Research Article

Addition of Moringa Leaf Meal in the Diet of Hy-Line Brown Laying Hens: Influence on Productive and Egg Quality Parameters

Eliseo Pelagio Fernández Ruelas1, Ali William Canaza-Cayo2,3*, Francisco Halley Rodriguez Huanca1, Uri Harold Perez Guerra1, Roxana Churata-Huacani3, Tales Jesus Fernandes3, Ysabel Mendoza Aguilar1

1Faculty of Medicine Veterinary and Zootecnics, National University of Altiplano, (051) 599430 Av. Floral Nº 1153, Puno, Peru; 2Faculty of Agrarian Sciences, Agronomic Engineering School, National University of Altiplano, (051) 599430 Av. Floral Nº 1153, Puno, Peru; 3Department of Statistics, Institute of Exact and Technological Sciences, Federal University of Lavras, Postal code 3037, CEP 37200-900 Lavras, MG, Brazil.

Received | December 09, 2022; Accepted | April 05, 2023; Published | May 30, 2023

*Correspondence | Ali William Canaza-Cayo, Faculty of Agrarian Sciences, Agronomic Engineering School, National University of Altiplano, (051) 599430 Av. Floral Nº 1153, Puno, Peru; Email: alicanaza@unap.edu.pe

Citation | Ruelas EPF, Canaza-Cayo AW, Huanca FHR, Guerra UHP, Churata-Huacani R, Fernandes TJ, Aguilar YM (2023). Addition of moringa leaf meal in the diet of hy-line brown laying hens: influence on productive and egg quality parameters. J. Anim. Health Prod. 11(2): 185-192.

DOI | http://dx.doi.org/10.17582/journal.jahp/2023/11.2.185.192

ISSN | 2308-2801

 

 

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

Poultry farming in Peru and around the world is a very important productive activity and is the most developed in the livestock sector. The poultry industry has achieved high levels of food production and food security to the growing population. In the year 2021, the national production of chicken eggs was 504,112 thousand tons, with a population of 28,938,922 laying birds, producing a total of 8,406 million eggs (Contreras, 2019). In Puno the chicken population is 371,554 units with a production of 1752 tons of eggs (MIDAGRI, 2022).

The demands for quality and low-cost food products, and since chicken egg producers face increased feed costs, alternative protein and energy resources are sought that improve productivity, and are organic (Aguirre y Pizarro, 2018; Contreras, 2019). There are plant species, native or introduced (i.e., Moringa oleifera), that are low-cost food resources and contribute to the productivity and quality of eggs, a staple food for consumers.

Moringa oleifera is a tree species with great forage and economic potential. It adapts to poor soils and has great power to withstand during periods of drought. Nutritionists have incorporated the plant in bird diets (Abbas, 2013) that leads to lower consumption, greater weight gain, excellent feed conversion (Abou-Elezz et al., 2012; Mendiola and Aguirre, 2015), larger eggs with greater shell weight, egg white and a lower proportion of yolk (D’Mello and Acamovic, 1989; Kakengi et al., 2004; Valdivié et al., 2016).

Moringa oleifera adapts to desert areas, tolerates water scarcity, and can sustain production of green matter. The nutrient content makes this plant a viable alternative to help boost the production of quality food to meet the needs of our society (El-Hack et al., 2018). So, the hypothesis of this study was that addition of Moringa oleifera leaf meal in Hy-Line Brown hens fed diets would increase productive parameters and egg quality characteristics. The aim of this study was to determine the effect of different levels of Moringa oleifera leaf meal on productive parameters and egg quality characteristics of Hy Line Brown laying hens in the Andean region of Peru.

MATERIALS AND METHOD

Location

This study was carried out at the experimental poultry farm of the Faculty of Veterinary Medicine and Zootechnics of the National University of the Altiplano located in Puno Department, Peru. The poultry farm is located at 3848 meters above sea level, 16°35’36” south latitude, 68°34’02’’ western length, whose temperatures vary between 8.4 and 15.6 °C, relative humidity between 64 and 77% and rainfall reaching 868.9 mm/year (SENAHMI, 2017).

