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Abanico veterinario

versión On-line ISSN 2448-6132versión impresa ISSN 2007-428X

Abanico vet vol.8 no.1 Tepic ene./abr. 2018 


Antibacterial and antihelmintic activity of plant secondary metabolites: approach in Veterinary Medicine

Jerelly Hernández-Alvarado1 

Adrian Zaragoza-Bastida2 

Gabino López-Rodríguez2 

Armando Peláez-Acero2 

Agustín Olmedo-Juárez3 

Nallely Rivero-Perez2   * 

1Universidad Politécnica de Huatusco. Veracruz. México.

2Universidad Autónoma del Estado de Hidalgo. Instituto de Ciencias Agropecuarias. Hidalgo, México.

3Centro Nacional de Investigación Disciplinaria en Parasitología Veterinaria, INIFAP. Jiutepec, Morelos, México.


Currently, the use of medicinal plants has become an alternative for treatment and control of diseases in both veterinary and human medicine. Recent studies have reported that secondary metabolites present in all plants have effects on production and animal health as they have bactericidal or bacteriostatic, anthelmintic (tannins and saponins), anticancer, antioxidant and immunostimulant (phenolic compounds, alkaloid saponins, and terpenes) effects; and for their content of secondary metabolites they have been proposed as an alternative in animal feed because can increase productive and reproductive parameters. The presence or absence of these effects depends on the kind of plant, the content of secondary metabolites, the kind of secondary metabolite and the quantity and the frequency in which they are consumed. The aim of the present review was to carry out a bibliography search of the main secondary metabolites of plants with antimicrobial and over gastrointestinal nematodes activity, reported in Veterinary Medicine

Keyword: secondary metabolites; antimicrobial; antihelmintic; Veterinary Medicine


En la actualidad el uso de plantas medicinales se ha convertido en una alternativa para el tratamiento y control de enfermedades tanto en medicina veterinaria como en medicina humana. En estudios recientes se ha reportado que los metabolitos secundarios presentes en la mayoría de las plantas ejercen efectos a nivel productivo y de salud; ya que poseen efectos bactericidas o bacteriostáticos, antihelmíntico (taninos y saponinas), anticancerígeno, antioxidante e inmunoestimulante (compuestos fenólicos, saponinas alcaloides y terpenos); e incluso gracias a su contenido de metabolitos secundarios se han propuesto como parte de la alimentación en animales debido a que pueden mejorar parámetros productivos y reproductivos. La presencia o ausencia de estos efectos dependerá del tipo de planta, tipo de metabolito secundario y la cantidad y frecuencia con la que se consuman. El objetivo de la presente revisión fue realizar una búsqueda bibliográfica de los principales metabolitos secundarios de plantas con actividades antimicrobianas y sobre nematodos gastrointestinales, reportadas en Medicina Veterinaria.

Palabras clave: metabolitos secundarios; antibacteriano; antihelmíntico; Medicina Veterinaria


Many of the diseases that occur in the practice of Veterinary Medicine are associated with the presence of bacteria and parasites, which have developed some resistance to commercial drugs (McKellar and Jackson, 2004, Cabrera et al., 2007, Epe and Kaminsky, 2013). Therefore, the use of secondary metabolites of plants as an alternative for the control and treatment of them has been chosen.

Secondary metabolites are compounds derived from the primary metabolism of plants (Augustin et al., 2011) these compounds play an important ecological role as they serve as a defense mechanism (Pérez and Jiménez, 2011). The majority of plant species have secondary metabolites, such as terpenes, phenolic compounds, glycosides and alkaloids (Ávalos and Pérez-Urria, 2009), of which, about 8000 polyphenols, 270 non-protein amino acids, 32 cyanogens, 10,000 alkaloids , several saponins and steroids (Domingo and López Brea, 2003; Duraipandiyan et al., 2006; Carmona, 2007).

