Does the Use of Emulsifier or Lipase Improve Weight Gain and Feed Conversion in Broilers? A Systematic Literature Review and Meta-Analysis

Fernandes, ML; Nascimento, DS; Cardoso, AS; Vieira, BS; Jolomba, MR; Oliveira, JGR; Macena, WG; Costa, FGP; Lima, MR

doi:10.1590/1806-9061-2023-1766

ML Fernandes

Postgraduate Program in Animal Science, State University of Santa Cruz, Rodovia BR 415, km 16, 45662-900, Ilhéus, Bahia, Brazil.

http://orcid.org/0000-0001-7618-0798

DS Nascimento

Postgraduate Program in Animal Science, State University of Santa Cruz, Rodovia BR 415, km 16, 45662-900, Ilhéus, Bahia, Brazil.

http://orcid.org/0000-0002-9688-4466

AS Cardoso

Postdoctoral fellow at the Postgraduate Program in Biosystems, Universidade Federal do Sul da Bahia, Avenida BR-415 , 45613-204, Itabuna, Bahia, Brazil.

http://orcid.org/0000-0002-8494-2032

BS Vieira

Instituto Federal de Ciência e Tecnologia do Mato Grosso, Rodovia MT 208, Lote 143-A, Loteamento Aquarela - Hamoa, 78580-000, Alta Floresta, Mato Grosso, Brazil.

http://orcid.org/0000-0003-2075-0565

MR Jolomba

Postdoctoral fellow at the Postgraduate Program in Biosystems, Universidade Federal do Sul da Bahia, Avenida BR-415 , 45613-204, Itabuna, Bahia, Brazil.

http://orcid.org/0000-0002-9098-2479

JGR Oliveira

Postdoctoral fellow at the Postgraduate Program in Biosystems, Universidade Federal do Sul da Bahia, Avenida BR-415 , 45613-204, Itabuna, Bahia, Brazil.

http://orcid.org/0000-0002-1364-5890

WG Macena

Postdoctoral fellow at the Postgraduate Program in Biosystems, Universidade Federal do Sul da Bahia, Avenida BR-415 , 45613-204, Itabuna, Bahia, Brazil.

http://orcid.org/0000-0002-6225-3965

FGP Costa

Universidade Federal da Paraíba. Rodovia PB 079 - km 12, 58.397-000, Areia, Paraíba, Brazil.

http://orcid.org/0000-0003-4075-1792

MR Lima

Universidade Federal Rural do Semi-Árido, Av. Francisco Mota, 572.59.625-900, Mossoró, RN, Brazil.

http://orcid.org/0000-0002-9897-6209

Corresponding author e-mail address Matheus Ramalho de Lima Universidade Federal Rural do Semi-Árido, UFERSA. R. Francisco Mota, 572 - Pres. Costa e Silva, Mossoró - RN, 59625-900, Brasil. Phone: +5584 9217-3987 Email: mlmatheus@ufersa.edu.br

