Efficacy of Moringa oleifera Lam. extracts &nbsp;and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken

Novita Wanda Karwanti; Dynda Febriana Arumdani; Andreas Berny Yulianto; Tabita Dameria Marbun; Anjum Sherasiya; Mohammad Anam Al Arif; Mirni Lamid; Widya Paramita Lokapirnasari

doi:10.12688/f1000research.130072.3

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Research Article

Revised

Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken

[version 3; peer review: 1 approved, 1 approved with reservations]

Novita Wanda Karwanti¹, Dynda Febriana Arumdani¹, Andreas Berny Yulianto², [...] Tabita Dameria Marbun³, Anjum Sherasiya⁴, Mohammad Anam Al Arif⁵, Mirni Lamid⁵, Widya Paramita Lokapirnasari ⁵

Novita Wanda Karwanti¹, Dynda Febriana Arumdani¹, [...] Andreas Berny Yulianto², Tabita Dameria Marbun³, Anjum Sherasiya⁴, Mohammad Anam Al Arif⁵, Mirni Lamid⁵, Widya Paramita Lokapirnasari ⁵

PUBLISHED 15 May 2023

Author details Author details

¹ Magister of Veterinary Agribusiness, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia., Universitas Airlangga, Indonesia., Surabaya, East Java, 60115, Indonesia
² Faculty of Veterinary Medicine, Universitas Wijaya Kusuma, Surabaya, East Java, 60115, Indonesia
³ Animal Nutrition Laboratory, Kyungpook National University, Kyungpook, South Korea
⁴ Veterinary World, Gujarat, 363621, India
⁵ Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, East Java, 60115, Indonesia

Novita Wanda Karwanti
Roles: Conceptualization, Data Curation, Formal Analysis, Writing – Original Draft Preparation, Writing – Review & Editing

Dynda Febriana Arumdani
Roles: Conceptualization, Data Curation, Investigation, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing

Andreas Berny Yulianto
Roles: Conceptualization, Methodology, Software, Writing – Review & Editing

Tabita Dameria Marbun
Roles: Conceptualization, Investigation, Methodology, Writing – Review & Editing

Anjum Sherasiya
Roles: Conceptualization, Methodology, Software, Writing – Original Draft Preparation, Writing – Review & Editing

Mohammad Anam Al Arif
Roles: Conceptualization, Investigation, Writing – Original Draft Preparation, Writing – Review & Editing

Mirni Lamid
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Widya Paramita Lokapirnasari
Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Methodology, Software, Supervision, Validation, Writing – Original Draft Preparation, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

This article is included in the Agriculture, Food and Nutrition gateway.

Abstract

Background: Probiotics and medicinal plants have been used to support human and livestock health. This research aimed to evaluate the efficacy of Moringa oleifera Lam. leaf extract on the growth of P. pentosaceus, L.acidophilus and L. plantarum during starter period on nutrient intake, body weight gain, FCR and feed efficiency in broiler chicken.
Methods: This study consisted of three sub studies:(1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by the Forth method. Triterpenoid tests were performed by the Liebermann-Bouchard method and the alkaloids test was conducted by the method of Mayer, Bouchardat and Wagner. (2) evaluation of level M.oleifera extract, where each test tube was added with 1 mL of each isolate and incubated at 37°C. The growth of probiotic bacteria was calculated by using the TPC. (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.
Results: (1)The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract could increased the growth of bacteria probiotic (p <0.05); (3) The use of probiotics and M. oleifera extract could improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p<0.05), but there was no significant difference (p >0.05) on nutrient intake.
Conclusions: The use of M.oleifera extract at doses of 0.1%, 0.2% and 0.3% increased the growth of P. pentosaceus, L. acidophilus and L. plantarum bacteria in vitro and the use of probiotics, M.oleifera extract and their combination by in vivo improved the growth performance on starter phase of broilers chicken.

Keywords

Moringa oleifera extract, public health, probiotic, growth performance

Corresponding author: Widya Paramita Lokapirnasari

Competing interests: Anjum Sherasiya is employed at the Veterinary World journal; other authors declare that they have no conflicts of interest.

Grant information: This research was supported by the Faculty of Veterinary Medicine (Fakultas Kedokteran Hewan), Universitas Airlangga (769/UN3.14/PT/2020)
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2023 Karwanti NW et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Karwanti NW, Arumdani DF, Yulianto AB et al. Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken [version 3; peer review: 1 approved, 1 approved with reservations]. F1000Research 2023, 12:215 (https://doi.org/10.12688/f1000research.130072.3) First published: 27 Feb 2023, 12:215 (https://doi.org/10.12688/f1000research.130072.1) Latest published: 15 May 2023, 12:215 (https://doi.org/10.12688/f1000research.130072.3)

Revised Amendments from Version 2

We have revised the abstract as suggested by the reviewers

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

See the authors' detailed response to the review by Ugbo Emmanuel Nnabuike

Introduction

Feed comprises ingredients provided to poultries to meet necessary dietary requirements for livestock growth, development, and reproduction. Breeders administer antibiotic growth promoters (AGP) to improve production, trigger growth, and act as an antibacterial.¹ However, the use of these growth promoters in animal production is gradually being restricted and banned in some countries. One antibiotic substitution which can be used in feed is probiotics.

Phytobiotics are feed additives derived from pure plant materials. Phytobiotics are able to control micro-organisms in the digestive tract of poultry. Phytobiotics are able to increase metabolic activities in the body, so these phytobiotics can be used as feed additives in poultry. Phytobiotics have proven to have several functions, such as a growth-promoting effect, antimicrobial activity, anti-inflammation activity and improving performance.²^–⁵ They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry.⁶^,⁷

Pediococcus pentosaceus is a lactic acid bacteria (LAB). LABs are the bacterial group that ferments carbohydrates into lactic acid.⁸ Probiotics are microorganisms capable of improving growth and feed efficiency. Several probiotics improving production performance in broilers are P. pentosaceus, Bifidobacterium sp, Lactobacillus casei, and Lactobacillus acidophilus.⁹^–¹⁴ P. pentosaceus is a Gram-positive bacteria, round-shaped, non-motile, not generating spores, and has negative catalase. As it grows, P. pentosaceus generates lactic acid and pediocin.¹⁵ Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources.¹⁶^–¹⁸

Moringa oleifera belongs to the family Moringaecea. M. oleifera is very useful as a feed supplement for animals, as its leaves are highly nutritious. Moringa leaf carbohydrates reach 38.2 g for 100 g of Moringa leaf powder.¹⁹ Moringa also contains proteins, fats, fibers, calcium, magnesium, phosphorus, potassium, copper, iron, vitamin B1, vitamin B2, vitamin B3, vitamin C, vitamin E, and essential amino acids, e.g., arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, and cysteine.²⁰ Probiotics containing L. acidophilus, L. casei, L. lactis, and Bifidobacterium spp. and M. oleifera extract can increase the production performance of Peking ducks.²¹

Moringa leaves are antioxidant, antibacterial, anti-inflamatory,²² and are rich in fats, proteins, vitamins, and minerals. Moringa leaves contain diversified phytochemicals such as flavonoids, saponins, tannins, phenols and alkaloids.²²^,²³ The high-nutrient profile of Moringa suggests potential growth promoter and immunomodulatory effects.²⁴ Moringa can be used as a source of micronutrients and as a dietary supplement in poultry.²⁵

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs.⁶^,⁷^,²⁶^,²⁷

The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Methods

This study was conducted in the Faculty of Veterinary Medicine, Universitas Airlangga, Surabaya. The trial design was a complete randomized design consisting of four treatments: P0, P1, P2, and P3, with five replications.

Moringa was extracted by mixing macerated moringa leaf with ethanol 70% and 96% as the solvent. Extraction with ethanol 70% can extract oligosaccharides.²⁸ The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Bacterial cell count measurement was conducted to measure the bacterial cell count of P. pentosaceus, L. acidophilus and L. plantarum before adding Moringa leaf extracts. A bacterial suspension comparison was performed using the McFarland 0.5 scale standard. After obtaining the same turbidity, a gradual dilution was conducted up to seven times to obtain a 10¹ bacterial concentration.