Secondary metabolites are a source of active ingredients of drugs and valuable chemicals, whose pharmaceutical applications are due to their function as analgesics, antibacterials, antihepatotoxics, antioxidants, antiviral, antitumorals, fungicides, immunostimulants, among others (Isaza, 2007, Pérez and Jiménez, 2011, Agustín et al., 2011).

It has been proposed that the active components of the extracts (secondary metabolites) can inhibit microbial growth by the same mechanisms as antibiotics: inhibition of cell wall synthesis and activation of enzymes that destroy this wall, the permeability of the cell membrane, interference with protein synthesis and alteration of nucleic acid metabolism among others (Ordaz et al., 2010).

On the other hand in the control of the gastrointestinal nematodes has been proposed the herbal as alternative, according to the analysis of the compounds in different plants, the tannins are those that take part in vital functions of the nematodes affecting the mobility, the nutrition and, possibly (Durmic and Blache, 2012, Hernandez et al., 2014). In the present study, the results obtained in this study are similar to those reported in the present study. Tannin plants may have direct antiparasitic activity but may also have an indirect effect through enhancing the animals' immune responses against gastrointestinal nematodes (Hoste et al., 2005).

There are reports that tannins can improve resilience (fewer clinical signs, better growth and wool production) and resistance (fewer nematode eggs in feces, lower parasite load and lower fertility of parasitic females) of infected goats and sheep with gastrointestinal nematodes (Torres-Acosta et al., 2008).

According to the aforementioned, the present review was proposed with the objective of carrying out a bibliographic search in the Scopus, SciELO and Redalyc databases of the main secondary metabolites of plants with antimicrobial activities and on gastrointestinal nematodes reported in Veterinary Medicine. The aim is to favor the use of these alternative sources in the treatment and control of some diseases associated with the presence of bacteria and parasites of importance in the Veterinary Medicine practice.

Secondary metabolites

Secondary metabolites (MS) are compounds derived from the biosynthesis routes of primary carbon metabolism in plants, which appear in the cytoplasm of most plant cells (Augustin et al., 2011).

These compounds do not have an apparent importance however; they play an important ecological role since many of the compounds serve as defense mechanism against herbivores, viruses, bacteria and fungi (Pérez and Jiménez, 2011).

Other MSs have physiological functions, such as alkaloids and pectins, which can serve to transport toxic nitrogen and other storage compounds, while phenolic compounds such as flavonoids play a role as ultraviolet ray protectors (Pérez and Jiménez, 2011). MSs as opposed to primary metabolites have a restricted distribution in the plant kingdom as they are synthesized in small quantities and in a specific way determined to the genus, family or plant species (Ávalos and Pérez-Urria, 2009).

Up to 2007, about 8000 polyphenols, 270 non-protein amino acids, 32 cyanogens, 10,000 alkaloids, various saponins and steroids had been reported (Domingo and López Brea, 2003; Duramandiyan et al., 2006; Carmona, 2007).

MSs are grouped into four main groups: Terpenes, phenolic compounds, glycosides and alkaloids, all with different pharmacological properties as shown in Table 1.

Table 1 Classification of secondary metabolites and their pharmacological properties 

Group Compounds present Main Features Pharmaceutical properties
Alkaloids Hormones, carotenoid pigments, sterols, latex and essential oils Group of major importance with more than 40,000 molecules, they are considered of importance for the survival of plants. They are insoluble in water and are derived from the union of isoprene units Anticarcinogenic, antiulcerous, antimalarial, antimicrobial, etc.
Phenolic compounds Coumarins, flavonoids, lignin and tannins. They are derived from a phenol group Antidiarrheals, antitumorals, antibacterials, antivirals and enzyme inhibitors (Isaza, 2007)
Glycosides Saponins, cardiac glycosides, cyanogenic glycosides and glucosinolates. They arise from the condensation of a sugar molecule with another containing a hydroxyl group, thus forming a glycosidic bond Antimicrobials, fungicides, insecticides, anticancer, anti-inflammatory and allelopathic (Agustín et al., 2011)
Terpenes Quinoline, isoquinoline, indole, tropane, quinolizidine, piperidine, purine, pyrrolizidene. Group with about 15000 secondary metabolites. They are soluble in water, contain at least one nitrogen atom and exhibit biological activity. Most are heterocyclic and some are aliphatic compounds. At high doses, most are very toxic, however, at low doses they work as muscle relaxants, tranquillizers, antitussives or analgesics.

