Growth Performance and Gut Microbiota of Broilers Administered Different Levels of Mango Seed Kernel Extract

ABSTRACT

The current global trend to eradicate the use of antibiotic growth promoters (AGPs) from the poultry industry has led to the exploration of effective alternatives for sustainable poultry production and to overcome intestinal diseases in the post-AGP era. Therefore, medicinal plants and their extracts are being used as safe and natural substitutes. In this study, a research trial was conducted to explore the effect of different levels of mango seed kernel extract on the growth performance, carcass characteristics and gut microbiota of broiler birds, since mango is well known for its antioxidant, antibacterial and anti-inflammatory properties. Broiler birds (n=720) were allocated to six treatment groups under a completely randomized design; T1: positive control (basal diet with antibiotic), T2: negative control (basal diet without antibiotic), and T3, T4, T5 and T6 representing treatment groups supplemented with respectively 10 mL/kg, 20 mL/kg, 30 mL/kg and 40 mL/kg of feed of mango seed kernel extract (MSKE). Among the different levels of mango seed kernel extract, birds supplemented with 30 mL/kg and 40 mL/kg showed decreased total bacterial and differential bacterial counts, better Lactobacillus counts, and increased leg quarter and breast quarter weights. However, among the groups supplemented with 30 and 40 mL/kg, increased body weight gain and better FCR was observed in the 30 mL/kg group. Hence, it can be concluded that mango seed kernel extract given in broilers’ diet at the dose level of 30 mL/kg of feed can improve birds’ growth performance and function well as an AGP replacement, being a good option for sustainable poultry production.

Keywords:
Antibiotic growth promoters; broiler; growth performance; gut microbiota: mango seed kernel extract

INTRODUCTION

A key concern of poultry farmers is to raise their birds and reach market weight within the shortest time possible. This has led to the use of antibiotic growth promoters (AGPs) in the feed to improve birds’ growth performance by modifying their intestinal microbiota and eliminating harmful bacteria. However, there are serious concerns regarding the use of AGPs. Despite rigorous withdrawal measures preventing antibiotic residues, their overuse has led to increased antibiotic resistance. The use of antibiotics as growth promoters has been banned by the World Health Organization (Arsene et al., 2022). Therefore, researchers are searching for AGP alternatives, capable of promoting growth performance and reducing bacterial loads (Abaza et al., 2008). The use of alternatives like medicinal plants and their herbal extracts as natural feed additives has recently been studied by many researchers (Seidavi et al., 2021; Kuralkar & Kuralkar, 2021; Pliego et al., 2022). The mechanism of action of the bioactive compounds present in plant extracts is mainly dependent on increased enzyme secretion, changes in the intestinal microbiota, and the histomorphological status of the gastrointestinal tract, and improvements to immune system efficacy. Enhanced growth performances and feed conversion ratios, as well as decreased bacterial counts, have been seen with the supplementation of herbal extracts in poultry feed (Allinson et al., 2013).

Mango (Mangifera indica) is a tropical fruit known for its medicinal potential, with studies exploring the use of its leaves, barks, peels and kernels (Ayoola et al., 2020). Numerous compounds have been detected in mango, including saponins, polygalacturonose, triterpenoid, and tetracyclic triterpenoid (Doughari & Manzara, 2008). Mango extract has been used as a nutritional supplement, for cosmetic purposes, and as phytomedicine on industrial scale. Throughout the globe, there are many medicinal uses of mango barks, leaves and roots. Mango has been listed in the Program of Applied Research to Popular Medicine as an effective agent for the treatment of diarrhea, fever, gastritis and ulcers (Devi & Bhimba, 2011). Mango possesses a wide range of uses, including immunostimulant (Jeevitha et al., 2023), analgesic, anti-inflammatory (Abbas, 2022), spasmolytic, antidiarrheal (Nguyen et al., 2023), antidiabetic (Zarasvand et al., 2023), antioxidant (Saleem et al., 2023), dyslipidemic (Yoopum et al., 2023), anthelminthic, and antibacterial (Choudhary et al., 2020). A study on M.indica flowers showed antiulcerogenic and healing effects, using an extraction via aqueous decoction (Lima et al., 2006). Due to the antimicrobial, antioxidant, and otherwise health promoting traits of mango peels, seeds, pulps, leaves, flowers and barks, there has been an important increase in the study of their phytochemicals contituents (Masibo & He, 2008). According to the World Health Organization, in order to understand the efficiency, properties, and safety of medicinal plants, they should be properly investigated, as they are going to be the sources of health boosting medicines. The activity of herbs is greatly influenced by the methods by which the crude extract has been prepared. The quality of the extract is also determined by the plant part used for extraction, the solvent used, and the method of extraction applied (Ayoola et al., 2020). Our research study aimed to evaluate the growth performance, carcass characteristics, total bacterial count, and differential bacterial count of broiler birds given mango seed kernel extract (MSKE) prepared via decoction method at different dose levels as an alternative to AGPs.

