REVIEW PAPER
Dietary supplementation with tomato waste to improve
performance and egg quality of laying hens: a meta-analysis
1
National Research and Innovation Agency, Post-doctoral of the Research Center for Animal Husbandry,
16915, Bogor, Indonesia
2
Universitas Muhammadiyah Kotabumi, Faculty of Agricultural and Animal Science, 34517, Kotabumi, Indonesia
3
National Research and Innovation Agency, Research Center for Animal Husbandry, 16915, Bogor, Indonesia
4
IPB University, Animal Feed and Nutrition Modelling Research Group (AFENUE), 16680, Bogor, Indonesia
5
National Research and Innovation Agency, Research Collaboration Center for Biomass and Biorefinery between BRIN
and Universitas Padjadjaran, 16911, Bogor, Indonesia
6
National Research and Innovation Agency, Research Center for Pharmaceutical Ingredients and Traditional Medicine,
16915, Bogor, Indonesia
7
Universitas Andalas, Faculty of Animal Science, 25175, Padang, Indonesia
Publication date: 2023-04-19
Corresponding author
A. Sofyan
Research Center for Animal Husbandry, National Research and Innovation Agency, 16915, Bogor, West Java, Indonesia
Research Center for Animal Husbandry, National Research and Innovation Agency, 16915, Bogor, West Java, Indonesia
J. Anim. Feed Sci. 2023;32(3):221-232
KEYWORDS
TOPICS
ABSTRACT
A meta-analysis was conducted to determine the effect of adding tomato waste to the diet of laying hens on their performance, egg quality,
and blood parameters. A total of 22 articles were selected from five scientific databases such as Scopus, PubMed, ScienceDirect, Web of Science, and Directory of Open Access Journals. R software version 4.2.0, with supporting libraries, including lme4 and lsmeans (least-squares means test), was used for modelling and statistical analysis. The results of meta-analysis showed that the addition of tomato waste to laying hen rations significantly increased feed intake (P < 0.01) and tended to correlate with a quadratic pattern of hen-day egg production (HDEP) (P < 0.061) and egg mass (P < 0.075); however, eggshell strength decreased significantly (P < 0.01). Our findings also demonstrated a significant effect on egg-yolk colour, as assessed by a quadratic pattern (P < 0.01). The lycopene content in egg yolk increased significantly (P < 0.05). Tomato waste supplementation had a significant (P < 0.05) effect on total triglyceride and cholesterol levels in blood serum, which followed a quadratic pattern. This meta-analysis has confirmed that feeding tomato waste to laying
hens exerts positive effects on animal performance and egg quality.
FUNDING
The first author would like to thank the National
Research and Innovation Agency, Indonesia,
for funding the study through the “Postdoctoral
Program”, contract number 64/II/HK/2022.
CONFLICT OF INTEREST
The Authors declare that there is no conflict of
interest.
REFERENCES (79)
1.
Agarwal S., Rao A.V., 1998. Tomato lycopene and low density lipoprotein oxidation: a human dietary intervention study. Lipids 33, 981–984, https://doi.org/10.1007/s117-4...
2.
Agarwal S., Rao A.V., 2000. Tomato lycopene and its role in human health and chronic diseases. Can. Med. Assoc. J. 163, 739–744
3.
Akdemir F., Orhan, C. Sahin N., Sahin K., Hayirli A., 2012. Tomato powder in laying hen diets: effects on concentrations of yolk carotenoids and lipid peroxidation. Br. Poult. Sci. 53, 675–680, https://doi.org/10.1080/000716...
4.
Al-Souti A., Gallardo W., Claereboudt M., Mahgoub O., 2019. Attractability and palatability of formulated diets incorporated with chicken feather and algal meals for juvenile gilthead seabream, Sparus aurata. Aquacult. Rep. 14, 100199, https://doi.org/-10.1016/j.aqr...
5.