Adapted of Ávalos and Pérez-Urria, 2009

Use of secondary metabolites as antibacterials

Plants have been considered as a sustainable option against pathogens and an important source of natural diversity due to the large number of compounds they synthesize; more than 100,000 MS have been reported in the nature of which there are some that have been shown to have an antibacterial effect (Montes-Belmont, 2009, Cruz-Carrillo et al., 2010, Borroto et al., 2011, Avello Lorca et al., 2012, Soto Vázquez et al., 2014).

It is clear that in veterinary practice there are a large number of pathologies associated with the presence of bacterial pathogens which cause significant economic losses in livestock production (Pugh, 2002), however, resistance to conventional antimicrobials is a factor that has limited the treatment and control of the infections caused by these pathogens (Pellegrino et al., 2011), that is why antimicrobial alternatives extracted from plants have been used.

The bacterial resistance generated is due to the increase in the use of antibiotics and the respective selective pressure exerted, has caused bacteria with multiple mechanisms such as biochemical, genetic and cellular, to develop strategies to evade the action of these compounds (Cabrera et al. 2007), for this reason antimicrobial alternatives extracted from plants have been used, some examples are described in Table 2.

Antibiotics have been used in veterinary medicine for three purposes: therapeutic, prophylactic and as growth promoters, the latter being a practice known since 1950, to discover that small doses of tetracycline improved the development of animals and shortly after this discovery were used other drugs such as penicillin and chloramphenicol (Puig et al., 2011), it is also known that veterinary hospitals play a role in the transmission of multiresistant organisms and not only by the continuous administration of antibiotics but also by the exchange of bacteria between people and animals (Ríos et al., 2015).

Resistance is a natural property of an organism (intrinsic) or achieved by mutation or acquisition of plasmids (self-replication, extrachromosomal DNA) or transposons (chromosome integrated into plasmids, transmissible DNA cassettes) (Cabrera et al., 2007). Plasmids and transposons are mobile genetic elements where resistance genes are transported (Pérez and Robles, 2013).

Antibiotic resistance may be the result of chromosomal mutations or the interaction of genetic material through the transport of resistance genes by means of transduction, conjugation or transposition mechanisms. There are 5 mechanisms of acquired resistance, of which the bacteria can use more than two: enzymatic modification or destruction of the antibiotic, impermeability to the antibiotic, alteration or production of new target sites, the presence of efflux pumps that expel the antibiotic and over expression of the target site (Cabrera et al., 2007), although there may also be alterations in the composition and content of bacterial wall glycoproteins (Puig et al., 2011).

Bacteria that are resistant to more than one antibiotic are called multiresistant bacteria, which present an even more serious problem because they have developed different resistance mechanisms (Pérez and Robles, 2013).

Similarly the mechanisms by which the active components of the extracts can inhibit microbial growth are known and already mentioned: inhibition of cell wall synthesis and activation of enzymes that destroy that wall, increased permeability of the cell membrane, interference with protein synthesis and alteration of nucleic acid metabolism among others (Ordaz et al., 2010).

In the case of Staphylococcus aureus, the antimicrobial effect of phenols has been associated with the ability of these compounds to produce alterations in the cytoplasmic membrane of the bacterium (Domingo and López Brea, 2003).

