Biomed Res Int. 2016; 2016: 3278359.
Published online 2016 Sep 25. doi: 10.1155/2016/3278359
PMCID: PMC5055920
Abstract
Necrotic
enteritis (NE) is an important concern in poultry industry since it
causes economic losses, increased mortality, reduction of bird welfare,
and contamination of chicken products for human consumption. For
decades, the use of in-feed antimicrobial growth promoters (AGPs) has
been the main strategy to control intestinal pathogens including Clostridium perfringens
(CP), the causative agent of NE. However, the use of AGPs in animal
diet has been linked to the emergence and transmission of antimicrobial
resistance through food-borne microorganisms, which has led to the ban
of AGPs in many countries. This scenario has challenged the poultry
industry to search for safer alternative products in order to prevent
NE. In this context, the utilization of natural plant extracts with
antimicrobial properties appears as a promising and feasible tool to
control NE in chicken. In this paper, we review the scientific studies
analyzing the potential of plant extracts as alternative feed additives
to reduce NE in poultry, with focus on two types of plant products that
arise as promising candidates: tannins and essential oils. Some of these
products showed antimicrobial activity against CP and coccidia in vitro and in vivo and are able to increase productive performance, emulating the bioactive properties of AGPs.
1. Necrotic Enteritis in Chickens and Clostridium perfringens
Necrotic enteritis (NE) is a worldwide extended disease caused by Clostridium perfringens
(CP). The disease was first reported in 1961 and from that moment
onwards many outbreaks have been documented in all countries where
intensive poultry breeding is carried out [1–3].
NE has different presentations: sudden, clinical, and subclinical;
among them, subclinical NE is one of the main causes of economic loss
for the poultry industry. The estimated prevention cost of NE is U$S
0.05 per chicken with a total global loss of nearly U$S 2 billion per
annum [4].
CP is a ubiquitous Gram-positive, spore forming, toxigenic, anaerobic
bacterium, generally classified according to the production of five
major toxins [5].
In poultry industry, CP type A is the most significant, since it is
capable of producing many toxins responsible for the disease [6].
CP
can be found in the environment in soil, feces, feed, and poultry
litter and in the intestines of animals as part of the normal gut
microbiota [7];
thus, the presence of CP by itself does not necessarily imply the
occurrence of the disease. NE reports showed that the disease is mostly
found in 2- to 5-week-old chickens and the incidence of the disease can
be low as well as high, as most CP strains are relatively innocuous.
Clinical presentation of NE in outbreaks depends on a complex
interaction of the microorganism with other predisposing factors such as
diet, the presence of other microorganisms, and the immunological
status of the birds [2, 4, 8, 9].
The ingredients included in diet, and even changes in it, may affect
both physical and chemical properties of intestinal contents. Presence
of Eimeria spp. and viral infections are important
NE-predisposing factors as they lead to the destruction of enterocytes
and increase the mucosal secretion. Stress, immunosuppression, or
medical treatment can also induce changes in the composition of the
microbiota. All of these factors contribute to facilitating the mucosal
colonization for pathogenic CP strains, which are able to degrade the
mucus and colonize the gut. When this happens, the bacteria begin to
synthesize enzymes, acting in the basement membrane and lateral part of
the enterocytes, spread through the lamina propria, and induce damage to
endothelial cells [6, 10–13].
Clinical
signs of NE include decreased appetite, diarrhea, weight loss, and
several nonspecific signs that can be found even without any gut lesion [1, 2].
Gross lesions are diverse, usually affecting the small intestine and
liver; jejunum and ileum are the most affected portions of the gut.
Intestines are visualized with gas as well as bleeding and blood clots
can be found in their contents. The mucosa can be either thickened by
edema or thinned by epithelial erosion [1, 2, 6, 8]
and sometimes a yellow or green pseudomembrane adhered to mucosa can be
found. It is likely to find in the same animal both changes in
different parts of the intestine [1–3, 6].
In the liver, necrotic foci and cholecystitis can appear dispersed
throughout the parenchyma. These injuries are commonly associated with a
subclinical presentation of the disease [2, 14].
Microscopic lesions comprise shortening villous, epithelium detachment
in the apical portion, and also intense mucosal necrosis extending to
the crypts or submucosa. Bacilli can sometimes be seen in the mucosa or
in lamina propria. The inflammatory cell infiltration in lamina propria
is a mixed type and more evident in some cases than others [1–3, 8].
The
treatment of NE outbreaks are based on antimicrobial therapy with the
aim of diminishing economic losses. Bacitracin, lincomycin,
virginiamycin, penicillin, and tylosin have been the antibiotics of
choice worldwide. However, the most important losses are associated with
subclinical presentation of NE, which has been controlled by the use of
subtherapeutic doses of antimicrobials in feed [15]. As it happens with several microorganisms, CP susceptibility to antibiotics has declined over the years.
2. Antimicrobial Control of NE and Alternatives
Control
of NE and predisposing factors in poultry often becomes a really
complex labor. For many years, antimicrobial therapy was the first, and
most of the times the only, strategy to control CP-induced NE.
Therapeutic antimicrobials administered at high doses over a short
period of time are generally used to control acute outbreaks [16].
To control subclinical NE presentations, antimicrobial growth promoters
(AGPs) are generally used. Although these compounds were first included
into feed to improve growth rate and feed conversion efficiency in
poultry [17], they are now used mostly to control CP and other Gram-positive pathogens [18].
Bacitracin (a polypeptide antimicrobial) and virginiamycin (a
streptogramin) are nowadays two commonly used AGPs in poultry production
to improve feed conversion ratios, body weight gain, and well-being of
animals [16].
Despite the longtime use of AGPs, mechanisms involved in the
improvement caused by the administration of subtherapeutic doses of the
antimicrobials in broilers flocks are far from being fully understood.
Proposed potential mechanisms include regulation of digestive functions
and gut immunological responses [19].
The most accepted mechanism is that AGPs modulate gut microbiota, which
plays a critical role in maintaining the host health [20].
The
use of AGPs at subinhibitory doses for long periods of time is
particularly favorable to select antimicrobial-resistant microorganisms.
In countries where AGPs are still used, reduced susceptibility of
poultry CP strains was reported [21].
Continuous administration of AGPs may lead to changes in the bacterial
environment by eliminating susceptible strains and allowing
antimicrobial-resistant bacteria (i.e., those with lower susceptibility
to AGPs) to survive and predominate [22]. Furthermore, continuous administration of APGs in the feed may cause cross-resistance to therapeutic antimicrobials [21]. Antimicrobial resistance together with a gradual decrease in sensitivity to anticoccidials by some strains of Eimeria spp. (an important predisposing factor to NE) has exacerbated the presence of such CP strains.
Establishment
of resistant and pathogenic CP strains in poultry farms also may lead
to the transfer of resistant bacteria and their resistant factors from
animals to humans. Studies considering Campylobacter spp., E. coli, and Enterococcus spp.
suggest that the use of nontherapeutic antimicrobial is linked to the
propagation of multidrug resistance, including resistance against drugs
that were never used in the farm [23].
The
impact of AGPs on the appearance and transmission of
antimicrobial-resistant bacteria has been the aim of several
investigations and has led to their ban in the European Union in 2006 [24]. After these measures were taken in Europe [25],
the consequence was the increase in NE incidence together with an
increase in the use of therapeutic antimicrobials to control diseases [26–28]. The European experience and recent moves toward reduction or termination of AGPs in North America [25]
have pressured the poultry industry to search for suitable alternatives
in order to control NE outbreaks, reduce productive consequences of
subclinical presentation under conditions of average management of the
farms [26],
and diminish resistance to antimicrobials. Natural substances with
antimicrobial properties can be an essential part of this control
strategy.
In this context, an
increasing number of antimicrobial-free tools and strategies have been
developed for prevention and control of CP-induced NE in poultry [27, 29].
Any alternative to AGPs is expected to be safe to the public health,
cost-effective, and friendly to the environment together with
antimicrobial activity to be considered as a viable option [30].
Proposed alternatives include vaccines, immunomodulatory agents,
bacteriophages and their lysins, antimicrobial peptides, pro-, pre-, and
synbiotics, plant extracts, inhibitors for bacterial quorum sensing,
biofilm, and virulence and feed enzymes [27, 31].
Vaccination against the pathogen and the use of probiotic and prebiotic
products have been suggested but at the present time are not yet
available for practical use in the farms. One of the most promising
alternatives to AGPs is the use of plant extracts added to the diet to
improve nutrition and health in farm animals and to control enteric
clostridial diseases; these additives have been used for many years in
poultry and their efficiency has been demonstrated [21, 32].
3. Plant Extracts
Plant materials are used widely in traditional systems of medicine [55].
Plant extracts, also known as phytobiotics, have been exploited in
animal nutrition, particularly for their antimicrobial,
anti-inflammatory, antioxidant, and antiparasitic activities [56–58].
Many
plants have beneficial multifunctional properties derived from their
specific bioactive components. Biologically active components of plants
are mostly secondary metabolites, such as terpenoids, phenolics,
glycosides, and alkaloids, present as alcohols, aldehydes, ketones,
esters, ethers, and lactones [17].