Alvi S.S., Ansari I.A., Khan I., Iqbal J., Khan M.S., 2017. Potential role of lycopene in targeting proprotein convertase subtilisin/kexin type-9 to combat hypercholesterolemia. Free Radic. Biol. Med. 108, 394–403, https://doi.org/10.1016/j.free...
6.
Alvi S.S., Iqbal D., Ahmad S., Khan M. S., 2016. Molecular rationale delineating the role of lycopene as a potent HMG-CoA reductase inhibitor: in vitro and in silico study. Nat. Prod. Res. 30, 2111–2114, https://doi.org/10.1080/147864...
7.
An B., Choo W., Kang C., Lee J., Lee, K., 2019. Effects of dietary lycopene or tomato paste on laying performance and serum lipids in laying hens and on malondialdehyde content in egg yolk upon storage. J. Poult. Sci. 56, 52–57, https://doi.org/10.2141/jpsa.0...
8.
Bala D.A., Matur E., Ekiz E.E., Akyazi I., Ergen E., Erek M., Atmaca G., Eseceli H., Keten M., 2020. Can dried tomato and red pepper powder be used as a dietary supplement to strengthen defence systems and production performance in laying hens? Eur. Poult. Sci. 84, 1–15, https://doi.org/10.1399/eps.20...
9.
Basmacioglu H., Ergul M., 2005. Research on the factors affecting cholesterol content and some other characteristics of eggs in laying hens, the effects of genotype and rearing system. Turk. J. Vet. Anim. Sci. 29, 157–164
10.
Basuny A.M., Gaafar A.M., Arafat S.M., 2009. Tomato lycopene is a natural antioxidant and can alleviate hypercholesterolemia. Afr. J. Biotechnol. 8, 6627–6633
11.
Bin-Jumah M.N., Nadeem M.S., Gilani S.J., Mubeen B., Ullah I., Alzarea S.I., Ghoneim M.M., Alshehri S., Al-Abbasi F.A., Kazmi I., 2022. Lycopene: a natural arsenal in the war against oxidative stress and cardiovascular diseases. Antioxidants 11, 1–21, https://doi.org/10.3390/antiox...
12.
Brenes A., Viveros A., Chamorro S., Arija I., 2016. Use of polyphenol-rich grape by-products in monogastric nutrition. A review. Anim. Feed Sci. Technol. 211, 1–17, https://doi.org/10.1016/j.anif...
13.
Calislar S., Uygur G., 2010. Effects of dry tomato pulp on egg yolk pigmentation and some egg yield characteristics of laying hens. J. Anim. Vet. Adv. 9, 96–98, https://doi.org/10.3923/javaa....
14.
Chauhan K., Sharma S., Agarwal N., Chauhan B., 2011. Lycopene of tomato fame: its role in health and disease. Int. J. Pharm. Sci. Rev. Res. 10, 99–15
15.
Cooperstone J.L., Francis D.M., Schwartz S.J., 2016. Thermal processing differentially affects lycopene and other carotenoids in cis-lycopene containing, tangerine tomatoes. Food Chem. 210, 466–472, https://doi.org/10.1016/j.food...
16.
Deehan, E.C., Zhang Z., Riva A., et al. 2022. Elucidating the role of the gut microbiota in the physiological effects of dietary fiber. Microbiome 10, 77, https://doi.org/10.1186/s40168...
17.
Dotas D., Zamanidis S., Balios J., 1999. Effect of dried tomato pulp on the performance and egg traits of laying hens. Br. Poult. Sci. 40, 695–697, https://doi.org/10.1080/000716...
18.
Elkin R.G., Yan Z., Zhong Y., Donkin S.S., Buhman K.K., Story J.A., Turek J.J., Porter R.E., Anderson M., Homan R., Newton R.S., 1999. Select 3-hydroxy-3-methylglutaryl-coenzyme a reductase inhibitors vary in their ability to reduce egg yolk cholesterol levels in laying hens through alteration of hepatic cholesterol biosynthesis and plasma VLDL composition. J. Nutr. 129, 1010–1019, https://doi.org/10.1093/jn/129...
