Livestock Science 189 (2016) 32–49
Contents lists available at ScienceDirect
Livestock Science
journal homepage: www.elsevier.com/locate/livsci
Review article
Antimicrobial activity of plant-food by-products: A review focusing
on the tropics
J.L. Guil-Guerrero a,b,n, L. Ramos a, C. Moreno a, J.C. Zúñiga-Paredes a, M. Carlosama-Yepez a,
P. Ruales a
a
b
Ecuadorian Agency for Quality Assurance in Agriculture, AGROCALIDAD, Tumbaco, Ecuador
Food Technology Division, Agrifood Campus of International Excellence, ceiA3, University of Almería, 04120 Almería, Spain
art ic l e i nf o
a b s t r a c t
Article history:
Received 19 November 2015
Received in revised form
14 April 2016
Accepted 26 April 2016
This review characterizes the antimicrobial potential of agricultural by-products from tropical countries,
assessing their suitability as substitutes for antibiotics in animal-production farms. This study responds
to an increasing trend in the use of antibiotics and other growth promoters in farm animals in tropical
areas. Such use is intended to improve the daily gastrointestinal welfare and also to provide resistance or
prevention against acute or chronic diseases, such as infectious diarrhoea and inflammatory bowel
diseases. Such diseases pose a major challenge in all countries, but tropical conditions encourage the
survival of bacteria and pathogens and commensal bacteria more than in temperate climates, and
therefore tropical countries need particular attention in order to solve this dilemma. Fortunately, as a
substitute to antibiotics, these countries have considerable antimicrobial potential in plants – that is,
agricultural by-products contain a diverse pool of bioactive compounds with antimicrobial properties,
which could be employed as feed supplements to improve animal health. By-products from tropical
countries constitute rich sources of bioactive compounds, such as phenolics, carotenoids, essential oils,
active peptides, saponins, and sterols. Among reviewed by-products, high activity has been detected for
avocado seeds, cocoa bean shell, and banana peels, while for isolated pure compounds, high activity has
been reported for: alkaloids from lupine and capsaicin; phenolics such as gallic and chlorogenic acids,
naringin, exiguaflavanone D, and kenusanone A; and saponins from Capsicum seeds. Some by-product
extracts have shown minimum inhibitory concentration (MIC) values very close to that of their isolated
pure components. In conclusion, plant-food by-products of tropical origin contain diverse active compounds which act effectively against most pathogenic bacteria tested, avoiding well-characterized cell
damage.
& 2016 Elsevier B.V. All rights reserved.
Keywords:
Tropical plant-food by-products
Antimicrobial activity
Antibiotic resistance
Minimum inhibitory concentration
Phenolics
Essential oils
Contents
1.
2.
3.
4.
5.
n
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Antimicrobial characteristics of active compounds usually found in tropical plant-food by-products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Alkaloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Essential oils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Glycosides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.
Phenolics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.5.
Peptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.6.
Saponins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Antimicrobial activity of extracts from plant-food by-products of tropical origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Comparative study on antimicrobial activity between pure active compounds and extracts from plant-food by-products . . . . . . . . . . . . . . . . .
Some considerations concerning using plant-food by-products to feed farm animals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Corresponding author at: Ecuadorian Agency for Quality Assurance in Agriculture, AGROCALIDAD, Tumbaco, Ecuador.
E-mail address: [email protected] (J.L. Guil-Guerrero).
http://dx.doi.org/10.1016/j.livsci.2016.04.021
1871-1413/& 2016 Elsevier B.V. All rights reserved.
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J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
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6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
1. Introduction
A major problem in animal production is to maintain the health
of farm animals. Diseases are critical in such contexts, not only
afflicting animal health and well-being, but also reducing economic profits of producers. For this, antibiotics are extensively
used. These can be administered to farm animals either to treat
and prevent infectious diseases or to boost animal productivity at
sub-therapeutic dosages (Sarmah et al., 2006). However, the latter
is the non-therapeutic use of valuable drugs, and these should be
reserved to special circumstances only (Alanis, 2005).
Currently, in tropical areas, the use of antibiotics and other
growth promoters in farm animals is following an increasing
trend. This poses a major problem, because tropical conditions
encourage the survival of bacteria, and more pathogens and
commensals are found in tropical environments than in temperate
ones (Okeke et al., 1999; Lipp et al., 2002; Hellberg and Chu, 2015).
Furthermore, once antibiotic-resistant organisms arise, they tend
to spread rapidly in developing tropical countries. Therefore, antibiotic-resistant bacterial strains selected in Western countries
might be introduced in developing countries before the drug to
which they are resistant becomes available (Okeke and Edelman,
2001). The spread of the resistance to antibiotics takes place by the
transmission of related genes which have become highly mobile
since antibiotic chemotherapy started. The most disturbing issue is
the use of antibiotics in agriculture as growth promoters and for
treatment of diseases in intensively reared farm animals. Such use
has led to pathogenic bacteria possessing resistance genes and the
spread of these genes to the soil bacterial community (Séveno et al.,
2002; Singer et al., 2006). Such genes have been characterized as
diverse, mobile, and abundant in, for example, Chinese swine farms,
where antibiotics and heavy metals used as feed supplements are
elevated in manures, suggesting the potential for selection of resistance traits. Also, the unmonitored use of antibiotics and metals is
causing the emergence and release of antibiotic resistance genes to
the environment (Zhu et al., 2013; Woappi et al., 2014).
There are many well-documented examples in the literature
concerning the emergence and quick spread of antibiotic resistance bacteria in tropical developing countries. A crucial fact
surrounding this problem is the abusive veterinary use of antibiotics, which occurs mainly for preventive purposes, with the
result that antibiotic residues appear in the environment, indicating the excessive use in animal-production farms (Farrar,
1985; Hart and Kariuki, 1998; Okeke et al., 2005, 1999). Surveys
have been made to determine the scope of this environmental
problem, for example in the Mekong Delta (Vietnam), where the
concentrations of sulfonamides have been measured as an indicator of inputs of veterinary medicines in local waters. The
concentrations, similar to those usually used in veterinary medicine, were found to be relatively high. Also, extremely high concentrations of sulfamethazine were detected in pig-farm wastewaters (Managaki et al., 2007). Especially the use of antibiotics in
aquaculture can cause the development of antibiotic resistance
among pathogens, thus constituting a potential pathway to infect
humans and farm animals. However, this problem has not yet been
thoroughly investigated. For instance, antibiotics are commonly
used on a regular basis in shrimp farming to prevent disease
outbreaks. To solve this dilemma, a more restrictive use of antibiotics could have positive effects for the individual farmer and,
simultaneously, decrease the impact on regional human medicine
and adjacent coastal ecosystems (Milewski, 2001; Holmström
et al., 2003; Heuer et al., 2009; Hamilton, 2011).
Although efforts are made to regulate and limit the use of antibiotics in agriculture, it is difficult to eradicate such activity,
unless substitutes for these are found. As mentioned above, the
problem is acute in tropical developing countries. However, in
terms of a substitute to antibiotics, these countries have considerable antimicrobial potential, which so far has hardly been
explored or used—that is, agricultural by-products. These contain
a diverse pool of bioactive compounds with antimicrobial properties which should be taken advantage of as feed supplements to
improve animal health (Greathead, 2003; Rochfort, 2008; Shabtay
et al., 2008; Bocquier and González-García, 2010).
This review characterizes the antimicrobial potential of agricultural by-products from tropical countries, with the aim of assessing their suitability as substitutes for antibiotics in animalproduction farms. Tropical crops have well-defined characteristics,
and those discussed here have been selected according to the
criteria of Morales (2009).
2. Antimicrobial characteristics of active compounds usually
found in tropical plant-food by-products
Several reports examine the microbiological activities of a small
number of secondary metabolites usually present in plant-food byproducts, such as tannins, terpenoids, alkaloids, and phenolics.
However, all these metabolites have a great number of subclasses of
active compounds, so that the list of compounds to check in byproducts is almost inexhaustible. Regardless of their better or worse
antimicrobial properties, it bears considering that the use of these
compounds in the pure state for animal production may induce similar problems to those encountered with synthetic ones, and thus a
careful assessment of the potential benefits of intake of each of them
is needed. Selected examples of antimicrobial activity of active
compounds found in plant-food by-products are presented in Table 1.
