Abstract
Background and Aim:
The continuous use of anthelmintic drugs has led to global issues of resistance. One breakthrough to address this problem is the utilization of bio-anthelmintics derived from active compounds in agro-industrial waste. This in vivo study investigated the effectiveness of Podang mango (Mangifera indica L.) fruit peel waste extract for anthelmintic purposes, using concentrations up to 5%.
Materials and Methods:
This study included 28 Etawa crossbred goats aged 17 months. Goats were randomly assigned to four groups: A negative control, an aqueous fruit peel extract (AFPE) group at 2.5%, another AFPE group at 5%, and a positive control receiving ivermectin. Goats chosen had egg per gram (EPG) counts surpassing 1000 before exposure to Haemonchus contortus. For 7 days within a 9-week study, AFPE from Podang mangoes was given. On the 7th day, the positive control group was administered ivermectin. AFPE dosage relied on the average abomasum fluid per kilogram of animal weight. The feeding regimen consisted of concentrate and Pennisetum purpureum cv. Mott is customized for the nutritional needs of livestock. Data on feed consumption, digestibility, average daily gain, percentage reduction in fecal egg count, body condition score, and clinical parameters were collected throughout the study.
Results:
At higher treatment levels (AFPE), there was a greater reduction in both EPG and fecal egg counts. The expected and normal ranges were maintained for consumption and digestibility. While body weight increased, FAMACHA parameters showed a decrease. Compared to the negative control group, substantial disparities (p < 0.05) existed for hemoglobin, red blood cells, and hematocrit in both the positive control and the treatment groups. Blood urea nitrogen and creatinine, indicative of liver and kidney health, were within normal ranges.
Conclusion:
At a concentration of up to 5%, Podang mango waste extract (AFPE) can function as a substitute for traditional helminth medicines or bio-anthelmintics in goats, enhancing their production.
Keywords: anthelmintic, feed additive, gastrointestinal helminth infection, goat, Haemonchus contortus, Mangifera indica L
Introduction
Due to the expanding human population, the need for animal protein has escalated [1]. Goats, an alternative in Indonesia, are gaining popularity for meeting the increasing demand for animal proteins [2]. According to Livestock and Animal Health Statistics [3], goat farming in East Java has markedly expanded (goat population of 19,400,000 by 2022) in Indonesia. In Indonesia’s community-based goat farming, health issues due to gastrointestinal nematode infections pose significant challenges. Studies by Baihaqi et al. [4, 5] highlighted Haemonchus contortus as the most common nematode infecting small ruminants in Indonesia. Parasite-related problems pose significant challenges in goat farming across Indonesian landscapes. Effective management of gastrointestinal nematode infections in goats is crucial for maintaining their health and productivity as significant contributors to animal protein production. The global ruminant sector grapples with a significant issue: Parasite offspring increasingly resist chemical drugs due to their misuse. Researchers seek plant-derived active compounds to address drug resistance [6]. To tackle resistance issues, researchers are exploring new anthelmintic options. Baihaqi et al. [7] revealed the untapped potential of Paraserianthes falcataria bark waste. According to SEM findings, P. falcataria bark waste harbors plant compounds essential for helminth death through damage to the helminth cuticle. Baihaqi et al. [8] demonstrated through an in vitro study that Carica pubescens seed waste damages H. contortus cuticle structure, thus eliminating it. This study found that Carica seeds did not impact ruminal fermentation while lowering methane gas production, supporting earlier findings by Baihaqi et al. [9].
Studies are essential to verify the anthelmintic properties of active plant compounds extracted from agro-industrial waste in living organisms [6]. Analyzing hematological and blood chemistry parameters is required for evaluating an individual’s health status [10]. According to Hajare et al. [11], helminth infections of the digestive tract result in approximately 200,000 ruminant deaths globally. Štrbac et al. [12] underline the importance of investigating alternative anthelmintics, especially those derived from natural plant sources.
The present study explored the effectiveness of aqueous fruit peel extract (AFPE) for anthelmintic purposes, using concentrations up to 5%. This study, by examining hematological and blood chemistry markers systematically, shed light on AFPE’s potential as a long-term, viable treatment for gastrointestinal helminth infections in ruminants. We seek alternative anthelmintic treatments in line with the global effort.
Materials and Methods
Ethical approval
The research protocol was approved by the Animal Care and Use Committee of the Universitas Brawijaya (reference number 144-KEP-UB-2023).
Study period and location
The study was conducted from July 2023 to October 2023 at Al Baihaqi Farm in Kediri, East Java, Indonesia. The samples were tested at the Faculty of Veterinary Medicine, Universitas Gadjah Mada, Indonesia.
Plant material and extraction
Podang mango (Mangifera indica L.) fruit peel was collected from small- and medium-sized enterprises in Banyakan Village, Kediri, East Java, Indonesia (CV. Sumber Mulyo). Experiments on water extracts and phytochemical (qualitative and quantitative) analyses were conducted using the method described by Dicko et al. [13] with some modifications (the filtration was done four times using absorbent cotton).