19.
FAOSTAT, 2022. Food and Agriculture Organization of the United Nations. Crops and Livestock Products. https://www.fao.org/faostat/en...
20.
Fuhrman B., Elis A., Aviram M., 1997. Hypocholesterolemic effect of lycopene and β-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages. Biochem. Biophys. Res. Commun. 233, 658–662, https://doi.org/10.1006/bbrc.1...
21.
Gümüşay Ö.A., Borazan A.A., Ercal N., Demirkol O., 2015. Drying effects on the antioxidant properties of tomatoes and ginger. Food Chem. 173, 156–162, https://doi.org/10.1016/j.food...
22.
Habanabashaka M., Sengabo M., Oladunjoye I.O., 2014. Effect of tomato waste meal on lay performance, egg quality, lipid profile and carotene content of eggs in laying hens. Iran. J. Appl. Sci. 4, 555–559
23.
Handayani U.F., Wizna, Suliansyah I., Rizal Y., Mahata M.E., 2018. Effect of heating method on lycopene, dry matter and nutrient content of tomato (Lycopersicon esculentum) waste as laying hen feed. Int. J. Poult. Sci. 17, 63–70, https://doi.org/10.3923/ijps.2...
24.
Hsu W.T., Chiang C.J., Chao Y.P., Chang C.H., Lin L.J., Yu B., Lee T.T., 2015. Effects of recombinant lycopene dietary supplement on the egg quality and blood characteristics of laying quails. J. Biosci. Bioeng. 120, 539–543, https://doi.org/10.1016/j.jbio...
25.
Jafari M., Pirmohammadi R., Bampidis V., 2006. The use of dried tomato pulp in diets of laying hens. Int. J. Poult. Sci. 5, 618–622, https://doi.org/10.3923/ijps.2...
26.
Jalalinasab A., Nobakht A., Razzaghzadeh S., 2014. The Effects of different levels of tomato pomace and processing methods on production performance and blood metabolites of native laying hens. Iran. J. Appl. Sci. 4, 379–385
27.
Jha R., Mishra P., 2021. Dietary fiber in poultry nutrition and their effects on nutrient utilization, performance, gut health, and on the environment: a review. J. Anim. Sci. Biotechnol. 12, 51, https://doi.org/10.1186/s40104...
28.
Jiang H., Wang Z., Ma Y., Qu Y., Lu X., Luo H., 2015. Effects of dietary lycopene supplementation on plasma lipid profile, lipid peroxidation and antioxidant defense system in feedlot bamei lamb. Asian Australas. J. Anim. Sci. 28, 958–965, https://doi.org/10.5713/ajas.1...
29.
Kaspers B., 2016. An egg a day – the physiology of egg formation. Lohmann Inf. 50, 12–17
30.
Kim J.H., Hong S.T., Lee H.S., Kimt H.J., 2004. Oral administration of pravastatin reduces egg cholesterol but not plasma cholesterol in laying hens. Poult. Sci. 83, 1539–1543, https://doi.org/10.1093/ps/83....
31.
Laranjeira, T., Costa A., Faria-Silva C., Ribeiro, D., de Oliveira J.M.P.F., Simões S., Ascenso A., 2022. Sustainable valorization of tomato by-products to obtain bioactive compounds: their potential in inflammation and cancer management. Molecules 27, 1701, https://doi.org/10.3390/molecu...
32.
Lee C., Kim J.H., Kil D.Y., 2022. Comparison of stress biomarkers in laying hens raised under a long-term multiple stress condition. Poult. Sci. 101, 101868, https://doi.org/10.1016/j.psj....
33.
Leke. J.R., Mandey J.S., Nangoy F.J., 2015. Nutrients and cholesterol of eggs affected by dried tomato meal in laying hens diet. Int. J. Adv. Sci. Eng. Inf. Technol. 5, 178–180, https://doi.org/10.18517/ijase...
34.