2.1. Alkaloids
With great structural diversity, alkaloids have no single classification. Among plant foods, such compounds occur mainly in
Solanaceae and Fabaceae, and in larger or smaller amounts in their
by-products. Pepper (Capsicum annuum, Solanaceae) contains alkamide alkaloids such as affinin and capsaicin (Fig. 1), which have
very low toxicity and are applied in pain therapy (Rios and Olivo,
2014). Potato (Solanum tuberosum, Solanaceae) contains several
toxic and teratogenic glycoalkaloids (Slanina, 1990). Lupine (Lupinus angustifolius, Fabaceae) contains a large number of quinolizidine alkaloids, notably 13α-hydroxylupanine and lupanine (Fig. 1).
Their toxicity varies largely depending of the species, the range of
minimal lethal dose from 20 to 200 mg/kg live weight (Keeler,
1989). Some of these (affinin, capsaicin, 13α-hydroxylupanine and
lupanine) have been assayed against pathogenic bacteria, namely
Staphylococcus aureus, Bacillus subtilis, and Escherichia coli (Wei
et al., 2006; Erdemoglu et al., 2007). The action mechanism of
highly unsaturated planar quaternary alkaloids is attributed to
their ability to intercalate with DNA (Cowan, 1999). Although this
strongly inhibitory action is promising, the bitter taste of alkaloids
34
Table 1
Selected examples of antimicrobial activity of active compounds found in plant-food by-products of tropical origin.
Active
compounds
Main compounds groups
Active compounds
Affinin and capsaicin
Alkaloids from
Capsicum
annuum
13α-Hydroxylupanine
Lupanine
13α-Tigloyloxylupanine
Essential oil from Terpene hydrocarbons
Mangifera indica
peels
Main components:
δ-3-carene
α-terpinolene
α-copaene
CaryophyIlene
Turmeric oil, a by- Terpene
product from
curcumin
manufacture
ar-turmerone
β-trans-farnesen
turmerone
curlone
Glucosides
– Seco-iridoid - oleuropein glucoside
Glucosinolates hydrolysis products:
– Allylisothiocyanate
– Benzylisothiocyanate
– 2-phenylethylisothiocyanate
Tyrosol, gallic, caffeic, ferulic, and chlorogenic acids
Phenolics
Simple phenolic acids
Phenolics
Simple phenolic acids
Phenolics
Simple phenolic acids
Phenolics
Simple phenolic acids
Chlorogenic, caffeic, p-coumaric and ferulic acids
Phenolics
Simple phenolic acids
Gallic acid, methyl gallate, ethyl gallate,
methyl m-digallate, p-hydroxybenzoic
acid,and succinic acid monomethyl ester
–
–
–
–
–
–
–
Chlorogenic acid
Caffeic acid
p-coumaric acid
Ferulic acid
Hydroxycinnamic acids
Benzoic acid
Phenylacetic phenylpropionic
Escherichia coli
Pseudomonas
solanacearum
Bacillus subtilis
Saccharomyces
cerevisiae
Staphylococcus aureus
B. subtilis
E. coli
Pseudomonas
aeruginosa
B. subtilis
S. aureus
E. coli
P. aeruginosa
Aspergillus flavus
Candida albicans
Bacillus cereus
Bacillus coagulans
B. subtilis
S. aureus
E. coli
P. aeruginosa
E. coli
P. aeruginosa
L. monocytogenes
S. aureus
E. coli
P. aeruginosa
L. monocytogenes
S. aureus
L. monocytogenes
E. coli
Lactobacillus spp.
S. aureus
P. aeruginosa
C. albicans.
L. monocytogenes strains
S. aureus
S. epidermidis
Corynebacterium
xerosis
Micrococcus luteus
P. aeruginosa.
Findings
References
Wei et al.
– Affinin inhibited the growth of E. coli and S. cerevisiae at 25 mg/ml.
– Capsaicin retarded the growth of E. coli and P. solanacearum, and strongly in- (2006)
hibited B. subtilis growth.
– These alkaloids exert high antibacterial activity.
Erdemoglu
et al. (2007)
– This essential oil showed a broad spectrum activity against Gram-positive and El-Hawary
and Rabeh
Gram-negative bacteria, specially hindi cultivar, and had significant activity
(2014)
against C. albicans.
– Turmeric oil had antibacterial activity against several bacteria.
Negi et al.
(1999)
– Isothiocyanates showed significant antimicrobial activities.
– P. aeruginosa was the most sensitive microorganism, and L. monocytogenes was
the most resistant.
– Synergy between streptomycin and allylisothiocyanate and 2-phenylethylisothiocyanate against Gram-negative bacteria.
– Phenolic acids showed low antibacterial efficiency.
– Synergy between streptomycin and phenolic acids against Gram-bacteria.
Saavedra et al.
(2010)
Saavedra et al.
(2010)
– Phenolic acids mixtures generally exhibited additive antilisterial effects.
– Strong relationship between pH and antilisterial activity.
Wen et al.
(2003)
Cueva et al.
– E. coli was susceptible to phenolic acids but to varying extents.
– Phenolic acids inhibited the growth of several lactobacilli species and pathogens (2010)
(C. albicans and S. aureus)
– Only P. aeruginosa was not susceptible to phenolic compounds.
– Phenolic acids exhibited activity against several L. monocytogenes strains.
– Concentration dependant and synergism for single compounds and mixtures of
phenolic acids, respectively.
– Both bactericidal and bacteriostatic activities were observed, and the effects
were contingent upon medium pH.
– Gallic acid was active against: S. aureus, S. epidermidis, Corynebacterium xerosis,
and Micrococcus luteus
– Methyl m-digallate was active against:
– P. aeruginosa
Wen et al.
(2003)
Liang et al.
(2010)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Alkaloids from
Lupinus
angustifolius
Target microorganism
Flavonol: Galangin
Phenolics
Flavonoids
Phenolics
Flavonoids
Phenolics
Flavonoids
Phenolics
Flavonoids
Phenolics
Flavonoids
Phenolics
Flavonoids
Phenolics
Flavonoids
B. cereus
Tea flavan-3-ol:
Gallocatechin, epigallocatechin, catechin, epicatechin, and theaflavin
gallates
Green tea flavan-3-ol:
E. coli O157:H7
epigallocatechin gallates
Fungi:
Flavan-3-ol:
C. albicans
Pyrogallol catechin
Catechol catechin.
Gram-negative
Bermagot peel flavanones:
bacteria:
Neohesperidin,
E. coli
Hesperetin (aglycone)
Pseudomonas putida
Neoeriocitrin
Salmonella enterica
Eriodictyol (aglycone)
Gram-positive
Naringin
bacteria:
Naringenin (aglycone)
Listeria innocua
B. subtili
S. aureus
Lactococcus lactis
Yeast:
S. cerevisiae
Favanol
Vibrio cholerae
Streptococcus mutans,
Campilobacter jejuni,
Clostridium perfringes
E. coli
Chalcones
S. aureus
E. coli
Proanthocyanidins
Uropathogenic E. coli,
Cariogenic S.mutans
Oxacillin-resistant S.
aureus
Phenolics
Poliphenolics
Tetrahydroxyflavanones
Phenolics
Natural or natural-based compounds and some synthetic
derivatives
Tannins
Phenolic acids, flavones, flavonols, flavanones, isoflavones, synthetic flavonoids,
coumarins, cathechins, gallates, stilbene
S. aureus
Tannic acid, gallic acid, ellagic acid,
(–)-epicatechin, (–)-epicatechin gallate and
(–)-epigallocatechin gallate
Penta-, hexa-, hepta-, 3 octa-, nona-, and
B. subtilis
deca-O-galloylglucose
B. cereus
Clostridium botulinum
C. jejuni
L. monocytogenes
Phenolics
Phenolics
Gallotannins isolated from
mango kernels
S. aureus NCTC 6571
Methicillin-resistant S.
aureus (MRSA)
Chlamydia pneumoniae
– Galangin induced aggregation of bacterial cells.