Within the genus of importance in Veterinary Medicine are Staphylococcus, Escherichia, Salmonella, Pseudomona and Bacillus among others. Within the genus Staphylococcus the species of veterinary importance are aureus, which produces great variety of suppurative infections in wounds, mastitis, endometritis, cystitis, osteomyelitis, pyoderma in most domestic species as well as companion animals; epidermidis, which generates mastitis in ruminants; hyicus, species associated with exudative epidermis in pigs, and intermedius, which causes pyoderma, otitis, conjunctivitis, osteomyelitis in dogs (Velasco and Yamasaki, 2002). In addition, this genus presents high morbidity and mortality in domestic and companion animals (Ríos et al., 2015).

Some pathogenic Escherichia serotypes are associated with diarrhea in pigs, cattle, sheep, goats and horses. This genus is considered an opportunistic pathogen in urinary and respiratory tract infections, mastitis, omphalitis and different infectious processes (Velasco and Yamasaki, 2002). The subspecies coli is a pathogen associated with the presence of diarrhea in small ruminants of less than 2 weeks of age, which present fever and diarrhea linked to severe damage in the intestinal epithelium altering the transport of electrolytes and water, causing a rapid dehydration to cause of hypersecretion of liquids, the morbidity rate is between 20 and 25 % and the mortality is usually greater than 50 %. On the other hand, E. coli has also been reported as a causal agent of clinical mastitis in cattle, sheep and goats producing milk, causing considerable losses due to the decrease in milk production, causing anorexia, fever, and even loss of the fourth or middle affected in extreme cases (Pugh, 2002).

For its part, Bacillus anthracis, belonging to the genus Bacillus, causes sudden deaths with haemorrhages in natural holes in cattle and sheep. Some other species cause enteritis in pigs and dogs, mastitis, abortions, food poisoning, corneal ulcers, among others (Velasco and Yamasaki, 2002).

Bacteria belonging to the genus Pseudomonas generate abscesses and purulent infections in different species, bovine mastitis, enteritis, pneumonia and myeloidosis in pigs as wel as in different animal species (Velasco and Yamasaki, 2002).

The serotypes abortus, of the genus Salmonella, cause abortions in bovines, horses and sheep, besides generating diarreas and septicemias in different species of animals; and in the case of S. cholerasuis it generates enteritis, septicemia and pneumonia in pigs (Velasco and Yamasaki, 2002).

Extracts of different species of plants with different solvents have been analyzed, while the identification of the compounds or compound groups present in these plants has been carried out, it has even been reported that these compounds tend to have a greater effect on bacterial genera which present multidrug resistance.

As a result, phenols exert an antimicrobial action against S. aureus, Salmonella thyphimurium, tannins on various bacterial genera and some viruses, flavones on Shigella and Vibrio, alkaloids against Gram positive cocci, Lactobacillus and fungi, the saponins obtained from Panax ginsen have an important effect inhibiting the growth of E. coli and S. aureus (Domingo and López Brea, 2003, Moreno et al., 2010, Pereira et al., 2013).

Saponins have an antibacterial activity and can modify ruminal fermentation by suppressing protozoa and selectively inhibiting ruminal and intestinal bacteria (Lactobacillus plantarum and Enterococcus faecium in lambs) (Salem et al., 2010).

In an experiment carried out in 2013 with hexanic extract of cedar, it was observed that this extract had a potent antimicrobial activity against Staphylococcus aureus; with inhibition halos of 12 mm that were responsible for this activity were the alkaloids, triterpenes or sterols, and quinones present in this extract (Pereira et al., 2013).

MS anthelmintic activity

The parasitic diseases caused by gastrointestinal nematodes in ruminants represent a serious problem worldwide as they affect host productivity causing reductions in growth rates in young animals, low body conditions, reduced fertility, increased susceptibility to diseases of different origins, and increased mortality, leading to significant economic losses in livestock production (Moreno et al., 2010, Felice, 2015)

Drug-based anthelmintic treatment is limited due to the development of resistance of some gastrointestinal nematode populations to most commercial anthelmintics (McKellar and Jackson, 2004, Epe and Kaminsky, 2013).