These secondary metabolites may have a protective function in vegetal
tissues. Final effect on animals will depend on both the combination and
concentration of these bioactive molecules and minor changes in these
aspects will explain why some of these compounds can have either
beneficial or detrimental effects in animals [59–61].
Plant
extracts are generally considered safe and effective against certain
bacteria. They are extensively used in feed as growth promoters and
health protectants [62, 63],
particularly in Asian, African, and South American countries, and in
recent years are gradually being used in developed countries. Effects of
phytogenic feed additives on the production performance of poultry are
also reported [57].
It is considered that plant extracts possess antibacterial activities
when their minimum inhibitory concentrations range from 100 to 1000 μg/mL according to in vitro bacterial susceptibility tests [64].
In
the last years, several studies reported that the use of raw plant
extracts and derived phytogenic compounds as poultry feed supplements [65]
may have a positive effect on birds health and productivity. NE gross
lesions and intestinal CP burden is a parameter commonly used to
evaluate the effects of including plant extract in chicken diets [35, 47].
Different plant extracts may have direct inhibitory effect either on CP
vegetative cells or in some of the toxins involved in NE pathogenesis [32].
Useful
antimicrobial phytochemicals can be divided into several categories,
such as polyphenols/tannins, essential oils (EOs), alkaloids, and
lectins/polypeptides [66].
Phytochemicals exert their antimicrobial activity through different
mechanisms. For example, (1) tannins act by iron deprivation and
interactions with vital proteins such as enzymes [67]; (2) cryptolepine, the main indoloquinoline alkaloid, is a DNA intercalator and inhibitor of topoisomerase [68];
and (3) saponins form complexes with sterols from the membrane of
microorganisms causing damage and consequent collapse of the cells [69]. EOs have long been recognized for their antimicrobial properties [70],
but their precise antimicrobial mechanism is poorly understood. In
fact, the antimicrobial activities of many plant extracts have not been
clearly elucidated yet [71]. In vivo
observations support the assumption that general antimicrobial
potential of phytogenic feed additives is due to a substantial reduction
of intestinal pathogen pressure [66].
In
the global context to reduce or avoid the use of antimicrobials in
animal production, not only biological activity of alternatives to AGPs
but also the suitability of the active principles to be produced and
applied at the industrial level should be considered. In the last years,
two types of plant-derived extracts emerged as promising candidates to
be used in poultry industry to control NE: tannins and essential oils.
4. Tannins
Tannins
are polyphenolic secondary metabolites found in almost all the parts of
the plants and therefore present in most animal diets. Tannins are
generally classified into two groups based on their chemical structure:
hydrolyzable tannins (HT) which are present in plants as gallotannins or
ellagitannins [72] and condensed tannins (CT), the most common type of tannins found in forage, which are polymers of flavonol units [73]. However, tannins have an enormous structural diversity, with molar masses ranging from 300 to 20,000 Da [74]. Multiple biological properties including anticancer [75, 76] and antimicrobial [67, 77, 78] activities have been attributed to tannins [79], mainly due to their ion-complexation, protein-binding, and antioxidant capabilities [80–82].
Scientific
evidence suggests significant potential for the use of tannins to
enhance nutrition and animal health in both cattle and poultry [30, 62, 65, 83]. Although tannins have been generally considered as antinutritional factors for monogastric animals [59, 84, 85],
it is now known that their beneficial or detrimental properties depend
on both tannin nature (i.e., plant source, chemical structure, and
astringency) and animal factors (i.e., animal species, physiological
state, and diet composition) [39, 57, 61, 66, 86, 87]
as well as administration factors such as dosage and formulation. The
antinutritional effects attributed to tannins are mostly based on assays
performed with elevated concentrations of CT or plant parts with
elevated tannin content, as may be the case of tannic acid in sorghum.
In
recent years, many reports showed that moderate tannin concentrations
from diverse vegetal sources can improve not only nutrition but also
health status in monogastric farm animals, including poultry.
Furthermore, inclusion of polyphenol-rich plant extracts has been found
to improve weight gain/feed ratio in growing pigs [88]. In poultry, Schiavone et al. (2008) [34]
showed that the use of a chestnut extract has a positive influence on
growth performance if included in the diet up to 2 g/kg of dry matter
and also a significant decrease in total nitrogen in the litter was
observed. This supports the observation that administration of chestnut
tannins often results in firmer droppings, which positively affects the
litter status thus improving the overall health status and welfare of
chickens in intensive production systems. Similarly, other authors have
observed that the inclusion of phenolic compounds in diet enhanced
growth performance, decreased lipid oxidation, decreased cholesterol
value, and increased beneficial fatty acids content in broiler chickens [89].
However, other tannin formulations are unable to enhance growth
performance but produce different beneficial effects in productive
aspects of chicken physiology, including delay of meat lipid oxidation [37, 41, 90–92], increase of protein digestibility and feed conversion [38, 42], enhancement of gut health and microbiota biodiversity [40, 93, 94], and higher capacity to overcome deleterious effects of persistent heat stress [95, 96].
Numerous in vitro and in vivo studies have verified the activity of tannins against several types of intestinal pathogens including helminthes [97–100], coccidia [33, 36, 101], viruses [45, 77], and bacteria [102–104] with particular interest in Salmonella Typhimurium [44, 105, 106], Campylobacter jejuni [43], and CP [32, 35], which are major disease-causing or food-borne bacteria in poultry [107].
Incidence of CP-associated NE in poultry has considerably increased in countries that stopped the use of AGP [26, 108]. Elizondo et al. (2010) [32] showed that two of the most common sources of tannins, chestnut (Castanea sativa, HT) and quebracho (Schinopsis lorentzii, CT), extracts have in vitro antibacterial and antitoxin activities against CP and its toxins. Similarly, other authors have observed in vitro antimicrobial activity against CP using tannins derived from chestnut and grape products [40, 109].
These findings are consistent with recent in vivo studies that tested the effect of tannins added to diet of chickens on Eimeria spp. and CP. Tosi et al. (2013) [35]
found that the addition of a chestnut tannin extract significantly
reduces the counts of CP and macroscopic gut lesions in broiler chickens
challenged with coccidia and CP. Subsequent results confirm the effects
of chestnut and quebracho tannins in a broiler NE model reducing the
incidence and severity of gross lesions and improving the productive
performance of the chicken [110].
Although chestnut tannins show strong bactericidal activity against CP,
most ingested HT are degraded in the intestinal tract and do not remain
in the feces. In contrast, quebracho-derived CT have lower
antibacterial activity but most of the administered tannins remain in
the feces and therefore in the litter. Combination of CT and HT may be
used to readily diminish the intestinal CP load and also to avoid the
reinfection by controlling the environmental contamination (i.e., feces
and bedding). In agreement with this, Cejas et al. (2011) [36] found that quebracho tannins also decreased oocyst excretion in Eimeria spp.
challenged broiler chicks. Consistent results were also obtained with
other tannin-rich plant extracts. McDougald et al. (2008) [33]
showed that inclusion of muscadine pomace in the diet significantly
reduced intestinal lesion scores and mortality rates using a similar NE
model of broilers challenged with Eimeria spp. and CP. Dietary supplementation of chicken diet with a polyphenol extract of Curcuma longa
enhanced coccidiosis resistance as demonstrated by increased body
weight gains, reduced fecal oocyst shedding, and decreased gut lesions,
and it was also shown to attenuate coccidia-induced
inflammation-mediated gut damage [101]. Artemisia annua leaves, which contain both EOs and tannins [111], showed antimicrobial activity against CP proliferation in vitro and were able to reduce intestinal load and severity of NE-related small intestinal lesions in vivo [47].
A
recent work reported that chestnut extracts improve lactobacilli
tolerance to gastric transit and tolerance to low pH values and bile
juice salts, indicating that tannins may also be used in combination
with probiotics for synergist enhancement of gut health [112].
An additional benefit of the use of tannins as alternative AGPs in
poultry is the difficulty of CP to multiply and develop resistance in
the presence of such diverse range of molecules these plant compounds
contain [21].
Although
tannins can have beneficial effects on poultry performance and gut
health, still little is known about the mechanisms involved in their
final in vivo antimicrobial and growth promoter effects. Some
authors suggest that low concentration of tannins can improve
palatability of feed thus increasing performance of monogastric animals
by stimulating feed intake [66].
Nevertheless, antimicrobial activity has been linked to their
biochemical properties including metabolism inhibition by enzyme
complexation and iron deprivation [67, 80, 113, 114].
Iron is essential for most pathogenic bacteria and tannic acid has been
shown to function like a siderophore that chelates iron from the
medium, making it unavailable for some microorganisms but without
affecting lactic acid bacteria [102].
Regarding the growth promotion effect, some of the explained modes of
action for antimicrobials may help to define tannin mechanisms. How
antimicrobials increase performance is not clear, but possible
mechanisms include reduction in total bacterial load, suppression of
pathogens, thinning of the mucosal layer, and direct modulation of the
immune system [115].
