarica et al., 2005; Cabuk et al., 2006; Jang et al.,
Effects on the Digestion Process 2007; Olugbemi et al., 2010; Mohammed and Yusuf,
2011; Pourmahmoud et al., 2013; Aguilar et al., 2013)
To date, the studies that have evaluated the growth (Table 1). Initial studies by Dale and co-workers (1980)
promoting effects of phytobiotics are not conclusive on reported a marked reduction in the average weight gain
their beneficial effects in poultry production (Table 2). in chicks when they were fed tannic acid and sorghum.
Some authors have reported different in vivo results in Similarly Botsoglou and co-workers (2002) did not ob-
poultry performance parameters using the same plants serve any difference in body weight and feed conversion
or plants extracts as additives (Jamroz and Kamel, ratio, after adding oregano EOs at the concentrations
2002; Guo et al., 2004; Cornelison et al., 2006; Cross of 50 and 100 ppm in broiler chicken diets over a 38-
et al., 2007; Al-Kassie, 2009; Peric et al., 2010; Tiihonen day time span. Lee and co-workers (2003) observed that
et al., 2010; Yesilbag et al., 2011; Amerah et al., 2012; a diet containing highly digestive ingredients can limit
Mathlouthi et al., 2012; Hashemipour et al., 2013; the proliferation of bacteria in the intestinal tract be-
Khattack et al., 2014). cause there is a reduction of the substrate left for bac-
The exact mode of action of growth-promoting feed teria present in the posterior portion of the GIT.
additives is still unknown. However, it is suggested that Other factors must also be considered including im-
the interaction of growth promoters with the intesti- mune regulation, (Freitas and Fonseca, 2001) environ-
nal microbiota community may result in their optimal mental, and dietary conditions (Hill et al., 1952; Lee
stabilization, and, therefore, better use of nutrients to et al., 2004b). Hyen Lee and co-workers (2013) demon-
enhance growth (Lin, 2011). Similarly, the use of EOs strated the activity of capsicum and turmeric oleoresins
as supplements in broiler diets may lead to shifts in stimulating the immune response against C. perfringes
the microbial population enhancing the growth of lac- colonization in chickens. Early studies have noted that
tic acid bacteria including Lactobacillus and Bifidobac- under extremely clean environments, the enhancing ef-
terium and, therefore, decrease the pH of the GIT fects of additives are less obvious (Hill et al., 1952).
(Bedford, 2000; Tiihonen et al., 2010). Optimal enzyme The efficiency of EOs as growth promoters is dose-
activity is dependent on pH and ,because EOs can re- dependent (Cross et al., 2003; Zhang et al., 2005;
duce the pH, the break down of feed can be enhanced Olugbemi et al., 2010; Gadzimarayi et al., 2012; Aguilar
(Kamel, 1999). et al., 2013). Viveros and co-workers (2011) reported
There is also evidence of beneficial activity of EOs growth depression when including GSE at 7.2g/kg in
on other factors of the digestion process. Lee and co- the chicken diet, whereas at lower doses the growth per-
workers in 2003 and Jang et al. (2007) observed that formance was not affected. Chamorro and co-workers
EOs enhance the activity of digestive enzymes such as (2013) confirmed that the use of GSE up to 2.5 g/kg
trypsin and amylase and also bile salts. Furthermore, it had no adverse effects on chicken growth. In order to in-
has been reported that EOs improve liver function and crease the effectiveness of the phytobiotics some studies
increase the concentration of the pancreatic digestive have used a combination of EOs at low concentrations
enzymes (Al-Kassie, 2009). Similarly, curcumin, cap- (Langhout, 2000; Lee et al., 2004c; Manzanilla et al.,
saicin, and piperine have been reported to stimulate 2004) or with enzymes (Amerah et al., 2012).
digestive enzyme activities of the pancreas (Platel and The form of herbal supplementation is also impor-
Srinivasan, 2004). Lee et al. (2004a,b) demonstrated the tant for its bioactivity. Cross and co-workers (2007) ob-
efficiency of cinnamaldehyde EOs to improve fat diges- served that yarrow appears to be more effective when
tion in broilers. fed as an herb than an extracted essential oil, because
By enhancing digestion, some phytobiotcs do not the precursors of the terpenes and another phytochem-
change final body weight but can improve feed con- ical compounds are present in the herb but not in the
version ratios (Windisch et al., 2008). To achieve im- oil. Also, Yesilbag and co-workers (2011) observed a
provements in feed conversion, it is important to select higher efficiency to improve live body weight and feed
the proper plants with the desired active components efficiency when rosemary EOs were administered, but
at an optimized dietary dose. It is suggested that the not the ground leaf form.
effectiveness of phytobiotics as feed additives rely on
the EOs components and the synergistic effects of the
active molecules in the plants or extracts (Jamroz et al., APPLICATIONS OF BOTANICALS IN FOOD
2003; Mitsch et al., 2004; Tiihonen et al., 2010; Math- SYSTEMS
louthi et al., 2012; Hashemipour et al., 2013; Hyen Lee
et al., 2013). Plant extracts have considerable promise in a wide
Not all botanicals or their derived products are ef- range of applications in the food industry, and because
fective. Some reports did not find any statistical differ- most of them are considered to have GRAS status (Over
ences when supplements were included in the diet even et al., 2009), there is no time delay for implementation.
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 1426 DIAZ-SANCHEZ ET AL.

Due to the complex nature of foods, a greater concen- otics can be delivered in the feed or water depending on
tration of EOs is needed in order to achieve the de- the composition of the product. However, a reduction
sired effect than what is needed during in vitro eval- in efficacy may occur when ground leaves are used as
uations using pure cultures of bacteria (Shelef, 1983; opposed to using extracts (Gonzalez-Gil et al. 2014).