MATERIALS AND METHODS

Preparation of Mango Seed Kernel

Mango seeds were procured from fruit juice processing industries. Mango seed kernels were removed from the seeds manually using a sharp knife, and the obtained seed kernels were then sun dried up to 10 % moisture level. The dried kernels were subsequently grinded and passed through a 40-mesh sieve. The sieved mango seed kernels were finally stored at 4˚C in sealed plastic bags until use for subsequent experiments.

Extraction via Decoction

Extraction via Decoction method was performed by boiling 1 g of dried mango seed kernel powder in 20 mL of distilled water (1:20) at 100°C for 30 minutes in the water bath. After cooling, it was filtered with eight layers of muslin cloth. The filtrate was collected and stored at 4˚C (Chanda et al., 2013; Kaneria et al., 2012).

Analyses of Mango Seed Kernel Extract

In vitro analyses of mango seed kernel extract included Total Phenolic Content (TPC), Total Flavonoid Content (TFC), HPLC analysis of phenolic compounds and antimicrobial activity. These procedures were carried out following the methodologies of Sultana et al. (2009), Hussain et al. (2012), Nouman et al. (2016) and Raju et al. (2011), respectively, with slight modifications. The results of these analyses are presented in Table 1:

Table 1
In vitro analysis of Mango Seed Kernel Extract.

Sr. No.	Traits
	Total Phenolic Content as GAE A = c × v/m		56.10 (mg/g)
	Total Flavonoid Content as CE A = c × v/m		7.44 (mg/g)
	Gallic Acid		3.14 (mg/g)
	Zone of Inhibition	Clostridium perfringens	12 (mm)
		Staphylococcus aureus	10 (mm)

Experimental Design

The approval from the Animal Care and Use Committee of the University of Veterinary and Animal Sciences, Lahore was received before the use of birds for experimental procedures (Letter no. DR/932). The total duration of the research study was 35 days. In total, 720 day-old male broiler chicks (Ross 308) were allocated to six treatment groups with 8 replicates each (15 birds/replicate), under a completely randomized design. The groups consisted of T1: positive control (basal diet with antibiotic, lincomycin at dose rate of 500 mg/kg of feed), T2: negative control (basal diet without antibiotic); and T3, T4, T5 and T6, respectively representing treatment groups supplemented with 10 mL/kg, 20 mL/kg, 30 mL/kg and 40 mL/kg of feed of mango seed kernel extract.

Parameters evaluated

Growth Performance

Upon the arrival of chicks, the body weight of birds was recorded on an individual basis. After the start of the experiment, feed intake, body weight gain, and FCR were recorded for each replicate by the end of each phase throughout the experimental trial (Yameen et al., 2020).

Carcass Characteristics

At the end of the experimental trial, three randomly selected birds per replicate were slaughtered. Carcass weights were measured after slaughtering, bleeding, de-feathering and eviscerating the birds, using a digital weighing balance. The carcass yield was calculated by dividing the carcass weight by the live weight at slaughter. Leg and breast quarter weight was weighed by using a digital weighing balance. Abdominal fat was measured by weighing fat around the cloaca and abdominal muscles, but not the fat surrounding the gizzard.

Gut Microbiota

For gut microbiota, total bacterial count and differential bacterial count was conducted. Caeca digesta samples were taken and transferred to sterile tubes. A 10-fold serial dilution was made, and 100 µl of each dilution was taken for the inoculation of agar containing plates. Nutrient agar for total bacterial count (Saleem et al., 2020), Salmonella Shigella (SS) agar for E. coli, Tryptose Sulfite Cycloserine (TSC) agar for Clostridium perfringens (Salem et al., 2021), and De Man, Rogosa and Sharpe (MRS) agar for Lactobacillus (Ravangard et al., 2017) were used. For 24 hours, incubation of the inoculated plates took place at 37˚C under aerobic conditions (anaerobic conditions for Clostridium perfringens). Microbial count was made by the colony counting method.