In general terms, like AGPs, tannins may be involved in the modulation
of gut microbiota and its highly complex interactions. As reported by
several authors, Gram-positive bacteria seem to be more sensitive to
tannin-rich plant extracts [104, 116].
Regardless of the mode of action, chemical characteristics of the
tannins are highly variable and different types of tannins can be found
in a single plant extract. The origin of the plant extract added to the
feed will be determinant in the final impact on microbiota and
consequently in growth performance. Table 1 summarizes the effects of different tannin-rich plant extracts on performance and health of poultry in vivo and their antimicrobial activities in vitro.
In vivo and in vitro effects of tannin-rich plant extracts on performance and health of poultry.
The
use of tannins appears as an attractive alternative to control NE since
these natural products do not leave residues in poultry-derived
products and given the complexity of their structures and bioactive
principles it is more difficult for tannins to induce selection of
resistant microorganisms in comparison with AGPs. Among the wide range
of tannin-rich plant extracts with beneficial effects in poultry
nutrition and health, chestnut and quebracho tannins are probably the
most readily available commercial products that are being used and there
are a significant number of publications that demonstrate their
properties. Further research needs to be done in order to elucidate the
mechanisms associated with antimicrobial activity of tannins as well as
their impact on the development of a healthy gut microbiota in poultry.
5. Essential Oils
Essential
oils (EOs) are considered to be secondary metabolites in plants which
are organic compounds that are not directly involved in the normal
growth, development, or reproduction of the plant [117]. These compounds are assumed to be involved in plant defense and most of them may possess antimicrobial properties [117, 118].
The
composition and the percentage of different components of EOs vary
amongst species and parts of the plants; most of these components are
chemically derived from terpenes and their oxygenated derivatives,
terpenoids, which are aromatic and aliphatic acid esters and phenolic
compounds. EOs can be extracted from plant tissues by extraction or
fermentation, but steam distillation is the most commonly used method in
industry. EOs have been historically included in the formulation of
perfumes and cosmetic products as well as herbs and spices for foods.
These oily components are generally recognized as safe (GRAS) by the
Food and Drug Administration (FDA) of the United States and have been
used as artificial flavorings and preservatives [119].
Also, herbs and spices and their EOs have been used as pharmaceuticals
in alternative or complementary medicine for many years [120].
Recently,
there was a renewed interest on the antimicrobial activity of EOs since
many reports demonstrated the potential to control bacterial pathogens [121–123]. The first scientific test of their bactericidal properties had been carried out by de la Croix in 1881 [123]. In more recent years, many EOs or their components have been shown to possess broad-range antibacterial properties [124, 125].
Antimicrobial
activities of EOs are related to chemical characteristics such as their
hydrophobicity which enables them to interact with the lipids of the
bacterial cell membrane thus disturbing bacteria metabolism and cell
wall and membrane permeability, leading to extensive leakage of critical
molecules and ions from bacterial cells. Phenolic groups present in EOs
molecules target bacterial cell membrane by changing its structure and
function [126];
microscopy studies demonstrate that low concentrations of some oils may
generate holes on the cell wall of sensitive bacteria including CP,
being vegetative forms particularly lysed [127].
Evidence
about inhibitory spectrum of EOs is contradictory. Some studies
concluded that Gram-positive bacteria are more resistant than
Gram-negative bacteria [128]. However, most works reported that Gram-positive bacteria are more susceptible to EOs than Gram-negative bacteria [123, 129].
The weaker antimicrobial activity against Gram-negative can be
explained considering the structure of their cellular walls, mainly with
regard to the presence of lipoproteins and lipopolysaccharides in the
external membrane that form a barrier to hydrophobic compounds [129, 130].
Unlike
common antibiotics that are often composed of only a single molecular
entity, EOs are multicomponent substances and the antibacterial efficacy
is related to the overall composition and relative concentrations of
active components. For example, thymol and carvacrol, two common
terpenoids present in many EOs, have similar antimicrobial properties
but act differently against Gram-positive or Gram-negative bacteria
based on the locations of one or more functional groups in these two
molecules [30, 131].
The mechanism underlying antibacterial activity against CP and other
Gram-positive bacterial pathogens is unclear at present and therefore
further studies are needed.
The use of EOs to control the proliferation of CP and reduce NE impact on poultry production has been explored [48, 49, 53, 54]. There are numerous reports about the antibacterial effects of Origanum vulgare, Piper nigrum, Syzygium aromaticum, and Thymus vulgaris, and their components, thymol, carvacrol, and eugenol, against Clostridium species [132, 133] including CP [46, 134].
EOs effects on CP-induced NE may be related to a direct antimicrobial
effect on bacterial cells and an indirect effect by modulating gut
microbiota and digestive functions. In vitro CP inhibition was described for many plant extracts and their EOs [127].
Antimicrobial activity was found in 50% of the tested plant species.
Great differences in the inhibitory effect and potency are found among
scientific studies on the activity of EOs that can be partially
explained by the variety of protocols used to obtain EOs solution and to
measure antimicrobial activity [127, 135]. For example, one report [135] used disc diffusion methods and reports high antimicrobial activity (inhibition > 95%) against CP for thyme (T. vulgaris) and oregano (O. vulgare), while Si et al. (2009) [127]
used broth microdilution methods and reported similar results for thyme
but low antimicrobial activity (inhibition between 50 and 80%) for
oregano. Since antimicrobial activity of EOs is related to the combined
effects of several molecules, most reported results choose one of the
main components as indicator of biological activity. Carvacrol and
thymol are two of the most common single molecules used to determine
spices/EOs antimicrobial activity [50, 123],
and differences in presence and concentration of these molecules will
contribute to explain the contradiction of published results. The
aforementioned molecules are main components of several EOs with
antimicrobial activity such as oregano, rosemary, and thyme oils [123, 136].
Differences in activity may also be related to vegetal growth conditions and storage conditions after harvest [137]. These authors compared several commercial stocks of spices Angelica (Angelica archangelica) and Japanese mint (Mentha arvensis var. piperascens) and found clear differences in antimicrobial activity [137]. Some works also reported variations in thymol and carvacrol concentrations within thyme and oregano [137]. Moreover, while some works mention that carvacrol is the main active molecule in thyme, Nevas et al. (2004) [137] described inhibitory effect against CP in Finnish thyme extract without detection of carvacrol.
In poultry, many works report that the inclusion of blends of EOs as dietary supplements has improved productive performance [52, 138]
including weight gain and body mass; however, none of these works
reported changes in intestinal microbiota, apparent metabolizable
energy, or the calculated coefficients of digestibility. According to
Jamroz et al. (2003) [139],
the inclusion of blended supplements containing carvacrol, capsaicin,
and cinnamaldehyde has improved body weight and feed conversion rate in
broilers even to a greater extent than avilamycin in 21-day-old
chickens.
The inclusion of EOs supplementation in
poultry feed alleviated intestinal gross lesions compatible with NE in a
dose-dependent manner on days 21 and 28 [50, 140].
Reduction of CP-induced intestinal damage can be achieved after
reducing the intestinal burden of the microorganism. Si et al. (2009) [127]
reported reductions of 2 or 3 log units of CP counts in chicken ileal
content by carvacrol or citronellol; these results agreed with previous in vivo
studies which showed that EOs containing thymol and/or carvacrol were
able to decrease CP counts in both small and large intestines [51].
One
important criterion that may be considered to select good candidates
for the substitution of AGPs to control CP-induced NE and other poultry
bacterial pathogens is their stability at low pH, as all compounds need
to pass through the stomach with a pH as low as 2. Some EOs like
carvacrol, chamomile roman oil, or citronellal resist acid and retained
their inhibitory activity toward CP after the in vitro preacidic treatment [127].
These results suggest that some EOs can be added to feed and have
intact effect against CP vegetative cells located in the intestinal
lumen. In vivo trials support this since they showed that birds
fed with EOs supplemented had lower concentrations of CP in jejunum,
cecum, cloaca, and feces on day 14, in jejunum, cecum, and feces on day
21, and feces on day 30. Chickens fed with EOs showed significantly
lower CP counts in all portions of the intestine and in the feces, while
the proportion of CP positive birds was also reduced [46]. Unlike tannins [32], no antitoxic activity against CP toxins was demonstrated for EOs.
Together
with direct antimicrobial effects of EOs against CP, changes in
intestinal microbiota also might be related to alleviation of
development of NE intestinal lesions. Several studies have reported that
changes in intestinal microbiota induced by essential oil dietary
supplementation are to the same extent as avilamycin [139].
Once again, evidence is contradictory and needs to consider variations
on EOs origins as well as feed supplement presentation. Cross et al.
(2007) [52] reported that the inclusion of rosemary (R. officinalis), yarrow (A. millefolium var. alba), and thyme (T. vulgaris)
in poultry diets reduced CP counts in cecum and increased coliforms
counts in the same intestinal portion in chickens given any of the
mentioned herbal treatments. Other works mention that blends of EOs
reduce the growth of E. coli and CP in broilers [141, 142]. EOs exhibited a minor or no inhibition on Lactobacillus spp. [52] and some works report an increased number of lactobacilli counts [142].