A sterile test tube was filled with Aquadest 9 mL mixed with Moringa leaf extracts with the following treatments: P0: Without M.oleifera extracts; P1: 0.1% M.oleifera extracts; P2: 0.2% M. oleifera extracts; P3: 0.3% M. oleifera extracts. Furthermore, each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 and 17 h. The growth of probiotic bacteria was calculated for the colonies.

Experimental design

The study material consisted of probiotics from W.P. Lokapirnasari’s and A.B.Yulianto’s collections and M. oleifera extract in drinking water. The commercial feed contained dry matter (86.00%), crude lipid (8.00%), ash (7.00%), crude protein (20.00 %), crude fiber (5.00%) and organic matter (93.00%). This study used a completely randomized design, using 100 day-old chicks divided into five treatments and ten replications; each replication contained two chicken. The treatments in this study were as follows: T0 = control, without feed additive; T1 = 1% P. pentosaceus; T2 = 1% L. acidophilus and L. plantarum; T3 = 0.5% P. pentosaceus + 0.5% L. acidophilus and L. plantarum; T4 = 0.5% P.pentosaceus + 0.5% L. acidophilus and L. plantarum + 1% M. oleifera extracts. The observed variables included dry matter intake, organic matter intake, ash intake, crude protein intake, ether extract intake, crude fiber intake, organic matter intake, feed conversion ratio and feed efficiency. All variables were calculated with the following⁹^,²⁹^–³¹:

Dry matter intake (g) = feed intake (g) \times feed dry matter (%)

Organic matter intake (g) = feed intake (g) \times feed organic matter (%) \times feed dry matter (%)

Ash intake (g) = feed intake (g) \times feed ash (%) \times feed dry matter (%)

Crude protein intake (g) = feed intake (g) \times feed crude protein (%) \times feed dry matter (%)

Crude fat intake (g) = feed intake (g) \times feed crude fat (%) \times feed dry matter (%)

Crude fibre intake (g) = feed intake (g) \times feed crude fibre (%) \times feed dry matter (%)

Feed efficiency (%) = (body weight gain (kg) / feed intake (kg)) \times 100 .

Feed conversion ratio = feed intake (kg) / body weight gain (kg)

Ethical considerations

This research has obtained approval from the Ethics Review Team Brawijaya University through a letter from the Head of the Ethics Review Team number 057-KEP-UB-2020. The treatment in this study used probiotics and herbal extracts as feed additives which are safe to use and are thought to have positive and beneficial properties and to not cause pain in experimental animals. Variable taking does not slaughter experimental animals.

Statistical analysis

All data collected during this study were statistically analyzed under a completely randomized design. All data were tested for distribution normality and homogeneity statistics (analysis of variance). The data were analyzed using Statistical Design for Social Sciences (SPSS) v.22 (IBM Corp., NY, USA). Differences among means were detected using a one-way analysis of variance. The differences among means were determined using Duncan's test (p < 0.05).

Results

Phytochemical screening of M. oleifera extract

Moringa leaf extract was tested for its chemical composition using a phytochemical screening test. At this stage, five kinds of tests were carried out: flavonoid test, tannin test, saponin test, triterpenoids test, and alkaloid test. The results of the phytochemical screening tests are presented in Table 1. The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the Figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Table 1. Phytochemical screening of M. oleifera extract.

No	Compound	Result (ethanol 70%)	Result (ethanol 96%)
1	Flavonoid	+	+
2	Tannin	+	+
3	Saponin	+	+
4	Triterpenoid	+	+
5	Alkaloid	+	+

Figure 1. A: Flavonoid test, B: Tannin test, C: Saponin.

Figure 2. Triterpenoid test.

Figure 3. Alkaloid test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+)].

Evaluation of several doses of M. oleifera extract

The growth results of the probiotics P. pentosaceus, L. acidophilus and L. plantarum with several levels of M. oleifera extract showed significant differences between the treatments (p < 0.05) (Table 2, Figure 4).

Table 2. The growth of P. pentosaceus, L. acidophilus and L. plantarum on MRS Agar at medium temperature 37°C.

Treatment	P. pentosaceus (Log CFU/mL)	L. acidophilus (Log CFU/mL)	L. plantarum (Log CFU/mL)
P0	0.44^a ± 0.550	1.20^a ± 7.07	0.86^a ± 26.08
P1	1.34^b ± 0.010	1.70^b ± 18.71	1.56^b ± 27.93
P2	2.93^d ± 0.074	2.40^c ± 39.37	1.98^bc ± 50.70
P3	2.52^c ± 0.017	2.74^d ± 23.02	2.104^c ± 31.62

Figure 4. The growth of P. pentosaceus, L. acidophilus and L. plantarum on MRS Agar medium temperature 37°C.

Evaluation of probiotics, M. oleifera and combination of probiotics + M. oleifera in vivo

The result of feed intake and nutrient intake of dry matter, ash, crude protein, crude fat, crude fiber and organic matter listed in Table 3. There was no significant difference (p > 0.05) between the treatments of feed intake, dry matter intake, ash intake, crude protein intake, crude fat intake, crude fiber intake, and organic matter intake in this study.

Table 3. Feed intake and nutrient intake after giving probiotic, M. oleifera extract and a combination of probiotic and extract during the starter phase of broiler chicken.

Treatment	T0	T1	T2	T3	T4
Feed intake (g/chicken/day)	97.12^a ± 11.60	104.63^a ± 10.88	99.10^a ± 12.73	103.59^a ± 13.16	97.99^a ± 8.32
Dry matter intake (g/chicken/day)	83.52^a ± 9.97	89.98^a ± 9.36	85.22^a ± 10.94	89.08^a ± 11.32	84.27^a ± 7.15
Ash intake (g/chicken/day)	6.79^a ± 0.81	7.32^a ± 0.76	6.93^a ± 0.89	7.25^a ± 0.92	6.85^a ± 0.58
Crude protein intake (g/chicken/day)	19.42^a ± 2.31	20.92^a ± 2.17	19.82^a ± 2.54	20.72^a ± 2.63	19.59^a ± 1.662
Crude fat intake (g/chicken/day)	7.76^a ± 0.92	8.37^a ± 0.87	7.92^a ± 1.01	8.28^a ± 1.05	7.83^a ± 0.66
Crude fiber intake (g/chicken/day)	4.85^a ± 0.58	5.23^a ± 0.54	4.95^a ± 0.63	5.17^a ± 0.66	4.89^a ± 0.41
Organic matter intake (g/chicken/day)	90.31^a ± 10.78	97.30^a ± 10.12	92.16^a ± 11.83	96.33^a ± 12.24	91.12^a ± 7.73

The result of body weight, daily body weight gain, feed conversion ratio, and feed efficiency are listed in Table 4. Body weight differed significantly (p < 0.05) between treatments. The control (T0) had the lowest body weight, which was different from all treatments. The average daily weight gain differed significantly (p < 0.05) between treatments. The control (T0), which differed from all treatments, had the lowest body weight gain. The FCR results revealed a significant difference (p < 0.05) between treatments. The feed efficiency results revealed a significant difference (p < 0.05) between treatments. T0 had the lowest feed efficiency value found.

Table 4. Production performance after giving probiotic, extract M. oleifera and a combination of probiotic and extract during the starter phase of broiler chicken.

Treatment	T0	T1	T2	T3	T4
Body weight (g/chicken)	801.20^a ± 82.91	935.40^b ± 96.37	949.10^b ± 45.16	926.70^b ± 76.96	899.60^b ± 90.06
Average daily weight gain (g/chicken/day)	45.32^a ± 7.62	65.72^b ± 8.11	70.60^b ± 9.35	62.52^b ± 7.12	68.50^b ± 13.33
Feed conversion ratio	2.16^c ± 0.20	1.60^b ± 0.15	1.41^a ± 0.09	1.65^b ± 0.04	1.48a^a ± 0.31
Feed efficiency (%)	46.57^a ± 4.52	62.92^b ± 5.60	71.30^c ± 4.86	60.45^b ± 1.40	70.26^c ± 14.43

Discussion

Phytochemical screening of M. oleifera extract

The phytochemical screening revealed flavonoids, tannins, saponins, terpenoids, and alkaloids which could serve as a natural source of antimicrobials. The results obtained from the flavonoid test were a change in color. There was a change in color to orange (Figure 1A). The orange to red color change is caused by the formation of flavilium salts. This indicates that the sample contained flavonoids.