Smid and Gorris, 1999; Kumudavally et al., 2008). Fur- Plant extracts are typically more effective than ground
thermore, nutrients are available in some food items, leaves because the active components are concentrated
which can facilitate bacterial repair of damaged cells in extracts. However, extracts can be more costly be-
(Gill et al., 2002). The intrinsic properties of the food cause chemicals are needed for the extraction process
(fat, protein, water content, antioxidants, preservatives, and a large quantity of the plant is required to produce
pH, salt, and other additives) and the extrinsic proper- a sufficient amount of extract.
ties (temperature, packaging, and atmospheric compo- New delivery systems are being investigated to tar-
sition) can also influence bacterial sensitivity (Shelef, get the site within the animal intestines so that phyto-
1983; Tassou et al., 1995). For example, at a low pH biotics exert their beneficial activities. Previous studies
the EOs increase the hydrophobicity, enabling them to based on the use of emulsifiers such lecithin, extensively
more easily dissolve in the lipids of the cell membrane used in food and non-food applications, reported en-
of target bacteria (Juven et al., 1994). hancement of the antimicrobials properties of carvacrol
and eugenol against gram-positive and gram-negative
bacterial pathogens (Li, 2011, Masters Thesis, Univer-
METABOLISM OF EOs AND FOOD SAFETY sity of Tennessee). Currently, microencapsulation is one
IMPLICATIONS of the most studied tools to achieve this goal (Chambers
and Gong, 2011) and has been reported to promote the
EOs are quickly absorbed after oral, pulmonary, or antimicrobial efficacy of extracted compounds against
dermal administration and then metabolized and typ- E. coli O157:H7 and L. monocytogenes (Lippens et al.,
ically eliminated by the kidneys in the form of glu- 2006; Gaysinsky et al., 2005a,b). Microencapsulation
curonides. Thus, their accumulation in the body is delays the absorption of the coated Eos, and, thus, the
unlikely due to rapid clearance and short half lives EOs will retain antimicrobial activity longer. A signifi-
(Kohlert et al., 2000). But, more toxicological studies cantly large part of current literature on the encapsula-
are needed to determinate the acute oral effects and tion of EOs deals with micrometric size capsules, which
dosage levels of EOs in poultry diets. Acute oral toxic- are used for the protection of the active compounds
ity studies are typically conducted in rats and mice, and against environmental factors (e.g., oxygen, light, mois-
some EOs have been evaluated including carvacrol, cin- ture, and pH). Other advantages attributed to the use
namaldehyde, beta-ionone, and thymol. Although there of microencapsulated additives are their capacity to re-
are scarce data about the toxicological effects of EOs duce any negative palatability or strong odors, and;
in chickens, some studies with cinnamaldehyde evalu- therefore, feed intake is not reduced (Lambert et al.,
ated its carcinogenicity and mutagenicity reporting ter- 2001; Cross et al., 2003; Lippens et al., 2006).
atogenic activity (Abramovici and Rachmuth-Roizman,
1983; Hoskins, 1984; Stammati et al., 1999; Smith et al.,
2000). Furthermore, handling of pure formulations must
be done safely because many are potentially irritating FUTURE AND PROSPECTS OF
and can cause allergic contact dermatitis (Burt, 2004). BOTANICALS IN ORGANIC POULTRY
Some studies have reported accumulations of phyto- Some commercial phytobiotic products are available,
biotic components in tissue and organs. Botsoglou et al. such as CRINA R
poultry, XTRACTTM , and Biomin
(2002) reported EOs continuously added to chicken P.E.P 125 poultry, developed as additives in poultry
diet, without withdrawal periods, lead to the deposi- feed and have had some success for controlling col-
tion of residues in various tissues in a dose-dependent iforms and C. perfringes (Mitsch et al., 2004; Jamroz
fashion. Although the impact on the sensory proper- et al., 2005; Peric et al., 2010; Viveros et al., 2011).
ties of poultry meat is recognized, more toxicological Other commercial products including Enviva EO 101
evidence of EO residues deposited in poultry meat is have been demonstrated to be effective at reducing S.
needed. Because many of the EOs, including thymol, Heidelberg in the ceca when combined with xylanase
carvacrol, cinnamaldehyde, and beta-ionone, are given (Viveros et al., 2011). In general most of the data gen-
GRAS status by the FDA (Furia and Bellanca, 1975), erated from evaluation of commercial phytobiotics, re-
it is implied that their use is safe. ported improvement in performance and antimicrobial
activity (Alcicek et al., 2004; Lippens et al., 2006; Peric
DELIVERY SYSTEMS et al., 2010; Amerah et al., 2012; Khattack et al., 2014).
Many phytobiotics show promising results for ap-
A large issue with some EOs is the reduction of the plications in organic and conventional poultry pro-
antimicrobial activity when they are delivered in feed duction. However, there are data gaps in production
(Si et al., 2006), mainly associated with the volatility performance and residue accumulation, which need
and poor solubility of the active components. Phytobi- to be filled before some phytobiotics are used in
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 BOTANICALS AND POULTRY 1427
commercial farms. Furthermore, delivery systems and Bikker, P., R. Fontanillas, and E. Roura. 2003. Dietary supple-
palatability issues should be resolved in order to opti- mentation with botanical compounds depresses piglet feed in-
take while faecal E. coli counts remain unchanged. J. Anim. Sci.
mize the efficacy of these compounds. 81:203.
Brenes, A., and E. Roura. 2010. Essential oils in poultry nutrition:
Main effects and modes of action. Anim. Feed Sci. Tech. 158:114.
Brennan, J., J. Skinner, D. A. Barnum, and J. Wilson. 2003. The
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