– Cytoplasmic membrane was a target site for the activity of this compound.
– Most flavonoids were found to be more active than antibiotics, such as tetracycline or vancomycin,.
Cushnie et al.
(2007)
Friedman
et al. (2006)
– Inhibitory effects on virulence phenotypes and gene expression regulated by
quorum sensing (QS)
– Pyrogallol catechin showed stronger antifungal activity against C. albicans than
catechol catechin.
– Synergism among catechin and different antimycotics.
– Synergism between eriodictyol and hesperetin against E. coli and S. enterica, and
between eriodictyol and naringenin against S. enterica and P. putida, which
could by due to the combined reaction with the cell membrane.
– Slight antagonistic interaction for naringenin and hesperetin against E. coli and
S. enterica, and for eriodictyol and hesperetin against P. putida. This could be due
to a competition for specific target sites or inhibition of uptake by the bacterial
cells.
Lee et al.
(2009)
Hirasawa and
Takada (2004)
Mandalari
et al. (2007)
– In vitro bacterial growth inhibition
Daglia (2012)
– The anti-staphylococcal activity of chalcones related to the energy difference
between the two highest occupied molecular orbitals (HOMO and HOMO-1).
– Several mechanisms were involved in the bacterial growth inhibition:
Destabilization of the cytoplasmic membranes.
Permeabilization of the cell membranes.
Inhibition of extracellular microbial enzymes.
Direct actions on microbial metabolism.
Deprivation of the substrates required for microbial growth, such as iron and
zinc (via proanthocyanidin chelation with the metals), whose depletion can
severely limit bacterial growth.
Batovska et al.
(2009)
Heinonen
(2007)
Dixon et al.
(2005)
– 2′,4′- or 2′,6′-dihydroxylation of the B ring and 5,7-dihydroxylation of the A ring
in the flavanone structure were important for significant anti-MRSA activity.
– Both natural phenolics and synthetic compounds derived from natural structures showed high activity.
– The most active group was that of gallates.
– Tannic acid inhibited the formation of fibrin and produced a marked increase in
the antistaphylococcal activity of oxacillin.
Tsuchiya et al.
(1996)
Alvesalo et al.
(2006)
Akiyama et al.
(2001)
– Gram- positive bacteria were generally more susceptible to gallotannins than Engels et al.
(2011)
Gram-negative ones.
– The inhibitory activity of gallotannins was attributable to their strong affinity to
iron, and probably was also related to the inactivation of membrane-bound
proteins.
35
Flavonoids
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Phenolics
36
Table 1 (continued )
Active
compounds
Main compounds groups
Active compounds
Peptide isolated from the seeds
of mango, Moringa oleifera
Proteins
Peptide from palm kernel cake
Saponins
Saponin fraction isolated from
the leaves of Solanum xanthocarpum and Centella asiatica
Saponins
Saponins isolated from the
shoots of oats (Avena sativa)
26-desglucoavenacoside and avenacosides
Saponins
Saponins from the seeds of
Capsicum annuum
Furostanol saponins: capsicoside E, capsicoside F capsicoside G
Saponins
Saponins from Medicago sp.
Saponins
Saponins from Yucca
Saponins,
Prosapogenins
Sapogenin mixtures
5β-spirostan-3β-ol saponins
S. aureus
Eenterotoxigenic E. coli
Salmonella enterica
Lactobacillus
plantarum
P. aeruginosa
Streptococcus
pyogenes
P. aeruginosa
Methicillin-resistant
S. aureus
B. cereus
B. subtilis
Bacillus thuringiensis
Lisinibacillus
sphaericus
Clostridium perfringens
Gram-negative
bacteria:
Klepsella pneumoniae,
E. coli
Gram -positive:
S. aureus
Fungi:
Aspergillus fumigatus
Aspergillus niger
Fungi:
Fusarium graminearum, Rhizoctonia solani
Pyrenophora teres and
spp.
Bacteria:
Pseudomonas spp.
Rathyibacter
Corynebacterium
Yeast:
S. cerevisiae
C. albicans, and others
Fungi:
Penicillium expansum
Phoma terrestris, and
others
Gram
–positive
bacteria:
B. subtilis B. cereus
S. aureus
E. faecalis
Fungi :
C. albicans, C. tropicalis
C. laurentii
B. capitatus
S. cerevisiae
Bacillus pasteurii
S. cerevisiae
Findings
References
– Peptides induced bacterial membrane damage.
– Bactericidal activity localized into a sequence prone to form a helix-loop-helix
structural motif.
– The assembly of various peptides into a branched structure enhances the
activity.
– Peptides had no toxic effects on human red blood cells.
– The peptide showed antibacterial activity against Gram-positive bacteria,
especially Bacillus species
Suárez et al.
(2005)
Tan et al.
(2013)
Kannabiran
et al. (2009)
Bahraminejad
– The bacterial growth was not inhibited.
et al. (2008)
– Activity of saponins on fungi:
Most Pyrenophora species were inhibited by the crude extract of oats.
No effects on: F. graminearum, Mycosphaerella pinodes and Rhizoctonia solani.
– The isolated pure saponins induced weak growth inhibition against both Gram- Iorizzi et al.
(2002)
positive and Gram-negative bacteria.
– The antiyeast activity related to the combination of the oligosaccharide chain
with an O-methyl group and hydroxyl groups.
– The presence of sugars in the saponin molecules was not determinant for an- Avato et al.
timicrobial efficacy.
(2006)
– Saponins inhibited microbial growth at low cell densities.
– Saponins had no effects on dense microbial populations.
– Implications for gut microbes differ according to their ecological niches.
Killeen et al.
(1998)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Proteins
Target microorganism
Gram – positive:
S. aureu
Gram-negative:
Salmonella
typhimurium
E. coli ATCC 933
– Saponins showed antimicrobial activity against Gram-positive bacteria and Hassan et al.
were not active against Gram-negative bacteria.
(2010)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
37
could be rejected by animals when such compounds surpass a
concentration limit. Therefore, cultivars with varying alkaloid
contents should be evaluated in feeding studies concerning antimicrobiological properties. It should also be considered that many
plant species are toxic for animals and humans due to their high
alkaloid content. This constitutes a major problem in tropical
countries due to their high plant biodiversity but lack of information on the toxicity of many of those plants (Díaz, 2015).
2.2. Essential oils
These include volatile compounds of terpenoid or non-terpenoid origin, all being hydrocarbons and oxygenated derivatives.
Most essential oils are GRAS (generally recognized as safe; Si et al.,
2006) and thus consumption of products containing these oils
should not exert any adverse effects on livestock. Among plant
foods, these oils are found mainly in the peels of some fruits, such
as mango and Citrus species, and therefore occur in their by-products. Essential oils have been checked in mango peels, a typical
by-product of mango cultures. Terpene hydrocarbons have been
found in such oils, with δ-3-carene, α-terpinolene, α-copaene, and
caryophyIlene at the top of the range (Fig. 2). These oils have a
broad spectrum activity against Gram-positive and Gram-negative
bacteria, as well as significant antifungal action (El-Hawary and
Rabeh, 2014). Another essential oil tested was turmeric oil, a byproduct from curcumin manufacture. It contains ar-turmerone, βtrans-farnesene, turmerone, and curlone, as the main components.
Such oil was found to be active against several Gram-positive and
Gram-negative bacteria (Negi et al., 1999). Essential oils displaying
high antibacterial activity against pathogens contain mainly phenolic compounds such as carvacrol, eugenol, and thymol (Lambert
et al., 2001; Burt et al., 2004). Thus, they act like other phenolics,
for example, disturbing the cytoplasmic membrane, disrupting the
proton motive force, electron flow, active transport, and coagulation of cell contents (Burt et al., 2004). Other crops yield by-products containing essential oils, such as Citrus species, the peels of
which are rich in these compounds; however, they have not been
considered in this work because they lack of a clear-cut tropical
crop distribution.