Experimental data and feed preparation

A total of 180 (average weight = 1820 ± 120 g, 30-week-old) Hy-Line Brown hens were assigned to three treatment diets including Moringa oleifera leaves (MOL) at 0, 2.5, and 4.5%, for nine weeks. Moringa oleifera leaves powder were added to a small amount of basal feed and mixed. The mixture was then added to the preset amount of feed for each treatment and mixed thoroughly before being fed to each group. Each treatment had 12 replicates with five hens each.

The moringa plants were collected from the Moquegua region. Leaves were dried in the shade, then ground and incorporated in the poultry feed in two proportions. The poultry house was 16m2 with 2 batteries and 12 battery cages incorporated with a gutter-type feeding and drinking trough.

Feeding

The ration was formulated through the AEZO- FD II program, the composition of the food was adjusted according to FEDNA (2010) and the adjustment of the nutritional requirements was carried out according to the laying stage. The basal diet (Table 1) was formulated to meet all the nutrient requirements for hens (NRC, 1994).

 

Table 1: Composition and nutrient levels of the basal diet formulated for hens in the laying stage (30-37 weeks).

Ingredients, %	Treatments
	Controlb	MOL2.5	MOL4.5
Ingredient (%, as fed basis)
MOLa	0	2.5	4.5
Yellow corn	35	35	35
Extruded whole soybeans	17.95	16.83	15.97
Rice powder	29.22	27.84	26.70
Fish flour	4	4	4
“Chako” Clay	0.5	0.5	0.5
Common salt	0.4	0.4	0.4
Minerals	1.17	1.17	1.17
Oil	2.95	2.95	2.95
Limestone	8.71	8.71	8.71
Vitamin Premixc	0.10	0.10	0.10
Chemical composition (DM basis)
Metabolizable energy (MJ/kg)	3.17	3.17	3.17
Crude protein	16.86	16.86	16.86
Calcium	3.39	3.40	3.40
Available phosphorus	0.25	0.24	0.23
ethereal extract	4.65	4.79	4.90
Crude fiber	3.13	3.01	2.92
Ash	1.34	1.29	1.24
Carbohydrate	5.16	4.48	4.59
Arginine	1.34	1.30	1.26
lysine	0.68	0.65	0.62
methionine	0.31	0.30	0.29
Cystine	0.30	0.28	0.27
Tryptophan	0.14	0.13	0.13

aMOL: Moringa oleifera leaf (MOL2.5 and MOL4.5, hens fed the basal diet with 2.5% or 4.5% MOL).

bControl group, hens fed a basal diet;

cProvided per kg of diet: 94.7% DM, 54,000,000 IU/kg vitamin A, 10,800,000 IU/kg vitamin D, 18,000 IU/kg vitamin E.

Productive Measurements

Food intake (FI) was evaluated by cages, the weight of the food offered and food not consumed was also recorded. The live weight (LW) was weighed every week by a digital balance with ± 0.01 g precision. Feed conversion ratio (FCR) was estimated as the ratio of feed consumed (g)/egg weight (g). The average egg weight/week (AEW), egg weight (EW), weight of the offered food and weight of the rejected food were calculated daily. Egg weight and its components such as whole egg weight (WEW), eggshell weight (ESW), egg yolk weight (EYW) and egg albumen weight (EAW) were weighed individually on a digital scale at 20, 40 and 60 days. Eggs were collected daily, and hen-day egg production was calculated.

Statistical Analysis

Experimental data were analyzed through one-way ANOVA by means a Completely Randomized Design, using the Minitab v.17 statistical software (Minitab Inc., State College, PA). We tested the null hypothesis that the addition of MOL in laying hens’ diets does not affect the productive parameters and egg quality characteristics when compared to the control group (no MOL). The Prior to ANOVA analysis, all data were tested for normality using the Shapiro-Wilk test. Data were expressed as mean ± standard error of the mean, and significance was considered at p < 0.05. Comparisons between the control and each of the treatments were performed using a Dunnett test at 5%.

RESULTS

Productive parameters

The addition of MOL meal showed significant effect on FI, LW and FCR with 2.5% MOL in the diet compared to the untreated group (P < 0.05, Table 2). However, there was no significant difference between 4.5% MOL and the untreated group. Moreover, FI and FCR in all dietary treatments slightly increased with age as shown in Figure 1 and 2, respectively. The trend in the initial and middle phase (1 to 5 weeks) is similar for all treatments, but from the 5th to 7th week, FI and FCR in the control group declined compared to the treated group. FI and FCR increased progressively in all treatment groups from the 7th week until the end of experiment. With the exception of the 1st, 2nd and 5th weeks, the hens fed on 2.5% MOL had the highest live weight followed by hens fed 4.5% MOL and the control diet (Figure 3).