This problem is common in gastrointestinal nematodes of sheep, goats, horses (Gonzalez et al., 2012) and cattle (Encalada et al., 2008), however this situation has been studied extensively in sheep because of the low effectiveness of the main chemicals such as benzimidazoles, imidazothiazoles and macrocyclic lactones, a study carried out in 2011 confirmed anthelmintic resistance to the main anthelmintics (Closantel, Albendazole, Ivermectin and Nitroxinil) used in the Sierra de Tabasco and North Chiapas region in sheep (González et al., 2012).

Table 2 Activity of plant extracts on different bacterial genera 

Used plants Bacteria Reference
Metanolic of Acacia modesta S. aureus, E. coli, P. aeruginosa, S. epidermis and B. subtilis. (Bashir et al., 2012)
Thymus serphylum S. aureus, E. coli, P. aeruginosa, S. epidermis and B. subtilis. (Bashir et al., 2012)
Syzygium comuni L. S. aureus, E. coli, P. aeruginosa, S. epidermis and B. subtilis. (Bashir et al., 2012)
Olea ferruginea S. aureus, E. coli, P. aeruginosa, S. epidermis and B. subtilis. (Bashir et al., 2012)
Family Lauraceae Fusarium oxysporum, E. coli, B. subtilis, P. aeruginosa and S. aureus. (Avello Lorca et al., 2012)
Family Atherospermateceae Fusarium oxysporum, E. coli, B. subtilis, P. aeruginosa and S. aureus. (Avello Lorca et al., 2012)
Allium sativum coli, B. subtilis, P.aeruginosa, S. aureus, S. tiphy. (Srinivasan et al., 2001)
Curcuma longa E. coli, P. aeruginosa, B. subtilis, S. aureus, S. tiphy. (Srinivasan et al., 2001)
Eucalyptus globulus E. coli, P. aeruginosa, B. subtilis, S. aureus, S. tiphy (Srinivasan et al., 2001)
Jatropha glandulifera E. coli, P. aeruginosa, B. subtilis, S. tiphy (Srinivasan et al., 2001)
Leucas aspera E. coli, P. aeruginosa, B. subtilis, S. aureus. (Srinivasan et al., 2001)
Tamarindus indica E. coli, P. aeruginosa, B. subtilis, S. aureus, S. tiphy (Srinivasan et al., 2001)
Sonneratia alba E. coli and P. aeruginosa (Kaewpiboon et al., 2012)
C. albicans S. aureus, E. coli and P. aeruginosa. (Kaewpiboon et al., 2012)
Albizia adianthifolia E. coli, Klebsiella pneumoniae, P. aeruginosa (Tchinda et al., 2017)
Laportea ovalifolia E. coli, Klebsiella pneumoniae (Tchinda et al., 2017)

One of the alternatives proposed for the control of gastrointestinal nematodes is the use of plants used in traditional herbal medicine with anthelmintic effect. The main compounds of these plants are terpenes, alkaloids, saponins, anthraquinones and tannins. Although, according to the analysis of the compounds in different plants, tannins are involved in vital functions of nematodes affecting mobility, nutrition and possibly reproduction (Medina et al., 2014).

The use of plants rich in bioactive secondary metabolites and especially those containing tannins have received great attention and have been proposed as a method of control of gastrointestinal nematodes in sheep and goats, some examples are shown in Table 3 (Durmic and Blache, 2012, Hernández et al., 2014).