Study	Participants	Group control	Intervention group
Aguilar et al. (2013Aguilar YM, Becerra JC, Bertot RR, et al. Growth performance, carcass traits and lipid profile of broiler chicks fed with an exogenous emulsifier and increasing levels of energy provided by palm oil. Journal of Food, Agriculture & Environment 2013;11:629-33.)	Ross 308 broilers, male, (n=320), evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant origin; EM level 2977kcal/kg	Control diet + emulsifier (0.05%)
Allahyari-Bake and Jahanian. (2017Allahyari-Bake S, Jahanian R. Effects of dietary fat source and supplemental lysophosphatidylcholine on performance, immune responses, and ileal nutrient digestibility in broilers fed corn/soybean meal- or corn/wheat/soybean meal-based diets. Poultry Science 2017; 96:1149-58. https://doi.org/10.3382/ps/pew330 https://doi.org/10.3382/ps/pew330... ) (Experiments I and II)	Ross 308 broilers, mixed, (n=576 experiments I and II), evaluated from 1 to 42 days.	Diet without emulsifier; lipid source of plant origin; EM level 2957kcal/kg	Control diet + emulsifier (0.1%)
Arshad et al. (2020Arshad MA, Bhatti SA, Hassan I, et al. Effects of bile acids and lipase supplementation in low-energy diets on growth performance, fat digestibility and meat quality in broiler chickens. Brazilian Journal of Poultry Science 2020;22:1-8. https://doi.org/10.1590/1806-9061-2020-1258 https://doi.org/10.1590/1806-9061-2020-1... )	Cobb 500 broilers, mixed, (n=280), evaluated from 1 to 35 days.	Lipase-free diet; Lipid source of animal origin; EM level 2968kcal/kg	Control diet + Lipase (0.018%)
Bontempo et al. (2015Bontempo V, Comi M, Jiang XR. The effects of a novel synthetic emulsifier product on growth performance of chickens for fattening and weaned piglets. Animal 2015;10:592-7. https://doi.org/10.1017/S1751731115002189 https://doi.org/10.1017/S175173111500218... )	Cobb 500 broilers, female, (n=480), evaluated from 1 to 34 days.	Diet without emulsifier; Lipid source of plant and animal origin; EM levels 3075kcal/kg	Control diet + emulsifier (0.07%)
Bontempo et al. (2018Bontempo V, Comi M, Jiang XR, et al. Evaluation of a synthetic emulsifier product supplementation on broiler chicks. Animal Feed Science and Technology 2018;240:157-64. https://doi.org/10.1016/j.anifeedsci.2018.04.010 https://doi.org/10.1016/j.anifeedsci.201... )	Ross 308 broilers, male, (n=600), evaluated from 1 to 44 days.	Diet without emulsifier; Lipid source of plant and animal origin; EM levels 3178 kcal/kg	Control diets + emulsifier (0.07%)
Castro and Kim. (2021Castro FLS, Kim WK. Applied research note: exogenous lipase supplementation to low-energy, low-protein, and low-amino acid diets for broiler chickens from one to 42 day. Journal of Applied Poultry Research 2021;30:100-17. https://doi.org/10.1016/j.japr.2020.100117 https://doi.org/10.1016/j.japr.2020.1001... )	Cobb 500 broilers, male, (n=480), evaluated from 1 to 42 days.	Lipase-free diet; Lipid source of plant origin; EM levels 3083 and 2983 kcal/kg	Control diet + Lipase (0.01%)
Cho et al. (2012Cho JH, Zhao P, Kim IH. Effects of emulsifier and multi-enzyme in different energy density diet on growth performance, blood profiles, and relative organ weight in broiler chickens. Journal of Agricultural Science 2012;4:161-8. https://doi.org10.5539/jas.v4n10p161 https://doi.org10.5539/jas.v4n10p161... )	Ross 308 broilers, male, (n=216), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM level 3070 kcal/kg	Control diet + emulsifier (0.05%)
Dabbou et al. (2019)	Ross 708 broilers, mixed, (n=224), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of plant origin; EM level 3509 kcal/kg	Control diet + emulsifier (0.05%)
Haetinger et al. (2021Haetinger VS, Dalmoro YK, Godoy GL, et al. Optimizing cost, growth performance, and nutrient absorption with a bio-emulsifier based on lysophospholipids for broiler chickens. Poultry Science 2021;100:1-14. https://doi.org/10.1016/j.psj.2021.101025 https://doi.org/10.1016/j.psj.2021.10102... )	Cobb 500 broilers, male, (n=1050), evaluated 1 to 42 days	Diet without emulsifier; Lipid source of plant origin; EM level 3142 kcal/kg	Control diet + emulsifier (0.05%)
Kaczmarek et al. (2015Kaczmarek SA, Bochenek M, Samuelsson AC, et al. Effects of glyceryl polyethylene glycol ricinoleate on nutrient utilisation and performance of broiler chickens. Archives of Animal Nutrition 2015;69:285-96. https://doi.org /10.1080/1745039X.2015.1061722. https://doi.org... )	Ross 308 broilers, male, (n=384), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of plant and animal origin; EM levels 3072 and 2972 kcal/kg	Control diet + emulsifier (0.04%)
Liu et al. (2020aLiu X, Yoon SB, Kim IH. Growth performance, nutrient digestibility, blood profiles, excreta microbial counts, meat quality and organ weight on broilers fed with de-oiled lecithin emulsifier. Animals 2020a;10:1-12. https://doi.org/10.3390/ani10030478 https://doi.org/10.3390/ani10030478... )	Ross 308 broilers, male, (n= 480), evaluated from 1 to 35 days	Diet without emulsifier; Lipid source of animal origin; EM level 3179 kcal/kg	Control diet + emulsifier (0.1%)
Liu et al. (2020bLiu X, Yun KS, Kim IO. Evaluation of sodium stearoyl-2-lactylate and 1, 3-diacylglycerol supplementation in diets with different energy content on the growth performance, meat quality, apparent total tract digestibility, and blood lipid profiles of broiler chickens. Poultry Science 2020b;57:55-62. https://doi.org/10.2141/jpsa.0190007. https://doi.org/10.2141/jpsa.0190007... )	Ross 308 broilers, male, (n=1024), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM levels 3169 and 3070 kcal/kg	Control diet + emulsifier (0.15%)
Majdolhosseini et al. (2019Majdolhosseini L, Ghasemi HA, Hajkhodadadi I, et al. Nutritional and physiological responses of broiler chickens to dietary supplementation with de-oiled soyabean lecithin at different metabolisable energy levels and various fat sources. British Journal of Nutrition 2019;122:863-72. https://doi.org/10.1017/S000711451900182X. https://doi.org/10.1017/S000711451900182... )	Ross 308 broilers, male, (n=800), evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant and animal origin; EM levels 3093 and 3017 kcal/kg	Control diet + emulsifier (0.1%)