Mahata M.E., Hidayat T., Nurhuda G.A., Rizal Y., Ardi., 2020. Performance and egg quality of laying hens fed with boiled tomato waste powder. J. World’s Poult. Res. 10, 12–16, https://doi.org/10.36380/JWPR....
35.
Mahata M.E., Rizal Y., Ardi, Hermansyah D., Nurhuda G.A., 2016. Effects of boiled tomato waste utilization in the diet on serum lipid profile and egg quality of laying-hens. Int. J. Poult. Sci. 15, 493–496, https://doi.org/10.3923/ijps.2...
36.
Mansoori B., Modirsanei M., Radfar M., Kiaei M.M., Farkhoy M., Honarzad J., 2008. Digestibility and metabolisable energy values of dried tomato pomace for laying and meat type cockerels. Anim. Feed Sci. Technol. 141, 384–390, https://doi.org/10.1016/j.anif...
37.
Meroni E., Raikos V., 2018. Lycopene in beverage emulsions: optimizing formulation design and processing effects for enhanced delivery. Beverages 4, 14, https://doi.org/10.3390/bevera...
38.
Mnisi C.M., Mhlongo G., Manyeula F., 2022. Fruit pomaces as functional ingredients in poultry nutrition: a review. Front. Anim. Sci. 3, 40, https://doi.org/10.3389/fanim....
39.
Moher D., Liberati A., Tetzlaff J., Altman D.G., 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Br. Med. J. 339, b2535, https://doi.org/10.1136/bmj.b2...
40.
Mulkalwar S.A., Munjal N.S., More U.K., More B., Chaudhari A.B., Dewda P.R., 2012. Effect of purified lycopene on lipid profile, antioxidant enzyme and blood glucose in hyperlipidemic rabbits. Am. J. PharmTech Res. 2, 460–470
41.
Nakagawa S., Johnson P.C.D., Schielzeth H., 2017. The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J. R. Soc. Interface 14, 20170213, https://doi.org/10.1098/rsif.2...
42.
Nakagawa S., Schielzeth H., 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142, https://doi.org/10.1111/j.2041...
43.
Nguyen T.M., Sawyer J.K., Kelley K.L., Davis M.A., Rudel L.L., 2012. Cholesterol esterification by ACAT2 is essential for efficient intestinal cholesterol absorption: evidence from thoracic lymph duct cannulation. J. Lipid Res. 53, 95–104, https://doi.org/10.1194/jlr.M0...
44.
Nobakht A., Safamehr A.R., 2007. The effects of inclusion different levels of dried tomato pomace in laying hens diets on performance and plasma and egg yolk cholesterol contents. J. Anim. Vet. Adv. 6, 1101–1106
45.
Olson J.B., Ward N.E., Koutsos E.A., 2008. Lycopene incorporation into egg yolk and effects on laying hen immune function. Poult. Sci. 87, 2573–2580, https://doi.org/10.3382/ps.200...
46.
Orhan C., Kucuk O., Sahin N., Tuzcu M., Sahin K., 2021. Lycopene supplementation does not change productive performance but lowers egg yolk cholesterol and gene expression of some cholesterol-related proteins in laying hens. Br. Poult. Sci. 62, 227–234, https://doi.org/10.1080/000716...
47.
Palozza P., Catalano A., Simone R.E., Mele M.C., Cittadini A., 2012. Effect of lycopene and tomato products on cholesterol metabolism. Ann. Nutr. Metab. 61, 126–134, https://doi.org/10.1159/000342...
48.
Post J., Rebel J.M., ter Huurne A.A., 2003. Physiological effects of elevated plasma corticosterone concentrations in broiler chickens. An alternative means by which to assess the physiological effects of stress. Poult. Sci. 82, 1313–1318, https://doi.org/10.1093/ps/82....
49.
R Core Team, 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna (Austria)
50.