A major problem when using plants containing essential oils or
when using pure essential oils as feed supplements is that the percentages of both their total and individual compounds can vary largely. For example, the carvacrol content of an essential oil blend can
vary from 19 ppm (Kücükyillmaz et al., 2012) to 300 ppm (Giannenas
et al., 2003). Such variation can negatively affect the metabolism,
performance, and immunity of farm animals (Lee et al., 2004).
Saponins
Saponin yuca-rich extract
containing 30% steroid
saponin
(Ultra Bio-Logic Inc. Rigadu,
Quebec, Canada)
2.3. Glycosides
Glycosides are molecules in which a sugar is bound to another
functional group via a glycosidic bond, and they are classified according to the chemical nature of the aglycone. For example, there
are phenolic glycosides and cyanogenic glycosides, the latter
containing a cyanide group such as aglycone. Many plants store
chemicals in the form of inactive glycosides, which can be activated by enzyme hydrolysis. Glucosinolates, the precursors of
isothiocyanates, are present in 16 dicotyledonous families including a large number of edible species, mainly in Brassica species
(Fahey et al., 2001). Depending on the concentration and structural
types of these compounds, their biological effects can be toxic,
antinutritional or beneficial to health. For livestock, most problems
are derived from rapeseed meal (Assayed and Abd El-Aty, 2009).
Products from glucosinolate hydrolysis have been evaluated as
antimicrobial agents in Gram-positive and Gran-negative bacteria.
Among tested species, isothiocyanates had significant antimicrobial activities, Pseudomonas aeruginosa being the most
38
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
sensitive microorganism, while Listeria monocytogenes proved the
most resistant. Synergy between streptomycin and allyl isothiocyanate and 2-phenylethyl isothiocyanate (Fig. 3) against
Gram-negative bacteria has been reported (Saavedra et al., 2010).
2.4. Phenolics
Phenolics are molecules having one or more unsaturated rings
with one or more hydroxyl groups, constituting an ubiquitous
group of secondary metabolites that occur profusely in species of
the plant kingdom with wide pharmacological activities. These
increase bile secretion, reduce blood-cholesterol and lipid levels,
and have antimicrobial activity against some strains of bacteria
(Ghasemzadeh and Ghasemzadeh, 2011). Plant phenolics include
phenolic acids, flavonoids, and tannins (Fig. 4), as the most frequent parent structures (Dai and Mumper, 2010).
Phenolic acids occur in most plant foods, mainly in seeds, fruit
peels, and leaves. Among these, caffeic acid is reportedly active
against viruses, bacteria, and fungi, while eugenol has been classified as bacteriostatic (Cowan, 1999). Low-molecular-weight
phenolic acids exert antimicrobial effects by the diffusion of the
undissociated acid across the membrane, leading to the acidification of the cytoplasm and, in some cases, cell death (SánchezMaldonado et al., 2014). However, factors related to the lipophilicity such as pH, ring substitutions (hydroxyl and methoxy groups),
and the saturation of the side chain are determinant for the activity of cinnamic acids (Almajano et al., 2007; Sánchez-Maldonado et al., 2014). The main reports concerning the antimicrobial action of phenolic acids are presented in Table 1. Notice
that on a regular basis, the targeted microorganisms were the
pathogens E. coli, Lactobacillus spp., Staphylococcus aureus, P. aeruginosa, and L. monocytogenes strains, while a wide spectrum of
compounds has been tested. Generally, all these compounds have
been found to be quite active, both as bactericidal and bacteriostatic, the effect being contingent upon a medium pH (Wen et al.,
2003), although some authors have found low efficiency for individual compounds (Saavedra et al., 2010). In any case, mixtures
of compounds have been described as more active than individual
ones (Wen et al., 2003). In addition, synergy between
Fig. 1. Chemical structure of alkaloids identified in pepper (Rios and Olivo, 2014)
and lupine (Keeler, 1989). Compounds were drawn using Chem Draw Ultras software (Chem Draw Ultra, Cambridge Soft Co., MA, USA).
streptomycin and phenolic acids against Gram-bacteria has been
reported (Saavedra et al., 2010).
Another group of phenolics are flavonoids, which are ubiquitous
in fruits and vegetables and their by-products. These have varied
activity due to their structural diversity, and their toxicity is low in
farm animals (Havsteen, 1983). All flavonoids have a common C6C3-C6 structure consisting of two aromatic rings (A and B) linked
through a three-carbon chain, organized mostly as an oxygenated
heterocycle (ring C). Properties include antibacterial activity and
suppression of bacterial virulence. In addition, they have been demonstrated to act in synergism with antibiotics. Their action mechanism is the inhibition of several bacterial virulence factors:
quorum-sensing signal receptors, enzymes, and toxins (Cushnie and
Lamb, 2011). Their activity is believed to be due to their capacity to
form complexes with both extracellular and soluble proteins as well
as bacterial cell walls, although high-lipophilic flavonoids can disrupt microbial membranes (Tsuchiya et al., 1996). Antimicrobial
experiments are listed in Table 1. Several flavonoids have been
tested against: pathogenic bacteria such as E. coli, Pseudomonas,
Salmonella, Listeria, Bacillus, Staphylococcus, Vibrio, Streptococcus,
Campilobacter, Clostridium, and Lactococcus species; yeast such as
Saccharomyces cerevisiae; and fungi such as Candida albicans. Few
authors have described some of the mechanisms by which these
compounds exert their effects: galangin, a flavonol, causes the aggregation of bacterial cells (Cushnie et al., 2007); epigallocatechin
gallates, flavanols, inhibits virulence phenotypes and gene expression regulated by quorum sensing (QS) (Lee et al., 2009); and
proanthocyanidins have different mechanisms, including destabilization and permeabilization of the cytoplasmic membrane, inhibition of extracellular microbial enzymes, and deprivation of the
substrates required for microbial growth, such as iron and zinc
(Heinonen, 2007; Dixon et al., 2005; Mandalari et al., 2007). Another noteworthy finding is that flavanones from bergamota peel
(e.g. hesperetin and naringenin) exhibited synergism against pathogenic bacteria, which could be due to the combined reaction
with the cell membrane, and also a slight antagonistic interaction
attributed to a competition for specific target sites or inhibition of
uptake by bacterial cells (Mandalari et al., 2007). Flavan-3-ols extracted from tea, such as catechin, epicatechin, have been tested on
bacteria and fungi (Table 1), proving more active than antibiotics,
such as tetracycline or vancomycin at comparable concentrations
(Friedman et al., 2006). Furthermore, synergism of the combination
of catechin and antimycotics has been detected (Hirasawa and Takada, 2004). Among flavonoids, chalcones have simple structures,
but also have multiple substitutions and thus these can display
different biological activities (Mahapatra et al., 2015). These have
been tested against S. aureus and E. coli, and it has been found that
their anti-staphylococcal activity is related to the energy difference
between the two highest occupied molecular orbitals (Batovska
et al., 2009). In addition to natural phenolic use, some are modified
to increase their effectiveness. That is, alkyl esters of phenolic acids
are synthesised from pure acids to reduce the polarity of molecules,
in order to increase their solubility in oil with the aim of facilitating
access to the lipophilic cell wall of targeted pathogens. It has been
established that the antimicrobial effect of such derivatives
strengthens with the lengthening of the alkyl chain; for example,
butyl esters of phenolic acids inhibit the growth of Bacillus cereus
and S. cerevisiae (Merkl et al., 2010; Alvesalo et al., 2006). Other
promising phenolics are tetrahydroxyflavanones, which occur mainly
in Leguminosae, and have proven effective to inhibit methicillin-resistant S. aureus, and thus they would be useful in the phytotherapeutic strategy against such infections (Tsuchiya et al., 1996).
The last phenolic group considered here is that of the tannins.