Egg quality characteristics

Dietary treatments showed no significant (P>0.05) effect on AEW and EYW. However, WEW and EAW of Hy-Line Brown hens fed diets including MOL were significantly higher compared to the control group (Table 3). WEW, ESW and EAW were significantly (P<0.05) decreased with increasing levels of MOL. Hy-Line Brown hens fed MOL at 2.5 and 4.5% produced heavier WEW (p<0.05) than those from untreated birds. Hy-Line Brown hens fed MOL at 2.5% produced heavier ESW (p<0.05) than control group hens during the 9-wk period. Hy-Line Brown hens offered a diet including MOL had higher (p<0.05) EAW than those from the untreated group. However, Hy-Line Brown hens given MOL, produced eggs with similar (p>0.05) EYW than those on untreated diets (Table 3).

 

Table 2: Effects of Moringa oleifera leaf meal on production parameters (mean ± standard deviation) in Hy-Line Brown hens.

Productive parameters	Treatments
	Control	MOL2.5	MOL4.5
Feed intake (FI), g/day	114.91 ± 0.98	112.70 ± 2.91*	113.34 ± 1.06
Live weight of hens (LW), kg	1.86 ± 0.15	1.98 ± 0.10*	1.97 ± 0.10
Feed conversion ratio (FCR), g feed/g eggs	1.89 ± 0.12	1.82 ± 0.05*	1.84 ± 0.04

Means marked with * were significantly different from the control by Dunnett test (p<0.05).

 

Table 3: Effects of Moringa oleifera leaf meal on egg characteristics (mean ± standard deviation) in Hy-Line Brown hens.

Eggs parameters	Treatments
	Control	MOL2.5	MOL4.5
Average egg weight/week (AEW), g	61.08 ± 2.80	62.10 ± 1.08	61.78 ± 0.77
Whole egg weight (WEW), g	61.29 ± 1.88	63.81 ± 1.39*	63.14 ± 2.08*
Eggshell weight (ESW), g	7.71± 0.52	8.31± 0.39*	7.53± 0.39
Egg albumen weight (EAW), g	37.61± 1.05	39.31± 1.71*	39.17± 1.73*
Egg yolk weight (EYW), g	15.97± 1.05	16.19± 0.77	16.44± 0.77

Means marked with * were significantly different from the control by Dunnett test (p<0.05)

 

Egg Laying Percentage

Hens fed MOL at 2.5% showed two production peaks (4th and 8th weeks) and had higher egg laying percentages than hens fed the control diet or MOL at 4.5% (Figure 4). As shown in Figure 5, inclusion of 2.5% MOL induced the highest egg production (81.94%) followed by 4.5% MOL (79.72%) and the control diet (75.83%).

 

DISCUSSION

Productive parameters

Feed intake: The results of this research showed that supplementation with MOL in the diet of Hy-Line Brown laying hens lead to a decrease in Feed intake (FI). These results are in agreement with other studies (Abou-Elezz et al., 2012; Ochi et al., 2015; Swain et al., 2017; Mabusela et al., 2018; Tesfaye et al., 2018; Sharmin et al., 2021; Shen et al., 2021; Umesh et al., 2022). No significant effects about supplemented diet with MOL on FI have been reported (Abou-Elkhair et al., 2020; Ashour et al., 2020; Abdel-Wareth and Lohakare, 2021; Rajesh et al., 2022). The decrease in IF could be attributed to the slight increase of antinutritional factors (e.g.., phytates) in the MOL diets; affecting the absorption and processing of nutrients by the bird, and consequently reducing their palatability and voluntary feed intake (Gadzirayi and Mupangwa, 2014; Tessera, 2016).