In the tannin test, a positive result is indicated by a change in the color of the filtrate to green or blackish blue. In this test, the color of the filtrate changed to a dark green-black color (Figure 1B), so the sample was considered test-positive for tannin. The test for the presence of saponin was indicated by the appearance of foam. The foam indicated the presence of glycosides which have the ability to form froth in water as they hydrolyze into glucose and other compounds. In the saponin test carried out, foam formed for approximately 10 minutes; with the addition of one drop of hydrochloric acid, the foam did not disappear and the sample tested positive for saponin (Figure 1C).

The addition of concentrated sulfuric acid causes water to hydrolyze, which reacts with acetyl derivatives to form a red ring. A positive test for the presence of triterpenoids is indicated by a color change to red or purplish red. In the test conducted, the color changed to red (Figure 2), therefore the sample tested positive for triterpenoid.

The alkaloid test in this study used three reagents: Mayer’s reagent, Bouchardat’s reagent and Wagner’s reagent. The test with Mayer's reagent showed no white precipitate (Figure 3A), so the result is negative. With the Bouchardat reagent, a precipitate appeared and the color changed to orange (Figure 3B), therefore the result is positive. With Wagner's reagent, a brown precipitate appeared (Figure 3C). The precipitate was indicated as a potassium-alkaloid. Of the three reagents used, two of them were positive, so it can be concluded that Moringa leaves contains alkaloids.

These results are in accordance with the research of Kandeepan et al. which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods.³² Secondary metabolites extracted from M.oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins.³³

Evaluation of several doses of M. oleifera extract

The lowest growth of P. pentosaceus, L. acidophilus and L. plantarum was found for the treatment without M. oleifera extract (P0), which was different from all treatments. The fastest growth of P. pentosaceus was found with the addition of 0.2% M. oleifera extract (P2), followed by 0.3% M. oleifera extract (P3) and 0.1% M.oleifera extract (P1). The highest growth of L. acidophilus was shown with the addition of 0.3% M. oleifera extract (P3), followed by the addition of 0.2% M. oleifera extract (P2) and 0.1% M. oleifera extract (P1). The highest growth of L. plantarum was shown in the 0.3% M. oleifera extract (P3) treatment, which was not different from 0.2% M.oleifera extract (P2), while P2 was not different from 0.1% M. oleifera extract (P1) (Table 2).

Bacterial growth of P. pentosaceus L. acidophilus and L. plantarum was significantly improved after the addition of 0.1%, 0.2%, and 0.3% M. oleifera extract. This shows that the higher the M. oleifera extract concentration, the faster the bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum. Microbial count difference was determined by the fermentation duration and nutrition availability. Primary nutrition required by P. pentosaceus, L. acidophilus and L. plantarum bacteria were carbon and nitrogen sources. Bacteria use carbon sources as the energy source and produced lactic acid while nitrogen is used to generate bacterial cell biomass.³⁴

M. oleifera extract contains the monosaccharides mannose, arabinose, xylose, and the oligosaccharides raffinose and stachyose.³⁵ These oligosaccharides can be used as nutrition for bacterial growth.³⁶ P. pentosaceus bacteria is an amylolytic bacterium that generates amylase and can hydrolyze carbohydrates into glucose. Glucose is a carbon source for bacteria as the energy fueling their growth and lactic acid formation. P. pentosaceus bacteria use oligosaccharides and monosaccharides in Moringa leaf as the energy source for fermentation.³⁷

P. pentosaceus is also classified into the proteolytic lactic acid bacterial group. Proteolytic bacteria are those capable of generating the protease enzyme to hydrolyze polypeptides in media into amino acids. Nitrogen is a constituting component of amino acids. Thus, bacteria can use amino acids as a nitrogen source for bacterial growth and DNA/RNA synthesis. Bacterial growth of P. pentosaceus on Agar MRS media ferments carbohydrates from Moringa leaf extracts into glucose and generate lactic acid. Metabolites of lactic acid are generated from glucose fermentation through glycolysis. P. pentosaceus metabolizes glucose into produce pyruvic acid through the Embden-Meyerhof pathway, which is then reduced into lactic acid by the lactase dehydrogenase enzyme and nicotinamide adenine dinucleotide phosphate (NADP).

High bacterial growth followed the high lactic acid concentration on the fermentation media. The pH reduction and total acid level increase on the fermentation media is beneficial since it hinders pathogenic microbes. The growth of P. pentosaceus bacteria produces pediocin, a bacteriocin that inhibits the growth of pathogenic bacteria.¹⁰ P. pentosaceus incubated with M. oleifera extract could be used to improve the nutritional quality of rice bran.³⁸

M. oleifera extract’s beneficial effects as phytobiotics are considered to be due to their antioxidant properties. Phytochemical compounds such as flavonoids, saponins and tannins, exhibit antimicrobial activity.³⁹ The phytochemical screening results in this study revealed flavonoids, tannins, saponins, triterpenoids, and alkaloids.

Evaluation of probiotics, M. oleifera and combination of probiotics + M. oleifera in vivo

The feed intake in this study showed that there was no significant difference (p > 0.05) between the treatments with values 97.12-104.63 (g/chicken/day). The dry matter intake showed that there was no significant difference (p > 0.05) between the treatments with values 83.52-89.98 (g/chicken/day). The results of ash intake in this study showed that there was no significant difference (p > 0.05) between treatments with values 6.79-7.32 (g/chicken/day). The results of crude protein intake showed no significant difference (p > 0.05) between treatments with values 19.42-20.92 (g/chicken/day). The results of crude fat intake showed no significant difference (p > 0.05) between treatments with values 7.76-8.37 (g/chicken/day). The results of crude fiber intake showed no significant difference (p > 0.05) between treatments with values 4.85-5.23 (g/chicken/day). The organic matter intake results in this study showed no significant difference (p > 0.05) between the T0, T1, T2, T3 and T4 treatments with values 90.31 – 97.30 (g/chicken/day) (Table 3).

Body weight was significantly different (p < 0.05) between the treatments. The lowest body weight was found in the control (T0), which was different from all treatments. For T1, T2, T3 and T4, there was no significant difference (p > 0.05), with values between 899.60-949.10 (g/chicken) in starter-phase broiler chickens.

Average daily weight gain was significantly different (p <0.05) between the treatments. The lowest body weight gain was found in the control (T0), which was different from all treatments. At T1, T2, T3 and T4, there was no significant difference (p > 0.05), with values between 62.52-70.60 (g/chicken/day).

The feed conversion ratio (FCR) results showed that there was a significant difference (p < 0.05) between the treatments. FCR values for T1, T2, T3 and T4 showed an improvement compared to the control (T0). The best FCR values were found for T2 (1.41) and T4 (1.48), which differed from all treatments. The FCR values at T1 and T3 showed no significant difference (p > 0.05), namely 1.60 and 1.65.

The feed efficiency results showed that there was a significant difference (p < 0.05) between the treatments. The lowest feed efficiency value was found for T0 (46.57%). The feed efficiency values for T1, T2, T3 and T4 showed an improvement compared with the control (T0). The best feed efficiency values were shown for T2 (71.30%) and T4 (70.26%), which were different from all treatments. The value of feed efficiency at T1 (62.92%) and T3 (60.45%) showed no significant difference (p > 0.05) (Table 4).