Thus, EOs may act in a different way compared to AGPs, which tend to
depress bacterial numbers in all the species. While some works report
higher susceptibility to EOs in Gram-positive bacteria, other studies
demonstrated the selectivity of EOs against CP over lactobacilli, both
groups of Gram-positive bacteria. Undoubtedly, further studies are
required to understand the mechanism underlying the group selectivity.
To
control CP-induced NE and other infectious diseases, it is important to
reduce intestinal and environmental bacteria burden. Some EOs
formulations also reduce bacterial populations when applied directly on
the soil and can be used to reduce potential contamination of fresh
organic products, including poultry feed. Previous works with different
bacterial pathogens on food products intended for human alimentation,
including products of plant or animal origin, suggest a promising scene [47, 143, 144].
In the actual poultry productive context where synthetic antimicrobials
are limited or banned, EOs could play an important role in the
innovation of preventive or therapeutic strategies. It is likely that it
will be more difficult for bacteria to develop resistance to the
multicomponent EOs than to common antibiotics that are often composed of
only a single molecular entity. Previous works with tannins [21],
another multicomponent natural antimicrobial substance, may reinforce
this idea. Nevertheless, the lack of studies to determine the safety and
toxicity evaluation of potential changes in flavor, odor, and other
organoleptic characteristics of poultry-derived food products may limit
the use of EOs in poultry. Available information regarding safety in
relation to oral administration of EOs in human and poultry is scanty,
so determinations upon the potential toxicity of EOs administered by
this route are required. The ways in which EOs are applied and the
concentrations at which they are used are important factors related to
their effectiveness. Inhibition studies showed that some pathogenic
bacteria can be inhibited by direct application of EOs components
without affecting the flavor of the food products [145]. Table 2
summarizes the available EOs additives for NE prevention in poultry as
well as their performance and intestinal and antimicrobial effects.
EOs additives for NE prevention in poultry.
6. Conclusions and Perspectives
The
European ban of AGPs in poultry products and recent restrictions on the
use of these compounds in other countries, including Australia and USA,
present several challenges to the poultry industry. Reports from the EU
have shown that the key problem of in-feed antibiotic withdrawal from
poultry diets is the control of NE. Therefore, the cost-benefit in
replacing AGPs with natural alternatives is critical for ensuring the
long-term sustainable poultry production. Plant extracts have a large
variety of bioactive ingredients and thus represent one of the most
promising alternatives to replace AGPs, particularly tannins and
essential oils. However, their application in poultry production has
been largely avoided due to inconsistent evaluation of their efficacy
and lack of full understanding of the modes of action behind them. In
order to support the use of natural plant products to maintain the
productivity rates achieved by AGPs and become acceptable by the
mainstream poultry industry market, different research groups provided
solid scientific evidence addressing the issue of inconsistency across
many studies in literature. In this sense, the development and
utilization of a standardized methodology for production of phytobased
feed additives and evaluation of their biological activity is urgently
needed in order to support the use of different additives. Furthermore, a
better understanding on the impact of phytogenic compounds on gut
microbiota, physiology, and immunology will allow a better use of these
products for economically effective and sustainable poultry production.
Besides
plant extracts, there are other suitable strategies to control NE in
poultry in order to fill the gap left by the ban of AGPs, including
competitive exclusion products, probiotics, prebiotics, organic acids,
enzymes, hen egg antibodies, bacteriophages, and vaccination. However,
to date, no single preventive therapy that can effectively substitute
AGPs and control NE has been found. Therefore, the combination of
different in-feed additives and limiting exposure to CP and other
NE-predisposing microorganisms through biosecurity and vaccination might
be a tool to reduce the incidence of NE and improve gut health in the
absence of AGPs. Effective nonantibiotic prevention of CP-associated
health and performance problems will only be achieved by means of
multidisciplinary research efforts, covering both in vitro molecular functionality approaches together with in vivo
feeding experiments. Plant extracts exert specific effects on gut
microbiota which influence both the emergence of intestinal pathogens
and growth performance of chickens. It has been shown that tannins and
essential oils possess activities in the digestive tract that cover many
of the requirements to control NE. The ability of some tannins to
remain active even in poultry bedding after fecal excretion appears as
an interesting feature to control CP reinfection. Moreover, it has been
proved that resistance of CP against tannins is not easily generated,
allowing a continuous use of these compounds over time. Therefore, these
products may play a key role as a viable, cost-efficient, and safe
alternative to AGPs that could be used to enhance chicken performance
and health as well.
Competing Interests
Some of the authors provide consulting services to companies related to poultry nutrition.
Authors' Contributions
J. M. Diaz Carrasco and L. M. Redondo contributed equally to this work.
References
1. Cooper K. K., Songer J. G. Virulence of Clostridium perfringens in an experimental model of poultry necrotic enteritis. Veterinary Microbiology. 2010;142(3-4):323–328. doi: 10.1016/j.vetmic.2009.09.065. [PubMed] [Cross Ref]
2. Cooper K. K., Songer J. G., Uzal F. A. Diagnosing clostridial enteric disease in poultry. Journal of Veterinary Diagnostic Investigation. 2013;25(3):314–327. doi: 10.1177/1040638713483468. [PubMed] [Cross Ref]
3. Keyburn A. L., Sheedy S. A., Ford M. E., et al. Alpha-toxin of Clostridium perfringens is not an essential virulence factor in necrotic enteritis in chickens. Infection and Immunity. 2006;74(11):6496–6500. doi: 10.1128/iai.00806-06. [PMC free article] [PubMed] [Cross Ref]
4. Van der Sluis W. Clostridial enteritis is an often underestimated problem. World Poultry. 2000;(16):42–43.
5. Songer J. G. Clostridial enteric diseases of domestic animals. Clinical Microbiology Reviews. 1996;9(2):216–234. [PMC free article] [PubMed]
6. Cooper K. K., Songer J. G. Necrotic enteritis in chickens: a paradigm of enteric infection by Clostridium perfringens type A. Anaerobe. 2009;15(1-2):55–60. doi: 10.1016/j.anaerobe.2009.01.006. [PubMed] [Cross Ref]
7. Vierheilig J., Frick C., Mayer R. E., et al.
Clostridium perfringens is not suitable for the indication of
fecal pollution from ruminant wildlife but is associated with excreta
from nonherbivorous animals and human sewage. Applied and Environmental Microbiology. 2013;79(16):5089–5092. doi: 10.1128/aem.01396-13. [PMC free article] [PubMed] [Cross Ref]
8. Gholamiandehkordi
A. R., Timbermont L., Lanckriet A., et al. Quantification of gut
lesions in a subclinical necrotic enteritis model. Avian Pathology. 2007;36(5):375–382. doi: 10.1080/03079450701589118. [PubMed] [Cross Ref]
9. Fukata T., Hadate Y., Baba E., Arakawa A. Influence of bacteria on Clostridium perfringens infections in young chickens. Avian Diseases. 1991;35(1):224–227. doi: 10.2307/1591319. [PubMed] [Cross Ref]
10. Rodgers
N. J., Swick R. A., Geier M. S., Moore R. J., Choct M., Wu S.-B. A
multifactorial analysis of the extent to which eimeria and fishmeal
predispose broiler chickens to necrotic enteritis. Avian Diseases. 2015;59(1):38–45. doi: 10.1637/10774-011614-Reg.1. [PubMed] [Cross Ref]
11. Prescott
J. F., Parreira V. R., Mehdizadeh Gohari I., Lepp D., Gong J. The
pathogenesis of necrotic enteritis in chickens: what we know and what we
need to know: a review. Avian Pathology. 2016;45(3):288–294. doi: 10.1080/03079457.2016.1139688. [PubMed] [Cross Ref]
12. Al-Sheikhly F., Al-Saieg A. Role of Coccidia in the occurrence of necrotic enteritis of chickens. Avian Diseases. 1980;24(2):324–333. doi: 10.2307/1589700. [PubMed] [Cross Ref]
13. Collier
C. T., Hofacre C. L., Payne A. M., et al. Coccidia-induced mucogenesis
promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Veterinary Immunology and Immunopathology. 2008;122(1-2):104–115. doi: 10.1016/j.vetimm.2007.10.014. [PubMed] [Cross Ref]
14. Onderka
D. K., Langevin C. C., Hanson J. A. Fibrosing cholehepatitis in broiler
chickens induced by bile duct ligations or inoculation of Clostridium perfringens
. Canadian Journal of Veterinary Research. 1990;54(2):285–290. [PMC free article] [PubMed]
15. Olazabal
E., Gonzalez R., Flores S., Alcina L. Efectividad de diferentes
combinaciones de tratamientos con antibioticos en la mortalidad por
Clostridium Perfringens en una empresa avicola. Revista Elecrtonica de Veterinaria. 2005;6(2):1–9.