Statistical Analyses

Data were analyzed through the one-way ANOVA technique using PROC GLM in SPSS software (version 9.1). Moreover, the orthogonal polynomial contrast was also computed. For the comparison of significant treatment means, Duncan’s Multiple Range test was applied considering p≤0.05.

The following mathematical model was applied:

$Yij=m+\tau i+\epsilon ij$

Where,

Yij = observation of dependent variable recorded on the ith treatment group

μ = population mean

τi = effect of the ith treatment group (i = 1, 2, 3, 4, 5, 6)

εij = effect of the jth observation on the ith treatment group, NID ~ 0, σ².

RESULTS AND DISCUSSION

Supplementation of different levels of mango seed kernel extract in broilers diet was able to improve body weight gain and FCR at the end of the experimental trial. The results are summarized in Table 2. Feed intake showed a non-significant (p=0.473) difference among treatment groups at day 35. Body weight gain was recorded at the end of the trial, and significant (p≤0.05) findings were found. MSKE (30 mL/kg) group had the heaviest broilers, reaching 1915 g at day 35. The results showed that body weight gain was increased with increasing levels of mango seed kernel extract (linear, p≤0.05) till 30 mL/kg. Significantly (p≤0.05) better FCR was recorded in broiler birds given 30 mL/kg of MSKE in comparison to positive and negative control groups. FCR linearly (p=0.05) improved with increasing levels of mango seed kernel extract from 10 to 30 mL/kg, from 1-35 days of age. The increased body weight gain and better FCR with increasing levels of mango seed kernel extract was partly due to the improved extraction of bioactive compounds that have beneficial effects on the growth performance of birds, since for the extraction of heat stable compounds and hard plant materials decoction is considered one of the most effective methods (Azwanida, 2015). The nutritive effect of MSKE was expected to be the most important factor responsible for good broiler growth performance. The use of plant materials such as herbs and extracts as dietary supplements positively influences poultry productive performance (Lee et al., 2003). Digestibility in poultry may be stimulated by phytogenic additives, which in turn results in improved feed conversion ratios (Lee et al., 2003). Significant improvement in broilers’ growth performances has been reported by various authors with the supplementation of phytogenic feed additives (Al-Kassie & Witwit, 2010; Wati et al., 2015). However, contrary reports by Cross et al. (2007) and Sadeghi et al. (2012) suggested no positive influences of plant additives, whereas (Javed et al., 2009; Mohammed & Abbas, 2009) reported increased production performances in birds. According to a study on several pure extracts, the anthocyanin present in cherries markedly improved feed intake in broiler birds, but relatively lower body weight gains were recorded, which ultimately resulted in poor feed efficiency (Csernus et al., 2020). Contrarily, Azizi et al. (2018) observed a gradual decrease in body weight when more than 5 % of dried apple pomace was added to the diet of birds. Results were similar to Khushdil et al. (2012), who showed non-significant (p>0.05) differences with the supplementation of medicinal plant infusions on feed intake, body weight gain, and FCR among all treatment groups in broiler chickens. No significant (p>0.05) difference on the growth performance of broiler birds was observed with the supplementation of pomegranate extract (Saleh et al., 2018). Results from previous studies showed that the addition of the aqueous extract of Moringa oleifera leaves to the feed led to a lower final body weight gain in broiler birds, in comparison to the control group (John et al., 2002; Portugaliza & Fernandez Jr, 2012). Conversely, a higher final body weight gain was observed when this same extract was incorporated in water instead of bird feed (Alabi et al., 2017). By feeding 2 % Berberis lyceum and Withania somnifera extract at the dose rate of 20 g/L, broiler birds had improved feed efficiency and weight gain, and their mortality was reduced (Javed et al., 2009). Better FCR in the MSKE-supplemented groups as compared to the positive and negative control groups was due to the presence of numerous growth performance enhancing polyphenols present in mango, including rhamnetin, kaempferol, derivatives of quercetin (Masibo & He, 2008), anthocyanin (Abbasi et al., 2015), proanthocyanidin (Kim et al., 2021), gallotannins (Sayago-Ayerdi et al., 2013) and mangiferin (Stohs et al., 2018). Results suggested that the use of herbal plants extracted via decoction enhanced the growth performance of broiler chickens when used as a substitute to feed additives. Increased feed efficiency compared to the positive control was observed with the supplementation of mint and onion extracts in drinking water (Goodarzi et al., 2014). Beneficial effects of plant extracts have been reported in previous research studies, showing reduced feed intake and improved body weight gain, ultimately resulting in better FCR (Hernandez et al., 2004; Windisch et al., 2008). Oregano and rosemary extracts showed no significant difference in feed intake or feed conversion ratio, but a faster growth rate was seen in birds fed plant extracts in comparison to the control (Hernandez et al., 2004). In this study, the better FCR and weight gain in MSKE-supplemented groups suggested a better utilization of the nutrients supplied, and the positive effects of the treatments applied.