The results of this study are in accordance with other studies that showed the administration of Lactobacillus probiotic can improve gut health and contributes to increased growth performance.⁴⁰ Probiotics play a role in modulating the balance of microbiota in the digestive tract and in developing intestinal health so that they affect feed consumption, digestibility, absorption of nutrients and improve feed conversion ratio and feed efficiency. The use of probiotics in poultry also plays a role in modulating the immune response, maintaining the health of the intestinal tract and influencing stress reduction.⁴¹^–⁴³

Other studies have shown that the use of L. acidophilus poses an obstacle to the invasion of pathogenic bacteria and modulates the immune response in vitro and in vivo. This is because L. acidophilus produces bacteriocin. Additionally, probiotics that are classified as lactic acid will produce acid thereby lowering the pH in the intestine. In poultry, the use of L. acidophilus can balance the intestinal microflora and reduce the proliferation of pathogenic bacteria through antagonism and competitive exclusion.⁴⁰^,⁴⁴ Protein availability can be increased by taking probiotics. Probiotics can improve the host’s health by increasing intestinal villi size and nutrient uptake.⁴⁵

The use of probiotics can modify the intestinal ecosystem by decreasing pH through acid production by lactic acid probiotic bacteria and modulating enzyme activation in the digestive tract.⁴⁶^,⁴⁷ Several factors can affect the colonization of probiotic microbes in the intestine depending on the availability of fermented substrates (prebiotics), pH in the intestine, frequency and dosage of probiotics, genetics, age, health, stress factors and the nutritional status of the host.⁴⁸^,⁴⁹ This relates to the ability of probiotic micro-organisms to secrete enzymes such as protease, lipase, and amylase to help digest proteins, fats, and starch so that they can increase the availability of nutrients and help increase the digestion of feed nutrients.⁵⁰

M. oleifera extract contains phenolic compounds in insoluble and soluble bound forms. The bound phenolic compounds cannot be absorbed by the small intestine because they are bound by insoluble macromolecules such as cellulose, hemicellulose, structural proteins and pectin; these compounds enter the large intestine (colon), a fermentation by the intestinal microbiota occurs, which releases bound phenolic compounds. The released phenolic compounds can decrease pH, inhibit the growth of pathogenic bacteria and modulate the development of fermentative microflora so that it can improve host health.⁵¹^,⁵² Moringa has no toxic effects and does not interfere with nutrient absorption.⁵³

In this study, giving probiotics, M. oleifera extract and a combination of probiotics and M. oleifera extract during the starter phase of broiler chicken increased body weight and average daily weight gain, increased feed efficiency and improved feed conversion compared with control. This is because the addition of probiotics to poultry can modulate the balance of microbiota in the intestine, increasing feed digestibility and nutrient absorption. This is also influenced by the viability requirements of probiotics, where probiotics must be able to survive and not be damaged during processing to storage. The addition of probiotics increases nutrient bioavailability and improves poultry feed conversion. Probiotics must be able to survive various stress factors during processing, storage and digestion. Several different probiotic strains can exhibit wide variations in their abilities, such as efficacy as probiotics, stability of process and functional properties at the targeted site.⁵⁴

The phytoconstituents present in M. oleifera are flavonoids, niazirinin, niazirin, proanthocyanidin, anthocyanins, kaempferol-3-O-(6”-malonyl-glucoside), β-sitosterol, β-sitosterone, 4-hydroxymellein, octacosanic acid.⁵⁵ M. oleifera with ethanol extraction has a strong antioxidant activity.⁵⁶ Hydro-alcoholic extract of Moringa leaves contain 21.1% polysaccharides (% of dry matter).⁵³

The addition of a combination of probiotics and M. oleifera extract also resulted in better body weight gain, FCR and feed efficiency than the control. This is due to their proanthocyanidins content, which are condensed tannins (epicatechins and catechins) found in plants that provide protection against biotic and abiotic stresses, and act as antimicrobial, antioxidant, anti-inflammatory, vascular and cardiac activity.⁵⁷^–⁵⁹

The use of M. oleifera extract improved FCR and increase feed efficiency due to the presence of secondary metabolites produced by the plant, which also play a role in giving flavor to feed, and are influenced by their ability to form complexes with macromolecules (polysaccharides and proteins) and metal ions.⁵⁹^,⁶⁰ The use of probiotics and M. oleifera extract for feed efficiency agrees with Nikpiran et al. (2013)⁶¹ who found a better FCR with the addition of prebiotics to broiler rations compared to controls. This is thought to be related to the availability of substrates and the presence of a better balance of microbiota in the gut, resulting in better feed efficiency.⁶²^,⁶³ The finding of increased average daily gain and improvement of FCR in this study by administering M. oleifera leaf extract to broiler chickens agrees with a previous study where the FCR value obtained was 1.41–1.65 and the average daily gain 62.52–70.60 g, while research by Akhouri (2013) using M. oleifera extract in starter phase broilers produced an FCR of 1.77 and average daily gain of 52.57 g.⁶⁴ The results of our study are also in line with Sjofjan's (2021) that the level of probiotics increased body weight gain, body weight, feed intake of broilers and improved FCR.⁶⁵

Conclusions

The phytochemical tests showed flavonoids, tannins, saponins, tripenoids, alkaloids. The use of M. oleifera extract at doses of 0.1%, 0.2%, and 0.3% increased the growth of P. pentosaceus, L. acidophilus and L. plantarum bacteria in vitro. The use of probiotics, M. oleifera extract and a combination of probiotics + M. oleifera extract used in vivo can improve the growth performance of starter-phase broilers chicken. Based on these results, the use of probiotics, M. oleifera extract or combination of both could be used as alternative antibiotic growth promoters in the poultry industry.

Data availability

Underlying data

Figshare: Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances of male broiler chicken, https://doi.org/10.6084/m9.figshare.21802944.v3.⁶⁶

This project contains the following underlying data:

- Widya PL excell.xlsx
- Untitled2 revised in english.savRaw CFU.xlsx
- Raw growth isolate-revised in english.sav

Reporting guidelines

Figshare: ARRIVE Essential 10 checklist for “Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken”, https://doi.org/10.6084/m9.figshare.21802944.v3.⁶⁶

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgements

This work was supported and funded by Ministry of Research and Technology of Higher Education (Kemenristekdikti), Chair of the Research and Innovation Institute, Rector Universitas Airlangga, Dean of Faculty of Veterinary Medicine Universitas Airlangga.

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66. Karwanti NW, Arumdani F, Yulianto AB, et al.: Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances of male broiler chicken. Dataset. figshare 2023. Publisher Full Text

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Version 3

VERSION 3 PUBLISHED 27 Feb 2023

Author details Author details

Novita Wanda Karwanti
Roles: Conceptualization, Data Curation, Formal Analysis, Writing – Original Draft Preparation, Writing – Review & Editing

Dynda Febriana Arumdani
Roles: Conceptualization, Data Curation, Investigation, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing

Andreas Berny Yulianto
Roles: Conceptualization, Methodology, Software, Writing – Review & Editing

Tabita Dameria Marbun
Roles: Conceptualization, Investigation, Methodology, Writing – Review & Editing

Anjum Sherasiya
Roles: Conceptualization, Methodology, Software, Writing – Original Draft Preparation, Writing – Review & Editing

Mohammad Anam Al Arif
Roles: Conceptualization, Investigation, Writing – Original Draft Preparation, Writing – Review & Editing

Mirni Lamid
Roles: Conceptualization, Methodology, Writing – Original Draft Preparation, Writing – Review & Editing

Competing interests

Anjum Sherasiya is employed at the Veterinary World journal; other authors declare that they have no conflicts of interest.

Grant information

This research was supported by the Faculty of Veterinary Medicine (Fakultas Kedokteran Hewan), Universitas Airlangga (769/UN3.14/PT/2020)
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Karwanti NW, Arumdani DF, Yulianto AB et al. Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken [version 3; peer review: 1 approved, 1 approved with reservations]. F1000Research 2023, 12:215 (https://doi.org/10.12688/f1000research.130072.3)

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Reviewer Report 11 Jul 2023

Asghar Abbas, Department of Fisheries and Aquacuture, Faculty of Veterinary and Animal Sciences, Muhammad Nawaz Sharif University of Agriculture, Multan, Pakistan

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https://doi.org/10.5256/f1000research.148052.r177039

I have reviewed the manuscript. The manuscript is written in suitable form however, it needs to address following comments

English and Scientific language should be improved.
Introduction section needs revision. Authors

I have reviewed the manuscript. The manuscript is written in suitable form however, it needs to address following comments

English and Scientific language should be improved.
Introduction section needs revision. Authors have ignored recent studies on used botanicals/plants in poultry. Authors should first consider to mention importance of some other plants and drug resistance problem as reported in latest latest studies to justify the research few studies I have suggested below to be include in introduction section before mentioning Moringa importance:

- A. Merdana IM, Watiniasih NL, Sudira IW, Arjana AAG, Gunawan IWNF, Sudimartini LM, and Budiasa K, 2021. The effect of ethanolic extract of Myrmecodia pendans on gentamicin induced nephrotoxicity in Wistar Rats. International Journal of Veterinary Science 10(2): 96-101¹

- B. Hussain K, Asghar Abbas, Alanazi HAH, Alharbi AMA, Alaiiri AA, Rehman A, Waqas MU, Raza MA, Yasin R, Ahmad B, Bano N, Khera HURA, 2023. Immunomodulatory effects of Artemisia brevifolia extract against experimentally induced coccidiosis in broiler chicken. Pak Vet J. http://dx.doi.org/10.29261/pakvetj/2023.026.²

- C. Tchoupou-Tchoupou EC, Ndofor-Foleng HM, Nwenya JM, Okenyi NJ, Ikeh Nnana E, Ngwu NR, Nwakpu PE, Ossei J and Onyimoniy EA, 2022. Effects of hexane extract of garlic on hematological, biochemical and histological parameters in F1 crossbred chicks non-infected and infected with Salmonella typhimurium. International Journal of Veterinary Science 11(4): 435-442³

- D. Nawaz M, Zhou J, Khalid I, Shamim A, Hussain A, Ahmed Z, Waqas M, Ahmed I and Malik MI, 2022. Antiparasitic activity of plants extract against gastrointestinal nematodes and Rhipicephalus microplus. International Journal of Veterinary Science 11(4): 474-478⁴

- E. Abbas A., Z. Iqbal, RZ. Abbas, MK. Khan, JA. Khan, ZD. Sindhu, MS. Mahmood, MK. Saleemi, 2017. In vivo anticoccidial effects of Beta vulgaris (sugar beet) in broiler chickens. Microb Path 111: 139-144.⁵
Which group served as control group? Kindly update in experimental design. Also in conclusion and result section clarify at which dose rate Moringa showed better results?
Discussion section also lacks the recent studies I suggest to add 3-4 latest studies in discussion section:

- A. Zhang K, Li X, Na C, Abbas A, Abbas RZ and Zaman MA, 2020. Anticoccidial effects of Camellia sinensis (green tea) extract and its effect on Blood and Serum chemistry of broiler chickens. Pakistan Veterinary Journal. 40: 77-80.⁶

- B. Mehnaz S, Abbas RZ, Kanchev K, Rafique MN, Aslam MA, Bilal M, Ather AS, Zahid A and Batool T, 2023. Natural control perspectives of Dermanyssus gallinae in poultry. Int J Agri Biosci, 12(3): 136-142.⁷ https://doi.org/10.47278/journal.ijab/2023.056

- C. Akhtar T, Shahid S, Asghar A, Naeem MI, Aziz S and Ameer T, 2023. Utilisation of herbal bullets against Newcastle disease in poultry sector of Asia and Africa (2012-2022). Int J Agri Biosci, 12(1): 56-65. https://doi.org/10.47278/journal.ijab/2023.044⁸

I suggest to address above mentioned comments in manuscript and Revision is required.

Thanks

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

References

1. Merdana IM, Watiniasih NL, Sudira IW, Arjana AAG, et al.: The Effect of Ethanolic Extract of Myrmecodia pendans on Gentamicin InducedNephrotoxicity in Wistar Rats. International Journal of Veterinary Science. 2020; 10 (2). Publisher Full Text | Reference Source
2. Hussain K, Abbas A, Alanazi HAH, Alharbi AMA, et al.: Immunomodulatory Effects of Artemisia brevifolia Extract against Experimentally Induced Coccidiosis in Broiler Chicken. Pak Vet J. 2023; 43 (2). Reference Source
3. Tchoupou-Tchoupou EC, Ndofor-Foleng HM, Nwenya JM, Okenyi NJ, et al.: Effects of hexane extract of garlic on hematological, biochemical andhistological parameters in F1 crossbred chicks non-infected and infected with Salmonella typhimurium. Journal of Veterinary Science. 2022; 11 (4). Publisher Full Text | Reference Source
4. Nawaz M, Zhou J, Khalid I, Shamim A, et al.: Antiparasitic activity of plants extract against gastrointestinal nematodes and Rhipicephalus microplus. Journal of Veterinary Science. 2022; 11 (4). Publisher Full Text | Reference Source
5. Abbas A, Iqbal Z, Abbas RZ, Khan MK, et al.: In vivo anticoccidial effects of Beta vulgaris (sugar beet) in broiler chickens.Microb Pathog. 2017; 111: 139-144 PubMed Abstract | Publisher Full Text
6. Zhang K, Li X, Na C, Abbas A, et al.: Anticoccidial effects of Camellia sinensis (green tea) extract and its effect on Blood and Serum chemistry of broiler chickens. Pak Vet J. 2020; 40 (1). Reference Source
7. Mehnaz S, Abbas RZ, Kanchev K, Rafique MN, et al.: Natural control perspectives of Dermanyssus gallinae in poultry. Int J Agri Biosci. 2023; 12 (3). Publisher Full Text | Reference Source
8. Akhtar T, Shahid S, Asghar A, Naeem MI, et al.: Utilisation of herbal bulletsagainst Newcastle disease in poultry sector of Asia and Africa (2012-2022). Int J Agri Biosci. 2023; 12 (1). Publisher Full Text | Reference Source

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Ethnomedicine

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report 05 Jun 2023

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

Approved

https://doi.org/10.5256/f1000research.148052.r173628

The article has been put in a ... Continue reading

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Author Response 12 Jun 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

12 Jun 2023

Author Response

Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Competing Interests: No competing interests were disclosed.
Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Competing Interests: No competing interests were disclosed. Close
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Author Response 12 Jun 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

12 Jun 2023

Author Response

Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Competing Interests: No competing interests were disclosed.
Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Dear Reviewer

Thank you so much to approved our manuscript

Best regards
Widya Paramita Lokapirnasari
Competing Interests: No competing interests were disclosed. Close
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PUBLISHED 05 May 2023

Revised

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Reviewer Report 09 May 2023

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

Approved

https://doi.org/10.5256/f1000research.147585.r172021

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Author Response 15 May 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

15 May 2023

Author Response

We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

... Continue reading We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

We want to thank to the editorial team and reviewers which improved the quality of the manuscript.
We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

We want to thank to the editorial team and reviewers which improved the quality of the manuscript.
Competing Interests: No competing interests were disclosed. Close
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Author Response 15 May 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

15 May 2023

Author Response

We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

... Continue reading We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

We want to thank to the editorial team and reviewers which improved the quality of the manuscript.
We have revised the abstract as suggested by the reviewers.

The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

We want to thank to the editorial team and reviewers which improved the quality of the manuscript.
Competing Interests: No competing interests were disclosed. Close
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Version 1

VERSION 1

PUBLISHED 27 Feb 2023

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Reviewer Report 24 Apr 2023

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

Approved with Reservations

https://doi.org/10.5256/f1000research.142800.r167980

This article addresses the role of Moringa oleifera Lam. leaf extract on the growth of Pediococcus pentosaceus, Lactobacillus acidophilus and L. plantarum probiotic as an alternative to antibiotic growth promoters (AGP) in livestock. The report of this article also proved the importance of probiotics in combating the current antimicrobial resistance organisms ravaging the livestock industrials today.

Abstract: The aim should capture the title; Summary of methods used need to be stated inside the abstract; Results should be written to flow with the methods used accordingly.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph; correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Conclusion: Ok

I therefore recommend Approved with Reservations. The authors need to make the minor corrections pointed out on the reviewers report before indexing.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Medical Microbiology/Epidemiology

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Author Response 05 May 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

05 May 2023

Author Response
Revised from author
- Abstract: The aim should capture the title
Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus ... Continue reading
Revised from author

Abstract: The aim should capture the title

Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) of male broiler chicken

Summary of methods used need to be stated inside the abstract.

Revised:
Methods: This study consisted of three sub studies: (1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf method and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by applying the Forth method. Triterpenoid tests were performed by applying the Liebermann-Bouchard method and the alkaloids test was conducted by implementing the method of Mayer, Bouchardat and Wagner. (2) in vitro evaluation of several doses of Moringa extract (0%, 0.1%, 0.2%, 0.3% ),where each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 h. The growth of probiotic bacteria was calculated for the colonies by using the total plate count; (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) on male broiler chicken. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.