Experimental design
Twenty-eight 17-month-old Etawa crossbred male goats were randomly distributed among four treatment groups in this research. The goats weighed between 24 and 27 kg. For 7 days, goats infected with H. contortus from a local farming area (with egg per gram [EPG] count exceeding 1000) received consecutive AFPE treatments at doses of 2.5% and 5%. On the 7th day, the positive control group was given a singular oral dose of ivermectin. Goats were housed individually with a diet of copra cake, palm oil cake, corn gluten feed, coffee peel, corn waste, cassava waste, molasses, premix, multivitamins, herbs, and Napier grass. An unlimited supply of water was available.
Parasitological examination
The parasitological examination in this study involved the collection of fecal samples from the rectum of goats using the grab sampling method at various time points during the pre-study period and on days 0, 7, 14, 21, and 28. The McMaster method determined EPG as indicated by Baihaqi et al. [4]. Two gram of stool was transferred to a beaker and 58 mL of saturated sugar solution was added to reach a final volume of 60 mL. The tea strainer was used to stir and filter the mixture. A McMaster counting chamber received the fecal suspension extracted with a pipette. After a 2–3 min soak, the samples were observed under a microscope (VHX-7000 KEYENCE, Indonesia) (magnification 40×). The total EPG was determined by identifying and counting H. contortus nematode eggs.
Body weight
Livestock were weighed once a week in the morning before their weekend feeding. Assessing body condition score (BCS) involves examining and feeling eight distinct body regions: The spinous and transverse processes, flanks, tuber coxae, and ischiatic tubers. The BCS assessment diagram employs a 1–4 scale (1 – very thin, 2 – skinny, 3 – moderate, and 4 – fat) [14].
Feed consumption and digestibility
The dry matter (DM), organic matter (OM), and crude protein (CP) content of both concentrate and forage animal feed samples were analyzed for feeding consumption calculation [2]. Stool samples were collected within 24-h post-treatment with M. indica fruit peel extract. About 10% of the samples were first dried in the sun and then oven-dried at 60°C. A Wiley Mill grinding maching (https://www.thomassci.com/Equipment/Mills/_/Wiley-Mill-4-12-Horse-Power-Unit-Accessories) with a 1-mm sieve size was used to grind dry feces for seven consecutive days. The contents of DM, OM, and CP in composite fecal samples were determined as described by Lokapirnasari et al. [15].
Blood samples and FAMACHA© system
Three-milliliter syringes were used to draw blood from the jugular veins of goats. Blood samples were collected on day 0 and day 28. A blood test was carried out to determine hemoglobin (Hb) levels, erythrocyte count, packed cell volume (PCV), leukocyte count, leukocyte differential, and blood chemistry [16]. Using FAMACHA© (University of Rhode Island, United States), the eyes were opened to assess animal health. The eyes’ upper and lower eyelids exhibited mucosal alterations. The color of the eyelids was compared to that of FAMACHA© for assessing anemia caused by H. contortus infection [14]. The image’s color was used to assess anemia’s severity. Anemic degree was compared with PCV results subsequently.
Statistical analysis
One-way analysis of variance was used to analyze data obtained from in vivo experiments. Duncan’s multiple-range test determined the statistical differences between the means. p < 0.05 was considered statistically significant. The data were analyzed using Statistical Package for the Social Sciences, version 20.0 (IBM Corp., NY, USA).
Results and Discussion
Qualitative and quantitative phytochemical analyses of Podang mangoes
Tables-1 and 2 present the findings of qualitative and quantitative phytochemical analyses. The analysis of active compounds such as tannins, alkaloids, flavonoids, saponins, and steroids from Podang APFE mangoes yielded positive qualitative findings, while the quantitative analysis revealed a total phenolic content of 9.8 (mgGallic acid equivalen/g dw), a flavonoid content of 6.3 (mg Rutin equivalent/g dw), and a total tannin content of 7.3%. The industrial waste is potentially valuable for multiple uses in the ruminant industry. The in vitro research proposes it as a potential alternative to control gastrointestinal helminth infections, decrease methane emissions, and safeguard proteins [5, 7, 8].
Table-1.
Phytochemicals | Tannin | Flavonoid | Saponin | Alkaloid | Steroid |
---|---|---|---|---|---|
AFPE samples | + | + | + | + | + |
(+) Presence of constituents, (−) absence of constituents, AFPE=Aqueous fruit peel extract
Table-2.
Material | AFPE of Podang mango (%) |
---|---|
Tannin total (%) | 7.3 |
Condensed tannin, CT (%) | 4.9 |
Hydrolyzed tannin (%) | 3.5 |
Total phenolic (mg GAE/g dw) | 9.8 |
Flavonoids content (mg RE/g dw) | 6.3 |
AFPE=Aqueous fruit peel extract of Podang mango, CT=Computed tomography, GAE=Gallic acid equivalent, RE=Rutin equivalent
EPG-fecal egg count reduction (FECR) parameters
The FECR and EPG indices decreased in all groups, with the values presented in Table-3 for the negative control, 2.5% AFPE of Podang mango, 5% AFPE treatment, and positive control. During the study, improved nutrition led to a decrease in helminth egg count for the negative control group. About 100% of reduction in EPG was observed in the positive control group given ivermectin. About 2.5% and 5% of AFPE significantly reduced H. contortus egg production in thin-tailed goats. Hazarika et al. [17] observed that the extracts of Nyctanthes arbor-tristis and Butea monosperma, rich in tannins, saponins, flavonoids, and phenols, decreased FECR significantly. Mesquita-Sousa et al. [18] noted that Citrus aurantium var. is effective when used in combination. Dulcis exhibited improved FECR due to the presence of active compounds.
