Moringa oleifera Leaves as Eco-Friendly Feed Additive in Diets of Hy-Line Brown Hens during the Late Laying Period
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Birds, Design and Feed Preparation
2.2. Diet Analysis and Preparation of Dried Moringa oleifera Leaves
2.3. Production Performance Parameters
2.4. Egg Quality
2.5. Blood Sampling and Laboratory Analyses
2.6. Statistical Analysis
3. Results
3.1. Productive Performance and Ammonia Concentrations
3.2. Egg Quality
3.3. Serum Biochemical Parameters
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Laptev, G.Y.; Yildirim, E.A.; Ilina, L.A.; Filippova, V.A.; Kochish, I.I.; Gorfunkel, E.P.; Dubrovin, A.V.; Brazhnik, E.A.; Narushin, V.G.; Novikova, N.I.; et al. Effects of essential oils-based supplement and salmonella infection on gene expression, blood parameters, cecal microbiome, and egg production in laying hens. Animals 2021, 11, 360. [Google Scholar] [CrossRef]
- Rabelo-Ruiz, M.; Ariza-Romero, J.J.; Zurita-González, M.J.; Martín-Platero, A.M.; Baños, A.; Maqueda, M.; Valdivia, E.; Martínez-Bueno, M.; Peralta-Sánchez, J.M. Allium-Based phytobiotic enhances egg production in laying hens through microbial composition changes in ileum and cecum. Animals 2021, 11, 448. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Wareth, A.A.A.; Kehraus, S.; Südekum, K.-H. Peppermint and its respective active component in diets of broiler chickens: Growth performance, viability, economics, meat physicochemical properties, and carcass characteristics. Poult. Sci. 2019, 98, 3850–3859. [Google Scholar] [CrossRef] [PubMed]
- Tufarelli, V.; Baghban-Kanani, P.; Azimi-Youvalari, S.; Hosseintabar-Ghasemabad, B.; Slozhenkina, M.; Gorlov, I.; Seidavi, A.; Ayaşan, T.; Laudadio, V. Effects of Horsetail (Equisetum arvense) and Spirulina (Spirulina platensis) Dietary supplementation on laying hens productivity and oxidative status. Animals 2021, 11, 335. [Google Scholar] [CrossRef]
- Abdel-Wareth, A.A.A.; Metwally, A.E. Productive and physiological response of male rabbits to dietary supplementation with thyme essential oil. Animals 2020, 10, 1844. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Wareth, A.A.A.; Lohakare, J.D. Effect of dietary supplementation of peppermint on performance, egg quality, and serum metabolic profile of Hy-Line Brown hens during the late laying period. Anim. Feed Sci. Technol. 2014, 197, 114–120. [Google Scholar] [CrossRef]
- Abdel-Wareth, A.A.A. Effect of dietary supplementation of thymol, synbiotic and their combination on performance, egg quality and serum metabolic profile of Hy- Line Brown hens. Br. Poult. Sci. 2016, 57, 114–122. [Google Scholar] [CrossRef] [PubMed]
- Brenes, A.; Roura, E. Essential oils in poultry nutrition: Main effects and modes of action. Anim. Feed Sci. Technol. 2010, 158, 1–14. [Google Scholar] [CrossRef]
- Lee, K.-W.; Everts, H.; Kappert, H.J.; Van der Kuilen, J.; Lemmers, A.G.; Frehner, M.; Beynen, A.A. Growth performance, intestinal viscosity, fat digestibility and plasma cholesterol in broiler chickens fed a rye-containing diet without or with essential oil components. Int. J. Poult. Sci. 2004, 3, 613–618. [Google Scholar]