Table 2
Growth performance of broiler chickens fed with different levels of Mango Seed Kernel Extract.

Treatments		Feed Intake (g)	Weight Gain (g)	FCR
Positive Control		2909.1	1789.8c	1.63a
Negative Control		2975.0	1750.9c	1.70a
MSK (10 mL/kg)		2978.5	1774.7c	1.68a
MSK (20 mL/kg)		3005.8	1877.3ab	1.61ab
MSK (30 mL/kg)		2933.3	1915.1a	1.54b
MSK (40 mL/kg)		2962.1	1811.7bc	1.64a
Pooled SEM		14.6	12.8	0.01
p-value	Combined	0.473	0.001	0.008
	Linear	0.580	0.002	0.050
	Quadratic	0.144	0.252	0.863

• ^a-c
  Superscripts on different means within a column differ significantly at p≤ 0.05.

Carcass characteristics parameters were recorded at the end of the research trial at day 35 by randomly selecting 3 birds from each replicate, including carcass weight, carcass yield, leg quarter weight, breast quarter weight, and abdominal fat (Table 3). A significant (p≤0.05) difference was recorded in live weight at slaughter, with highest being recorded in the group supplemented with 30 mL/kg of feed of mango seed kernel extract, in comparison to the control positive and negative groups. However, no significant difference was recorded for carcass weight (p=0.233) and carcass yield (p=0.692) among the different treatment groups. Leg quarter weight showed significant (p≤0.05) difference in mango seed kernel extract supplemented groups as compared to the positive and negative control groups. Results showed that leg quarter weight increased with increasing levels of mango seed kernel extract till the 30 mL/kg supplemented group (linear, quadratic, p≤0.05). Breast quarter weight was significantly (p≤0.05) increased in groups supplemented with mango seed kernel extract in comparison to the control negative group. Breast quarter weight caused linear (p≤0.05) improvements in groups supplemented with mango seed kernel. No significant (p=0.184) difference was recorded in abdominal fat with increasing levels of MSKE. Conversely, by adding plant feed additives to the diet, no significant (p>0.05) difference was observed in carcass characteristics including breast meat, relative liver weight, and overall meat yield of broiler birds (Rao et al., 2018). Another study showed no significant (p>0.05) difference in the carcass characteristics of broiler birds supplemented with different dose levels of aqueous extract of tamarind in drinking water (Banjo et al., 2018). Intrinsic and extrinsic elements were responsible for varying effects on broiler performance, especially the environmental factors used to test the aptness of plant extracts as a replacement to antibiotic growth promoters (Windisch et al., 2008).

Table 3
Carcass Characteristics of broiler birds given different levels of Mango Seed Kernel Extract.

Treatments		WAS	CW	CY	LQW	BW	AF
Positive Control		1779.8b	1313.8	74.0	664.3b	505.3ab	28.1
Negative Control		1754.5b	1299.3	74.2	654.8b	467.3b	32.1
MSK (10 mL/kg)		1848.4ab	1350.1	73.2	736.5a	532.8a	32.8
MSK (20 mL/kg)		1831.1ab	1313.3	71.8	751.8a	530.8a	26.5
MSK (30 mL/kg)		1903.8a	1363.8	71.7	754.8a	543.3a	27.7
MSK (40 mL/kg)		1795.6b	1326.5	74.0	738.3a	533.3a	30.8
Pooled SEM		14.4	8.6	0.57	9.2	7.0	0.8
p-value	Combined	0.030	0.233	0.692	0.001	0.012	0.184
	Linear	0.066	0.206	0.479	0.001	0.007	0.718
	Quadratic	0.099	0.543	0.290	0.040	0.612	0.886

• ^a-c
  Superscripts on different means within a column differ significantly at p≤0.05. WAS = weight at slaughter (g); CW = carcass weight (g); CY = carcass yield %; LQW = leg quarter weight (g); BW = breast weight (g); AF = abdominal fat (g)