Feed conversion ratio: On the other hand, the feed conversion ratios (FCR) indicate the quality and utilization of feed given to the hens. A lower FCR indicates a better utilization of the feed by the hens, due to better quality of the ingredients used to formulate the diet, which are more digestible. In this experiment low FCR values of laying hens were achieved with 2.5% MOL, but above this level, these values tended to rise. These values are comparable with those reported in other studies where FCR values increased with increased MOL (Lu et al., 2016; Teteh et al., 2016; Ahmad et al., 2017; Tesfaye et al., 2018; Abou-Elkhair et al., 2020; Shen et al., 2021; Rajesh et al., 2022; Umesh et al., 2022). The low FCR found in this study may be due to higher quality of ingredients; making the feed more digestible and palatable. In addition, it is important to consider future work in the initial, maximum and late stages of growth, because there could be an influence of the inclusion of MOL during the laying time.

Live weight of hens

In general, the study showed that addition of MOL at 2.5% tends to increase live weight (LW) of Hy-Line Brown laying hens compared to the untreated group (Figure 3, Table 2). This implies that a certain level of MOL in laying hens’ diets does not affect palatability. Above this level, FI and LW are negatively affected, possibly due to the anti-nutritional effects present in MOL (Abou-Elezz et al., 2011). This result is in close agreement with other studies (Gadzirayi and Mupangwa, 2014; Alebachew et al., 2016; Mabusela et al., 2018; Tesfaye et al., 2018; Voemesse et al., 2019) that indicated that MOL had a positive influence on growth and egg production in laying hens. However, our result disagrees with other studies (Valdivié et al., 2016; Siti et al., 2019; Bidura et al., 2020; Tutubalang et al., 2022) who reported a non-significant effect on the body weight of laying hens. The difference can be attributed to dietary composition, rearing conditions, environment, genetic variability and different MOL levels.

Egg quality characteristics

Egg weight: In the present study both average egg weight/week (AEW) and whole egg weight (WEW) followed the same trend (r = 0.98) with increasing MOL levels thus, WEW was used to compare egg weight. The WEW was higher in hens fed MOL at 2.5%. These results would indicate that MOL addition at low levels improves egg weights; which is in agreement with other studies (Abou-Elezz et al., 2012; El-Sheikh et al., 2015; Antara et al., 2019; Abou-Elkhair et al., 2020; Abdel-Wareth and Lohakare, 2021; Rajesh et al., 2022; Umesh et al., 2022). N’nanle et al. (2020) who reported positive effect of 1% MOL on egg weight of Sasso breeder hens, suggest that this improvement might be due to the presence of selenium and sulfurous amino acids in moringa leaves. However, in others studies the WEW values were not influenced by the addition of MOL in laying diets (Ebenebe et al., 2013; Gakuya et al., 2014; Ahmad et al., 2017; Mabusela et al., 2018; Ashour et al., 2020; Gayathri et al., 2020; Sharmin et al., 2021; Shen et al., 2021). The difference of our results with the other reports could be associated with factors such as feeding, strain, stage of laying and climate.

Eggshell weight: In the present study, the eggshell weight (ESW) improved significantly with the addition of MOL2.5 compared to control group. These findings agree with those reported in other studies (El-Sheikh et al., 2015; Valdivié et al., 2016; Tesfaye et al., 2018; Sharmin et al., 2021; Rajesh et al., 2022), that show the same trend of improvement with relatively low levels of MOL in the diet. The reason may be that only low MOL levels are tolerated by the hens due to the anti-nutritional factors as mentioned in other studies (Abou-Elezz et al., 2011; Gadzirayi and Mupangwa, 2014; Tessera, (2016). However, ESW values in this report contradict the studies of Raphaël et al. (2015) and Shen et al. (2021) who reported that shell weight was not influenced by MOL addition in the laying hen’s diet. Mabusela et al. (2018) who tested three levels of moringa supplementation (1, 3 and 5%) in Hy-Line laying hens, reported that ESW was not affected and concluded that, although Moringa inclusion improved some egg quality traits, the deleterious effect that it had on layer performance indicated that maybe is should not be fed to early-lay hens at these levels.

Egg albumen weight: The addition of MOL significantly increased egg albumen weight (EAW) compared to the control group. A similar trend was reported by Ebenebe et al. (2013) who reported that the albumen weight of Isa Brown laying hens was significantly affected by the incorporation of MOL in the diet, with a maximum increase at 2.5% MOL and then decreasing at higher levels of MOL. The present result is in close agreement with the finding of Valdivié et al. (2016) and Tesfaye et al. (2018) who found the same trend in their study with L-33 laying hens with higher percentages of MOL (0 to 20%) in the diet. El-Sheikh et al. (2015) reported an increase albumin weight at a dose of 1.5 and 2mg/kg of moringa. The present study is in disagreement with those reported in other studies (Mabusela et al., 2018; Siti et al., 2019; Garcia et al., 2021) who found no differences in EAW with the inclusion of moringa at different doses ranging from 0 to 6%. The differences might be due to factors such as breed, feeding dose, environment, etc.