Table-3.
Treatment group | EPG | FECR (%) | |
---|---|---|---|
| |||
Pre-treatment | Post-treatment | ||
Negative control | 1385.29 ± 12.22a | 1172.51 ± 26.39b | 15.37 |
AFPE 2.5% | 1283.28 ± 18.35a | 673.31 ± 2.33b | 47.54 |
AFPE 5% | 1316.37 ± 24.52a | 218.42 ± 3.11b | 83.43 |
Positive control | 1251.22 ± 16.21a | 0.00 ± 0.00b | 100.00 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE: Aqueous fruit peel extract of Podang mango, EPG-FECR=Egg per gram-fecal egg count reduction
Nutrient intakes
Table-4 shows that the average consumption of DM, OM, and CP in all treatment groups with AFPE, regardless of the concentration (up to 5%), did not significantly differ between pre- and post-treatment stages (p > 0.05). The consumption of DM, OM, and CP by Arabi goats remains unaffected by Albizia lebbeck tannins, according to Ardeshiri et al. [19]. Faryabi et al. [20] reported no significant difference in feed consumption, water intake, final body weight, daily weight gain, or feed conversion ratio on substituting sheep feed with Artemisia sieberi leaves.
Table-4.
Treatment group | Parameter | Pre- treatment (g) | Post- treatment (g) |
---|---|---|---|
Negative control | DMI | 869.16 ± 0.28 | 873.28 ± 0.17 |
OMI | 832.72 ± 0.29 | 839.62 ± 0.21 | |
CPI | 193.71 ± 0.21 | 197.26 ± 0.16 | |
AFPE 2.5% | DMI | 851.73 ± 0.24 | 874.27 ± 0.14 |
OMI | 836.28 ± 0.37 | 840.53 ± 0.26 | |
CPI | 185.73 ± 0.28 | 189.16 ± 0.25 | |
AFPE 5% | DMI | 821.73 ± 0.25 | 824.39 ± 0.16 |
OMI | 817.53 ± 0.16 | 821.27 ± 0.15 | |
CPI | 171.88 ± 0.24 | 174.38 ± 0.25 | |
Positive control | DMI | 836.53 ± 0.29 | 841.39 ± 0.17 |
OMI | 827.36 ± 0.25 | 830.62 ± 0.16 | |
CPI | 173.35 ± 0.89 | 177.32 ± 0.25 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of podang mango, DMI=Dry matter intake, OMI=Organic matter intake, CPI=Crude protein intake
Nutrient digestibility
Digestibility parameters of DM, OM, and CP for goats in groups with up to 5% AFPE and the negative and positive control groups remained unchanged (p > 0.05) from pre- to post-treatment (Table-5). According to Ibidhi and Salim [21], goats given Trigonella foenum graecum L. seeds, known for phenolic compounds, experienced no substantial decrease in digestibility. Shilwant et al. [22] discovered varied outcomes: Their composite plant extract improved digestibility of DM and OM, while CP remained unaffected.
Table-5.
Treatment group | Parameters | Pre- treatment (%) | Post- treatment (%) |
---|---|---|---|
Negative control | DM digestibility | 72.19 ± 0.16 | 71.28 ± 0.24 |
OM digestibility | 73.31 ± 0.17 | 72.23 ± 0.25 | |
CP digestibility | 74.11 ± 0.28 | 73.03 ± 0.28 | |
AFPE 2.5% | DM digestibility | 73.20 ± 0.21 | 72.17 ± 0.41 |
OM digestibility | 72.12 ± 0.17 | 71.16 ± 0.28 | |
CP digestibility | 73.15 ± 0.24 | 72.04 ± 0.25 | |
AFPE 5.0% | DM digestibility | 73.06 ± 0.12 | 72.66 ± 0.15 |
OM digestibility | 72.13 ± 0.41 | 71.58 ± 0.34 | |
CP digestibility | 73.25 ± 0.18 | 72.42 ± 0.21 | |
Positive control | DM digestibility | 72.36 ± 0.11 | 71.26 ± 0.25 |
OM digestibility | 72.24 ± 0.16 | 71.94 ± 0.23 | |
CP digestibility | 73.12 ± 0.24 | 72.43 ± 0.21 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango
Effect of AFPE Podang mango on hematology parameters
In Table-6, Hb, red blood cells (RBC), and hematocrit levels significantly differed between groups treated with 2.5% and 5% of AFPE, as well as the positive control, versus the negative control group, before and after treatment (p < 0.05). No significant change in these parameters was observed for the untreated group with gastrointestinal nematodes (GIN) (negative control). Suppressing H. contortus’ EPG count was demonstrated by this. Dubey et al. [23] found goats treated with Tecoma stans seed ethanol extract had significant increases (p > 0.05) in white blood cells, Hb, RBC, and PCV compared to the untreated group. The increase in hematological variables in this study can be explained by the body’s reaction to H. contortus, a blood-feeding parasite causing gastrointestinal inflammation. According to Sambodo et al. [14], the negative control group had lower RBC and leukocyte parameters, indicating that GIN infection in goats could lead to anemia through blood loss.