These are naturally occurring compounds which precipitate protein, having high molecular weight and many phenolic groups
(Hagerman et al., 1998). Tannins can affect rumen metabolism by
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
39
bacteriostatic and bactericidal activities and by inactivating several
enzymes, such as carboxymethyl cellulase, proteases, glutamate
dehydrogenase). Furthermore, sulphur and iron bioavailability are
limited to animals consuming tannin-rich organs, and thus the
prolonged consumption of tannins induces toxicity (Kumar and
Vaithiyanathan, 1990). The mechanisms by which they exert antimicrobial activity are related to the inhibition of extracellular
microbial enzymes, deprivation of the substrates needed for microbial growth and inhibition of oxidative phosphorylation, which
affects microbial metabolism (Scalbert, 1991). Furthermore,
Akiyama et al. (2001) indicated that tannic acid inhibits the formation of fibrin and prompts a marked increase in the antistaphylococcal activity of oxacillin. Notably, gallotannins isolated
from mango kernels (gallotannins) were tested on several pathogens, showing that Gram-positive bacteria were generally more
susceptible to these compounds than were Gram-negative. This
inhibitory activity of gallotannins has been attributed to their
strong affinity for iron and possibly to the inactivation of membrane-bound proteins (Engels et al., 2011).
2.5. Peptides
The only known cases of active compounds of such nature in
plant-food by-products are those isolated from mango seeds
(Suárez et al., 2005), and from palm-kernel cake (Tan et al., 2013).
Both show antibacterial activity against several pathogenic bacteria (Table 1). It has been demonstrated that treatment with
peptides from mango seeds results in bacterial membrane damage, and that such activity is located in a sequence prone to form
a helix-loop-helix structural motif, without affecting human cells
(Suárez et al., 2005). Thus, such compounds might be used without problems to improve the livestock health.
2.6. Saponins
These are structurally diverse compounds derived from steroids or triterpenoid glycosides, which occur in many plant foods
and plant-food by-products. Their activity has been linked to
their
membrane-permeabilizing
properties,
being
immunostimulant and affecting growth, feed intake, and reproduction in animals. These impede protein digestion as well as
vitamin and mineral uptake in the gut, leading also to hypoglycaemia, and they can act as antifungal and antiviral agents, affecting animals in both positive and negative ways (Price et al.,
1987; Francis et al., 2002; Sparg, 2004). For example, some saponins may obstruct the absorption of micronutrients such as
iron (Francis et al., 2002), while in chicks they reportedly reduce
growth and feed efficiency and interfere with the absorption of
dietary lipids, cholesterol, bile acids, and vitamins A and E (Jenkins and Atwal, 1994). Similarly, condensed tannins may inhibit
plant-protein degradation in the rumen while depressing the
digestibility of plant cell walls.
The antimicrobial effects of such compounds extracted from
plant foods have been studied in Solanum (Kannabiran et al.,
2009), shoots of oats (Avena sativa) (Bahraminejad et al., 2008),
seeds of C. annuum (Iorizzi et al., 2002), Medicago sp. (Avato et al.,
2006), Yucca (Killeen et al., 1998), and saponin-containing Yucca
extract (Hassan et al., 2010). All these have been tested against
several Gram-positive and Gram-negative bacteria, yeast, and
fungi (Table 1). Findings vary because of the high diversity of saponins from diverse sources; for instance, saponins from Yucca
(Fig. 5) exhibit antimicrobial activity against Gram-positive bacteria but do not affect Gram-negative bacteria (Hassan et al., 2010).
3. Antimicrobial activity of extracts from plant-food by-
Fig. 2. Chemical structure of essential oil components identified in mango peels
(Osman and Ramlan, 2015) and turmeric oil (Xie et al., 2009). Compounds were
drawn using Chem Draw Ultras software (Chem Draw Ultra, Cambridge Soft Co.,
MA, USA).
products of tropical origin
As explained above, the pure compounds extracted from plants
are usually characterized in order to establish their antimicrobial
properties with good accuracy. Studies on the antimicrobial properties of by-products have examined the antimicrobial effect of different extracts and have characterized the profiles of active compounds.
The list of pathogens against which by-product extracts have been
tested is generally similar to that discussed previously: pathogens
such as Gram-positive and Gram-negative bacteria, and sometimes
yeast, fungi, and mould. However, despite the interest raised by the
antimicrobial activity of the extracts of raw by-products, few studies
deal with the activity of those of tropical origin (see Table 2).
Avocado peels constitute a by-product that contains different
phenolics, including phenolic acids, such as hydroxycinnamic and
hydroxybenzoic acids, and several flavonoids. Gram-positive bacteria
have been found to be generally more sensitive than Gram negative, E.
coli being the most sensitive species among the latter group (Rodríguez-Carpena et al., 2011). Bergamota peel yields essential oil (Citrus aurantium bergamia peel oil) and a by-product resulting from the
extraction, which has been characterized as an enriched source of
flavonoids, namely eriodictyol, hesperetin, naringenin, and others,
which have been found to be active against Gram-bacteria (Al-Delaimy
and Ali, 1970; Mandalari et al., 2007). Cacao bean husk, a by-product
from cacao processing, contains alkaloids (caffeine, theobromine, and
theophylline) and polyphenols. Extracts from this by-product have
been tested against pathogenic bacteria, with promising results
(Cuéllar et al., 2012). Coconut palm fronds and the husks of the coconut fruits are extensively used as sources for fibres, which are used
for a variety of applications (Reddy and Yang, 2015). This raw material
has been extracted in water infusion to produce phenolics, in which
flavonoids such as catechins and procyanidins have been found, both
active against S. aureus (Esquenazi et al., 2002).
The total antioxidant capacity and phenolic content of edible
40
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Fig. 3. Chemical structure of isothiocyanates active against Gram-negative bacteria
(Saavedra et al., 2010). Compounds were drawn using Chem Draw Ultras software
(Chem Draw Ultra, Cambridge Soft Co., MA, USA).
portions and seeds of mango seed kernel has been extensively
investigated, and seeds have shown a much higher antioxidant
activity and phenolic content than the edible portions have (Soong
and Barlow, 2004). Thus, this by-product has strong interest, as
reflected by the research conducted on it. Phenolics from extracts
of this by-product show high activity against all tested bacteria.
Such activity is related to the chelating effect on iron of gallotannins (Kabuki et al., 2000; Abdalla et al., 2007; Engels et al.,
2009; Khammuang and Sarnthima, 2011). Hydrolyzable tannins
from this source, in which penta-O-galloylglucose, hexa-O-galloylglucose, and hepta-O-galloylglucose occur, have major interest.
Gram-positive bacteria were generally more susceptible than
Gram-negative, with the minimal inhibitory concentration (MIC)
against B. subtilis, B. cereus, Clostridium botulinum, Campilobacter
jejuni, L. monocytogenes, and S. aureus were .2 mg mL 1 or less,
while enterotoxigenic E. coli and S. enterica were inhibited by .5–
1 mg mL 1. However, lactic acid bacteria showed strong resistance
(Engels et al., 2009).
Potato peel is a worthwhile source of phenolic acids, in which
chlorogenic, caffeic, gallic, and protocatechuic acids predominate.
Crude extracts have been tested against Gram-positive and Gramnegative bacteria, yeast, and mould. Bacteriocidal and bacteriostatic effects have been noted, but only at high concentrations
(Sotillo et al., 1998). Ethanol extract from sugarcane bagasse has
been characterized as a rich source of phenolics, in which flavonoids as well as simple phenolic acids predominate. In an assessment against Gram-positive and Gram-negative bacteria, the
authors indicated that the bacteriostatic mechanism was probably
due to the toxicity of polyphenolic compounds (Zhao et al., 2015).
Extracts from tamarind stem, bark, and leaves were assayed
against Gram-positive and Gram-negative bacteria, fungi, and
yeast. Phytochemical analyses have yielded phenolics, saponins,
alkaloids, and essential oils. The authors indicated that this plant
has a broad spectrum of antibacterial activity (Doughari, 2007).
Finally, tomato seed extracts from two varieties were tested for
phenolics and other compounds. Phenolic glycosides (quercetin,
kaempferol and isorhamnetin derivatives) organic acids and fatty
acids were found in the extracts tested. These were active only
against Gram-positive bacteria, Enterococcus faecalis proving to be
the most susceptible. Antifungal activity was exercised mainly by
“Bull's heart”, while C. albicans was the most susceptible species
(Taveira et al., 2010).