Results should be written to flow with the methods used accordingly.

Revised:
Results: The results showed (1) the phytochemical screening test M. oleifera extract contained positive of flavonoids, tannins, saponins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract at doses of 0.1%, 0.2%, 0.3% increased the growth of bacteria P. pentosaceus, L. acidophilus and L. plantarum (p<0.05); (3) The use of probiotics in vivo evaluation, M. oleifera extract and their combination showed improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p <0.05) between the treatments, but there was no significant difference (p > 0.05) between the treatments on nutrient intake (dry matter, ash, crude protein, crude fiber and organic matter) on broiler chicken starter phase.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph;

Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources^16,17,18

16. Pereira WA, Mendonça CM, Urquiza AV, Marteinsson VÞ, LeBlanc JG, Cotter PD, Villalobos EF, Romero J, Oliveira RP: Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 2022;10(9):1705.
17. Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M: Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Frontiers in microbiology. 2021;12:709959.
18. Anh Thu NP, Hong Thuy DT, Nghia NH, Phuong Thao DT: Heterologous Expression of Pediocin PA-1 in Escherichia coli. bioRxiv. 2019;12:607630.

They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry^6,7.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7.Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs^6,7,26,27.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7. Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.
26. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals. 2020 Oct 13;10(10):1863.
27. Andriani AD, Lokapirnasari WP, Karimah B, Hidanah S, Al-Arif MA: Potency of probiotic on broiler growth performance and economics analysis. Indian Journal of Animal Sciences. 2020;90(8):1140-5.

correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Revised:
The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Revised: The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Revised:
The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Revised:
These results are in accordance with the research of Kandeepan et al which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods³². Secondary metabolites extracted from M. oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins³³.

32. Kandeepan C, Sabitha M, Parvathi K, Senthilkumar N, Ramya S, Boopathi NM, Jayakumararaj R: Phytochemical screening, GCMS profile, and In-silico properties of bioactive compounds in methanolic leaf extracts of Moringa oleifera. Journal of Drug Delivery and Therapeutics. 2022;12(2):87-99.
33. Oladeji OS, Odelade KA, Oloke JK: Phytochemical screening and antimicrobial investigation of Moringa oleifera leaf extracts. African Journal of Science, Technology, Innovation and Development. 2020;12(1):79-84.
Revised from author

Abstract: The aim should capture the title

Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) of male broiler chicken

Summary of methods used need to be stated inside the abstract.

Revised:
Methods: This study consisted of three sub studies: (1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf method and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by applying the Forth method. Triterpenoid tests were performed by applying the Liebermann-Bouchard method and the alkaloids test was conducted by implementing the method of Mayer, Bouchardat and Wagner. (2) in vitro evaluation of several doses of Moringa extract (0%, 0.1%, 0.2%, 0.3% ),where each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 h. The growth of probiotic bacteria was calculated for the colonies by using the total plate count; (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) on male broiler chicken. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.

Results should be written to flow with the methods used accordingly.

Revised:
Results: The results showed (1) the phytochemical screening test M. oleifera extract contained positive of flavonoids, tannins, saponins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract at doses of 0.1%, 0.2%, 0.3% increased the growth of bacteria P. pentosaceus, L. acidophilus and L. plantarum (p<0.05); (3) The use of probiotics in vivo evaluation, M. oleifera extract and their combination showed improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p <0.05) between the treatments, but there was no significant difference (p > 0.05) between the treatments on nutrient intake (dry matter, ash, crude protein, crude fiber and organic matter) on broiler chicken starter phase.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph;

Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources^16,17,18

16. Pereira WA, Mendonça CM, Urquiza AV, Marteinsson VÞ, LeBlanc JG, Cotter PD, Villalobos EF, Romero J, Oliveira RP: Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 2022;10(9):1705.
17. Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M: Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Frontiers in microbiology. 2021;12:709959.
18. Anh Thu NP, Hong Thuy DT, Nghia NH, Phuong Thao DT: Heterologous Expression of Pediocin PA-1 in Escherichia coli. bioRxiv. 2019;12:607630.

They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry^6,7.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7.Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs^6,7,26,27.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7. Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.
26. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals. 2020 Oct 13;10(10):1863.
27. Andriani AD, Lokapirnasari WP, Karimah B, Hidanah S, Al-Arif MA: Potency of probiotic on broiler growth performance and economics analysis. Indian Journal of Animal Sciences. 2020;90(8):1140-5.

correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Revised:
The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Revised: The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Revised:
The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Revised:
These results are in accordance with the research of Kandeepan et al which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods³². Secondary metabolites extracted from M. oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins³³.

32. Kandeepan C, Sabitha M, Parvathi K, Senthilkumar N, Ramya S, Boopathi NM, Jayakumararaj R: Phytochemical screening, GCMS profile, and In-silico properties of bioactive compounds in methanolic leaf extracts of Moringa oleifera. Journal of Drug Delivery and Therapeutics. 2022;12(2):87-99.
33. Oladeji OS, Odelade KA, Oloke JK: Phytochemical screening and antimicrobial investigation of Moringa oleifera leaf extracts. African Journal of Science, Technology, Innovation and Development. 2020;12(1):79-84.
Competing Interests: No competing interests were disclosed Close
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COMMENTS ON THIS REPORT

Author Response 05 May 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

05 May 2023

Author Response
Revised from author
- Abstract: The aim should capture the title
Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus ... Continue reading
Revised from author

Abstract: The aim should capture the title

Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) of male broiler chicken

Summary of methods used need to be stated inside the abstract.

Revised:
Methods: This study consisted of three sub studies: (1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf method and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by applying the Forth method. Triterpenoid tests were performed by applying the Liebermann-Bouchard method and the alkaloids test was conducted by implementing the method of Mayer, Bouchardat and Wagner. (2) in vitro evaluation of several doses of Moringa extract (0%, 0.1%, 0.2%, 0.3% ),where each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 h. The growth of probiotic bacteria was calculated for the colonies by using the total plate count; (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) on male broiler chicken. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.

Results should be written to flow with the methods used accordingly.

Revised:
Results: The results showed (1) the phytochemical screening test M. oleifera extract contained positive of flavonoids, tannins, saponins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract at doses of 0.1%, 0.2%, 0.3% increased the growth of bacteria P. pentosaceus, L. acidophilus and L. plantarum (p<0.05); (3) The use of probiotics in vivo evaluation, M. oleifera extract and their combination showed improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p <0.05) between the treatments, but there was no significant difference (p > 0.05) between the treatments on nutrient intake (dry matter, ash, crude protein, crude fiber and organic matter) on broiler chicken starter phase.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph;

Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources^16,17,18

16. Pereira WA, Mendonça CM, Urquiza AV, Marteinsson VÞ, LeBlanc JG, Cotter PD, Villalobos EF, Romero J, Oliveira RP: Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 2022;10(9):1705.
17. Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M: Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Frontiers in microbiology. 2021;12:709959.
18. Anh Thu NP, Hong Thuy DT, Nghia NH, Phuong Thao DT: Heterologous Expression of Pediocin PA-1 in Escherichia coli. bioRxiv. 2019;12:607630.

They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry^6,7.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7.Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs^6,7,26,27.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7. Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.
26. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals. 2020 Oct 13;10(10):1863.
27. Andriani AD, Lokapirnasari WP, Karimah B, Hidanah S, Al-Arif MA: Potency of probiotic on broiler growth performance and economics analysis. Indian Journal of Animal Sciences. 2020;90(8):1140-5.

correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Revised:
The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Revised: The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Revised:
The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Revised:
These results are in accordance with the research of Kandeepan et al which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods³². Secondary metabolites extracted from M. oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins³³.

32. Kandeepan C, Sabitha M, Parvathi K, Senthilkumar N, Ramya S, Boopathi NM, Jayakumararaj R: Phytochemical screening, GCMS profile, and In-silico properties of bioactive compounds in methanolic leaf extracts of Moringa oleifera. Journal of Drug Delivery and Therapeutics. 2022;12(2):87-99.
33. Oladeji OS, Odelade KA, Oloke JK: Phytochemical screening and antimicrobial investigation of Moringa oleifera leaf extracts. African Journal of Science, Technology, Innovation and Development. 2020;12(1):79-84.
Revised from author

Abstract: The aim should capture the title

Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) of male broiler chicken

Summary of methods used need to be stated inside the abstract.