Table-6.
Treatment group | Hematology parameters | Pre-treatment | Post-treatment |
---|---|---|---|
Negative control | Hb (g/dL) | 8.32 ± 0.17 | 8.94 ± 0.23 |
HCT (%) | 23.16 ± 0.44 | 23.95 ± 0.35 | |
MCV (fL) | 40.19 ± 0.22 | 40.27 ± 0.15 | |
MCH (pg) | 11.27 ± 0.25 | 12.28 ± 0.17 | |
MCHC (%) | 33.24 ± 0.28 | 33.21 ± 0.18 | |
RBC (×106/μL) | 8.16 ± 0.89 | 8.46 ± 0.24 | |
Leukocyte (×103/mm3) | 16.25 ± 0.27 | 15.94 ± 0.25 | |
Neutrophil (%) | 40.15 ± 0.29 | 39.22 ± 0.25 | |
Eosinophil (%) | 29.58 ± 0.21 | 28.24 ± 0.44 | |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 | |
Lymphocytes (%) | 59.28 ± 0.21 | 57.24 ± 0.29 | |
Monocytes (%) | 3.00 ± 0.00 | 3.00 ± 0.00 | |
AFPE 2.5% | Hb (g/dL) | 11.95 ± 0.21 | 13.57 ± 0.45 |
HCT (%) | 26.13 ± 0.25b | 28.13 ± 0.18a | |
MCV (fL) | 40.14 ± 0.17a | 37.12 ± 0.16b | |
MCH (pg) | 12.03 ± 0.13 | 11.36 ± 0.25 | |
MCHC (%) | 27.51 ± 0.29 | 26.24 ± 0.21 | |
RBC (×106/μL) | 9.03 ± 0.15 | 11.14 ± 0.23 | |
Leukocyte (×103/mm3) | 14.03 ± 0.22a | 11.27 ± 0.56b | |
Neutrophil (%) | 25.12 ± 0.28a | 29.13 ± 0.15b | |
Eosinophil (%) | 32.04 ± 0.25a | 26.22 ± 0.13b | |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 | |
Lymphocytes (%) | 58.23 ± 0.14a | 45.25 ± 0.21b | |
Monocytes (%) | 3.00 ± 0.00 | 3.00 ± 0.00 | |
AFPE 5% | Hb (g/dL) | 10.81 ± 0.18 | 13.24 ± 0.18 |
HCT (%) | 24.15 ± 0.12b | 28.27 ± 0.15a | |
MCV (fL) | 39.13 ± 0.17a | 35.12 ± 0.15b | |
MCH (pg) | 13.23 ± 0.15 | 11.53 ± 0.23 | |
MCHC (%) | 27.14 ± 0.13 | 26.11 ± 0.24 | |
RBC (×106/μL) | 9.05 ± 0.21 | 11.88 ± 0.24 | |
Leukocyte (×103/mm3) | 14.28 ± 0.13a | 11.05 ± 0.22b | |
Neutrophil (%) | 25.47 ± 0.21a | 30.46 ± 0.12b | |
Eosinophil (%) | 28.33 ± 0.25a | 23.86 ± 0.22b | |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 | |
Lymphocytes (%) | 48.25 ± 0.25a | 42.98 ± 0.21b | |
Monocytes (%) | 3.00 ± 0.00 | 3.00 ± 0.00 | |
Positive control | Hb (g/dL) | 10.35 ± 0.27 | 12.14 ± 0.21 |
HCT (%) | 25.26 ± 0.13b | 27.83 ± 0.23a | |
MCV (fL) | 41.28 ± 0.24a | 36.38 ± 0.21b | |
MCH (pg) | 12.88 ± 0.13 | 11.13 ± 0.31 | |
MCHC (%) | 28.63 ± 0.28 | 27.12 ± 0.17 | |
RBC (×106/μL) | 8.18 ± 0.25 | 10.26 ± 0.25 | |
Leukocyte (×103/mm3) | 15.21 ± 0.28a | 12.14 ± 0.27b | |
Neutrophil (%) | 27.35 ± 0.24a | 31.22 ± 0.17b | |
Eosinophil (%) | 30.18 ± 0.42a | 23.19 ± 0.27b | |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 | |
Lymphocytes (%) | 50.02 ± 0.31a | 43.02 ± 0.35b | |
Monocytes (%) | 3.00 ± 0.00 | 3.00 ± 0.00 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango, Hb=Hemoglobin, RBC=Red blood cells, HCT=Hematocrit, MCH=Mean corpuscular hemoglobin, MCV=Mean corpuscular volume
Effect of AFPE Podang mango on chemical blood parameters
Table-7 details the blood chemistry values of the goats before and after treatment. In the negative control groups, the aspartate transaminase (AST) and alanine transaminase (ALT) levels in goat blood remained unchanged, whereas a significant reduction (p < 0.05) was observed in the treated groups. A gastrointestinal helminth infection may cause damage to the digestive tract and liver, as indicated by this pattern. Administering extracts with active compounds led to decreased AST and ALT values in goats by Tanwar and Misra [24], suggesting an improvement in their liver tissue. Radostits et al. [25] reported an increased blood albumin level in the group given plant extracts and active compounds. The goats’ enhanced protein nutrition and improved liver function are suggested by this increase. In goats, decreased creatinine levels due to active plant compounds suggest a possible enhancement of kidney function or protein nutrition. Triterpenoids and saponins have been reported to exhibit hepatoprotective properties [26].