Rakonjac S., Bogosavljević-Bošković S., Pavlovski Z., Škrbić Z., Dosković V., Petrović M.D., Petričević V., 2014. Laying hen rearing systems: a review of major production results and egg quality traits. Worlds Poult. Sci. J. 70, 93–104, https://doi.org/10.1017/S00439...
51.
Rao A.V., Ray M.R., Rao L.G., 2006. Lycopene. Adv. Food Nutr. Res. 51, 99–164, https://doi.org/10.1016/S1043-...
52.
Reboul E., 2019. Mechanisms of carotenoid intestinal absorption: Where do we stand? Nutrients 11, 838, https://doi.org/10.3390/nu1104...
53.
Rodriguez-Amaya D.B., 2015. Carotenes and xanthophylls as antioxidants. In: F. Shahidi (Editor). Handbook of Antioxidants for Food Preservation. Elselvier Inc. Amsterdam (Netherlands), pp. 17–50, https://doi.org/10.1016/B978-1...
54.
Rotolo L., Strazzullo G., Pagella M., Brugiapaglia A., Pozzo L., Schiavone A., 2010. Effect of a tomato extract-supplemented diet on egg yolk pigmentation and lycopene transfer efficiency. Ital. J. Food Sci. 22, 180–185
55.
Saed Z.J.M., Abdulateef S.M., Mohammed T.T., AL-Khalani F.M.H., 2018. Effect of dried tomato pomace as alternative to vitamin C supplemented diets in hematological indices and oxidative stability of egg yolk of laying hens in high-ambient temperature. Biochem. Cell. Arch. 18, 1647–1652
56.
Safamehr A., Malek H., Nobakhat A., 2011. The Effect of different levels of tomato pomace with or without multi–enzyme on performance and egg traits of laying hens. Iran. J. Appl. Sci. 1, 39–47
57.
Sahin K., Onderci M., Sahin N., Gursu M.F., Khachik F., Kucuk O., 2006. Effects of lycopene supplementation on antioxidant status, oxidative stress, performance and carcass characteristics in heat-stressed Japanese quail. J. Therm. Biol. 31, 307–312, https://doi.org/10.1016/j.jthe...
58.
Salajegheh M.H., Ghazi S., Mahdavi R., Mozafari O., 2012. Effects of different levels of dried tomato pomace on performance, egg quality, and serum metabolites of laying hens. Afr. J. Biotechnol. 11, 15373–15379
59.
Sauvant D., Schmidely P., Daudin J.J., St-Pierre N.R., 2008. Meta-analyses of experimental data in animal nutrition. Animal 2, 1203–1214, https://doi.org/10.1017/S17517...
60.
Searle S.R., Speed F.M., Milliken G.A., 1980. Population marginal means in the linear model: an alternative to least squares means. Am. Stat. 34, 216–221, https://doi.org/10.1080/000313...
61.
Senbeta E.K., Zeleke N.A., Molla Y.G., 2015. Attitudes and perceptions of consumers to chicken egg attributes in eastern ethiopia. J. Anim. Prod. Adv. 5, 705–710, https://doi.org/10.5455/japa.2...
62.
Ševčíková S., Skřiva M., Dlouhá G., 2008. The effect of lycopene supplementation on lipid profile and meat quality of broiler chickens. Czech J. Anim. Sci. 53, 431–440, https://doi.org/10.17221/350-C...
63.
Shahsavari K., 2015. Influences of different sources of natural pigments on the color and quality of eggs from hens fed a wheat-based diet. Iran. J. Appl. Sci. 5, 167–172
64.
Shakeri M., Zulkifli I., Soleimani A.F., O’Reilly E.L., Eckersall P.D., Anna A.A., Kumari S., Abdullah F.F.J., 2014. Response to dietary supplementation of L-glutamine and L-glutamate in broiler chickens reared at different stocking densities under hot, humid tropical conditions. Poult. Sci. 93, 2700–2708, https://doi.org/10.3382/ps.201...
65.