Egg yolk weight: Egg yolk weight (EYW) was similar in all groups. This finding is similar to other studies (Tesfaye et al., 2018; Swain et al., 2017; Ahmad et al., 2017) who also reported no significant differences in EYW with the inclusion of MOL in the diet of laying hens. Similarly, Abou-Elezz et al. (2011), Mabusela et al. (2018), Gayathri et al. (2020) and Abdel-Wareth et al. (2021) found that MOL supplementation at different levels (ranging 0 to 5%) had no adverse effect on EYW. However, our results differ from others (Ebenebe et al., 2013; El-Sheikh et al., 2015; Raphaël et al., 2015; Valdivié et al., 2016; Tesfaye et al., 2018; Abou-Elkhair et al., 2020; Shen et al., 2021) who concluded that MOL inclusion at 0-20% in laying hens’ diets improves egg quality characteristics.

Egg Laying Percentage: Figure 4 shows that laying hens fed MOL2.5 presented higher laying percentages (90.5%) than the untreated group, indicating that inclusion of MOL has a positive effect on egg production (Figure 5). Similar trends were reported by Bidura et al. (2020) and Abdel-Wareth and Lohakare (2021), who reported that hens supplemented with MOL achieved higher egg production compared to the control group. Likewise, Valdivié et al. (2016) reported high values of laying percentage in L-33 hens fed with 10% MOL compared to the control group. These results could be due to several factors such as how birds were able to meet their needs for crude protein, metabolizable energy (ME) and other nutrients. However, increasing the MOL to 20%, causes the laying percentage to decrease due to the lower consumption of ME. Kakengi et al. (2007) and Abou-Elezz et al. (2011), reports a reduction in egg production when feeding 15 or 20% MOL in the diet. Our results are different from those observed by Sharmin et al. (2021) and Shen et al. (2021) who do not report significant effects on the rate of laying and egg production in hens supplemented with MOL. The differences are due to a series of factors such as the bird line used, the age of the hen, the uniformity of body weight, the altitude of the environment, and others, as mentioned by North and Bell, (1993).

CONCLUSIONS

The results of the present study suggest that addition of MOL at 2.5% might be used successfully as a sustainable and cheap feed resource for Hy-Line Brown hens, without affecting production performance and egg quality.

ACKNOWLEDGMENTS

The authors are grateful for valuable assistance of all staff of Experimental Poultry Farm of the Faculty of Veterinary Medicine and Zootechnics of the National University of the Altiplano.

CONFLICT OF INTEREST

The authors declare that there is no any conflict of interest for this publication.

novelty statement

The research The study of Addition of Moringa leaf meal in the diet of Hy-Line Brown laying hens: influence on productive and egg quality parameters is novel conducted under altiplano conditions is novel.

AUTHORS CONTRIBUTIONS

Ali William Canaza-Cayo; Investigation, Writing, Data analysis, Formal analysis. Ali William Canaza-Cayo, Tales Jesus Fernandes, Francisco Halley Rodriguez Huanca, Uri Harold Perez Guerra; Statistical analysis, Methodology, Writing of Original draft. Eliseo Pelagio Fernandez Ruelas, Roxana Churata-Huacani, Ysabel Mendoza Aguilar; Editing, Review.

REFERENCES

Abbas TE (2013). The use of Moringa oleifera in poultry diets. Turkish J. Vet. Anim. Sci. 37(5): 492-496. https://doi.org/10.3906/vet-1211-40

Abdel-Wareth AA, Lohakare J (2021). Moringa oleifera leaves as eco-friendly feed additive in diets of hy-line brown hens during the late laying period. Animals. 11(4): 1116. https://doi.org/10.3390/ani11041116

Abou-Elezz FMK, Sarmiento-Franco L, Santos-Ricalde R, Solorio-Sanchez F (2011). Nutritional effects of dietary inclusion of Leucaena leucocephala and Moringa oleifera leaf meal on Rhode Island Red hens’ performance. Cuban J. Agr. Sci. 45:163–169.