- Liu, M.; Lu, Y.; Gao, P.; Xie, X.; Li, D.; Yu, D.; Yu, M. Effect of curcumin on laying performance, egg quality, endocrine hormones, and immune activity in heat-stressed hens. Poult. Sci. 2020, 99, 2196–2202. [Google Scholar] [CrossRef]
- Ahmed, S.T.; Islam, M.; Mun, H.-S.; Sim, H.-J.; Kim, Y.-J.; Yang, C.-J. Effects of Bacillus amyloliquefaciens as a probiotic strain on growth performance, cecal microflora, and fecal noxious gas emissions of broiler chickens. Poult. Sci. 2014, 93, 1963–1971. [Google Scholar] [CrossRef]
- Wang, H.; Ni, X.; Qing, X.; Liu, L.; Xin, J.; Luo, M.; Khalique, A.; Dan, Y.; Pan, K.; Jing, B.; et al. Probiotic Lactobacillus johnsonii BS15 Improves blood parameters related to immunity in broilers experimentally infected with subclinical necrotic enteritis. Front. Microbiol. 2018, 9, 49. [Google Scholar] [CrossRef] [Green Version]
- Kristensen, H.H.; Wathes, C.M. Ammonia and poultry welfare: A review. World’s Poult. Sci. J. 2000, 56, 235–245. [Google Scholar] [CrossRef]
- Ferket, P.R.; van Heugten, E.; van Kempen, T.A.T.G.; Angel, R. Nutritional strategies to reduce environmental emissions from nonruminants. J. Anim. Sci. 2002, 80, E168–E182. [Google Scholar] [CrossRef]
- Park, J.W.; Jeong, J.S.; Lee, S.I.; Kim, I.H. Effect of dietary supplementation with a probiotic (Enterococcus faecium) on production performance, excreta microflora, ammonia emission, and nutrient utilization in ISA brown laying hens. J. Appl. Poult. Res. 2016, 95, 2829–2835. [Google Scholar] [CrossRef] [PubMed]
- Ushida, K.; Hashizume, K.; Miyazaki, K.; Kojima, Y.; Takakuwa, S. Isolation of Bacillus SP. as a volatile sulfur-degrading bacterium and its application to reduce the fecal odor of pig. Asian Aust. J. Anim. Sci. 2003, 16, 1795–1798. [Google Scholar] [CrossRef]
- Hippenstiel, F.; Abdel-Wareth, A.A.A.; Kehraus, S.; Südekum, K.-H. Effects of selected herbs and essential oils, and their active components on feed intake and performance of broilers—A review. Arch. Fur Geflugelkunde 2011, 75, 226–234. [Google Scholar]
- Makkar, H.P.S.; Becker, K. Nutritional value and antinutritional components of whole and ethanol extract of Moringa oleifera leaves. Anim. Feed Sci. Technol. 1996, 63, 211–228. [Google Scholar] [CrossRef]
- Marrufo, T.; Nazzaro, F.; Mancini, E.; Fratianni, F.; Coppola, R.; Martino, L.D.; Agostinho, A.B.; Feo, V.D. Chemical composition and biological activity of the essential oil from leaves of Moringa oleifera Lam. cultivated in Mozambique. Molecules 2013, 18, 10989–11000. [Google Scholar] [CrossRef] [Green Version]
- Briones, J.; Leung, A.; Bautista, N.; Golin, S.; Caliwag, N.; Carlos, M.A.; Guevarra, J.; Miranda, J.; Guevarra, J.K.; Pili, N.L.; et al. Utilization of Moringa oleifera Lam. in animal production. Acta Hortic. 2017, 1158, 54. [Google Scholar] [CrossRef]
- Lu, W.; Wang, J.; Zhang, H.J.; Wu, S.G.; Qi, G.H. Evaluation of Moringa oleifera leaf in laying hens: Effects on laying performance, egg quality, plasma biochemistry and organ histopathological indices. Ital. J. Anim. Sci. 2016, 15, 658–665. [Google Scholar] [CrossRef] [Green Version]
- NRC [National Research Council]. Nutrient Requirements of Poultry, 9th revised ed.; National Academic Press: Washington, DC, USA, 1994; p. 155.