4. Comparative study on antimicrobial activity between pure
active compounds and extracts from plant-food by-products
The precise knowledge of the active-compound composition in
by-products enables their effective use in animal-production
farms. However, an important issue involves the use of by-products. Few authors have described some of the mechanisms by
which these compounds exert their effects the removal of their
active compounds. That is, the question is whether it would be
worth extracting the bioactive compounds present in these materials to add to feed, or whether the by-products could be used
directly to achieve the similar health benefits. To resolve this
important issue, the antimicrobial action of pure active compounds vs. crude by-product extracts should be compared. The
latter contain mixtures of bioactive compounds alongside a wide
range of plant components, such as sugars, fats, amino acids, etc.;
thus, the crude extracts made with solvents of different polarity
greatly resemble the whole by-product. An important index to
measure antimicrobial activity is the minimum inhibitory concentration (MIC), which is the lowest concentration of an antimicrobial when inhibiting the visible growth of a microorganism
after overnight incubation. The MIC constitutes an adequate tool to
monitor the activity of new antimicrobial agents (Andrews, 2001).
Selected cases of antimicrobial activity of pure compounds
against microorganisms expressed as MIC are presented in Table 3,
while selected cases of antimicrobial activity exercised by extracts
of crude by-product against microorganisms expressed as MIC
appear in Table 4. Most of the species tested belong to different
strains of Salmonella, Bacillus, Staphylococcus, Listeria, Streptococcus, Pseudomonas, Vibrio spp., and E. coli.
It bears highlighting, among the active pure compounds tested,
the large differences found by various authors for the same compounds when checking against the same species, as happens with
gallic acid against S. aureus, the activity of which varies between
.039 (e Silva et al., 2013) and 8 mg mL 1 (Akiyama et al., 2001), the
latter figure referring to methicillin-resistant strains. It is clear that
the differences between authors are due to the use of different
experimental procedures and also to the use of different strains in
the experiment. In fact, many authors have indicated sharp differences in sensitivity between strains when checking the different bioactive compounds. For example, according to Özçelik et al.
(2011), chlorogenic acid used for MIC indicated a variation between .008 and 1.28 mg mL 1 when tested against different Escherichia coli strains.
Among the various active compounds checked, alkaloids appear
to register the highest activity. That is, alkaloids from lupine (Lupinus angustifolius) and capsaicin tested against B. subtilis induced a
MIC of .062 (Erdemoglu et al., 2007) and .002–.064 (Özçelik et al.,
2011) mg mL 1, respectively, values very close to others found for
doxycycline against B. subtilis strains (.0001–.002 mg mL 1) (Grujić
et al., 2015). Although this activity is notable, it is necessary to
consider the negative taste of these compounds.
A great number of phenolics have also shown high activity,
such as: gallic acid with MIC values of .039 against S. aureus
(e Silva et al., 2013), .008–.016 against B. subtilis, .016–.128 against
S. aureus, .004–.13 against E. coli, .002–.03 against P. aeruginosa,
and .008 against C. albicans (Özçelik et al., 2011); chlorogenic acid,
naringin, and quercetin with very similar values to these (Özçelik
et al., 2011). In addition, exiguaflavanone D and Kenusanone A,
two flavanones, also displayed very low MIC values (.003–.006
and .006–.12 mg mL 1 respectively) against methicillin-resistant S.
aureus. For this latter species, Karthy and Ranjitha (2011) indicated
a MIC of .03 mg mL 1 for tannins extracted from mango-seed
kernel. With respect to saponins, such compounds extracted from
Capsicum seeds were found to induce a MIC of .02–.05 mg mL 1 in
Candida albicans (Iorizzi et al., 2002).
By-product extracts (Table 4) registered MIC values very close
to those presented above. For example, the chloroform extract
from avocado seeds showed a MIC of .02 mg mL 1 against Mycobacterium avium (Jiménez-Arellanes et al., 2013), while for S. aureus inhibition, banana-peel extract and coconut-root extract
reached .065 and .08 mg mL 1, respectively (Karadi et al., 2011).
Similar values were reported by both authors for the same extracts
when inhibiting P. aeruginosa, E. coli, and B. subtilis. However, other
by-product extracts showed higher values than these.
Given the above data, it would be enlightening to compare MIC
data for by-product extracts with those found for pure compounds
contained in these extracts. For example, 8, octa-O-galloylglucose
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
41
Fig. 4. Chemical structures of phenolics (phenolic acids, flavonoids and tannins) identified in plant food by-products. Phenolic acids and flavonoids structures were identified
from Dai and Mumper (2010), and tannins from Ma et al. (2015). Structures were drawn using Chem Draw Ultras software (Chem Draw Ultra, Cambridge Soft Co., MA, USA).
and 9 nona-O-galloylglucose are tannin components isolated from
mango-seed kernels, which have been tested on several bacteria,
yielding MIC between .1 and 3.3 mg mL 1 (Engels et al., 2011),
while the by-product from which they are derived, mango kernel
(Table 2), displayed MIC values between .2 (Sahu et al., 2013) and
1.4 mg mL 1 (Engels et al., 2011). Another noteworthy example
concerns bergamota peel extract (Table 2). It contains flavonoids
such as eriodictyol, hesperetin, and naringenin. When bergamota
peel ethanol extract was tested for MIC against several bacteria, the
values were 1.0 (B. subtilis), .2–.6 (E. coli), .5–1.0 (P. putida), and 4–1.0
(S. typhimurium) mg mL 1; while for phenolics isolated from this
extract MIC values for the same bacteria were between .8–
1.0 mg mL 1 (Mandalari et al., 2007). As indicated by authors, the
Fig. 5. Chemical structure of sarsasapogenin, the major saponnin identified in
Yucca extracts (Uematsu et al., 2000). Compounds were drawn using Chem Draw
Ultras software (Chem Draw Ultra, Cambridge Soft Co., MA, USA).
interactions between different compounds can alter the antimicrobial effectiveness of the flavonoids against food-borne bacteria. Therefore, synergism was noted between several compounds,
for example between eriodictyol and hesperetin against E. coli and
S. enterica, and between eriodictyol and naringenin against S. enterica and P. Putida, which was attributed to their combined reaction
with the cell membrane as a possible primary target site but with
different modes of inhibitory action (Sikkema et al., 1994). Thus, in
some cases, the whole by-product can act more effectively to inhibit
bacterial growth than their isolated compounds acting separately.
5. Some considerations concerning using plant-food by-products to feed farm animals
Today, agrifood production is increasing to meet the requirements of global food demand. Sometimes plant foods are not
consumed directly by humans, but first undergo processes to separate the desired value product from other constituents of the
plant (Ayala-Zavala et al., 2011). Moreover, a growing trend in
Western societies is to partially transform all fresh fruits and vegetables, with the aim of facilitating trade by making these more
attractive to consumers as well as cleaner and easier to store. Such
activities generate large amounts of plant by-products, although
there are considerable losses when processing. By-products derived from plant-food processing constitute a major disposal
problem for the industry concerned, but they are also promising
sources of compounds which may be used because of their nutritional properties (Schieber et al., 2001).
An idea of the volume of plant-food by-products either of
42
Table 2
Selected examples of antimicrobial activity of extracts from plant-food by-products of tropical origin.
Byproduct sources
Phytochemicals
Phenolics
Avocado peel, pulp, and
seed extracts from ‘Hass’
and ‘Fuerte’ varieties
Active compounds
Phenolic acids:
Hydroxycinnamic acids
Hydroxybenzoic acids
Flavonoids:
Procyanidins, catechins
Flavonoids:
Eriodictyol, hesperetin,
naringenin, and others
Models used
Findings
Reference
Bacillus cereus Staphylococcus aureus Listeria
monocytogenes Escherichia coli Pseudomonas spp.
Yarrowia lipolytica Aspergillus niger
– Gram-positive bacteria were generally more sensitive than Gram negative.
– Gram-positive B. cereus and L. monocytogenes were more sensitive,
– Among tested Gram-negative bacteria: E. coli was the most sensitive.
RodríguezCarpena et al.
(2011)
Bacteria
– Active against several Gram negative bacteria
– Activity may be due to a large number of mechanisms, such as competition
for specific target sites or inhibition of uptake by the bacterial cells.