16. Diarra M. S., Malouin F. Antibiotics in Canadian poultry productions and anticipated alternatives. Frontiers in Microbiology. 2014;5, article 282 doi: 10.3389/fmicb.2014.00282. [PMC free article] [PubMed] [Cross Ref]
17. Huyghebaert G., Ducatelle R., Van Immerseel F. An update on alternatives to antimicrobial growth promoters for broilers. Veterinary Journal. 2011;187(2):182–188. doi: 10.1016/j.tvjl.2010.03.003. [PubMed] [Cross Ref]
18. Engberg
R. M., Petersen J. S. Poultry production with and without questionable
feed additives and ingredients. Proceedings of the 13th European
Symposium on Poultry Nutrition; October 2001; Blankenberge, Belgium. pp.
118–124.
19. Page S. W. Antimicrobial Growth Promoters: Where Do We Go from Here? 2006. Current use of antimicrobial growth promoters in food animals: the benefits; pp. 19–51.
20. Tuohy
K. M., Rouzaud G. C. M., Brück W. M., Gibson G. R. Modulation of the
human gut microflora towards improved health using prebiotics—assessment
of efficacy. Current Pharmaceutical Design. 2005;11(1):75–90. doi: 10.2174/1381612053382331. [PubMed] [Cross Ref]
21. Redondo
L. M., Dominguez J. E., Rabinovitz B. C., Redondo E. A., Fernández
Miyakawa M. E. Hydrolyzable and condensed tannins resistance in Clostridium perfringens
. Anaerobe. 2015;34:139–145. doi: 10.1016/j.anaerobe.2015.05.010. [PubMed] [Cross Ref]
22. O'Brien
T. F. Emergence, spread, and environmental effect of antimicrobial
resistance: how use of an antimicrobial anywhere can increase resistance
to any antimicrobial anywhere else. Clinical Infectious Diseases. 2002;34(supplement 3):S78–S84. doi: 10.1086/340244. [PubMed] [Cross Ref]
23. Marshall B. M., Levy S. B. Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews. 2011;24(4):718–733. doi: 10.1128/cmr.00002-11. [PMC free article] [PubMed] [Cross Ref]
24. Castanon J. I. R. History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science. 2007;86(11):2466–2471. doi: 10.3382/ps.2007-00249. [PubMed] [Cross Ref]
25. Casewell
M., Friis C., Marco E., McMullin P., Phillips I. The European ban on
growth-promoting antibiotics and emerging consequences for human and
animal health. Journal of Antimicrobial Chemotherapy. 2003;52(2):159–161. doi: 10.1093/jac/dkg313. [PubMed] [Cross Ref]
26. Van Immerseel F., De Buck J., Pasmans F., Huyghebaert G., Haesebrouck F., Ducatelle R.
Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathology. 2004;33(6):537–549. doi: 10.1080/03079450400013162. [PubMed] [Cross Ref]
27. Dahiya
J. P., Wilkie D. C., Van Kessel A. G., Drew M. D. Potential strategies
for controlling necrotic enteritis in broiler chickens in
post-antibiotic era. Animal Feed Science and Technology. 2006;129(1-2):60–88. doi: 10.1016/j.anifeedsci.2005.12.003. [Cross Ref]
28. Grave
K., Kaldhusdal M., Kruse H., Fevang Harr L. M., Flatlandsmo K. What has
happened in Norway after the ban of avoparcin? Consumption of
antimicrobials by poultry. Preventive Veterinary Medicine. 2004;62(1):59–72. doi: 10.1016/j.prevetmed.2003.08.009. [PubMed] [Cross Ref]
29. Caly
D. L., D'Inca R., Auclair E., Drider D. Alternatives to antibiotics to
prevent necrotic enteritis in broiler chickens: a microbiologist's
perspective. Frontiers in Microbiology. 2015;6, article 1336 doi: 10.3389/fmicb.2015.01336.01336 [PMC free article] [PubMed] [Cross Ref]
30. Yang
C., Chowdhury M. A. K., Huo Y., Gong J. Phytogenic compounds as
alternatives to in-feed antibiotics: potentials and challenges in
application. Pathogens. 2015;4(1):137–156. doi: 10.3390/pathogens4010137. [PMC free article] [PubMed] [Cross Ref]
31. Millet S., Maertens L. The European ban on antibiotic growth promoters in animal feed: from challenges to opportunities. The Veterinary Journal. 2011;187(2):143–144. doi: 10.1016/j.tvjl.2010.05.001. [PubMed] [Cross Ref]
32. Elizondo A. M., Mercado E. C., Rabinovitz B. C., Fernandez-Miyakawa M. E. Effect of tannins on the in vitro growth of Clostridium perfringens
. Veterinary Microbiology. 2010;145(3-4):308–314. doi: 10.1016/j.vetmic.2010.04.003. [PubMed] [Cross Ref]
33. McDougald
L. R., Hofacre E. C., Mathis G., et al. Enhancement of resistance to
coccidiosis and necrotic enteritis in broiler chickens by dietary
muscadine pomace. Avian Diseases. 2008;52(4):646–651. doi: 10.1637/8306-041508-reg.1. [PubMed] [Cross Ref]
34. Schiavone
A., Guo K., Tassone S., et al. Effects of a natural extract of
chestnut wood on digestibility, performance traits, and nitrogen balance
of broiler chicks. Poultry Science. 2008;87(3):521–527. doi: 10.3382/ps.2007-00113. [PubMed] [Cross Ref]
35. Tosi
G., Massi P., Antongiovanni M., et al. Efficacy test of a hydrolysable
tannin extract against necrotic enteritis in challenged broiler
chickens. Italian Journal of Animal Science. 2013;12(3):386–389. doi: 10.4081/ijas.2013.e62. [Cross Ref]
36. Cejas E., Pinto S., Prosdócimo F., et al. Evaluation of quebracho red wood (Schinopsis lorentzii) polyphenols vegetable extract for the reduction of coccidiosis in broiler chicks. International Journal of Poultry Science. 2011;10(5):344–349. doi: 10.3923/ijps.2011.344.349. [Cross Ref]
37. Brenes
A., Viveros A., Goñi I., et al. Effect of grape pomace concentrate and
vitamin E on digestibility of polyphenols and antioxidant activity in
chickens. Poultry Science. 2008;87(2):307–316. doi: 10.3382/ps.2007-00297. [PubMed] [Cross Ref]
38. Brenes
A., Viveros A., Goñi I., Centeno C., Saura-Calixto F., Arija I. Effect
of grape seed extract on growth performance, protein and polyphenol
digestibilities, and antioxidant activity in chickens. Spanish Journal of Agricultural Research. 2010;8(2):326–333. doi: 10.5424/sjar/2010082-1199. [Cross Ref]
39. Cross
D. E., McDevitt R. M., Acamovic T. Herbs, thyme essential oil and
condensed tannin extracts as dietary supplements for broilers, and their
effects on performance, digestibility, volatile fatty acids and
organoleptic properties. British Poultry Science. 2011;52(2):227–237. doi: 10.1080/00071668.2011.559454. [PubMed] [Cross Ref]
40. Viveros
A., Chamorro S., Pizarro M., Arija I., Centeno C., Brenes A. Effects of
dietary polyphenol-rich grape products on intestinal microflora and gut
morphology in broiler chicks. Poultry Science. 2011;90(3):566–578. doi: 10.3382/ps.2010-00889. [PubMed] [Cross Ref]
41. Chamorro
S., Viveros A., Rebolé A., Rica B. D., Arija I., Brenes A. Influence of
dietary enzyme addition on polyphenol utilization and meat lipid
oxidation of chicks fed grape pomace. Food Research International. 2015;73:197–203. doi: 10.1016/j.foodres.2014.11.054. [Cross Ref]
42. Liu
H. N., Liu Y., Hu L. L., et al. Effects of dietary supplementation of
quercetin on performance, egg quality, cecal microflora populations, and
antioxidant status in laying hens. Poultry Science. 2014;93(2):347–353. doi: 10.3382/ps.2013-03225. [PubMed] [Cross Ref]
43. Anderson R. C., Vodovnik M., Min B. R., et al. Bactericidal effect of hydrolysable and condensed tannin extracts on Campylobacter jejuni in vitro. Folia Microbiologica. 2012;57(4):253–258. doi: 10.1007/s12223-012-0119-4. [PubMed] [Cross Ref]
44. Costabile A., Sanghi S., Martín-Pelaez S., et al. Inhibition of Salmonella Typhimurium by tannins in vitro. Journal of Food, Agriculture and Environment. 2011;9(1):119–124.