Abou-Elezz FMK, Sarmiento-Franco L, Santos-Ricalde R, Solorio-Sanchez JF (2012). The nutritional effect of Moringa oleifera fresh leaves as feed supplement on Rhode Island Red Hen egg production and quality. Trop. Anim. Health Prod. 44(5): 1035-1040. https://doi.org/10.1007/s11250-011- 0037-5

Abou-Elkhair R, Abdo Basha H, Slouma Hamouda Abd El Naby W, Ajarem JS, Maodaa SN, Allam AA, Naiel MA (2020). Effect of a diet supplemented with the Moringa oleifera seed powder on the performance, egg quality, and Gene expression in Japanese laying quail under heat-stress. Animals. 10(5): 809. https://doi.org/10.3390/ani10050809

Aguirre R, Pizarro M (2018). Panorama y mercado del huevo. Oficina de Estudios y Políticas Agrarias del Ministerio de Agricultura del Gobierno de Chile. https://www.odepa.gob.cl/wp-content/uploads/2018/04/Huevos.pdf

Ahmad S, Khalique A, Pasha TN, Mehmood S, Hussain K, Ahmad S, Shaheen MS, Naeem M, Shafiq M (2017). Effect of Moringa oleifera (Lam.) pods as feed additive on egg antioxidants, chemical composition and performance of commercial layers. S. Afr. J. Anim. Sci. 47(6): 864-874. http://dx.doi.org/10.4314/sajas.v47i6.14

Alebachew W, Tesfaye E, Tamir B (2016). Effects of feeding different dietary levels of Moringa oleifera leaf meal on egg production, fertility and hatchability of dual purpose Koekoek hens. Middle East J. Sci. Res. 24(9): 2909-2920. https://doi.org/10.5829/idosi.mejsr.2016.24.09.23907

Antara IKJ, Bidura IGNG, Siti NW (2019). Effects of Moringa oleifera leaf and probiotics mixed fermented extract on the egg production and cholesterol contents in egg of laying hens. Int. J. Fauna Biol. Stud. 6(5): 06-12

Ashour EA, El-Kholy MS, Alagawany M, Abd El-Hack ME, Mohamed LA, Taha AE, El Sheikh AI, Laudadio V, Tufarelli V (2020). Effect of dietary supplementation with Moringa oleifera leaves and/or seeds powder on production, egg characteristics, hatchability and blood chemistry of laying Japanese quails. Sustainability, 12(6): 2463. https://doi.org/10.3390/su12062463

Bidura IGNG, Partama IBG, Utami IAP, Candrawati DPMA, Puspani E, Suasta IM, Warmadewi DA, Okarini IA, Wibawa AAP, Nuriyasa IM, Siti NW (2020). Effect of Moringa oleifera leaf powder in diets on laying hens performance, β-carotene, cholesterol, and minerals contents in egg yolk. In IOP Conference Series: Materials Science and Engineering (Vol. 823, No. 1, p. 012006). IOP Publishing. https://doi.org/10.1088/1757-899X/823/1/012006

Contreras ST (2019). Panorama y Mercado del Huevo de Gallina. Nota técnica. Obtenido de [descargado el 01-11-2022] https://cdn.www.gob.pe/uploads/document/file/438987/panorama__mercado_huevo_de_gallina.pdf

D’Mello JPF, Acamovic T (1989). Leucaena leucocephala in poultry nutrition—a review. Anim. Feed Sci. Technol. 26(1-2): 1-28. https://doi.org/10.1016/0377-8401(89)90003-5

Ebenebe CI, Anigbogu CC, Anizoba MA, Ufele NA (2013). Effect of various levels of Moringa leaf meal on the egg quality of ISA Brown breed of layers. Adv. Life Sci. Technol. 14(1): 35-49.

