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Revista mexicana de ciencias pecuarias
On-line version ISSN 2448-6698Print version ISSN 2007-1124
Rev. mex. de cienc. pecuarias vol.12 n.1 Mérida Jan./Mar. 2021 Epub Sep 20, 2021
https://doi.org/10.22319/rmcp.v12i1.5131
Articles
In vivo anthelmintic activity of Acacia cochliacantha leaves against Haemonchus contortus in Boer goat kids
a Universidad Autónoma del Estado de México, Centro Universitario UAEM-Temascaltepec.
b Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias, Centro Nacional de Investigación en Disciplinaria en Salud Animal e Inocuidad, carretera Federal Cuernavaca, Cuautla No. 8534/ Col. Progreso. 62550 Jiutepec, Morelos/A.P. 206-CIVAC, México.
c Instituto Mexicano del Seguro Social. Centro de Investigación Biomédica del Sur. México.
d Universidad Autónoma de San Luís Potosí. Facultad de Agronomía
e Universidad Autónoma de Baja California. Instituto de Ciencias Agrícolas
This study aimed to evaluate the effect of supplementing the maintenance diet of Boer goat kids with Acacia cochliacantha leaves. The endpoints evaluated were Haemonchus contortus fecal egg count (FEC) and water and dry matter intake. Two experimental treatments were evaluated on ten recently weaned goat kids (16.850 ± 1.630 kg of initial live weight and three months of age) experimentally infested with H. contortus larvae (L3) (350 larvae per live weight kilogram). Treatment 1 (T1) served as the control and consisted of infested animals without diet supplementation with A. cochliacantha leaves. Treatment 2 (T2) consisted of infested animals fed diets supplemented with 5% of A. cochliacantha leaves. Animals were grouped from highest to lowest based on their FEC. The two animals groups with the highest values were randomly assigned to T1 or T2; this was repeated until completing five repetitions per treatment. The evaluated variables were: FEC (per gram of feces), water intake, and dry matter intake (DMI). The results show that goat kids fed diets with 5% of A. cochliacantha leaves have lower (P<0.05) FEC than the control. There were no significant differences in water intake and DMI (g d-1) between treatments. This study demonstrates the anthelmintic activity of diets supplemented with A. cochliacantha leaves in goat kids. Thus, this arboreal legume could represent a viable option for the comprehensive management of the nematodiasis of growing Boer goat kids.
Key words Goat kids; Anthelmintic; Acacia cochliacantha; Haemonchus contortus
El objetivo del presente trabajo fue evaluar el efecto de la inclusión de hojas de Acacia cochliacantha en una dieta de mantenimiento para cabritos de la raza Boer en el conteo fecal de huevos (CFH) de Haemonchus contortus, consumo de agua y materia seca. Diez cabritos recién destetados (16.850 ± 1.630 kg de peso vivo inicial y 3 meses de edad), fueron experimentalmente infestados con larvas (L3) de H. contortus (350 larvas por kilogramo de peso vivo), para probar dos tratamientos: T1: testigo (animales infectados con larvas L3 de H. contortus, sin inclusión de hojas de A. cochliacantha) y T2: animales infectados con larvas L3 de H. contortus, con inclusión de 5% hojas de A. cochliacantha en la dieta. Antes de asignar los tratamientos a los animales, se realizó un CFH por gramos de heces en cada uno de ellos y de esta manera agruparlos de mayor a menor en relación a la cantidad de huevos presentes en las heces, en los dos animales con valores más altos se asignaron aleatoriamente T1 o T2 y así sucesivamente hasta completar cinco repeticiones verdaderas para cada tratamiento. Las variables medidas fueron: CFH (por gramo de heces), consumo de agua y consumo de materia seca (CMS). Los resultados encontrados demostraron reducción (P<0.05) en el CFH de H. contortus en los cabritos donde se incluyó el 5% de hojas de A. cochliacantha en su dieta. Para el consumo de agua y CMS (g día-1) no existieron diferencias entre tratamientos (P> 0.05). Se concluye que la adición de hojas de A. cochliacantha en dietas para cabritos tienen actividad antihelmíntica, por lo que esta leguminosa arbórea podría representar una opción en el manejo integral de la nematodiasis de cabritos Boer en crecimiento.