45. Lupini
C., Cecchinato M., Scagliarini A., Graziani R., Catelli E. In vitro
antiviral activity of chestnut and quebracho woods extracts against
avian reovirus and metapneumovirus. Research in Veterinary Science. 2009;87(3):482–487. doi: 10.1016/j.rvsc.2009.04.007. [PubMed] [Cross Ref]
46. 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. Poultry Science. 2004;83(4):669–675. doi: 10.1093/ps/83.4.669. [PubMed] [Cross Ref]
47. Engberg
R. M., Grevsen K., Ivarsen E., et al. The effect of Artemisia annua on
broiler performance, on intestinal microbiota and on the course of a
Clostridium perfringens infection applying a necrotic enteritis disease
model. Avian Pathology. 2012;41(4):369–376. doi: 10.1080/03079457.2012.696185. [PubMed] [Cross Ref]
48. Lee
S. H., Lillehoj H. S., Jang S. I., Lillehoj E. P., Min W., Bravo D. M.
Dietary supplementation of young broiler chickens with Capsicum and turmeric oleoresins increases resistance to necrotic enteritis. British Journal of Nutrition. 2013;110(5):840–847. doi: 10.1017/s0007114512006083. [PubMed] [Cross Ref]
49. Yang
Y., Wang Q., Diarra M. S., Yu H., Hua Y., Gong J. Functional assessment
of encapsulated citral for controlling necrotic enteritis in broiler
chickens. Poultry Science. 2016;95(4):780–789. doi: 10.3382/ps/pev375. [PubMed] [Cross Ref]
50. Du
E., Gan L., Li Z., Wang W., Liu D., Guo Y. In vitro antibacterial
activity of thymol and carvacrol and their effects on broiler chickens
challenged with Clostridium perfringens
. Journal of Animal Science and Biotechnology. 2015;6(1, article 58) doi: 10.1186/s40104-015-0055-7. [PMC free article] [PubMed] [Cross Ref]
51. Cho
J. H., Kim H. J., Kim I. H. Effects of phytogenic feed additive on
growth performance, digestibility, blood metabolites, intestinal
microbiota, meat color and relative organ weight after oral challenge
with Clostridium perfringens in broilers. Livestock Science. 2014;160(1):82–88. doi: 10.1016/j.livsci.2013.11.006. [Cross Ref]
52. Cross
D. E., McDevitt R. M., 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. British Poultry Science. 2007;48(4):496–506. doi: 10.1080/00071660701463221. [PubMed] [Cross Ref]
53. Timbermont L., Lanckriet A., Dewulf J., et al. Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils. Avian Pathology. 2010;39(2):117–121. doi: 10.1080/03079451003610586. [PubMed] [Cross Ref]
54. Jerzsele
A., Szeker K., Csizinszky R., et al. Efficacy of protected sodium
butyrate, a protected blend of essential oils, their combination, and Bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. Poultry Science. 2012;91(4):837–843. doi: 10.3382/ps.2011-01853. [PubMed] [Cross Ref]
55. Savoia D. Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiology. 2012;7(8):979–990. doi: 10.2217/fmb.12.68. [PubMed] [Cross Ref]
56. Vondruskova
H., Slamova R., Trckova M., Zraly Z., Pavlik I. Alternatives to
antibiotic growth promoters in prevention of diarrhoea in weaned
piglets: a review. Veterinarni Medicina. 2010;55(5):199–224.
57. Hashemi S. R., Davoodi H. Phytogenies as new class of feed additive in poultry industry. Journal of Animal and Veterinary Advances. 2010;9(17):2295–2304. doi: 10.3923/javaa.2010.2295.2304. [Cross Ref]
58. Steiner T. Phytogenics in Animal Nutrition: Natural Concepts to Optimize Gut Health and Performance. Nottingham University Press; 2009.
59. Smulikowska S., Pastuszewska B., Świȩch E., et al. Tannin content affects negatively nutritive value of pea for monogastrics. Journal of Animal and Feed Sciences. 2001;10(3):511–523.
60. Longstaff M., McNab J. M. The inhibitory effects of hull polysaccharides and tannins of field beans (Vicia faba L.) on the digestion of amino acids, starch and lipid and on digestive enzyme activities in young chicks. British Journal of Nutrition. 1991;65(2):199–216. doi: 10.1079/bjn19910081. [PubMed] [Cross Ref]
61. Longstaff
M. A., McNab J. M. The effect of concentration of tannin-rich bean
hulls (Vicia faba L.) on activities of lipase (EC 3.1.1.3) and α-amylase (EC 3.2.1.1) in digesta and pancreas and on the digestion of lipid and starch by young chicks. British Journal of Nutrition. 1991;66(1):139–147. doi: 10.1079/BJN19910017. [PubMed] [Cross Ref]
62. Hashemi S. R., Davoodi H. Herbal plants and their derivatives as growth and health promoters in animal nutrition. Veterinary Research Communications. 2011;35(3):169–180. doi: 10.1007/s11259-010-9458-2. [PubMed] [Cross Ref]
63. Abreu A. C., McBain A. J., Simões M. Plants as sources of new antimicrobials and resistance-modifying agents. Natural Product Reports. 2012;29(9):1007–1021. doi: 10.1039/c2np20035j. [PubMed] [Cross Ref]
64. Simões
M., Bennett R. N., Rosa E. A. S. Understanding antimicrobial activities
of phytochemicals against multidrug resistant bacteria and biofilms. Natural Product Reports. 2009;26(6):746–757. doi: 10.1039/b821648g. [PubMed] [Cross Ref]
65. Redondo
L. M., Chacana P. A., Dominguez J. E., Fernandez Miyakawa M. E.
Perspectives in the use of tannins as alternative to antimicrobial
growth promoter factors in poultry. Frontiers in Microbiology. 2014;5, article 118 doi: 10.3389/fmicb.2014.00118. [PMC free article] [PubMed] [Cross Ref]
66. Windisch W., Schedle K., Plitzner C., Kroismayr A. Use of phytogenic products as feed additives for swine and poultry. Journal of Animal Science. 2008;86(14, supplement):E140–E148. [PubMed]
67. Scalbert A. Antimicrobial properties of tannins. Phytochemistry. 1991;30(12):3875–3883. doi: 10.1016/0031-9422(91)83426-L. [Cross Ref]
68. Karou D., Savadogo A., Canini A., et al. Antibacterial activity of alkaloids from Sida acuta. African Journal of Biotechnology. 2005;4(12):1452–1457.
69. Morrissey J. P., Osbourn A. E. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews. 1999;63(3):708–724. [PMC free article] [PubMed]
70. Lee
K.-W., Everts H., Kappert H. J., Wouterse H., Frehner M., Beynen A. C.
Cinnamaldehyde, but not thymol, counteracts the carboxymethyl
cellulose-induced growth depression in female broiler chickens. International Journal of Poultry Science. 2004;3(9):608–612. doi: 10.3923/ijps.2004.608.612. [Cross Ref]
71. Stavri M., Piddock L. J. V., Gibbons S. Bacterial efflux pump inhibitors from natural sources. Journal of Antimicrobial Chemotherapy. 2007;59(6):1247–1260. doi: 10.1093/jac/dkl460. [PubMed] [Cross Ref]
72. Mueller-Harvey I. Analysis of hydrolysable tannins. Animal Feed Science and Technology. 2001;91(1-2):3–20. doi: 10.1016/S0377-8401(01)00227-9. [Cross Ref]
73. Schofield P., Mbugua D. M., Pell A. N. Analysis of condensed tannins: a review. Animal Feed Science and Technology. 2001;91(1-2):21–40. doi: 10.1016/s0377-8401(01)00228-0. [Cross Ref]
74. Khanbabaee K., van Ree T. Tannins: classification and definition. Natural Product Reports. 2001;18(6):641–649. doi: 10.1039/b101061l. [PubMed] [Cross Ref]
75. Huang
W.-Y., Cai Y.-Z., Zhang Y. Natural phenolic compounds from medicinal
herbs and dietary plants: potential use for cancer prevention. Nutrition and Cancer. 2010;62(1):1–20. doi: 10.1080/01635580903191585. [PubMed] [Cross Ref]
76. Szliszka
E., Krol W. The role of dietary polyphenols in tumor necrosis
factor-related apoptosis inducing ligand (TRAIL)-induced apoptosis for
cancer chemoprevention. European Journal of Cancer Prevention. 2011;20(1):63–69. doi: 10.1097/CEJ.0b013e32833ecc48. [PubMed] [Cross Ref]
77. Ueda
K., Kawabata R., Irie T., Nakai Y., Tohya Y., Sakaguchi T. Inactivation
of pathogenic viruses by plant-derived tannins: strong effects of
extracts from persimmon (Diospyros kaki) on a broad range of viruses. PLoS ONE. 2013;8(1) doi: 10.1371/journal.pone.0055343.e55343 [PMC free article] [PubMed] [Cross Ref]
78. Marín
L., Miguélez E. M., Villar C. J., Lombó F. Bioavailability of dietary
polyphenols and gut microbiota metabolism: antimicrobial properties. BioMed Research International. 2015;2015:18. doi: 10.1155/2015/905215.905215 [PMC free article] [PubMed] [Cross Ref]
79. Serrano
J., Puupponen-Pimiä R., Dauer A., Aura A.-M., Saura-Calixto F. Tannins:
current knowledge of food sources, intake, bioavailability and
biological effects. Molecular Nutrition and Food Research. 2009;53(2):S310–S329. doi: 10.1002/mnfr.200900039. [PubMed] [Cross Ref]
80. Haslam E. Natural polyphenols (vegetable tannins) as drugs: possible modes of action. Journal of Natural Products. 1996;59(2):205–215. doi: 10.1021/np960040. [PubMed] [Cross Ref]
81. Santos-Buelga
C., Scalbert A. Proanthocyanidins and tannin-like compounds—nature,
occurrence, dietary intake and effects on nutrition and health. Journal of the Science of Food and Agriculture. 2000;80(7):1094–1117.