– Inhibitory activity.
– Bergamot fractions were active against all the Gram-negative bacteria tested, and their antimicrobial potency increased after enzymatic
deglycosylation.
Al-Delaimy
and Ali
(1970)
Phenolics
Bergamot peel ethanolic
extract
Phenolics
Flavonoids:
Neohesperidin,
Hesperetin (aglycone)
Neoeriocitrin
Eriodictyol (aglycone)
Naringin
Naringenin (aglycone)
Cacao bean husk extracts
Alkaloids
Caffeine, theobromine,
theophylline;
poliphenols
Hydrolysable tannin
Salmonella typhimurium
Chesnut, sweet chestnut
Tannins
wood extract (Globatan)
Coconut; water infusion of Phenolics
husk fiber
Mango seed kernel extract Phenolics
Flavonoids:
catechins
procyanidins
Polyphenols
Mango seed kernel
Phenolics
Polyphenols
Mango seed kernel
Phenolics
Mango seed kernel
Phenolics
Potato peel
Phenolics
Sugarcane bagasse ethanolic extract
Phenolics,
flavonoids
Tamarind, Stem bark exPhenolics, sapotracts and leave extracts nins, alkaloids,
Gallotannins:
penta-O-galloylglucose
hexa-O-galloylglucose
hepta-O-galloylglucose
Phenolic acids:
chlorogenic,
caffeic,
gallic, and protocatechuic acids
Phenolics: 4.3152 mg of
GAE/g dry wt.
Phenolic acids: Gallic,
fumaric,
coumaric,
p-Hydroxybenzoic acid
Total flavonoids: 0.47 g
quercetin/g polyphenol.
Tannins, saponins,
sesquiterpenes,
Gram-negative bacteria:
Escherichia coli, Pseudomonas putida, Salmonella
enterica
Gram-positive bacteria: Listeria innocua
Bacillus subtilis, Staphylococcus aureus, Lactococcus lactis
Yeast:
Saccharomyces cerevisiae
Bacillus cereus ATCC 11778
Streptococcus agalactiae (native).
Staphylococcus aureus
Enterophathogenic E. coli.
Several strains of:
E. coli
Salmonella,
Aeromonas, Staphylococcus
Bacillus
B. cereus; B. subtilis, Salmonella typhi
Pseudomonas aeruginosa
Bacillus subtilis
Bacillus amyloliquefaciens
Listeria monocytogenes
Staphylococcus aureus
Gram negatives: Escherichia coli, Salmonella
typhimurium;
Gram positives: Staphylococcus aureus, Bacillus
cereus
Yeast: Sacharomyces cerevisiae
Mold: Aspergillus niger
S. aureus
L. monocytogenes
E. coli
S. typhimurium
Gram negatives:
Escherichia coli
– Chloroform fraction exerts antibacterial activity through an inhibition percentage of 34.90% (100 mg ml-1) for Bacillus cereus ATCC 11778 and 52.40%
(100 mg ml-1) for Streptococcus agalactiae (native).
– Globatan exhibited a bacteriostatic effect on Salmonella typhimurium in vitro
cultures.
– Selective antibacterial activity of C. nucifera against Staphylococcus aureus.
Mandalari
et al. (2007)
Cuéllar et al.
(2012)
Van Parys
et al. (2010)
Esquenazi
et al. (2002)
– Mango seed kernel extract had antimicrobial effect against the micro- Abdalla et al.
organisms of raw milk, i.e., lactic acid bacteria and other gram-positive and (2007)
gram-negative bacteria.
– High activity of mango kernel extract on Gram-positive bacteria.
Kabuki et al.
(2000)
– All extracts showed antibacterial activity in all tested bacteria.
Khammuang
and Sarnthima (2011)
– The chelating effect on iron of gallotannins related to their antibacterial Engels et al.
activity.
(2009)
– Potato peel freeze-dried extract was found not to be mutagenic. It has Sotillo et al.
bacteriocidal and bacteriostatic effects only at a high concentration.
(1998)
– The bacteriostatic mechanism of the sugarcane bagasse extract was prob- Zhao et al.
ably due to the toxicity of polyphenolics.
(2015)
– This plant has broad spectrum antibacterial activity and constitutes a po- Doughari
tential source of new classes of antibiotics that could be useful for infectious (2007)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Bergamota peel extracts
Extracts active only against Gram-positive bacteria
E. faecalis was the most susceptible bacteria.
Antifungal activity: “Bull’s heart” extracts were the most active.
Candida albicans was the most susceptible species
Proteus mirabilis, Pseudomonas aeruginosa,
Salmonella typhi
Samonella paratyphi
Shigella flexnerri
Gram positive :
Staphylococcus aureus, Bacillus subtilis
Streptococcus pyogenes
Fungal isolates :
Aspergillus flavus
fumigatus, A. niger
Yeast :
Candida albicans
Gram-positive:
Staphylococcus
aureus,
S.
epidermidis
Micrococcus luteus Enterococcus faecalis
Bacillus cereus
Gram-negative
Proteus mirabilis,
Escherichia coli, Pseudomonas aeruginosa Salmonella typhimurium
Fungi:
Candida albicans Aspergillus fumigatus Trichophyton rubrum
–
–
–
–
disease chemotherapy and control.
Taveira et al.
(2010)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
43
tropical or global origin, the agro-industrial production of plant
foods for 2013 can be consulted in the web page of the Food and
Agriculture Organization of the United Nations, Statistical Division
(http://faostat3.fao.org/download/Q/QC/E). Typically, plant-food
by-products are composed by unused peels, pulp, flesh, seeds,
kernels, and pomace. The amount of waste generated worldwide is
immense. For example, potato (Solanum tuberosum) reached a
production of 376.4 MMT/year in 2013, with by-products yielding
30% (Negesse et al., 2009) or 112.9 MMT. In mango (Mangifera
indica), production reached 43.3 MMT in 2013, producing 35–60%
by-products, representing 15.2–72.2 MMT/year (Larrauri et al.,
1996).
This vast potential could be used to increase the health status of
farm animals in a relatively simple way, given that extraction
processes of active compounds are not necessary for direct livestock feeding, considering the digestive capacity of the animals.
However, adequate characterization of the active-compound profiles is needed in each case before deciding on the use of any
product, and animal studies would be useful to establish the ratio
of each by-product in feeds in order to establish the optimal health
status. Moreover, the processing of plant-food by-products to be
used as livestock feed is relatively simple: after plant-food processing, the wastes should be quickly dehydrated using low-temperature air-flow dehydration for stabilization. Afterwards, the byproduct can be crushed to suitable particle size, and the resulting
meal could be mixed at the suitable ratio with the usual feed of
each targeted farm animal.
In the not-too-distant past, by-products were utilized to feed
livestock due to the nutritious contents of these substances, and
thus they did not constitute a waste-disposal problem, because
most farm animals consume humanly inedible foodstuffs and
convert them into high-quality foods for human consumption
(Oltjen and Beckett, 1996). However, recently, this practice has
been abandoned for the use of industrial feed in modern farming
systems, leading to the use of antibiotics and other pharmaceutical
products to maintain health and improve the productivity of farm
animals. In an effort to solve two problems–by-product waste
disposal and abusive use of antibiotics and other treatments—the
return of such by-products to the animal-production systems
would be useful.
Flavonoid glycosides:
Quercetin, kaempferol
and isorhamnetin
derivatives.
Phenolics glycosides, organic
acids, Fatty acids
Tomato seeds extracts
from “Bull’s heart” and
“Cherry” varieties
and
alkaloids,
phlobatamins
terpenes
6. Conclusions
As explained above, plant-food by-products of tropical origin
contain diverse active compounds, which act effectively against
most pathogenic bacteria tested, inducing well-characterized pathogen-cell damage. These compounds are alkaloids, essential oils,
glucosides, phenolics (simple phenolic acids, flavonoids, tannins),
saponins, and peptides. High activity has been detected in byproduct extracts from avocado seeds, cocoa-bean shell, and banana peels, while for isolated pure compounds, high activity has
been reported for alkaloids from lupine and capsaicin; phenolics
such as gallic and chlorogenic acids, naringin, exiguaflavanone D
and kenusanone A; and saponins from Capsicum seeds. It has been
noted that by-product extracts registered MIC values very close to
those found for their isolated pure components. This is due to
interactions between different compounds, which can in some
cases increase their antimicrobial effectiveness against pathogenic
bacteria, with noted synergism appearing among several
compounds.