- AOAC International. Official Methods of Analysis, 18th ed.; American Association of Official Analytical Chemists: Arlington, TX, USA, 2006. [Google Scholar]
- Haugh, R.R. The Haugh unit for measuring egg quality. U. S. Egg Poult. Mag. 1937, 43, 552–555. [Google Scholar]
- SAS Institute. User’s Guide: Statistics. Version 9.2; SAS Institute, Inc.: Cary, NC, USA, 2009. [Google Scholar]
- Shousha, W.G.; Aboulthana, W.M.; Salama, A.H.; Saleh, M.H.; Essawy, E.A. Evaluation of the biological activity of Moringa oleifera leaves extract after incorporating silver nanoparticles, in vitro study. Bull. Natl. Res. Cent. 2019, 43, 212. [Google Scholar] [CrossRef] [Green Version]
- Mahfuz, S.; Piao, X.S. Application of Moringa (Moringa oleifera) as natural feed supplement in poultry diets. Animals 2019, 9, 431. [Google Scholar] [CrossRef] [Green Version]
- Voemesse, K.; Teteh, A.; Nideou, D.; N’nanle, O.; Gbeassor, M.; Decuypere, E.; Tona, K. Effect of Moringa oleifera leaf meal on growth performance and blood parameters of egg type chicken during juvenile growth. Int. J. Poult. Sci. 2018, 17, 154–159. [Google Scholar] [CrossRef] [Green Version]
- Moreki, J.C.; Gabanakgosi, K. Potential use of Moringa oleifera in poultry diets. Glob. J. Anim. Sci. Res. 2014, 2, 109–115. [Google Scholar]
- Abou-Elezz, F.M.K.; Sarmiento-Franco, L.; Santos-Ricalde, R.; Solorio-Sanchez, J.F. The nutritional effect of Moringa oleifera fresh leaves as feed supplement on Rhode Island Red hen egg production and quality. Trop. Anim. Health Prod. 2012, 44, 1035–1040. [Google Scholar] [CrossRef]
- Ashour, E.A.; El-Kholy, M.S.; Alagawany, M.; Abd El-Hack, M.E.; Mohamed, L.A.; Taha, A.E.; El Sheikh, A.I.; Laudadio, V.; Tufarelli, V. 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 2020, 12, 2463. [Google Scholar] [CrossRef] [Green Version]
- Olugbemi, T.S.; Mutayoba, S.K.; Lekule, F.P. Evaluation of Moringa oleifera leaf meal inclusion in cassava chip-based diets fed to laying birds. Livest. Res. Rural Dev. 2010, 22, 27–37. [Google Scholar]
- Sethiya, N.K. Review on natural growth promoters available for improving gut health of poultry: An alternative to antibiotic growth promoters. Asian J. Poult. Sci. 2016, 10, 1–29. [Google Scholar] [CrossRef]
- Hong, J.-C.; Steiner, T.; Aufy, A.; Lien, T.-F. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livest. Sci. 2012, 144, 253–262. [Google Scholar] [CrossRef]
- Chepete, H.J.; Xin, H.; Mendes, L.B.; Li, H.; Bailey, T.B. Ammonia emission and performance of laying hens as affected by different dosages of Yucca schidigera in the diet. J. Appl. Poult. Res. 2012, 21, 522–530. [Google Scholar] [CrossRef]