Revised:
Methods: This study consisted of three sub studies: (1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf method and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by applying the Forth method. Triterpenoid tests were performed by applying the Liebermann-Bouchard method and the alkaloids test was conducted by implementing the method of Mayer, Bouchardat and Wagner. (2) in vitro evaluation of several doses of Moringa extract (0%, 0.1%, 0.2%, 0.3% ),where each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 h. The growth of probiotic bacteria was calculated for the colonies by using the total plate count; (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) on male broiler chicken. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.

Results should be written to flow with the methods used accordingly.

Revised:
Results: The results showed (1) the phytochemical screening test M. oleifera extract contained positive of flavonoids, tannins, saponins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract at doses of 0.1%, 0.2%, 0.3% increased the growth of bacteria P. pentosaceus, L. acidophilus and L. plantarum (p<0.05); (3) The use of probiotics in vivo evaluation, M. oleifera extract and their combination showed improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p <0.05) between the treatments, but there was no significant difference (p > 0.05) between the treatments on nutrient intake (dry matter, ash, crude protein, crude fiber and organic matter) on broiler chicken starter phase.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph;

Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources^16,17,18

16. Pereira WA, Mendonça CM, Urquiza AV, Marteinsson VÞ, LeBlanc JG, Cotter PD, Villalobos EF, Romero J, Oliveira RP: Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 2022;10(9):1705.
17. Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M: Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Frontiers in microbiology. 2021;12:709959.
18. Anh Thu NP, Hong Thuy DT, Nghia NH, Phuong Thao DT: Heterologous Expression of Pediocin PA-1 in Escherichia coli. bioRxiv. 2019;12:607630.

They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry^6,7.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7.Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs^6,7,26,27.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7. Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.
26. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals. 2020 Oct 13;10(10):1863.
27. Andriani AD, Lokapirnasari WP, Karimah B, Hidanah S, Al-Arif MA: Potency of probiotic on broiler growth performance and economics analysis. Indian Journal of Animal Sciences. 2020;90(8):1140-5.

correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Revised:
The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Revised: The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Revised:
The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Revised:
These results are in accordance with the research of Kandeepan et al which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods³². Secondary metabolites extracted from M. oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins³³.

32. Kandeepan C, Sabitha M, Parvathi K, Senthilkumar N, Ramya S, Boopathi NM, Jayakumararaj R: Phytochemical screening, GCMS profile, and In-silico properties of bioactive compounds in methanolic leaf extracts of Moringa oleifera. Journal of Drug Delivery and Therapeutics. 2022;12(2):87-99.
33. Oladeji OS, Odelade KA, Oloke JK: Phytochemical screening and antimicrobial investigation of Moringa oleifera leaf extracts. African Journal of Science, Technology, Innovation and Development. 2020;12(1):79-84.
Competing Interests: No competing interests were disclosed Close
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VERSION 3 PUBLISHED 27 Feb 2023

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Version 1 27 Feb 23	read

Ugbo Emmanuel Nnabuike, Ebonyi State University, Abakaliki, Nigeria
Asghar Abbas, Muhammad Nawaz Sharif University of Agriculture, Multan, Pakistan

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11 Jul 2023 | for Version 3

Asghar Abbas, Department of Fisheries and Aquacuture, Faculty of Veterinary and Animal Sciences, Muhammad Nawaz Sharif University of Agriculture, Multan, Pakistan

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Approved With Reservations

I have reviewed the manuscript. The manuscript is written in suitable form however, it needs to address following comments

English and Scientific language should be improved.
Introduction section needs revision. Authors have ignored recent studies on used botanicals/plants in poultry. Authors should first consider to mention importance of some other plants and drug resistance problem as reported in latest latest studies to justify the research few studies I have suggested below to be include in introduction section before mentioning Moringa importance:

- A. Merdana IM, Watiniasih NL, Sudira IW, Arjana AAG, Gunawan IWNF, Sudimartini LM, and Budiasa K, 2021. The effect of ethanolic extract of Myrmecodia pendans on gentamicin induced nephrotoxicity in Wistar Rats. International Journal of Veterinary Science 10(2): 96-101¹

- B. Hussain K, Asghar Abbas, Alanazi HAH, Alharbi AMA, Alaiiri AA, Rehman A, Waqas MU, Raza MA, Yasin R, Ahmad B, Bano N, Khera HURA, 2023. Immunomodulatory effects of Artemisia brevifolia extract against experimentally induced coccidiosis in broiler chicken. Pak Vet J. http://dx.doi.org/10.29261/pakvetj/2023.026.²

- C. Tchoupou-Tchoupou EC, Ndofor-Foleng HM, Nwenya JM, Okenyi NJ, Ikeh Nnana E, Ngwu NR, Nwakpu PE, Ossei J and Onyimoniy EA, 2022. Effects of hexane extract of garlic on hematological, biochemical and histological parameters in F1 crossbred chicks non-infected and infected with Salmonella typhimurium. International Journal of Veterinary Science 11(4): 435-442³

- D. Nawaz M, Zhou J, Khalid I, Shamim A, Hussain A, Ahmed Z, Waqas M, Ahmed I and Malik MI, 2022. Antiparasitic activity of plants extract against gastrointestinal nematodes and Rhipicephalus microplus. International Journal of Veterinary Science 11(4): 474-478⁴

- E. Abbas A., Z. Iqbal, RZ. Abbas, MK. Khan, JA. Khan, ZD. Sindhu, MS. Mahmood, MK. Saleemi, 2017. In vivo anticoccidial effects of Beta vulgaris (sugar beet) in broiler chickens. Microb Path 111: 139-144.⁵
Which group served as control group? Kindly update in experimental design. Also in conclusion and result section clarify at which dose rate Moringa showed better results?
Discussion section also lacks the recent studies I suggest to add 3-4 latest studies in discussion section:

- A. Zhang K, Li X, Na C, Abbas A, Abbas RZ and Zaman MA, 2020. Anticoccidial effects of Camellia sinensis (green tea) extract and its effect on Blood and Serum chemistry of broiler chickens. Pakistan Veterinary Journal. 40: 77-80.⁶

- B. Mehnaz S, Abbas RZ, Kanchev K, Rafique MN, Aslam MA, Bilal M, Ather AS, Zahid A and Batool T, 2023. Natural control perspectives of Dermanyssus gallinae in poultry. Int J Agri Biosci, 12(3): 136-142.⁷ https://doi.org/10.47278/journal.ijab/2023.056

- C. Akhtar T, Shahid S, Asghar A, Naeem MI, Aziz S and Ameer T, 2023. Utilisation of herbal bullets against Newcastle disease in poultry sector of Asia and Africa (2012-2022). Int J Agri Biosci, 12(1): 56-65. https://doi.org/10.47278/journal.ijab/2023.044⁸

I suggest to address above mentioned comments in manuscript and Revision is required.

Thanks

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

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No competing interests were disclosed.

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Ethnomedicine

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05 Jun 2023 | for Version 3

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

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Approved

The article has been put in a nice form. I therefore recommend for indexing.

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09 May 2023 | for Version 2

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

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Approved

I have gone through the corrections I pointed out. The authors made the correction as requested.

I only discovered grammatical error under the Abstract part. The authors should correct the first statement of the results to be: The phytochemical screening test of M. Oleifera extract showed the presence of flavonoids, saponins, tannins, triterpenoids and alkaloids.

I recommend that the Article should be Approved for indexing.

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24 Apr 2023 | for Version 1

Ugbo Emmanuel Nnabuike, Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Ebonyi, Nigeria

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Approved With Reservations

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Yes
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

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Author Response

05 May 2023

Widya Paramita Lokapirnasari, Division of Animal Husbandry, Faculty of Veterinary Medicine, Universitas Airlangga, Indonesia, Surabaya, 60115, Indonesia

Revised from author

Abstract: The aim should capture the title

Revised: This research aimed to evaluate the efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performances (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) of male broiler chicken

Summary of methods used need to be stated inside the abstract.