Palabras clave: Cabritos; Antihelmíntico; Acacia cochliacantha; Haemonchus contortus
Introduction
The diseases caused by gastrointestinal nematodes (GIN) affect the health and productivity of small ruminants, representing an important problem worldwide. Haemonchus contortus is the main GIN responsible for the greatest economic losses in the livestock industry in Mexico; this problem can represent up to 445.1 million dollars annually1-3. In the last decades, the indiscriminate use of antiparasitic agents against GIN has generated anthelmintic resistance, in addition to the residual effects of some drugs on the organisms and the environment4,5. This problem has prompted research on sustainable control alternatives focused on studying the anthelmintic properties of the secondary metabolites in legume plants6-9. Among these compounds are condensed tannins, terpenes, saponins, and flavonoids10. Specifically, the synergistic nematicide activity of flavonoids and free condensed tannins against GIN has been demonstrated11,12. Acacia cochliacantha is a legume known as “cubata,” used in traditional medicine to treat gastrointestinal diseases13. Various studies have reported the in vitro nematicide activity of leaf extracts13 or specific compounds like tannins, quercetin, and caffeic, coumaric, and ferulic acids12. This study aimed to evaluate the effect of a diet supplemented with A. cochliacantha leaves on egg shedding, dry matter and water intakes in growing Boer goat kids experimentally infested with H. contortus.
Material and methods
Area of study
This study was carried out in the Experimental unit for small ruminants of the UAEM, Temascaltepec. This area has a mean altitude of 1,740 m asl, with a tropical savanna climate with summer precipitations (Aw)14.
Plant material
Fresh leaves (young and mature) from A. cochliacantha were collected in Salitre Palmarillos, municipality of Amatepec, Mexico State, Mexico; located at 18°43'28'' N and 100°17'03'' W. The plant material was collected between March and April 2016 during the early hours of the morning. Leaves were stored in a freezer to inhibit changes in their chemical structure due to photooxidation and were then transported to the Animal Nutrition laboratory at the UAEM, Temascaltepec; here, a specimen was selected for its identification in the Herbario Nacional de México of the Universidad Nacional Autónoma de México (UNAM). The plant material was identified by Prof. Rafael Torres-Colín and deposited in the Herbario Nacional under the collection code OD07042016. The fresh leaves were shadow-dried at room temperature until reaching constant weight; after drying, leaves were ground to a particle size of 4 to 6 mm using an electrical Wiley® mill (Mod. TS3375E15).
Chemical analysis
The bromatological analysis of the experimental diets and the A. cochliacantha leaves was performed using the following methods: dry matter (DM), organic matter (OM), crude protein (CP), and ether extract (EE)15; cell wall fractions (NDF and ADF) were evaluated using the methodology described by Van Soest et al16. The content of total condensed tannins (TCT) in the percentage of inclusion of A. cochliacantha leaves was determined following the technique described by Terrill et al17 and modified by López et al18; the protein- and fiber-bound condensed tannins were determined with the method reported by Porter et al19 and modified by Hagerman20.
Biological material
Infective larvae of H. contortus (L3, INIFAP strain) were obtained from a donor sheep (22.3 ( 0.5 kg of live weight) infected with a single oral dose of 350 L3 per kg of live weight. The lamb was cared for according to the NOM-062-ZOO-1999. The infective larvae of H. contortus were obtained from cultures following the technique reported by Baermann21.
Experimental animals
A total of 14 male Boer goat kids (16.850 ± 1.6 kg of live weight and 3 mo of age) from the Salitre farm, UAEM, Temascaltepec, were used. Before initiating the experiment, all animals were dewormed with a single dose of commercial ivermectin (0.22 mg-1 kg of live weight) to eliminate any natural infection with GIN. After applying the antiparasitic agent, goat kids were housed in individual cages (equipped with shade and drinking and feeding troughs). Then, it was confirmed that animals were negative for GIN infection using the McMaster technique22, and on d 16, animals were inoculated with a single dose of 350 L3 of H. contortus per kilogram of live weight. Once goat kids were diagnosed as positive for H. contortus (d 30), they were assigned into two groups (n=7) based on their FEC and their body weight. Before infection, animals received an adaptation diet without A. cochliacantha leaves (Table 1). Diets were balanced based on the requirements of growing goat kids using the NRC tables of 2007 for small ruminants23.
Table 1 Ingredients, protein, and metabolizable energy of the experimental maintenance diets fed to goat kids infected with H. contortus
| Ingredient (%) | Treatment | |
|---|---|---|
| 1 | 2 | |
| Acacia cochliacantha | 0.00 | 5.00 |
| Alfalfa hay | 33.00 | 28.00 |
| Ground corn | 5.00 | 5.00 |
| Ground sorghum | 17.50 | 17.50 |
| Soybean meal | 7.00 | 7.00 |
| Wheat bran | 10.00 | 10.00 |
| Oat straw | 25.00 | 25.00 |
| Molasses | 0.00 | 0.00 |
| Vitamins and minerals premix | 2.50 | 2.50 |
| Total | 100.00 | 100.00 |
| Crude protein | 12.78 | 12.76 |
| Metabolizable energy (MJ/kg DM) 1 | 2.84 | 2.83 |
T1: control (animals infected, without diet supplementation with A. cochliacantha leaves); T2: animals infected, fed diets supplemented with 5% of A. cochliacantha leaves.