- Nadia, L.R.; Hassan, R.A.; Qota, E.; Fayek, H. Effect of natural antioxidant on oxidative stability of eggs and productive and reproductive performance of laying hens. Int. J. Poult. Sci. 2008, 7, 134–150. [Google Scholar] [CrossRef] [Green Version]
- Özek, K.; Wellmann, K.T.; Ertekin, B.; Tarim, B. Effects of dietary herbal essential oil mixture and organic acid preparation on laying traits, gastro-intestinal tract characteristics, blood parameters and immune response of laying hens in a hot summer season. J. Anim. Feed Sci. 2011, 20, 575–586. [Google Scholar] [CrossRef]
- Williams, K.C. Some factors affecting albumen quality with particular reference to Haugh unit score. World’s Poult. Sci. J. 1992, 48, 5–16. [Google Scholar] [CrossRef]
- Ahmad, S.; Khalique, A.; Pasha, T.N.; Mehmood, S.; Hussain, K.; Ahmad, S.; Shaheen, M.S.; Naeem, M.; Shafiq, M. Effect of Moringa oleifera (Lam.) pods as feed additive on egg antioxidants, chemical composition and performance of commercial layers. South Afr. J. Anim. Sci. 2017, 47, 864–873. [Google Scholar] [CrossRef] [Green Version]
- Gupta, A.; Gautam, M.K.; Singh, R.K.; Kumar, M.V.; Rao, C.V.; Goel, R.K.; Anupurba, S. Immunomodulatory effect of Moringa oleifera Lam. extract on cyclophosphamide induced toxicity in mice. Indian J. Exp. Biol. 2010, 48, 1157–1160. [Google Scholar] [PubMed]
- Azzam, M.M.M.; Dong, X.Y.; Xie, P.; Wang, C.; Zou, X.T. The effect of supplemental l-threonine on laying performance, serum free amino acids, and immune function of laying hens under high-temperature and high-humidity environmental climates. J. Appl. Poult. Res. 2011, 20, 361–370. [Google Scholar] [CrossRef]
- Bozkurt, M.; Hippenstiel, F.; Abdel-Wareth, A.A.A.; Kehraus, S.; Küçükyilmaz, K.; Südekum, K.-H. Effects of selected herbs and essential oils on performance, egg quality and some metabolic activities in laying hens—A review. Euro. Poult. Sci. 2014, 78, 15. [Google Scholar]
- Ghasi, S.; Nwobodo, E.; Ofilis, J.O. Hypocholesterolemic effects of crude extract of the leaf of Moringa oleifera Lam in high-fat diet fed Wistar rats. J. Ethnopharmacol. 2000, 69, 21–25. [Google Scholar] [CrossRef]
- Maheshwari, K.; Yadav, R.K.; Malhotra, J.; Dhawan, N.G.; Mohan, L. Fascinating nutritional, prophylactic, therapeutic and socio-economic reconcile attributable to drum stick tree (Moringa oleifera Lam.). Glob. J. Med. Res. B Pharm. Drug Discov. Toxicol. Med. 2014, 14, 11–22. [Google Scholar]
- Jain, P.G.; Patil, S.D.; Haswani, N.G.; Girase, M.V.; Surana, S.J. Hypolipidemic activity of Moringa oleifera Lam., Moringaceae, on high fat diet induced hyperlipidemia in albino rats. Rev. Bras. Framacogn. 2010, 20, 969–973. [Google Scholar] [CrossRef]
- Alnidawi, A.; Ali, F.; Abdelgayed, S.; Ahmed, F.; Farid, M. Moringa oleifera leaves in broiler diets: Effect on chicken performance and health. Food Sci. Qual. Manag. 2016, 58, 40–48. [Google Scholar]