Table-7.
Treatment group | Blood chemical parameters | Pre-treatment | Post-treatment |
---|---|---|---|
Negative control | TP (g/dL) | 6.27 ± 0.14 | 5.98 ± 0.17 |
Albumin (g/dL) | 2.58 ± 0.11 | 2.49 ± 0.12 | |
Globulin (g/dL) | 2.91 ± 0.28 | 2.83 ± 0.15 | |
Glucose (mg/dL) | 45.58 ± 0.21 | 45.43 ± 0.18 | |
BUN (mg/dL) | 15.82 ± 0.13 | 15.75 ± 0.16 | |
AST (IU/L) | 130.26 ± 0.21 | 130.18 ± 0.13 | |
ALT (IU/L) | 38.26 ± 0.14 | 38.37 ± 0.12 | |
Creatinine (mg/dL) | 1.13 ± 0.27 | 1.12 ± 0.14 | |
AFPE 2.5% | TP (g/dL) | 5.84 ± 0.13 | 5.62 ± 0.29 |
Albumin (g/dL) | 3.58 ± 0.27 | 3.43 ± 0.18 | |
Globulin (g/dL) | 2.92 ± 0.26 | 2.83 ± 0.21 | |
Glucose (mg/dL) | 45.84 ± 0.17 | 45.62 ± 0.16 | |
BUN (mg/dL) | 14.74 ± 0.21a | 19.91 ± 0.27b | |
AST (IU/L) | 132.25 ± 0.16a | 92.03 ± 0.24b | |
ALT (IU/L) | 37.01 ± 0.18a | 25.22 ± 0.73b | |
Creatinine (mg/dL) | 1.22 ± 0.12 | 1.23 ± 0.15 | |
TP (g/dL) | 5.84 ± 0.13 | 5.62 ± 0.29 | |
Albumin (g/dL) | 3.58 ± 0.27 | 3.43 ± 0.18 | |
AFPE 5% | TP (g/dL) | 5.83 ± 0.12 | 5.63 ± 0.22 |
Albumin (g/dL) | 3.79 ± 0.17 | 3.64 ± 0.13 | |
Globulin (g/dL) | 2.84 ± 0.26 | 2.75 ± 0.13 | |
Glucose (mg/dL) | 45.32 ± 0.19 | 46.74 ± 0.14 | |
BUN (mg/dL) | 16.22 ± 0.12a | 22.27 ± 0.28a | |
AST (IU/L) | 142.17 ± 0.27a | 93.92 ± 0.21b | |
ALT (IU/L) | 38.37 ± 0.13a | 26.35 ± 0.23b | |
Creatinine (mg/dL) | 1.24 ± 0.13 | 1.25 ± 0.24 | |
Positive control | TP (g/dL) | 5.53 ± 0.21 | 5.41 ± 0.87 |
Albumin (g/dL) | 3.83 ± 0.27 | 3.72 ± 0.25 | |
Globulin (g/dL) | 2.82 ± 0.16 | 2.79 ± 0.19 | |
Glucose (mg/dL) | 57.13 ± 0.24 | 56.28 ± 0.18 | |
BUN (mg/dL) | 15.24 ± 0.17b | 21.23 ± 0.13a | |
AST (IU/L) | 127.22 ± 0.12a | 98.21 ± 0.15b | |
ALT (IU/L) | 39.42 ± 0.15a | 26.28 ± 0.13b | |
Creatinine (mg/dL) | 1.25 ± 0.23 | 1.24 ± 0.21 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango, TP=Total protein, BUN=Blood urea nitrogen, AST=Aspartate transaminase, ALT=Alanine transaminase
The goats treated in the study had blood urea nitrogen (BUN) and creatinine levels within the normal range for average goats (10–35 mg/dL for BUN and 1.2–1.9 mg/dL for creatinine). Rams given Kyasuwa grass had a BUN value of 14 mg/dL. In desert Bighorn goats, the BUN reference interval is 5–28 mg/dL and the creatinine range is 1.6–2.6 mg/dL. 5 mg/mL AFPE Podang mango and ivermectin did not impact kidney function. At this concentration, AFPE Podang mangoes did not harm the kidneys. The study by Meenakshisundaram et al. [27] supports the observation that the given plant extracts did not impair kidney function. The plant extracts administration did not harm the kidneys based on normal BUN and creatinine levels.