El-Hack A, Mohamed E, Samak DH, Noreldin AE, El-Naggar K, Abdo M (2018). Probiotics and plant-derived compounds as eco-friendly agents to inhibit microbial toxins in poultry feed: a comprehensive review. Environ. Sci. Pollut. Res. 25(32): 31971-31986. https://doi.org/10.1007/s11356-018-3197-2

El-Sheikh NI, El-Shazly ES, Abbas EA, Ghada IA (2015). Effect of moringa leaves on lipid content of table eggs in layer hens. Egypt. J. Chem. Environ. Health. 1: 291-302. https://doi.org/10.21608/EJCEH.2015.233103

FEDNA - Fundación Española Desarrollo Nutrición Animal (2010). De Blas, C., Mateos, G.G., García-Rebollar, P.G., Normas FEDNA de Composición y Valor Nutritivo de Alimentos para la Fabricación de Piensos Compuestos, 3rd ed. Fundación Española Desarrollo Nutrición Animal, Madrid, Spain

Gadzirayi CT, Mupangwa JF (2014). Feed intake and growth performance of indigenous chicks fed diets with Moringa oleifera leaf meal as a protein supplement during early brooding stage. Int. J. Poult. Sci. 13(3): 145-150. https://doi.org/10.3923/ijps.2014.145.150

Gakuya DW, Mbugua PN, Mwaniki SM, Kiama SG, Muchemi GM, Njuguna A (2014). Effect of supplementation of Moringa oleifera (LAM) leaf meal in layer chicken feed. Int. J. Poult. Sci. 13(7): 379-384. https://doi.org/10.3923/ijps.2014.379.384

Garcia RG, Gandra ERS, Burbarelli MFC, Valentim JK, Felix GA, Lopes BA Bacha FB, Melo CMF, Silva JP, Komiyama CM, Caldara FR (2021). Moringa oleifera: an alternative ingredient to improve the egg quality of Japanese quail. Arq. Bras. Med. Vet. Zootec. 73(3): 721-732. https://doi.org/10.1590/1678-4162-12191

Gayathri SL, Babu LK, Panda AK (2020). Effect of dietary supplementation of Moringa oleifera leaf meal on production performance and egg quality of vanaraja laying hens. Anim. Nutr. Feed Technol. 2(20): 279-287. https://doi.org/10.5958/0974-181X.2020.00025.6

Kakengi AMV, Kaijage JT, Sarwatt SV, Mutayoba SK, Shem MN, Fujihara T (2007). Effect of Moringa oleifera leaf meal as a substitute for sunflower seed meal on performance of laying hens in Tanzania. Livest. Res. Rural Dev. 19: 436-446

Lu W, Wang J, Zhang HJ, Wu SG, Qi GH (2016). Evaluation of Moringa oleifera leaf in laying hens: Effects on laying performance, egg quality, plasma biochemistry and organ histopathological indices. Ital. J. Anim. Sci. 15(4): 658-665. https://doi.org/10.1080/1828051X.2016.1249967

Mabusela SP, Nkukwana TT, Mokoma M, Muchenje V (2018). Layer performance, fatty acid profile and the quality of eggs from hens supplemented with Moringa oleifera whole seed meal. S. Afr. J. Anim. Sci. 48(2): 234-243. https://doi.org/10.4314/sajas.v48i2.4

Mendiola JM, Aguirre R (2015). Evaluación preliminar de la adición de moringa (Moringa oleifera) en la alimentación de pollos parrilleros. UCEBOL. Univ. Cienc. Soc. (14): 55-62. http://www.revistasbolivianas.ciencia.bo/pdf/ucs/n14/n14_a09.pdf

Ministerio de Desarrollo Agrario y Riego - MIDAGRI. 2022. Lima: Ministerio de Agricultura. [internet], [noveember 2022]. Disponible en: https://www.midagri.gob.pe/portal/datero/40-sector-agrario/situacion-de-las-actividades-de-crianza-y-producci/297-aves

N’nanle O, Tété‐Bénissan A, Nideou D, Onagbesan OM, Tona K (2020). Use of Moringa oleifera leaves in broiler production chain. 1‐Effect on Sasso breeder hens performances, internal quality of hatching eggs and serum lipids. Vet. Med. Sci. 6(3): 485-490. https://doi.org/10.1002/vms3.235

North MO, Bell DD (1993). Manual de producción avícola. México: 3ºed.

NRC- National Research Council. (1994). Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC.