- Enemor, V.H.A.; Anosike, J.C.; Nwoke, B.E.B.; Chikezie, P.C. Serum aminotransferase and bilirubin levels in malaria patients. Int. J. Nat. Appl. Sci. 2005, 1, 85–89. [Google Scholar] [CrossRef]
- Halaby, M.S.; Elmetwaly, M.M.; Omar, A.A.A. Effect of Moringa Oleifera on serum lipids and kidney function of hyperlipidemic rats. J. Appl. Sci. Res. 2013, 9, 5189–5198. [Google Scholar]
- Divya, A.B.; Mandal, A.; Biswas, A.; Yadav, A.S.; Biswas, A.K. Effect of dietary Moringa oleifera leaves powder on growth performance, blood chemistry, meat quality and gut microflora of broiler chicks. Anim. Nutr. Feed Tech. 2014, 14, 349–357. [Google Scholar] [CrossRef]
Ingredients | % |
---|---|
Yellow corn | 68.15 |
Soybean meal 44% CP | 17.79 |
Soybean oil | 0.81 |
Corn gluten 60% CP | 2.5 |
Di-calcium phosphate | 1.92 |
Limestone | 7.97 |
Premix * | 0.21 |
Dl-Methionine | 0.25 |
Choline chloride (50%) | 0.4 |
Total | 100 |
Determined analysis, | % |
Dry matter | 89 |
Ash | 11.8 |
Crude protein | 18.5 |
Ether extract | 4.21 |
Calcium | 3.73 |
Phosphorus | 0.58 |
Gross energy (MJ/kg) | 16.3 |
Retention Time | g/100 g Essential Oil | Compounds |
---|---|---|
17.75 | 0.71 | thymol |
25.14 | 1.68 | α-curcumene |
26.17 | 0.40 | β-bisabolene |
26.82 | 1.6 | β-sesquiphellandrene |
29.05 | 0.45 | caryophyllene oxide |
29.16 | 1.03 | p-cymene |
30.14 | 0.94 | trans-nuciferol |
30.42 | 5.51 | hexacosane |
31.11 | 0.63 | 7-epi-cis-sesquisabinene hydrate |
32.55 | 55.46 | Ar-turmerone |
32.63 | 5.73 | tumerone |
33.84 | 13.94 | curlone |
35.33 | 0.89 | heptacosane |
38.54 | 1.88 | 6-dodecanone |
40.93 | 0.97 | farnesyl acetone |
47.11 | 1.33 | phytol |
55.76 | 3.23 | 14-β-H-PREGNA |
57.28 | 3.62 | tetrapentacontane, 1,54-dibromo |
Items | Moringa oleifera Leaves (g/kg) | SEM 1 | p Value | ||||
---|---|---|---|---|---|---|---|
0 | 3 | 6 | 9 | Linear | Quadratic | ||
64–68 weeks of age | |||||||
Egg weight, (g/hen/day) | 60.89 | 63.58 | 64.75 | 63.49 | 0.57 | 0.008 | 0.009 |
Egg mass, (g/hen/day) | 49.46 | 53.47 | 56.02 | 54.41 | 0.61 | <0.001 | 0.002 |
Hen-day production, (%) | 81.24 | 84.09 | 86.53 | 85.67 | 0.81 | 0.003 | 0.042 |
Feed intake, (g/hen/day) | 105.6 | 103.7 | 106.0 | 105.3 | 1.01 | 0.773 | 0.532 |
Feed conversion ratio | 2.136 | 1.939 | 1.893 | 1.937 | 0.03 | 0.002 | 0.006 |
68–72 weeks of age | |||||||
Egg weight, (g/hen/day) | 60.89 | 63.23 | 65.92 | 63.98 | 0.42 | <0.001 | 0.001 |
Egg mass, (g/hen/day) | 49.64 | 53.37 | 57.46 | 54.81 | 0.29 | <0.001 | 0.001 |
Hen-day production, (%) | 81.52 | 84.42 | 87.18 | 85.67 | 0.53 | <0.001 | 0.003 |
Feed intake, (g/hen/day) | 105.7 | 102.6 | 105.3 | 105.0 | 1.08 | 0.894 | 0.252 |
Feed conversion ratio | 2.128 | 1.923 | 1.833 | 1.916 | 0.02 | 0.001 | 0.001 |