Movagharnejad et al. (2020Movagharnejad M, Kazemi-fard M, Rezaei M, et al. Effects of lysophospholipid and lipase enzyme supplementation to low metabolizable energy diets on growth performance, intestinal morphology and microbial population and some blood metabolites in broiler chickens. Brazilian Journal of Poultry Science 2020;22:1-10. https://doi.org/10.1590/1806-9061-2019-1118 https://doi.org/10.1590/1806-9061-2019-1... )	Ross 308 broilers, male, (n=120), evaluated from 1 to 38 days.	Diet without Lipase and/or Emulsifier; Lipid source of plant origin; EM level 2911 kcal/kg	Control diet + emulsifier (0.15%); lipase (ND)
Oliveira et al. 2019Oliveira LS, Balbino EM, Silva TNS, et al. Use of emulsifier and lipase in feeds for broiler chickens. Seminar: Agricultural Sciences 2019;40:3181-96. https://doi.org/10.5433/1679-0359.2019v40n6Supl2p3181 https://doi.org/10.5433/1679-0359.2019v4...	Cobb 500 broilers, male, (n=840), evaluated from 1 to 37 days.	Diet without Lipase and/or Emulsifier; Lipid source of plant origin; EM level 3036 kcal/kg	Control diet + Lipase and/or emulsifier (0.1%)
Park et al. (2018Park JH, Nguyen DH, Kim IH. Effects of exogenous lysolecithin emulsifier supplementation on the growth performance, nutrient digestibility, and blood lipid profiles of broiler chickens. Japan Poultry Science Association 2018;55:190-4. https://doi.org/10.2141/jpsa.0170100 https://doi.org/10.2141/jpsa.0170100... )	Ross 308 broilers, male, (n=816), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM levels 3100 kcal/kg	Control diet + emulsifier (0,03; 0,06; 09%)
Saleh et al. (2020Saleh A, Amber KA, Mousa MM, et al. A mixture of exogenous emulsifiers increased the acceptance of broilers to low energy diets: growth performance, blood chemistry, and fatty acids trait. Animals 2020;10:437)	Ross 308 broilers, male, (n=200), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of plant origin; EM level 2436 kcal/kg	Control diet + emulsifier (0.05%)
Shen et al. (2021Shen Y, Zhang S, Zhao X, et al. Evaluation of a lecithin supplementation on growth performance, meat quality, lipid metabolism, and cecum microbiota of broilers. Animals 2021;11:1-13. https://doi.org/10.3390/ani11092537 https://doi.org/10.3390/ani11092537... )	Arbor Acres broilers, male, (n=192), evaluated from 1 to 42 days	Diet without emulsifier; Lipid source of plant origin; EM level 3000 kcal/kg	Control diet + emulsifier (0.01%)
Silva et al. (2018Silva, VC, Fonseca SS, Valentim JK, et al. Performance of broiler chickens fed energy-reduced diets containing different types of emulsifiers. Academic Journal: Animal Science 2018;16:1-11.)	Cobb 500 broilers, mixed, (n=768) evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant origin; EM level 3067 kcal/kg	Control diet + emulsifier (0.025; 0.025; 0.035%)
Upadhaya et al. (2017aUpadhaya SD, Park JW, Park JH, et al. Efficacy of 1,3-diacylglycerol as a fat emulsifier in low-density diet for broilers. Poultry Science 2017a; 96:1672-8. https://doi.org/ 10.3382/ps/pew425. https://doi.org/ 10.3382/ps/pew425... )	Ross 308 broilers, male, (n=384), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM levels 3120 kcal/kg	Control diet + emulsifier (0.075; 0.10; 0.15%)
Upadhaya et al. (2017bUpadhaya SD, Lee JS, Jung KJ, et al. Influence of emulsifier blends having different hydrophilic-lipophilic balance value on growth performance, nutrient digestibility, serum lipid profiles, and meat quality of broilers. Poultry Science 2017b;1:255-61. https://doi.org/ 10.3382/ps/pex303 https://doi.org/ 10.3382/ps/pex303... )	Ross 308 broilers, male, (n=768), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM levels 3010 kcal/kg	Control diet + emulsifier (0.05; 0.075; 0.010%)
Wang et al. (2016Wang JP, Zhang ZF, Yan L, et al. Effects of dietary supplementation of emulsifier and carbohydrase on the growth performance, serum cholesterol and breast meat fatty acids profile of broiler chickens. Animal Science Journal 2016;87:250-6. https://doi.org/ 10.1111/asj.12412 https://doi.org/... )	Ross broilers, male, (n=216), evaluated from 1 to 35 days.	Diet without emulsifier; Lipid source of animal origin; EM levels 3070 kcal/kg	Control diet + emulsifier (0.05%)
Wang et al. (2020Wang J, Choi H, Kim W. Effects of dietary energy level and 1,3-diacylglycerol on growth performance and carcass yield in broilers. Journal of Applied Poultry Research 2020;29:665-72. https://doi.org/10.1016/j.japr.2020.04.004 https://doi.org/10.1016/j.japr.2020.04.0... )	Cobb 500 broilers, male, (n=640), evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant origin; EM level 3101 and 3026 kcal/kg	Diet with emulsifier (0.1%)
Zampiga et al. (2016Zampiga M, Meluzzi A, Sirri F. Effect of dietary supplementation of lysophospholipids on productive performance, nutrient digestibility and carcass quality traits of broiler chickens. Italian Journal of Animal Science 2016;15:521-8. https://doi.org/10.1080/1828051X.2016.1192965 https://doi.org/10.1080/1828051X.2016.11... )	Ross broilers, male, (n=1765), evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant origin; EM level 3131 kcal/kg	Control diet + emulsifier (0.15% and 0.1%)
Zhang et al. (2011Zhang B, Haitao L, Zhao D, et al. Effect of fat type and lysophosphatidylcholine addition to broiler diets on performance, apparent digestibility of fatty acids, and apparent metabolizable energy content. Animal Feed Science and Technology 2011;163:177-84. https://doi.org/10.1016/j.anifeedsci.2010.10.004 https://doi.org/10.1016/j.anifeedsci.201... )	Arbor Acres broilers, male, (n=252), evaluated from 1 to 42 days.	Diet without emulsifier; Lipid source of plant and animal origin; EM levels 4168 kcal/kg	Control diet + emulsifier (0.05%)