However, although positive effects are expected in most cases,
precautions are needed when supplying plant-food by-products to
farm animals, since, as occurs with the plant from which comes,
bioactive compounds can also occasionally be toxic. Thus, more
research is needed, both in the laboratory and in feeding farm
44
Table 3
Antimicrobial activity of active compounds usually found in plant food by-products of tropical origin against several microorganisms expressed as MIC (mg mL 1).
Active
compounds
Main compounds
Alkaloids
13α-Hydroxylupanine
Lupanine
13α-Tigloyloxylupanine
Capsaicin
Alkaloids
Bacillus
cereus
Bacillus
subtilis
Staphylococcus
aureus, S.epidermidis Corynebacterium
xerosis Micrococcus luteus
Staphylococcus
aureus
Listeria
spp.
L. monocytogenes
Streptococcus
mutans St.
sobrinus
Enterobacter
aerogenes
Escherichia
coli
.062
.062
.5
.002–.064
.064
.004–.032
Coumarins
.62
Pseudomonas
aeruginosa
Pseudomonas
fluoresecens
Pseudomonas
putida
Salmonella
typhimurium
.004–.032
.008
1.25
2.5
Carvacrol
3
1
Essential oils
( þ)-carvone
10
10
Essential oils
Thymol
3
1
Glucoside
Dehydrodiconiferylalcohol9′-O-b-D-glucopyranoside
4.0
Glucosides
Isoorientin-7, 3′-O-dimethyl ether
4.0
Phenolic
aldehyde
Trans-cinnamaldehyde
3
3
Gallic acid
50–100
Gallic acid
.039
Gallic acid
8a
Phenolic
acid
Phenolic
acid
Phenolic
acid
Gallic acid
.008–.016
.016–.128
.004-.13
.002–.03
.008
Chlorogenic acid
.008–.016
.016–.128
.008-.128
.004–.132
.008
Phenolic
acid
Hydroxytyrosol
Phenolic
acid
Cinnamic
Coumaric
Ferulic
Caffeic
Flavone
Phenolics,
flavones
Ellagic acid
8
a
.6
1.5–3.0
4.2a
Phenolics,
flavanones
Eriodictyol
.25
.8
.25
Phenolics,
flavanones
Neohesperedin, hesperetin,
neoeriocitrin, naringin,
naringenin
Naringin
41.0
41.0
4.8
.008–.016
.016–.128
.004–.128
Phenolics,
flavanones
Phenolics,
flavanones
Phenolics,
flavanones
Naringenin
.4a
Fiavanone
4.2a
.8
1.0
.002–0.03
1.0
.008
Reference
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(2007)
Özçelik
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et al. (2011)
Özçelik
et al. (2011)
Akiyama
et al.
(2001)
BubonjaSonje et al.
(2011)
Wen et al.
(2003)
Tsuchiya
et al.
(1996)
Mandalari
et al.
(2007)
Mandalari
et al.
(2007)
Özçelik
et al. (2011)
Tsuchiya
et al.
(1996)
Tsuchiya
et al.
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Essential oils
Phenolic
acid
Phenolics
acid
Phenolic
acid
Candida
albicans
Exiguaflavanone D
.003–.006a
Phenolics,
flavanone
Kenusanone A
.006–.12a
Phenolics,
flavanol
Epicatechin
Phenolics,
flavanol
Epicatechin
8a
Phenolics,
flavanol
Epicatechin gallate
1a
Phenolics,
flavanol
Epigallocatechin gallate
.25a
Phenolics,
flavonol
Phenolics,
tannins
Quercetin
Phenolics,
tannins
Phenolics,
tannins
Phenolics,
tannins
Phenolics,
tannins
Phenolics,
tannins
hepta-O-6 galloylglucose
.1
8, octa-O-galloylglucose
.8
.1– 43.3
o .1
o .1
2.8
9, nona-O-galloylglucose
o .1
.1– 43.3
o .1
o .1
2.8
.002–.064
.004–.032
Tannin from mango seed
kernel
Saponins
Saponins from Yucca
shidigeras
Saponins
Saponins from Yucca
shidigeras
Saponins
Saponins from Capsicum
seeds
.004–.032
.008
.25–1a
.1–3.3
o .1
o .1
Tannin rich-extract
Cocoa polyphenols extract
b
.002-.064
Tannic acid
Phenolics,
a
3.7
Several S. aureus strains.
Methicillin resistant S. aureus (MRSA).
2.5
1.2–5.0
.03b
1.2
12.5
28
.02–.05
(1996)
Tsuchiya
et al.
(1996)
Tsuchiya
et al.
(1996)
BubonjaSonje et al.
(2011)
Akiyama
et al.
(2001)
Akiyama
et al.
(2001)
Akiyama
et al.
(2001)
Özçelik
et al. (2011)
Akiyama
et al.
(2001)
Engels
et al. (2011)
Engels
et al. (2011)
Engels
et al., 2011
Li et al.
(2014)
Karthy and
Ranjitha
(2011)
BubonjaSonje et al.
(2011)
Hassan
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Killeen
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(1998)
Iorizzi et al.
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J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Phenolics,
flavanone
45
46
Table 4
Antimicrobial activity of extracts from plant food by-products of tropical origin against several microorganisms expressed as MIC (mg mL 1).
By-product
extract
Bacillus Bacillus Listeria mono- Micrococcus Enterococcus Staphylococcus Staphylococcus Streptococcus Escherichia Pseudomonas Pseudomonas Salmonella Salmonella Vibrio paracereus subtilis cytogenes
luteus
faecalis
aureus
epidermidis
mutans
coli
aeruginosa
putida
sp.
typhimurium haemolyticus
Avocado seeds
water extract
.35
.1
.02
31.0
25.5
.06
42.0
.065
.85
1.0
.07
.2-.6
.07
.94
.47
.08
.06
.5–1.0
Raymond Chia
and Dykes
(2010)
Jiménez-Arellanes et al.
(2013)
Jiménez-Arellanes et al.
(2013)
Padam et al.
(2012)
Karadi et al.
(2011)
Mandalari
et al. (2007)
Nsor-Atindana
et al. (2012)
.4–1.0
.94
.06
Karadi et al.
(2011)
e Silva et al.
(2013)
.156
50
Jose (2014)
1.25
Akinyele et al.
(2011)
1.25
Akinyele et al.
(2011)
1.4
.2
Engels et al.
(2009)
Sahu et al.
(2013)
.225
2.0
1.25
.625
2.5
8–18
8–20
15–18
20
5
5
10
Oliveira et al.
(2011)
Zhao et al.
(2015)
2.5
14–18
10–15
–
Doughari
(2006)
Taveira et al.
(2010)
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
Avocado seeds
ethanol
extract
Avocado seeds
chloroform
extract
Banana buds
16.5
methanol
extract
Banana fruit
peels extract
Bergamot ethanol fractions
Cocoa Bean
.47
Shell acetone
extract
Coconut roots
extract
Coconut husk
aqueous
extract
Coconut husk
ethanolic
extract
Coconut husk
aqueous
extract
Coconut husk
hexane
extract
Mango kernel
extract
Mango kernel
ethanol
extract
Mango peel
extract
Sugarcane bagasse ethanol
extract
Tamarind ethanol extract
Tomato cherry 20
seeds hexane
extract
.09
Mycobacterium Reference
avium
J.L. Guil-Guerrero et al. / Livestock Science 189 (2016) 32–49
animals, with the aim of establishing precise combinations of byproducts in order to effectively inhibit the growth of pathogenic
bacteria without adversely affecting farm animals.
Acknowledgements
This work has been sponsored by the Prometeo Project, the
Ministry of Higher Education, Science, Technology and Innovation
of the Republic of Ecuador (SENESCYT).
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