Effect of AFPE Podang mango on FAMACHA parameters
In Table-8, the statistical analysis showed significant effects on FAMACHA parameters for the positive control group and the 5% AFPE treatment group (p < 0.05), while no significant differences were observed between the negative control and the 2.5% AFPE group. Kumar et al. [28] emphasized the value of FAMACHA for detecting Haemonchus spp. infection and proposed Carica papaya seed extract as an effective alternative to control haemonchosis in goats. Sambodo et al. [14] observed an increase in FAMACHA values coinciding with hematological changes following AFPE administration.
Table-8.
Treatment group | Pre-treatment | Post-treatment |
---|---|---|
Negative control | 4.16 ± 0.29 | 3.75 ± 0.26 |
AFPE 2.5% | 3.99 ± 0.17 | 3.64 ± 0.18 |
AFPE 5.0% | 3.95 ± 0.14a | 2.28 ± 0.19b |
Positive control | 4.04 ± 0.18a | 2.15 ± 0.31b |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango
Effect of AFPE Podang mango on body weight
In Table-9, the in vivo study results showed that goats in both the AFPE treatment and positive control groups had significantly higher average body weights (p < 0.05), whereas goats in the negative control group had lower average body weights. Jamarun et al. [29] reported a 65.25 g/head/day increase in body weight gain when supplementing Rhizophora apiculata leaves, Hay, and Fermented Tithonia diversifolia with active compounds. Morais-Costa et al. [30] found significant weight gain using Piptadenia viridiflora water extract (p < 0.05). 5% AFPE administration, along with positive controls, led to an increase in body weight likely from decreased helminth infections. The goat’s increase in body weight did not negatively impact feed consumption, digestibility, or health conditions, as indicated by consistent hematology and blood chemistry readings.
Table-9.
Treatment group | Pre-treatment (kg) | Post-treatment (kg) |
---|---|---|
Negative control | 25.41 ± 0.19a | 23.19 ± 0.13b |
AFPE 2.5% | 26.84 ± 0.23b | 31.27 ± 0.25a |
AFPE 5.0% | 27.93 ± 0.15b | 32.63 ± 0.25a |
Positive control | 24.93 ± 0.24b | 31.72 ± 0.27a |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango
Effect of AFPE Podang mango on BCS parameters
The BCS rose significantly (p > 0.05) by up to 5% in the AFPE treatment group and 5% in the positive control group. A decrease in helminth infections in goats corresponded to an improvement in their BCS (Table-10), implying that AFPE mango pods did not negatively impact their health and nutritional status. Mahachi et al. [31] showed that incorporating up to 25% Sericea lespedeza in goat feedlots suppressed H. contortus infections, maintaining body weight and BCS unchanged. Likewise, Soto-Barrientos et al. [32] found a close relationship between goats’ low BCS and severe gastrointestinal nematode infection.
Table-10.
Treatment group | Pre-treatment | Post-treatment |
---|---|---|
Negative control | 3.00 ± 0.27 | 2.85 ± 0.14 |
AFPE 2.5% | 3.00 ± 0.14 | 3.32 ± 0.18 |
AFPE 5% | 3.20 ± 0.16 | 3.58 ± 0.42 |
Positive control | 3.00 ± 0.18 | 3.42 ± 0.25 |
a,bDifferent superscripts on the same line indicate significant differences (p < 0.05). AFPE=Aqueous fruit peel extract of Podang mango, BCS scale: 1=very thin, 2=skinny, 3=moderate, 4=fat
Conclusion
About 5% of Podang mango peel waste usage shows potential as a bioanthelmintic without negatively impacting livestock productivity and health. The study effectively decreased EPG while keeping feed consumption and digestibility constant, boosted body weight, reduced FAMACHA scores, and kept BUN and creatinine levels within normal limits.
Authors’ Contributions
ENP, ZAB, ER, and SS: Designed the study, collected the samples, and performed the examinations. ZAB: Conducted field surveys. All authors have drafted, revised, and approved the final manuscript.
Acknowledgments
This study was supported by the Collaborative Research between Higher Education Institutions, ITS-LLDIKTI, Indonesia, VII Batch 1, 2023 (grant number 1776/PKS/ITS/2023).
Competing Interests
The authors declare that they have no competing interests.