1 Calculated based on the individual energy contents of each feed included in the diet23.
Experimental design
During the experiment, the life of four goat kids was endangered due to post-weaning stress. These animals showed decreased packed-cell volumes (PCV), which indicate a severe anemic state, and high fecal egg counts (FEC > 12,500); therefore, these animals were removed from the experiment, leaving only ten goat kids, which were assigned into the two previously established treatments: T1: control (animals infected with L3 larvae of H. contortus, without diet supplementation with A. cochliacantha leaves) and T2: treatment (animals infected with L3 larvae of H. contortus fed diets supplemented with 5% of A. cochliacantha leaves). Response variables were: FEC per gram of feces, dry matter and water intake. Samples were collected weekly (post-infection d 1, 7, 14, 21, and 28) directly from the rectum. The FEC per gram of feces was determined following the McMaster technique22. Dry matter and water intake were determined daily by subtracting the rejected water or feed from what was offered. The antiparasitic efficacy was estimated using Abbott's formula:
Efficacy (reduction of FEC per g of feces, %) = [(FEC of control group - FEC of treated group) / FEC of control group)]*100
Statistical analysis
Results were processed through an analysis of variance using the GLM procedure of SAS24. The experiment followed a completely randomized design; when there were differences between treatments, means were separated using the PDIFF test, STDERR statement. Statistical difference was declared at a P≤0.05 and the 0.05 < P ≤ 0.10 trend25.
Results
Chemical analysis
The chemical composition of the experimental diets and the tannin content in A. cochliacantha leaves are shown in Tables 1 and 2.
Table 2 Chemical proximate analysis and tannin content of dehydrated A. cochliacantha leaves
| OM | CP | NDF | ADF | FCT | PBCT | FBCT | TCT | |
|---|---|---|---|---|---|---|---|---|
| A. cochliacantha | 937.0 | 163.0 | 698.6 | 581.7 | 140.0 | 26.0 | 36.0 | 202.0 |
OM= organic matter, CP= crude protein, NDF= neutral detergent fiber, ADF= acid detergent fiber, FCT= free condensed tannins, PBCT= protein-bound condensed tannins, FBCT= fiber-bound condensed tannins, TCT= total condensed tannins.
Fecal egg count
Table 3 shows the results for FEC and efficacy percentage of the diet supplemented with A. cochliacantha leaves. The reduction percentage caused by this legume ranged between 32.8-70.8 from day 14 to 28, respectively.
Table 3 Fecal egg count of H. contortus (FEC, mean ± standard deviation) and efficacy percentage of the diet supplemented with A. cochliacantha leaves
| Days of sampling | ||||||
|---|---|---|---|---|---|---|
| Treatment | 1 | 7 | 14 | 21 | 28 | |
| T1 | FEC (/g of feces) | 1100±120 | 3250±735b | 2980±345ª | 5300±435a | 6850±1432.90ª |
| % Efficacy | ---- | ---- | ---- | ---- | ---- | |
| T2 | FEC (/g of feces) | 1100±133 | 6850±828ª | 2000±367b | 2050±432b | 2000±178b |
| % Efficacy | ---- | -110.7 | 32.8 | 81.1 | 70.8 | |
| P value | > 0.15 | <0.05 | < 0.01 | < 0.01 | < 0.01 | |
T1: control (animals infected with L3 larvae of H. contortus); T2: animals infected with L3 larvae of H. contortus supplemented with 5% of A. cochliacantha leaves.
Water and dry matter intake
Table 4 shows the results for water and dry matter intake. No effect was observed in both variables (P>0.05).
Table 4: Water intake (WI) and dry matter intake (DMI) per day in goat kids infected with H. contortus and fed a diet supplemented with A. cochliacantha leaves
| Days of sampling | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 7 | 14 | 21 | 28 | ||||||
| T | WI | DMI | WI | DMI | WI | DMI | WI | DMI | WI | DMI |
| 1 | 1.7±0.3 | 436.3±47.6 | 1.6±0.1 | 530.0±80.4 | 1.8±0.1 | 650.4±173.2 | 1.7±0.08 | 647.7±206.7 | 1.8±0.2 | 651.5±211.0 |
| 2 | 1.6±0.3 | 448.7±100.0 | 1.5±0.4 | 559.7±141.3 | 1.8±0.5 | 625.0±216.6 | 1.7±0.4 | 745.1±272.5 | 1.7±0.4 | 694.5±194.2 |
| P | 0.71 | 0.80 | 0.69 | 0.69 | 0.76 | 0.84 | 0.90 | 0.52 | 0.75 | 0.76 |
T= treatment; 1= control (animals infected with L3 larvae of H. contortus); T2= infected animals supplemented with 5% of A. cochliacantha leaves. Water intake in liters and dry matter intake in grams per day.