Shevchenko L.V., Iakubchak O.M., Davydovych V.A., Honchar V.V., Ciorga M., Hartung J., Kołacz R., 2021. Influence of lycopene and astaxanthin in feed on metabolic parameters of laying hens, yolk color of eggs and their content of carotenoids and vitamin A when stored under refrigerated conditions. Pol. J. Vet. Sci. 24, 525–535, https://doi.org/10.24425/pjvs....
66.
Shi J., Le Maguer M., Kakuda Y., Liptay A., Niekamp F., 1999. Lycopene degradation and isomerization in tomato dehydration. Food Res. Int. 32, 15–21, https://doi.org/10.1016/S0963-...
67.
St-Pierre N.R., 2001. Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84, 741–75, https://doi.org/10.3168/jds.S0...
68.
Stahl W., Sies H., 2003. Antioxidant activity of carotenoids. Mol. Asp. Med. 24, 345–351, https://doi.org/10.1016/S0098-...
69.
Tapiero H., Townsend D.M., Tew K.D., 2004. The role of carotenoids in the prevention of human pathologies. Biomed. Pharmacother. 58, 100–110, https://doi.org/10.1016/j.biop...
70.
Tejeda O.J., Kim W.K., 2021. Role of dietary fiber in poultry nutrition. Animals 11, 461, https://doi.org/10.3390/ani110...
71.
Tufarelli V., Baghban-Kanani P., Azimi-Youvalari S., Hosseintabar-Ghasemabad B., Slozhenkina M., Gorlov I., Viktoronova F.M., Seidavi A., Laudadio V., 2022. Effect of dietary flaxseed meal supplemented with dried tomato and grape pomace on performance traits and antioxidant status of laying hens. Anim. Biotechnol. 33, 1525–1532, https://doi.org/10.1080/104953...
72.
Valko M., Leibfritz D., Moncol J., Cronin M.T.D., Mazur M., Telser J., 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44–84, https://doi.org/10.1016/j.bioc...
73.
Varzaru I., Untea A.E., Panaite T., Olteanu M., 2021. Effect of dietary phytochemicals from tomato peels and rosehip meal on the lipid peroxidation of eggs from laying hens. Arch. Anim. Nutr. 75, 18–30, https://doi.org/10.1080/174503...
74.
Verghese M., Richardson J.E., Boateng J., Shackelfor L.A., Howard C., Walker L.T., Chawan C.B., 2008. Dietary lycopene has a protective effect on cardiovascular disease in New Zealand male rabbits. J. Biol. Sci. 8, 268–277, https://doi.org/10.3923/jbs.20...
75.
Wang S., Wu H., Zhu Y., Cui H., Yang J., Lu M., Cheng H., Gu L., Xu T., Xu L., 2022. Effect of lycopene on the growth performance, antioxidant enzyme activity, and expression of gene in the keap1-nrf2 signaling pathway of arbor acres broilers. Front. Vet. Sci. 9, 833346, https://doi.org/10.3389/fvets....
76.
Wang J., Yue H., Wu S., Zhang H., Qi G., 2017. Nutritional modulation of health, egg quality and environmental pollution of the layers. Anim. Nutr. 3, 91–96, https://doi.org/10.1016/j.anin...
77.
Xue F., Li C., Pan S., 2013. In vivo antioxidant activity of carotenoid powder from tomato byproduct and its use as a source of carotenoids for egg-laying hens. Food Funct. 4, 610–617, https://doi.org/10.1039/c3fo30...
78.
Yannakopoulos A.L., Tserveni-Gousi A.S., Christaki E.V., 1992. Effect of locally produced tomato meal on the performance and the egg quality of laying hens. Anim. Feed Sci. Technol. 36, 53–57, https://doi.org/10.1016/0377-8...
79.
Zhong V.W., Van Horn L., Cornelis M.C. et al., 2019. Associations of dietary cholesterol or egg consumption with incident cardiovascular disease and mortality. JAMA-J. Am. Med. Assoc. 321, 1081–1095, https://doi.org/10.1001/jama.2...
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