Subgroup	Mean Difference (MD) (g/broiler/day)			Heterogeneity
Sex	k	IV, Random, 95% CI	p-value	Tau²	p-value	I²
Male	39	1.46 [1.07, 1.85]	<0.00001	0.91	<0.00001	78%
Female	1	9.10 [7.71, 10.49]	<0.00001	NE	NE	NE
Mixed	11	1.24 [-0.24, 2.73]	0.10	4.30	<0.0001	75%
Strain
Arbor Acres	4	1.16 [-1.57, 3.90]	0.41	7.46	<0.00001	96%
Cobb	12	2.02 [0.45, 3.59]	0.01	6.41	<0.00001	94%
Ross	35	1.65 [1.26, 2.04]	<0.00001	0.64	<0.00001	66%
Lipid source
Animal origin	20	1.52 [0.97, 2.07]	<0.00001	1.04	<0.00001	80%
vegetable origin	27	1.25 [0.70, 1.80]	<0.00001	0.97	<0.00001	68%
mixed origin	4	3.42 [-0.17, 7.01]	0.06	13.01	<0.00001	98%
Concentration of the lipid source in the diet (%)
up to 2%	20	2.36 [1.56, 3.17]	<0.00001	0.00	0.91	0%
of 2 at 3.5%	27	1.00 [0.48, 1.52]	0.0002	1.31	<0.00001	76%
Above 3.5%	4	2.52 [1.71, 3.34]	<0.00001	2.01	<0.00001	89%
metabolizable energy of the feed (kcal/kg)
Up to 3000 kcal/kg	14	1.22 [-0.10, 2.55]	0.07	3.35	<0.00001	83%
From 3001 to 3200 kcal/kg	33	1.88 [1.36, 2.40]	<0.00001	1.61	<0.00001	84%
Above 3200 kcal/kg	4	0.26 [-0.85, 1.38]	0.64	0.98	0.004	77%
Additive type
emulsifier	46	1.62 [1.15, 2.10]	<0.00001	1.80	<0.00001	85%
lipase	5	1.23 [-1.12, 3.58]	0.31	5.12	<0.00001	90%
concentration of the additive in the diet (%)
Up to 0.05%	20	1.04 [0.41, 1.66]	0.001	1.35	<0.00001	81%
From 0.051 to 0.1%	25	2.01 [1.29, 2.74]	<0.00001	2.30	<0.00001	86%
Above 0.1%	5	1.83 [0.87, 2.78]	0.0002	0.58	0.03	65%
Uninformed	1	NE	NE	NE	NE	NE