82. Okuda T. Systematics and health effects of chemically distinct tannins in medicinal plants. Phytochemistry. 2005;66(17):2012–2031. doi: 10.1016/j.phytochem.2005.04.023. [PubMed] [Cross Ref]
83. Frutos P., Hervás G., Giráldez F. J., Mantecón A. R. Review. Tannins and ruminant nutrition. Spanish Journal of Agricultural Research. 2004;2(2):p. 191. doi: 10.5424/sjar/2004022-73. [Cross Ref]
84. Butler L. G. Antinutritional effects of condensed and hydrolyzable tannins. Basic Life Sciences. 1992;59:693–698. [PubMed]
85. Khajali F., Slominski B. A. Factors that affect the nutritive value of canola meal for poultry. Poultry Science. 2012;91(10):2564–2575. doi: 10.3382/ps.2012-02332. [PubMed] [Cross Ref]
86. Hofmann
T., Glabasnia A., Schwarz B., Wisman K. N., Gangwer K. A., Hagerman A.
E. Protein binding and astringent taste of a polymeric procyanidin,
1,2,3,4,6-penta-O-galloyl-β-D-glucopyranose, castalagin, and grandinin. Journal of Agricultural and Food Chemistry. 2006;54(25):9503–9509. doi: 10.1021/jf062272c. [PMC free article] [PubMed] [Cross Ref]
87. Surai P. F. Polyphenol compounds in the chicken/animal diet: from the past to the future. Journal of Animal Physiology and Animal Nutrition. 2014;98(1):19–31. doi: 10.1111/jpn.12070. [PubMed] [Cross Ref]
88. Fiesel
A., Gessner D. K., Most E., Eder K. Effects of dietary polyphenol-rich
plant products from grape or hop on pro-inflammatory gene expression in
the intestine, nutrient digestibility and faecal microbiota of weaned
pigs. BMC Veterinary Research. 2014;10(1, article 196) doi: 10.1186/s12917-014-0196-5. [PMC free article] [PubMed] [Cross Ref]
89. Starčević
K., Krstulović L., Brozić D., et al. Production performance, meat
composition and oxidative susceptibility in broiler chicken fed with
different phenolic compounds. Journal of the Science of Food and Agriculture. 2015;95(6):1172–1178. doi: 10.1002/jsfa.6805. [PubMed] [Cross Ref]
90. Goñi
I., Brenes A., Centeno C., et al. Effect of dietary grape pomace and
vitamin E on growth performance, nutrient digestibility, and
susceptibility to meat lipid oxidation in chickens. Poultry Science. 2007;86(3):508–516. doi: 10.1093/ps/86.3.508. [PubMed] [Cross Ref]
91. Fellenberg
M. A., Espinoza A., Peña I., Alarcon J. Antioxidant and bacteriostatic
effects of the addition of extarct of quillay polyphenols (Quillaja saponaria) in the marinade of broiler chicken. Brazilian Journal of Poultry Science. 2011;13(1):71–79.
92. Goliomytis
M., Tsoureki D., Simitzis P. E., Charismiadou M. A., Hager-Theodorides
A. L., Deligeorgis S. G. The effects of quercetin dietary
supplementation on broiler growth performance, meat quality, and
oxidative stability. Poultry Science. 2014;93(8):1957–1962. doi: 10.3382/ps.2013-03585. [PubMed] [Cross Ref]
93. Kamboh
A. A., Zhu W.-Y. Individual and combined effects of genistein and
hesperidin on immunity and intestinal morphometry in
lipopolysacharide-challenged broiler chickens. Poultry Science. 2014;93(9):2175–2183. doi: 10.3382/ps.2014-03971. [PubMed] [Cross Ref]
94. Mansoori
B., Rogiewicz A., Slominski B. A. The effect of canola meal tannins on
the intestinal absorption capacity of broilers using a D-xylose test. Journal of Animal Physiology and Animal Nutrition. 2015;99(6):1084–1093. doi: 10.1111/jpn.12320. [PubMed] [Cross Ref]
95. Kamboh
A. A., Hang S. Q., Bakhetgul M., Zhu W.-Y. Effects of genistein and
hesperidin on biomarkers of heat stress in broilers under persistent
summer stress. Poultry Science. 2013;92(9):2411–2418. doi: 10.3382/ps.2012-02960. [PubMed] [Cross Ref]
96. Liu
L. L., He J. H., Xie H. B., Yang Y. S., Li J. C., Zou Y. Resveratrol
induces antioxidant and heat shock protein mRNA expression in response
to heat stress in black-boned chickens. Poultry Science. 2014;93(1):54–62. doi: 10.3382/ps.2013-03423. [PubMed] [Cross Ref]
97. Athanasiadou S., Kyriazakis I., Jackson F., Coop R. L. Effects of short-term exposure to condensed tannins on adult Trichostrongylus colubriformis
. Veterinary Record. 2000;146(25):728–732. doi: 10.1136/vr.146.25.728. [PubMed] [Cross Ref]
98. Butter N. L., Dawson J. M., Wakelin D., Buttery P. J. Effect of dietary condensed tannins on gastrointestinal nematodes. Journal of Agricultural Science. 2001;137(4):461–469.
99. Min B. R., Hart S. P. Tannins for suppression of internal parasites. Journal of Animal Science. 2003;81(2):102–109.
100. Marzoni M., Castillo A., Romboli I. Dietary inclusion of Quebracho (Schinopsis lorentzii) tannins on productive performances of growing pheasant females. Italian Journal of Animal Science. 2005;4(2):507–509. doi: 10.4081/ijas.2005.2s.507. [Cross Ref]
101. Kim D. K., Lillehoj H. S., Lee S. H., Jang S. I., Lillehoj E. P., Bravo D. Dietary Curcuma longa enhances resistance against Eimeria maxima and Eimeria tenella infections in chickens. Poultry Science. 2013;92(10):2635–2643. doi: 10.3382/ps.2013-03095. [PubMed] [Cross Ref]
102. Chung
K.-T., Lu Z., Chou M. W. Mechanism of inhibition of tannic acid and
related compounds on the growth of intestinal bacteria. Food and Chemical Toxicology. 1998;36(12):1053–1060. doi: 10.1016/s0278-6915(98)00086-6. [PubMed] [Cross Ref]
103. Sakanaka S., Juneja L. R., Taniguchi M. Antimicrobial effects of green tea polyphenols on thermophilic spore-forming bacteria. Journal of Bioscience and Bioengineering. 2000;90(1):81–85. doi: 10.1016/S1389-1723(00)80038-9. [PubMed] [Cross Ref]
104. Engels C., Schieber A., Gänzle M. G. Inhibitory spectra and modes of antimicrobial action of gallotannins from mango kernels (Mangifera indica L.) Applied and Environmental Microbiology. 2011;77(7):2215–2223. doi: 10.1128/aem.02521-10. [PMC free article] [PubMed] [Cross Ref]
105. Kubena L. F., Byrd J. A., Young C. R., Corrier D. E. Effects of tannic acid on cecal volatile fatty acids and susceptibility to Salmonella typhimurium colonization in broiler chicks. Poultry Science. 2001;80(9):1293–1298. doi: 10.1093/ps/80.9.1293. [PubMed] [Cross Ref]
106. Van Parys A., Boyen F., Dewulf J., Haesebrouck F., Pasmans F. The use of tannins to control Salmonella typhimurium infections in pigs. Zoonoses and Public Health. 2010;57(6):423–428. doi: 10.1111/j.1863-2378.2009.01242.x. [PubMed] [Cross Ref]
107. Saif Y. M., Fadly A. M., Glisson J. R., McDougald L. R., Nolan L. K., Swayne D. E. Diseases of Poultry. Blackwell; 2008.
108. M'Sadeq
S. A., Wu S., Swick R. A., Choct M. Towards the control of necrotic
enteritis in broiler chickens with in-feed antibiotics phasing-out
worldwide. Animal Nutrition. 2015;1(1):1–11. doi: 10.1016/j.aninu.2015.02.004. [Cross Ref]
109. Graziani
R., Tosi G., Denti R. In vitro antimicrobial activity of SILVA FEED
ENC® on bacterial strains of poultry origin. Proceedings of the 12th
European Poultry Conference (EPC '06); September 2006; Verona, Italy.
110. Redondo
L. M., Redondo E. A., Delgado F., et al. Control of Clostridium
perfringens necrotic enteritis by tannins added to the diet. Proceedings
of the 8th International Conference on the Molecular Biology and
Pathogenesis of the Clostridia (ClostPath 8); 2013; Palm Cove,
Australia.
111. Song Y., Desta K. T., Kim G., et al. Polyphenolic profile and antioxidant effects of various parts of Artemisia annua L. Biomedical Chromatography. 2016;30(4):588–595. doi: 10.1002/bmc.3587. [PubMed] [Cross Ref]
112. Blaiotta
G., La Gatta B., Di Capua M., Di Luccia A., Coppola R., Aponte M.