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References
- 1.Floret C, Monnet A.F, Micard V, Walrand S, Micho C. Replacement of animal proteins in food:How to take advantage of nutritional and gelling properties of alternative protein sources. Crit. Rev. Food Sci. Nutr. 2023;63(7):920–946. doi: 10.1080/10408398.2021.1956426. [DOI] [PubMed] [Google Scholar]
- 2.Suwignyo B, Baihaqi Z.A, Utomo R, Sarmin S, Widiyon I. Effects of different feed restrictions on Kacang Goats. Pak. J. Nutr. 2017;16(4):236–241. [Google Scholar]
- 3.Livestock and Animal Health Statistics. Directorate General of Livestock and Animal Health Ministry of Agriculture Republic Indonesia. Vol. 1. Livestock and Animal Health Statistics, Indonesia. 2022 [Google Scholar]
- 4.Baihaqi Z.A, Widiyono I, Nurcahy W. Prevalence of gastrointestinal worms in Wonosobo and thin-tailed sheep on the slope of Mount Sumbing, Central Java, Indonesia. Vet. World. 2019;12(11):1866–1871. doi: 10.14202/vetworld.2019.1866-1871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Baihaqi Z.A, Widiyono I, Nurcahy W. Potential of Carica pubescens fruit peel as an alternative method to control Haemonchus contortus in small ruminants. Livest. Res. Rural Dev. 2020;32(7):106. [Google Scholar]
- 6.Qamar W, Alkheraij K.A. Anthelmintic resistance in Haemonchus contortus of sheep and goats from Asia - a review of in vitro and in vivo studies. Pak. Vet. J. 2023;43(3):376–387. [Google Scholar]
- 7.Baihaqi Z.A, Widiyono I, Nurcahy W. In vitro anthelmintic activity of aqueous and ethanol extracts of Paraserianthes falcataria bark waste against Haemonchus contortus obtained from a local slaughterhouse in Indonesia. Vet. World. 2020;13(8):1549–1554. doi: 10.14202/vetworld.2020.1549-1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Baihaqi Z.A, Widiyono I, Angeles A.A, Suwignyo B, Nurcahy W. Anthelmintic activity of Carica pubescens aqueous seed extract and its effects on rumen fermentation and methane reduction in Indonesian thin-tailed goat:An in vitro study. Vet. World. 2023;16(7):1421–1428. doi: 10.14202/vetworld.2023.1421-1428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Baihaqi Z.A, Widiyono I, Suwignyo B, Angele A.A. Alternative strategies of plant metabolite secondary “Tannin”for methane emissions reduction on ruminant livestock - a review of the last 5 years literature. Adv. Anim. Vet. Sci. 2022;10(3):599–606. [Google Scholar]
- 10.Baihaqi Z.A, Widiyono I, Nurcahy W. Prevalence naturally infected gastrointestinal parasites and complete blood count condition on Wonosobo goat at Wonosobo District, Central Java, Indonesia. Biodiversitas. 2020;21(7):3057–3061. [Google Scholar]
- 11.Hajare S.T, Gobena R.K, Chauhan N.M, Eris F. Prevalence of intestinal parasite infections and their associated factors among food handlers working in selected catering establishments from Bule hora, Ethiopia. Biomed Res. Int. 2021;2021:6669742. doi: 10.1155/2021/6669742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Štrbac F, Krnjajić S, Stojanović D, Ratajac R, Simin N, Orčić D, Rinaldi L, Ciccone E, Maurelli M.P, Cringoli G, Bosc A. In vitro and in vivo anthelmintic efficacy of peppermint (Mentha x piperita L.) essential oil against gastrointestinal nematodes of sheep. Front. Vet. Sci. 2023;10:1232570. doi: 10.3389/fvets.2023.1232570. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Dicko A, Konaté A, Azokou A, Sylla Y, Tindano B, Ahoua A.R.C, Koné M.W, Kaboré A, Traoré A, Bayala B, Tambour H.H. In vitro anthelmintic activity of Euphorbia forskalii J. Gay aqueous extracts evaluation on different life stages of Haemonchus contortus. Vet. Parasitol. Reg. Stud. Rep. 2023;44:100918. doi: 10.1016/j.vprsr.2023.100918. [DOI] [PubMed] [Google Scholar]
- 14.Sambodo P, Prastowo J, Kurniasih K, Mubarokah W.W, Indarjuliant S. In vivo efficacy of Biophytum petersianum on Haemonchus contortus in goats. Adv. Anim. Vet. Sci. 2020;8(3):238–244. [Google Scholar]
- 15.Lokapirnasari W.P, Al-Arif M.A, Hidayatik N, Safiranisa A, Arumdani D.F, Zahirah A.I, Yulianto A.B, Lamid M, Marbun T.D, Lisnanti E.F, Baihaqi Z.A, Khairullah A.R, Kurniawan S.C, Pelawi E.B.S, Hasi A. Effect of probiotics and acidifiers on feed intake, egg mass, production performance, and egg yolk chemical composition in late-laying quails. Vet. World. 2024;17(2):462–469. doi: 10.14202/vetworld.2024.462-469. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Lisnanti E.F, Lokapirnasari W.P, Hestianah E.P, Al Arif M.A, Baihaq Z.A. The effectiveness of giving marsh fleabane (Pluchea indica l.) Water extract on broiler hematology and blood glucose. Adv. Anim. Vet. Sci. 2023;11(8):1348–1356. [Google Scholar]