Subgroup	Mean Difference			Heterogeneity
Sex	k	IV, Random, 95% CI	p-value	Tau²	p-value	I²
Male	39	-0.04 [-0.05,-0.03]	<0.00001	<0.00	<0.00001	69%
Female	1	0.00 [-0.03,0.03]	1.00	NA	NA	NA
Mixed	11	-0.04 [-0.07,-0.01]	0.02	<0.00	0.001	66%
Strain
Arbor Acres	4	-0.01 [-0.05, -0.02]	0.41	<0.00	0.09	55%
Cobb	12	-0.02 [-0.03, -0.00]	0.02	<0.00	0.06	43%
Ross	35	-0.05 [-0.06, 0.04]	<0.00001	<0.00	<0.00001	59%
lipid source
Animal origin	20	-0.06 [-0.07,-0.04]	<0.00001	<0.00	<0.00001	78%
vegetable origin	27	-0.03 [-0.04,-0.02]	<0.00001	<0.00	0.21	18%
mixed origin	4	0.00 [-0.01,0.01]	1.00	<0.00	1.00	0%
Concentration of the lipid source in the diet (%)
up to 2%	20	-0.06 [-0.09, -0.03]	0.0005	<0.00	0.03	59%
From 2 to 3.5%	27	-0.04 [-0.05, -0.02]	<0.00001	<0.00	<0.00001	64%
More than 3.5%	4	-0.04 [-0.06,-0.03]	<0.00001	<0.00	<0.00001	76%
Feed metabolizable energy (kcal/kg)
Up to 3000 kcal/kg	14	-0.04 [-0.07, -0.01]	0.003	<0.00	<0.0001	69%
From 3000 to 3200 kcal/kg	33	-0.04 [-0.05, -0.03]	<0.00001	<0.00	<0.00001	70%
More than 3200 kcal/kg	4	-0.02 [-0.06, 0.01]	0.15	<0.00	0.11	51%
Additive type
emulsifier	46	-0.04 [-0.05, -0.04]	<0.00001	<0.00	<0.00001	63%
lipase	5	-0.03 [-0.03, 0.01]	0.29	<0.00	0.04	60%
Concentration of the additive in the diet (%)
Up to 0.05%	20	-0.03 [-0.04, -0.02]	<0.00001	<0.00	0.005	50%
From 0.05 to 0.1%	25	-0.04 [-0.06, -0.03]	<0.00001	<0.00	<0.00001	73%
More than 0.1%	5	-0.07 [-0.10, -0.05]	<0.00001	<0.00	0.01	69%
Uninformed	1	-0.06 [-0.12, -0.00]	0.03	NE	NE	NE

[1] Corresponding author e-mail address Matheus Ramalho de Lima Universidade Federal Rural do Semi-Árido, UFERSA. R. Francisco Mota, 572 - Pres. Costa e Silva, Mossoró - RN, 59625-900, Brasil. Phone: +5584 9217-3987 Email: mlmatheus@ufersa.edu.br

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Does the Use of Emulsifier or Lipase Improve Weight Gain and Feed Conversion in Broilers? A Systematic Literature Review and Meta-Analysis

ABSTRACT