Effect of chestnut extract and chestnut fiber on viability of potential
probiotic Lactobacillus strains under gastrointestinal tract conditions. Food Microbiology. 2013;36(2):161–169. doi: 10.1016/j.fm.2013.05.002. [PubMed] [Cross Ref]
113. Hee
Dong Bae, McAllister T. A., Yanke J., Cheng K.-J., Muir A. D. Effects
of condensed tannins on endoglucanase activity and filter paper
digestion by Fibrobacter succinogenes S85. Applied and Environmental Microbiology. 1993;59(7):2132–2138. [PMC free article] [PubMed]
114. Mila I., Scalbert A., Expert D. Iron withholding by plant polyphenols and resistance to pathogens and rots. Phytochemistry. 1996;42(6):1551–1555. doi: 10.1016/0031-9422(96)00174-4. [Cross Ref]
115. Allen
H. K., Levine U. Y., Looft T., Bandrick M., Casey T. A. Treatment,
promotion, commotion: antibiotic alternatives in food-producing animals.
Trends in Microbiology. 2013;21(3):114–119. doi: 10.1016/j.tim.2012.11.001. [PubMed] [Cross Ref]
116. Nohynek
L. J., Alakomi H.-L., Kähkönen M. P., et al. Berry phenolics:
antimicrobial properties and mechanisms of action against severe human
pathogens. Nutrition and Cancer. 2006;54(1):18–32. doi: 10.1207/s15327914nc5401_4. [PubMed] [Cross Ref]
117. Fraenkel
G. S. The raison d'ĕtre of secondary plant substances; these odd
chemicals arose as a means of protecting plants from insects and now
guide insects to food. Science. 1959;129(3361):1466–1470. [PubMed]
118. Tajkarimi M. M., Ibrahim S. A., Cliver D. O. Antimicrobial herb and spice compounds in food. Food Control. 2010;21(9):1199–1218. doi: 10.1016/j.foodcont.2010.02.003. [Cross Ref]
119. Hyldgaard
M., Mygind T., Meyer R. L. Essential oils in food preservation: mode of
action, synergies, and interactions with food matrix components. Frontiers in Microbiology. 2012;3:12. doi: 10.3389/fmicb.2012.00012. [PMC free article] [PubMed] [Cross Ref]
120. Mitscher L. A., Drake S., Gollapudi S. R., Okwute S. K. A modern look at folkloric use of anti-infective agents. Journal of Natural Products. 1987;50(6):1025–1040. doi: 10.1021/np50054a003. [PubMed] [Cross Ref]
121. Baratta
M. T., Dorman H. J. D., Deans S. G., Figueiredo A. C., Barroso J. G.,
Ruberto G. Antimicrobial and antioxidant properties of some commercial
essential oils. Flavour and Fragrance Journal. 1998;13(4):235–244. doi: 10.1002/(sici)1099-1026(1998070)13:4<235::aid-ffj733>3.0.co;2-t. [Cross Ref]
122. Kalemba D., Kunicka A. Antibacterial and antifungal properties of essential oils. Current Medicinal Chemistry. 2003;10(10):813–829. doi: 10.2174/0929867033457719. [PubMed] [Cross Ref]
123. Burt S. Essential oils: their antibacterial properties and potencial applications in foods—a review. International Journal of Food Microbiology. 2004;22(3):201–206.
124. Deans S. G., Ritchie G. Antibacterial properties of plant essential oils. International Journal of Food Microbiology. 1987;5(2):165–180. doi: 10.1016/0168-1605(87)90034-1. [Cross Ref]
125. Oussalah
M., Caillet S., Saucier L., Lacroix M. Inhibitory effects of selected
plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes
. Food Control. 2007;18(5):414–420. doi: 10.1016/j.foodcont.2005.11.009. [Cross Ref]
126. Solórzano-Santos F., Miranda-Novales M. G. Essential oils from aromatic herbs as antimicrobial agents. Current Opinion in Biotechnology. 2012;23(2):136–141. doi: 10.1016/j.copbio.2011.08.005. [PubMed] [Cross Ref]
127. Si
W., Ni X., Gong J., et al. Antimicrobial activity of essential oils
and structurally related synthetic food additives towards Clostridium perfringens
. Journal of Applied Microbiology. 2009;106(1):213–220. doi: 10.1111/j.1365-2672.2008.03994.x. [PubMed] [Cross Ref]
128. Lin C. M., Preston J. F., Wei C. I. Antibacterial machanism of allyl isothiocyanate. Journal of Food Protection. 2000;63(6):727–734. [PubMed]
129. Inouye
S., Takizawa T., Yamaguchi H. Antibacterial activity of essential oils
and their major constituents against respiratory tract pathogens by
gaseous contact. Journal of Antimicrobial Chemotherapy. 2001;47(5):565–573. doi: 10.1093/jac/47.5.565. [PubMed] [Cross Ref]
130. Mann C. M., Cox S. D., Markham J. L. The outer membrane of Pseudomonas aeruginosa NCTC 6749 contributes to its tolerance to the essential oil of Melaleuca alternifolia (tea tree oil) Letters in Applied Microbiology. 2000;30(4):294–297. doi: 10.1046/j.1472-765x.2000.00712.x. [PubMed] [Cross Ref]
131. Kamatou
G. P., Vermaak I., Viljoen A. M. Eugenol—from the remote Maluku Islands
to the international market place: A review of a remarkable and
versatile molecule. Molecules. 2012;17(6):6953–6981. doi: 10.3390/molecules17066953. [PubMed] [Cross Ref]
132. Paster N., Nitzan R. Inhibitory effect of oregano and thyme essential oils. Thymus. 1990:33–37.
133. Dorman H. J. D., Deans S. G. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology. 2000;88(2):308–316. doi: 10.1046/j.1365-2672.2000.00969.x. [PubMed] [Cross Ref]
134. Briozzo
J., Núñez L., Chirife J., Herszage L., D'Aquino M. Antimicrobial
activity of clove oil dispersed in a concentrated sugar solution. Journal of Applied Bacteriology. 1989;66(1):69–75. doi: 10.1111/j.1365-2672.1989.tb02456.x. [PubMed] [Cross Ref]
135. Silva
N., Alves S., Gonçalves A., Amaral J. S., Poeta P. Antimicrobial
activity of essential oils from mediterranean aromatic plants against
several foodborne and spoilage bacteria. Food Science and Technology International. 2013;19(6):503–510. doi: 10.1177/1082013212442198. [PubMed] [Cross Ref]
136. O'Bryan
C. A., Pendleton S. J., Crandall P. G., Ricke S. C. Potential of plant
essential oils and their components in animal agriculture—in vitro studies on antibacterial mode of action. Frontiers in Veterinary Science. 2015;2, article 35:8. doi: 10.3389/fvets.2015.00035. [PMC free article] [PubMed] [Cross Ref]
137. Nevas
M., Korhonen A.-R., Lindström M., Turkki P., Korkeala H. Antibacterial
efficiency of finnish spice essential oils against pathogenic and
spoilage bacteria. Journal of Food Protection. 2004;67(1):199–202. [PubMed]
138. Hernández
F., Madrid J., García V., Orengo J., Megías M. D. Influence of two
plant extracts on broilers performance, digestibility, and digestive
organ size. Poultry Science. 2004;83(2):169–174. doi: 10.1093/ps/83.2.169. [PubMed] [Cross Ref]
139. Jamroz
D., Orda J., Kamel C., Wilczkiewicz A., Wertelecki T., Skorupinska J.
The influence of phytogenic extracts on performance nutrient
digestibility, carcass characteristics, and gut microbial status in
broiler chickens. Journal of Animal and Feed Sciences. 2003;12(3):583–596.
140. Mathlouthi
N., Bouzaienne T., Oueslati I., et al. Use of rosemary, oregano, and a
commercial blend of essential oils in broiler chickens: in vitro
antimicrobial activities and effects on growth performance. Journal of Animal Science. 2012;90(3):813–823. doi: 10.2527/jas.2010-3646. [PubMed] [Cross Ref]
141. Losa
R., Kohler B. Prevention of colonisation of Clostridium perfringens in
broilers intestine by essential oils. Proceedings of the 13th European
Symposium on Poultry Nutrition; 2001; Blankenberge, Belgium. pp.
133–134.
142. Tucker
L. Maintaining poultry performance in antibiotic free diets by
supplementation with commercial botanical feed ingredients. Proceedings
of the 7th WPSA Asian Pacific Federation Conference; 2002; Gold Coast,
Australia. pp. 227–230.
143. Yossa N., Patel J., Millner P., Lo M. Inactivation of Salmonella in organic soil by cinnamaldehyde, eugenol, ecotrol, and sporan. Foodborne Pathogens and Disease. 2011;8(2):311–317. doi: 10.1089/fpd.2010.0685. [PubMed] [Cross Ref]
144. Lu Y., Wu C. Reduction of Salmonella enterica contamination on grape tomatoes by washing with thyme oil, thymol, and carvacrol as compared with chlorine treatment. Journal of Food Protection. 2010;73(12):2270–2275. [PubMed]
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