- 17.Hazarika A, Debnath S, Sarma J, Dek D. Evaluation of in vivo anthelmintic efficacy of certain indigenous plants against experimentally-induced Ascaridia galli infection in local birds (Gallus domesticus) Exp. Parasitol. 2023;247:108476. doi: 10.1016/j.exppara.2023.108476. [DOI] [PubMed] [Google Scholar]
- 18.Mesquita-Sousa D, Campos N.R.C.L, Pereira J.R.F, Gomes M.N, Silva C.R, Cutrim-Júnior J.A.A, Brito D.R.B, Sampaio R.M, Sargison N.D, Lifschitz A, Costa-Junio L.M. Evaluation of a combination of Citrus aurantium var. Dulcis essential oil and albendazole for the treatment of sheep gastrointestinal nematodes. Vet. Parasitol. 2023;318:109929. doi: 10.1016/j.vetpar.2023.109929. [DOI] [PubMed] [Google Scholar]
- 19.Ardeshiri H, Chaji M, Khorasan O. Effects of using siris (Albizia lebbeck) foliage in the diet of fattening lambs on nutrient digestibility, blood and rumen parameters, growth performance, and meat quality characteristics. Trop. Anim. Health Prod. 2022;54:247. doi: 10.1007/s11250-022-03239-y. [DOI] [PubMed] [Google Scholar]
- 20.Faryabi R, Mousaie A, Bahrampour J, Barazande A. The effect of dietary inclusion of Artemisia sieberi leaves on growth performance, feeding behaviors, ruminal fermentation, feed digestibility, and blood hemato-biochemical profile of growing male lambs. Trop. Anim. Health Prod. 2023;55(1):41. doi: 10.1007/s11250-023-03455-0. [DOI] [PubMed] [Google Scholar]
- 21.Ibidhi R, Sale H.B. Effect of daily or intermittent addition of fenugreek (Trigonella foenum graecum L.) seeds to concentrate on intake, digestion, and growth performance of Barbarine lamb. Small Rumin. Res. 2022;216:106792. [Google Scholar]
- 22.Shilwant S, Hundal J.S, Singla M, Patr A.K. Ruminal fermentation and methane production in vitro, milk production, nutrient utilization, blood profile, and immune responses of lactating goats fed polyphenolic and saponin-rich plant extracts. Environ. Sci. Pollut. Res. 2023;30(4):10901–10913. doi: 10.1007/s11356-022-22931-y. [DOI] [PubMed] [Google Scholar]
- 23.Dubey A, Pandey M, Yadav S, Tripathi D, Kumari M, Purohi D. Hypolipidemic and haematological effects of ethanolic extract of Tecoma stans linn (bignoniaceae) seeds in alloxan-induced diabetic albino rats. Korean J. Physiol. Pharmacol. 2023;27(1):85–90. [Google Scholar]
- 24.Tanwar R.K, Mishr S. Clinico-Haemato-biochemical studies on intestinal helminthiasis in poultry. Vet. Pract. 2021;2:137–140. [Google Scholar]
- 25.Radostits O.M, Blood D.C, Ga C.C. Veterinary Medicines. 8th ed. Bailliere Tindal, London: 1994. pp. 1223–1272. [Google Scholar]
- 26.Sakna S.T, Maghraby Y.R, Abdelfatta M.S. Phytochemical diversity and pharmacological effects of triterpenes from genus Ziziphus:A comprehensive review. Phytochem. Rev. 2022;22:1611–1636. [Google Scholar]
- 27.Meenakshisundaram A, Harikrishnan T.J, Ann T. Anthelmintic activity of Indigofera tinctoria against gastrointestinal nematodes of goat. Vet. World. 2016;9(1):101–106. doi: 10.14202/vetworld.2016.101-106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Kumar S, Shekhar P, Kumar A, Bhatt S, Singh V.K, Da A.K. Clinico-therapeutic studies on haemonchosis in Goats. Ind. J. Anim. Res. 2023;B-5066:1–6. [Google Scholar]
- 29.Jamarun N, Pazla R, Elihasridas A, Yanti G, Sari R.W.W, Ikhla Z. The impact of mangrove (Rhizophora apiculata) leaves hay and fermented Tithonia diversifolia on intake, nutrient digestibility and body weight gain of goat. Adv. Anim. Vet. Sci. 2023;11(9):1441–1450. [Google Scholar]
- 30.Morais-Costa F, Bastos G.A, Soares A.C.M, Costa E.G.L, Vasconcelos V.O, Oliveira N.J.F, Braga F.C, Duarte E.R, Lim W.S. In vitro and in vivo action of Piptadenia viridiflora (Kunth) Benth against Haemonchus contortus in sheep. Vet. Parasitol. 2016;223:43–49. doi: 10.1016/j.vetpar.2016.04.002. [DOI] [PubMed] [Google Scholar]
- 31.Mahachi L.N, Chikwanha O.C, Katiyatiya C.L.F, Marufu M.C, Aremu A.O, Mapiy C. Haemato-biochemical responses, worm burdens and Haemonchus contortus ultrastructural changes in lambs fed diets containing graded inclusion levels of Sericea lespedeza. Anim. Prod. Sci. 2023;63(14):1394–1409. [Google Scholar]
- 32.Soto-Barrientos N, Chan-Pérez J.I, España-España E, Novelo-Chi L.K, Palma-Ávila I, Ceballos-Mendoza A.C, Sarabia-Hernández J.A, Santos-Ricalde R.H, Cámara-Sarmiento R, Torres-Acost J.F.J. Comparing body condition score and FAMACHA© to identify hair-sheep ewes with high faecal egg counts of gastrointestinal nematodes in farms under hot tropical conditions. Small Rumin. Res. 2018;167:92–99. [Google Scholar]