Total bacterial count and differential bacterial count were determined at the end of the trial, day 5, and the results are presented in Table 4. Significantly (p<0.05) decreased total bacterial count was recorded in the groups supplemented with mango seed kernel extract (30 and 40 mL/kg) in comparison to positive and negative control groups. Decreased total bacterial count was seen with increasing levels of mango seed kernel extract (linear, quadratic; p≤0.05). Differential bacterial count included colony count of Clostridium perfringens, E. coli, and Lactobacillus. Decreased (p≤0.05) Clostridium perfringens colony count was observed for treatment groups supplemented with different levels of mango seed kernel extract in comparison to the positive and negative control groups. Increasing mango seed kernel extract levels linearly decreased Clostridium perfringens colony count (linear, quadratic, p≤0.05). E. coli colony count was decreased (p≤0.05) in groups supplemented with mango seed kernel extract in comparison to control positive and negative groups. A linear decrease was observed with increasing levels of MSKE (linear, quadratic, p≤0.05). A significantly (p≤0.05) better Lactobacillus colony count was determined in groups supplemented with mango seed kernel extract in comparison to the positive and negative control groups. Increasing levels of mango seed kernel extract improved Lactobacillus colony count linearly (linear, quadratic, p≤0.05). The large intestine bacterial population mainly consists of anaerobes, specifically Clostridium perfringens, and an increase in its colony count is directly linked with necrotic enteritis in birds, both clinical and subclinical (Williams et al., 2003). The supplementation of extract of pomegranate led to a significant (p<0.05) drop in bacterial colony count (Hamady et al., 2015). The intestinal secretion of mucus was reported to be stimulated by the supplementation of phytogenic feed additives, which caused impairment of pathogen adherence and contributed in microbial flora stabilization in broiler guts, consequently improving the digestive processes (Jamroz et al., 2003). Modification in the gut environment might be the mode of action by which plants and their extracts exert certain effects: gut environment might be modified by the bioactive compounds present in the plant extracts, resulting in sparing nutrients and increasing their availability, decreasing microbial count, and ultimately increasing efficiency (Windisch et al., 2008).

Table 4
Total and Differential Bacterial Count of birds given different levels of Mango Seed Kernel Extract. Values are expressed in log colony forming units (CFU)/g.

Treatments		Total Bacterial Count	Differential Bacterial Count
			Clostridium perfringens	E. coli	Lactobacillus
Positive Control		7.26b	5.11b	5.14a	5.34d
Negative Control		7.38a	5.17a	5.24a	5.31e
MSK (10 mL/kg)		7.02c	4.99c	4.68b	5.41c
MSK (20 mL/kg)		6.95d	4.87d	4.57b	5.44b
MSK (30 mL/kg)		6.88e	4.60e	3.96c	5.46a
MSK (40 mL/kg)		6.87e	4.51f	3.81c	5.46a
Pooled SEM		0.03	0.05	0.11	0.01
p-value	Combined	0.001	0.001	0.001	0.001
	Linear	0.001	0.001	0.001	0.001
	Quadratic	0.001	0.001	0.025	0.002

• ^a-c
  Superscripts on different means within a column differ significantly at p≤0.05.

CONCLUSIONS

Different levels of mango seed kernel extract resulted in increased body weight gain, better FCR, decreased total bacterial, Clostridium perfringens, and E. coli colony count, increased Lactobacillus colony count, and better leg and breast quarter weight in comparison to the negative control group. Among different levels of mango seed kernel extract, birds supplemented with 30 mL/kg and 40 mL/kg of feed showed decreased total bacterial and differential bacterial count, better Lactobacillus count, increased leg quarter and breast quarter weight. However, among 30 and 40 mL/kg supplemented groups, increased body weight gain and better FCR was observed among birds receiving 30 mL/kg of feed of mango seed kernel extract. Hence, it can be concluded that mango seed kernel extract given in broilers’ diets at the dose level of 30 mL/kg of feed can improve birds’ growth performance, be a good AGP replacement, and serve as a good option for sustainable poultry production.

ACKNOWLEDGMENTS

The authors gratefully acknowledge the administration at IDRC lab for their support.

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• Funding
  This research was funded by the UK Government Department of Health and Social Care (DHSC), Global AMR Innovation Fund (GAMRIF), and the International Development Research Centre, Ottawa, Canada, (Grant No. 109051-003). The views expressed herein do not necessarily represent those of IDRC or its Board of Governors.
• Data availability statement
  Data will be available upon request.
• Disclaimer/Publisher’s Note
  The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.

Data availability

Data will be available upon request.

Publication Dates

• Publication in this collection
  27 Sept 2024
• Date of issue
  2024

History

• Received
  02 Sept 2023
• Accepted
  10 Mar 2024