Discussion
This study demonstrated the antiparasitic effect of a diet supplemented with A. cochliacantha leaves in goat kids; the prolonged consumption of this legume has benefits on animal health. Recently, this legume was evaluated in vitro against sheep and cattle gastrointestinal parasites with positive results8,12. These studies demonstrated the ovicidal and larvicidal activities against different GIN, Haemonchus contortus among them. With this background, the results confirm the in vivo antiparasitic effect against the most important gastrointestinal nematodes in small ruminants.
Similar results were previously reported in hair sheep infected with L3 larvae of H. contortus and fed diets supplemented with Lysiloma acapulcensis dehydrated leaves; these sheep showed a 67.7 % decrease in fecal egg count per gram of feces9. A different study in Brazil reported a decrease of up to 70 % after supplying Mimosa caesalpiniifolia leaves in sheep infected with H. contortus26.
Moreover, ruminants fed legume trees not only obtain health benefits, but they also increase their daily protein intake as a result of the high CP content, more than 18 %, in the organic matter of these forage resources, which are high concentrations compared to those of grasses that rarely exceed 10 %. Therefore, these plants exert a nutraceutical effect on animals27. Consequently, several studies have hypothesized that in animals fed grasses and legumes, the intake proportion will depend on the protein content of grasses. If it is lower than 8 %, legume intake would increase; legumes can be arboreal or shrubs. Méndez-Ortíz et al28 observed that sheep infected with H. contortus consumed more arboreal legume (Havardia albicans) rich in secondary metabolites. However, these legumes can have positive or negative effects on confined animals, directly affecting the level of dietary intake and metabolizable protein, which is directly related to the amount of condensed tannins per gram of dry matter. A previous report mentioned that to obtain benefits, condensed tannins must not exceed 5 % of the total diet29.
In this study, there were no negative effects on water and dry matter intake in animals fed a diet supplemented with A. cochliacantha, which demonstrated that the intake of total condensed tannins did not affect dry matter intake. According to that reported in the literature, high dietary levels of secondary compounds, particularly free condensed tannins (greater than 50 g kg-1 of DM), could inhibit the microbial activity in the rumen and thus affect the digestibility of the potentially digestible fraction of the nutrients, decreasing dry matter intake as a result of the increase in the rumen mean retention time30. Although this phenomenon could have a positive effect on the metabolism of nitrogenous compounds by decreasing ruminal proteolysis, which would increase the bypass protein and the amino acid flux to the duodenum, it would increase the metabolizable protein for productive purposes in the animals31.
The analysis of the condensed tannins in A. cochliacantha (Table 2) revealed that this plant could have similar effects to that explained before since it contains 20.2 % of total condensed tannins and 14.0 % of free condensed tannins (FCT), which are the bioactive compounds and can sequester carbohydrates and proteins from the diet. However, since it was only included 5% of A. cochliacantha leaves in the total diet, the intake of total condensed tannins (TCT) was 5.70 g, and of these, only 3.9 g were FCT; this concentration was not enough to decrease dry matter intake in the animals fed a diet supplemented with A. cochliacantha leaves. These results are similar to those reported by León-Castro et al32; they observed a significant decrease in the FEC per gram of feces in goat kids artificially infected with H. contortus and fed diets supplemented with 10 % of A. cochliacantha leaves without negative health effects.
Future studies should consider the dose-response on dry and organic matter intake, and the digestibility of basal diets with different amounts of A. cochliacantha leaves. Plants rich in secondary metabolites, such as tannins, contain nutraceutical properties7, and it has been confirmed in numerous animal nutrition studies that tannins are the polyphenols responsible for improving the nutritional value of livestock diets. Similarly, plant extracts rich in tannins have been reported to have antiparasitic properties32-35. However, although it could be inferred that the high amounts of condensed tannins in A. cochliacantha are responsible for the antiparasitic activity, Castillo-Mitre et al12 reported that the compounds with antiparasitic properties derived from the hydroxycinnamic acid (caffeic, coumaric, ferulic, and methyl caffeate acids). Hence, the antiparasitic activity of this legume could be due to these compounds, and tannins could act as secondary collaborators on the control of H. contortus by protecting the dietary protein from the rumen microorganisms. Therefore, this in vivo study, in addition to previous in vitro studies12 with A. cochliacantha, could be important for future research on its nutraceutical properties in small ruminants.
Acknowledgments
This study was partially funded by INIFAP (project SIGI 8215734475), the Universidad Autónoma del Estado de México (UAEM project 4585/2018/CIP), and the Red Temática de Farmoquímicos, CONACYT (Project number 294727, 2018). This study was part of the doctoral thesis of Gastón Federico Castillo-Miter under the direction of Dr. Rolando Rojo-Rubio and Dr. Agustín Olmedo-Juárez.
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Received: October 28, 2018; Accepted: October 28, 2019
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