64–72 weeks of age | |||||||
Egg weight, (g/hen/day) | 61.43 | 63.93 | 65.37 | 64.31 | 0.45 | 0.001 | 0.005 |
Egg mass, (g/hen/day) | 50.70 | 54.15 | 57.67 | 55.29 | 0.62 | <0.001 | 0.002 |
Hen-day production, (%) | 82.52 | 84.71 | 88.23 | 85.91 | 0.81 | 0.006 | 0.024 |
Feed intake, (g/hen/day) | 106.8 | 104.6 | 106.7 | 106.1 | 1.68 | 0.997 | 0.664 |
Feed conversion ratio | 2.106 | 1.932 | 1.851 | 1.920 | 0.033 | 0.002 | 0.006 |
Ammonia, g/100 g excreta | 6.044 | 3.919 | 2.743 | 3.585 | 0.266 | <0.001 | <0.001 |
Items | Moringa oleifera Leaves (g/kg) | SEM 1 | p Value | ||||
---|---|---|---|---|---|---|---|
0 | 3 | 6 | 9 | Linear | Quadratic | ||
68 weeks of age | |||||||
Haugh units, score | 81.23 | 85.01 | 89.01 | 84.56 | 1.079 | 0.004 | 0.001 |
Shell thickness (mm) | 0.378 | 0.396 | 0.408 | 0.399 | 0.043 | 0.006 | 0.014 |
Shell (%) | 10.75 | 11.62 | 12.84 | 11.64 | 0.382 | 0.028 | 0.061 |
Albumen (%) | 62.57 | 61.33 | 60.08 | 60.78 | 0.653 | 0.127 | 0.063 |
Yolk (%) | 26.68 | 27.25 | 27.08 | 27.38 | 0.451 | 0.156 | 0.146 |
72 weeks of age | |||||||
Haugh units, score | 82.13 | 86.11 | 89.51 | 85.76 | 1.081 | 0.001 | 0.001 |
Shell thickness (mm) | 0.381 | 0.399 | 0.409 | 0.401 | 0.054 | 0.001 | 0.024 |
Shell (%) | 10.85 | 11.73 | 12.88 | 11.74 | 0.883 | 0.013 | 0.032 |
Albumen (%) | 62.67 | 61.21 | 60.04 | 60.56 | 0.991 | 0.063 | 0.451 |
Yolk (%) | 26.48 | 27.16 | 27.18 | 27.7 | 0.654 | 0.076 | 0.236 |
Items | Moringa oleifera Leaves (g/kg) | SEM 1 | p Value | ||||
---|---|---|---|---|---|---|---|
0 | 3 | 6 | 9 | Linear | Quadratic | ||
Cholesterol (mg/dL) | 154.41 | 144.51 | 137.36 | 142.70 | 1.260 | 0.001 | 0.001 |
Triglycerides (mg/dL) | 138.29 | 128.13 | 124.17 | 128.91 | 0.556 | 0.001 | 0.004 |
ALT (U/L) | 29.69 | 25.50 | 21.51 | 22.97 | 0.824 | 0.001 | 0.001 |
AST (U/L) | 67.79 | 61.56 | 57.01 | 61.19 | 0.992 | 0.001 | 0.001 |
Creatinine (mg/dL) | 0.624 | 0.456 | 0.401 | 0.415 | 0.009 | 0.001 | 0.001 |
Uric acid (mg/dL) | 4.253 | 3.574 | 2.710 | 3.490 | 0.207 | 0.001 | 0.001 |
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Abdel-Wareth, A.A.A.; Lohakare, J. Moringa oleifera Leaves as Eco-Friendly Feed Additive in Diets of Hy-Line Brown Hens during the Late Laying Period. Animals 2021, 11, 1116. https://doi.org/10.3390/ani11041116
Abdel-Wareth AAA, Lohakare J. Moringa oleifera Leaves as Eco-Friendly Feed Additive in Diets of Hy-Line Brown Hens during the Late Laying Period. Animals. 2021; 11(4):1116. https://doi.org/10.3390/ani11041116
Chicago/Turabian StyleAbdel-Wareth, Ahmed A. A., and Jayant Lohakare. 2021. "Moringa oleifera Leaves as Eco-Friendly Feed Additive in Diets of Hy-Line Brown Hens during the Late Laying Period" Animals 11, no. 4: 1116. https://doi.org/10.3390/ani11041116