On the other hand, plants rich in tannins have attracted the greatest attention for their effect on the gastrointestinal nematodes of ruminants. Tannin plants may have direct antiparasitic activity but may also have an indirect effect through enhancing the animals' immune responses against gastrointestinal nematodes (Hoste et al., 2005). There are reports that tannins can improve resilience (fewer clinical signs, better growth and wool production) and resistance (fewer nematode eggs in feces, lower parasite load and lower fertility of parasitic females) of infected goats and sheep with gastrointestinal nematodes (Torres-Acosta et al., 2008). The antiparasitic property of the secondary metabolites depends on the structure of the secondary compound, the level of ingestion and their availability in the gastrointestinal tract of the animals (Athanasiadou and Kyriazakis, 2004).

Apparently the action mechanism of tannins on the infective larvae (L3) of Haemonchus contortus and Trichostrongylus colubriformis is to prevent these parasites from drawing, this prevents the gastrointestinal nematodes can be established in their site of action and can continue with their evolutionary cycle, while in adult parasites the tannins apparently attach to the mouth and possibly to the reproductive apparatus of the parasites, by the affinity of the tannins to the proline-rich proteins of the nematode cuticle (Torres-Acosta et al., 2008).

Table 3 Effect of different plants on gastrointestinal nematodes of small ruminants 

Used plant Effect Evaluated helminth Reference
Casuarina cunninghamiana, %IEH and %IDL H. contortus and T. colubriformis (Moreno et al., 2010).
Acacia farnesiana, %IEH and %IDL H. contortus and T. colubriformis (Moreno et al., 2010).
Acacia holosericea %IDL H. contortus and T. colubriformis (Moreno et al., 2010).
Acacia nilotica %IDL H. contortus and T. colubriformis (Moreno et al., 2010).
Mentha piperita %IEH and %IDL H. contortus (Carvalho et al., 2012)
Lippia sidoides %IEH and %IDL H. contortus (Carvalho et al., 2012)
Piper tuberculatum %IEH and %IDL H. contortus (Carvalho et al., 2012)
Azadirachta indica %IEH and %IDL H. contortus (Costa et al., 2008)
Leucas martinicensis %IEH and %IDL H. contortus (Eguale et al., 2011)
Leonotis ocymifolia %IEH and %IDL H. contortus (Eguale et al., 2011)
Senna occidentalis %IEH and %IDL H. contortus (Eguale et al., 2011)
Hura crepitans %IDL H. contortus (Carvalho et al., 2012)
Albizia schimperian %IDL H. contortus (Eguale et al., 2011)
Melia azedarach %IEH H. contortus and Trichostrongylus sp. (Cala et al., 2012)
Trichilia clausseni %IEH and %IDL H. contortus and Trichostrongylus sp. (Cala et al., 2012)
Annona squamosa %IEH and %IDL H. contortus (Kamaraj et al., 2010)
Eclipta prostrata %IEH and %IDL H. contortus (Kamaraj et al., 2010)
Solanum torvum %IEH and %IDL H. contortus (Kamaraj et al., 2010)
Terminalia chebula %IEH and %IDL H. contortus (Kamaraj et al., 2010)
Catharantus roseus %IEH and %IDL H. contortus (Kamaraj et al., 2010)
Cymbopongon schoenanthus %IEH and %IDL H. contortus and Trichostrongylus sp. (Katiki et al., 2011)

%IEH: Egg hatching inhibition rate, % IDL: Percent inhibition of larval development

The nematode Haemonchus contortus has been considered the one with the highest prevalence in small ruminants (Encalada et al., 2008) and one of the main causes of economic losses in sheep production, which is why most of the in vitro studies already performed have been with Haemonchus contortus (López-Ruvalcaba et al., 2013).


At present, the treatment of bacterial and parasitic diseases of importance in Veterinary Medicine has been complicated by the resistance to commercial drugs, so it is necessary to use alternatives for the control of these resistant or multiresistant pathogens, one of which may be the use of secondary metabolites of plants with antibacterial activity and/or gastrointestinal nematodes.

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Received: April 25, 2017; Accepted: August 11, 2017

* Author responsible and correspondence: Nallely Rivero-Perez, email:

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