Revised:
Methods: This study consisted of three sub studies: (1) Screening test for phytochemical compounds. The flavonoid test was conducted by Bate Smith-Metcalf method and Wilstatter method. The Tannin test with Denis’ reagent. The saponin test was performed by applying the Forth method. Triterpenoid tests were performed by applying the Liebermann-Bouchard method and the alkaloids test was conducted by implementing the method of Mayer, Bouchardat and Wagner. (2) in vitro evaluation of several doses of Moringa extract (0%, 0.1%, 0.2%, 0.3% ),where each test tube was added with 1 mL of each isolate and incubated for 24 h at 37°C, after each isolate bacteria was grown in the Agar MRS media using the pour plate method and incubated for 12 h. The growth of probiotic bacteria was calculated for the colonies by using the total plate count; (3) evaluation of probiotics and M. oleifera in vivo to prove growth performance (nutrient intake, body weight gain, feed conversion ratio and feed efficiency) on male broiler chicken. All results were analyzed by analysis of variance (ANOVA) then followed by the Duncan test.

Results should be written to flow with the methods used accordingly.

Revised:
Results: The results showed (1) the phytochemical screening test M. oleifera extract contained positive of flavonoids, tannins, saponins, triterpenoids and alkaloids; (2) in vitro evaluation of M. oleifera extract at doses of 0.1%, 0.2%, 0.3% increased the growth of bacteria P. pentosaceus, L. acidophilus and L. plantarum (p<0.05); (3) The use of probiotics in vivo evaluation, M. oleifera extract and their combination showed improve growth performance. The result of body weight, body weight gain, FCR and feed efficiency signifcantly differed (p <0.05) between the treatments, but there was no significant difference (p > 0.05) between the treatments on nutrient intake (dry matter, ash, crude protein, crude fiber and organic matter) on broiler chicken starter phase.

Introduction: Add Reference in last statement in paragraph three(3) and second to last paragraph;

Pediocin is a bacteriocin generated by P. pentosaceus, which, in a sufficient amount, can eliminate pathogenic bacteria such as Listeria monocytogens, Staphylococcus aureus, Escherichia coli, Vibrio alginolyticus, Pseudomonas stutzeri, and Aeromonas. P. pentosaceus bacterial growth requires nutrition with carbon, nitrogen, and mineral sources^16,17,18

16. Pereira WA, Mendonça CM, Urquiza AV, Marteinsson VÞ, LeBlanc JG, Cotter PD, Villalobos EF, Romero J, Oliveira RP: Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 2022;10(9):1705.
17. Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M: Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Frontiers in microbiology. 2021;12:709959.
18. Anh Thu NP, Hong Thuy DT, Nghia NH, Phuong Thao DT: Heterologous Expression of Pediocin PA-1 in Escherichia coli. bioRxiv. 2019;12:607630.

They allows to control micro-organism growth in the digestive tract of poultry by increasing the metabolic activities in the body, making them potential feed additives in poultry^6,7.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7.Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.

Nutrition consumed by poultry is used for maintenance and production. Feed efficiency in broilers is influenced by the level of feed consumption and body weight gain. High feed efficiency is produced due to low feed intake followed by a high rate of body weight gain. A high level of feed efficiency can reduce livestock production costs^6,7,26,27.

6.Yadav S, Jha R: Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of animal science and biotechnology. 2019;10(1):1-1.
7. Krysiak K, Konkol D, Korczyński M: Overview of the use of probiotics in poultry production. Animals. 2021;11(6):1620.
26. Jha R, Das R, Oak S, Mishra P. Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animals. 2020 Oct 13;10(10):1863.
27. Andriani AD, Lokapirnasari WP, Karimah B, Hidanah S, Al-Arif MA: Potency of probiotic on broiler growth performance and economics analysis. Indian Journal of Animal Sciences. 2020;90(8):1140-5.

correct ‘ffectiveness’ to ‘effectiveness in last paragraph.

Revised:
The study aimed to analyze the phytochemical properties of Moringa leaf extract and the effectiveness of M. oleifera extract with different dosages and incubation times on in vitro bacterial growth of P. pentosaceus, L. acidophilus and L. plantarum probiotic, as well as their effect on growth performance on broiler chicken starter phase in vivo.

Method: Correct to; "Phytochemical screening test was carried out to determine the presence of Flavonoid, tannin..."

Revised: The phytochemical screening test was carried out to determine the presence of the flavonoid, tannin, saponin, triterpenoid and alkaloid.

Result: Good; but you need to put all the results together; some part of your result interpretation was added to the discussion.

Revised:
The results of positive flavonoid test indicated by change in color, there was a change in color to orange. The interpretation of positive tannin, indicated by the color of the filtrate changed to a dark green-black color and the presence of saponin indicated by the foam. The interpretation of flavonoid, tannin , saponin were indicate in Figure 1A, B, C. The Figure 2 showed the result of positive triterpenoid test and the figure 3 showed the result of alkaloid Test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+).

Discussion: Result interpretation (Fig 1A, 2, 3) should be part of results. Cut the result interpretations and add to the Results part. Try to comparing your findings with the findings of previous researchers.

Revised:
These results are in accordance with the research of Kandeepan et al which showed that the results of phytochemical analysis of M.oleifera revealed the presence of alkaloids, flavonoids, saponins, tannins and terpenoids. M. oleifera leaf extracts contain a substantial amount of phenolic chemicals, which are principally responsible for antioxidant activities. Secondary metabolites with bioactive properties. M. oleifera leaves continue to be excellent sources of micronutrients and phytochemicals for the creation of nutraceuticals and functional foods³². Secondary metabolites extracted from M. oleifera leaves using chloroform, ethyl acetate, and ethanol contain bioactive substances such as such as steroids, saponins, tannins, flavonoids, terpernoids and phlobatannins³³.

32. Kandeepan C, Sabitha M, Parvathi K, Senthilkumar N, Ramya S, Boopathi NM, Jayakumararaj R: Phytochemical screening, GCMS profile, and In-silico properties of bioactive compounds in methanolic leaf extracts of Moringa oleifera. Journal of Drug Delivery and Therapeutics. 2022;12(2):87-99.
33. Oladeji OS, Odelade KA, Oloke JK: Phytochemical screening and antimicrobial investigation of Moringa oleifera leaf extracts. African Journal of Science, Technology, Innovation and Development. 2020;12(1):79-84.

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Competing Interests

No competing interests were disclosed

Alongside their report, reviewers assign a status to the article:

Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions

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Efficacy of Moringa oleifera Lam. extracts and Pediococcus pentosaceus, Lactobacillus acidophilus, Lactobacillus plantarum probiotic during starter period on growth performance of male broiler chicken

Abstract

Keywords

Revised Amendments from Version 2

Introduction

Methods

Experimental design

Ethical considerations

Statistical analysis

Results

Phytochemical screening of M. oleifera extract

Table 1. Phytochemical screening of M. oleifera extract.

Figure 1. A: Flavonoid test, B: Tannin test, C: Saponin.

Figure 2. Triterpenoid test.

Figure 3. Alkaloid test [Mayer reagent (-), Bouchardat reagent (+) and Wagner reagent (+)].

Evaluation of several doses of M. oleifera extract

Table 2. The growth of P. pentosaceus, L. acidophilus and L. plantarum on MRS Agar at medium temperature 37°C.

Figure 4. The growth of P. pentosaceus, L. acidophilus and L. plantarum on MRS Agar medium temperature 37°C.

Evaluation of probiotics, M. oleifera and combination of probiotics + M. oleifera in vivo

Table 3. Feed intake and nutrient intake after giving probiotic, M. oleifera extract and a combination of probiotic and extract during the starter phase of broiler chicken.

Table 4. Production performance after giving probiotic, extract M. oleifera and a combination of probiotic and extract during the starter phase of broiler chicken.

Discussion

Phytochemical screening of M. oleifera extract

Evaluation of several doses of M. oleifera extract

Evaluation of probiotics, M. oleifera and combination of probiotics + M. oleifera in vivo

Conclusions

Data availability

Underlying data

Reporting guidelines

Acknowledgements

References

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