Ochi EB, Elbushra ME, Fatur M, Abubakr O, Ismail HA (2015). Effect of Moringa (Moringa oleifera Lam) seeds on the performance and carcass characteristics of broiler chickens. J. Nat. Sci. Res. 5(8): 66-73. https://doi.org/10.7176/JNSR

Rajesh P, Kumari NN, Nagalakshmi D, Rao MH, Gurram S (2022). Dietary inclusion of Moringa oleifera leaf meal with enzyme supplementation on egg production and egg quality of laying hens. Indian J. Anim. Nutr. 39(1): 88-96. https://doi.org/10.5958/2231-6744.2022.00012.3

Raphaël KJ, Christian KT, Juliano RS, Lisita F, Soultan MY, Hervé MK, Alexis T (2015). Effects of Substituting Soybean with Moringa oleifera Meal in Diets on Laying and Eggs Quality Characteristics of KABIR Chickens. J. Anim. Res. Nutr. 1:4. https://doi.org/10.21767/2572-5459.100004

SENAMHI - Servicio Nacional de Meteorología e Hidrología del Perú. (2017). Ministerio del Ambiente. Available at: https://www.senamhi.gob.pe/. Accessed October 29, 2017.

Sharmin F, Sarker MSK, Sarker NR, Faruque S (2021). Dietary effect of Moringa oleifera on native laying hens’ egg quality, cholesterol and fatty-acid profile. Ital. J. Anim. Sci. 20(1): 1544-1553. https://doi.org/10.1080/1828051X.2021.1987846

Shen M, Li T, Qu L, Wang K, Hou Q, Zhao W, Wu P (2021). Effect of dietary inclusion of Moringa oleifera leaf on productive performance, egg quality, antioxidant capacity and lipid levels in laying chickens. Ital. J. Anim. Sci. 20(1): 2012-2021. https://doi.org/10.1080/1828051X.2021.1964387

Siti NW, Bidura IGNG, Mayuni SN, Suasta, IM, Wibawa AAPP, Utami IAP (2019). Effect of Moringa oleifera leaf powder in diets on feed digestibility and external egg quality characteristics in laying hens. Int. J. Fauna Biol. Stud. 6(4): 113-118.

Swain BK, Naik PK, Chakurkar EB, Singh NP (2017). Effect of supplementation of Moringa oleifera leaf meal (MOLM) on the performance of Vanaraja laying hens. Indian J. Anim. Sci. 87(3): 353-355.

Teteh A, Gbeassor M, Decuypere E, Tona K (2016). Effects of Moringa oleifera leaf on laying rate, egg quality and blood parameters. Int. J. Poult. Sci. 15(7): 277-282. https://doi.org/10.3923/ijps.2016.277.282

Tesfaye E, Alebachew W, Tamir B (2018). Performance of Koekoek Chicken Fed with Different Levels of Moringa oleifera Leaf Meal. J. Anim. Sci Res. 2 (3): 1-9. https://dx.doi.org/10.16966/2576-6457.115

Tessera GM (2016). Analysis of Some Mineral Compositions and Anti-Nutritional Factors of Moringa Stenopetala Leaf Powder. J. Nutr. Ecol. Food Res. 3(2): 139-143. https://doi.org/10.1166/jnef.2016.1125

Tutubalang K, Sebola NA, Mokoboki HK, Mosetle KQ, Manyeula F, Mabelebele M (2022). Inclusion of Moringa oleifera leaf meal in the diet of locally bred chickens: effects on growth performance, semen and hatchability traits. J. Appl. Anim. Res. 50(1): 239-245. https://doi.org/10.1080/09712119.2022.2058515

Umesh BU, Bharat Bhushan M, Ananda Manegar G, Ashok M, Satheesha GM, Venkatesha MM, Nataraju OR (2022). Effect of Replacing Moringa Olifera Leaf Meal for Soybean Meal on the production performance of commercial laying hens. Pharma innov. 11(3): 562-565

Valdivié M, Mesa O, Rodríguez B (2016). Utilización de dietas con harina de Moringa oleifera (tallos + hojas) en gallinas ponedoras. Cuba. J. Agric. Sci. 50(3): 445-454.

Voemesse K, Teteh A, Nideou D, N’nanlé O, Tété-Benissan A, Oke OE, Gbeassor M, Decuypere E, Tona K (2019). Effects of Moringa oleifera leave meal in the diet on layer performance, haematological and serum biochemical values. Europ. Poult. Sci. 83:1-12. https://doi.org/10.1399/eps.2019.263