The effects of lactic acid bacteria and yeast as probiotics on the performance, blood parameters, nutrient digestibility, and carcase quality of rabbits: a meta-analysis

Figures & data

Figure 1. Diagram flow of article selection in the meta-analysis using SYRCLE method.

Table 1. Studies included in the meta-analyses of the effects of probiotics on the performance, blood parameters, nutrient digestibility, and carcases quality of rabbit.

No.	References	Kind of probiotic	Form	Periods (d)	Strain of rabbit
1.	Rotolo et al. 2014	Lactic acid bacteria	Powder	37 to 84	New Zealand White
2.	Seyidoglu et al. 2014	Yeast	Powder	36 to 84	New Zealand White
3.	Phuoc and Jamikorn 2017	Lactic acid bacteria	Powder	28 to 70	New Zealand White
4.	Fathi et al. 2017	Lactic acid bacteria	Powder	56 to 112	Spanish
5.	Attia et al. 2013	Lactic acid bacteria	Powder	16 to 61	New Zealand White
6.	Simonova et al. 2015	Lactic acid bacteria	Powder	21 to 36	Hyplus
7.	Belhaseen et al. 2016	Yeast	Powder	35 to 77	Pannon White
8.	Bhatt et al. 2016	Lactic acid bacteria	Powder	42 to 91	Chincilla
9.	El-Shafei et al. 2019	Lactic acid bacteria	Powder	28 to 84	New Zealand White
10.	El-Sagheer et al. 2014	Lactic acid bacteria	Powder	30 to 72	New Zealand White
11.	Ezema et al. 2012	Yeast	Powder	Not reported	New Zealand White
12.	Wang et al. 2017	Lactic acid bacteria	Powder	35 to 85	Rex
13.	Wallace et al. 2012	Lactic acid bacteria	Powder	30 to 36	New Zealand White
14.	Simonova et al. 2013	Lactic acid bacteria	Powder	35 to 77	Hyplus
15.	Trocino et al. 2005	Lactic acid bacteria	Liquid	37 to 79	Hyla
16.	Liu et al. 2019	Lactic acid bacteria	Powder	60 to 80	Sichuan
17.	El-deep et al. 2021	Yeast	Powder	35 to 85	Not Reported
18.	Nicodemus et al. 2004	Lactic acid bacteria	Liquid	7 to 30	New Zealand White
19.	Simonova et al. 2020	Lactic acid bacteria	Powder	35 to 77	Hycole
20.	Chrastinova et al. 2010	Lactic acid bacteria	Powder	35 to 77	New Zealand White
21.	Kritas et al. 2008	Lactic acid bacteria	Powder	38 to 93	New Zealand White
22.	Kurchaeva et al. 2019	Lactic acid bacteria	Powder	1 to 120	New Zealand White
23.	Dimova et al. 2018	Lactic acid bacteria	Powder	36 to 84	New Zealand White
24.	Simonova et al. 2020	Lactic acid bacteria	Liquid	42 to 77	Hyplus
25.	Kalma et al. 2018	Yeast	Powder	35 to 77	Soviet Chincilla
26.	Helal et al. 2021	Yeast	Powder	Not reported	New Zealand White
27.	El-Dimerdash et al. 2011	Lactic acid bacteria	Powder	10 to 40	New Zealand White
28.	Oso et al. 2013	Lactic acid bacteria	Powder	35 to 70	New Zealand White
29.	Seyidoğlu et al. 2014	Yeast	Powder	30 to 90	New Zealand White
30.	Shah et al. 2020	Lactic acid bacteria	Powder	42 to 92	Not reported
31.	Shehu et al. 2014	Yeast	Powder	36 to 84	New Zealand White
32.	Emmanuel et al. 2019	Yeast	Powder	16 to 81	New Zealand White
33.	Ahmed et al. 2019	Yeast	Powder	36 to 84	New Zealand White
34.	Abd El-Aziz et al. 2021	Yeast	Powder	16 to 81	Rex X V-line
35.	Chowdhury et al. 2022	Lactic acid bacteria and yeast	Powder	42 to 98	New Zealand White

Figure 2. Linear Regression of correlation between probiotic level and nutrient digestibility of rabbit. $OM\mathrm{ }(\mathrm{\%}\mathrm{ }of\mathrm{ }DM)=53.8-0.14X^2+1.46X;$ n = 19; p-value = 0.03 $CP (\mathit{\text{\% of DM}}) = 55.9 - 0.15X^2 + 1.55X;$ n = 27; p-value = 0.026

$\mathit{NDF} (\mathit{\text{\% of DM}}) = 30.9 - 0.46X^2 + 4.45X;$ n = 13; p-value = 0.013. OM: organic matter; CP: crude protein; NDF: neutral detergent fibre; DM: dry matter.

Figure 3. Linear Regression of Correlation between probiotic level (log 10 CFU/kg of feed) and blood profile (mg/dL) of rabbit.

$\mathit{LDL}=19.9+0.72X^2-6.64X;$ n = 7; p-value = 0.011 $\mathit{Cholesterol} (mg/dL)=62.85-0.9X;$ n = 35; p-value = 0.03 $\mathit{Triglyceride} (mg/dL)=79.96-0.82X;$ n = 27; p-value = 0.057. OM: organic matter; CP: crude protein; NDF: neutral detergent fibre; DM: dry matter.

Figure 4. Principal Component Analysis (PCA) Biplot of probiotic in liquid and powder form based on the performance, blood parameters, nutrient digestibility, and carcases quality of rabbit.

Figure 5. Individual of principal component analysis (PCA) Biplot of group form liquid and powder of probiotics level (log 10 CFU/kg of feed).

Figure 6. Principal component analysis (PCA) Biplot of groups of Lactic acid Bacteria (BAL), control, yeast, both lactic acid bacteria (BAL) and yeast on the performance, blood parameters, nutrient digestibility, and carcases quality of rabbit.

Figure 7. Principal Component Analysis (PCA) Biplot of probiotic in liquid and powder form based on the performance of rabbit.

Table 2. Regression linear model of effect of probiotic of probiotics on the performance, blood parameters, nutrient digestibility, and carcases quality of rabbit.

No.	Response	Unit	Model	N	Intercept	SE Intercept	Slope	SE Slope	P-Value	RMSE	AIC	Trend	P X L	LAB X Y
1.	IBW	G	L	100	977	133	−0.92	1.37	0.5	2.85	1284	–	0.21	0.34
2.	FBW	G	L	98	2277	134	9.51	2.71	0.0008	1.65	1349	+	0.33	0.21
3.	BWG	G	L	77	743	128	3.97	2.22	0.01	1.68	1012	+	0.25	0.35
4.	FCR	g feed / g weight	L	85	3.79	0.3	0.01	0.01	0.43	2.44	234	+	0.34	0.45
5.	ADG	G	L	71	36	5.81	0.27	0.21	0.2	2.03	573	+	0.33	0.32
6.	Mortality	%	L	46	6.13	2.22	0.02	0.1	0.81	1.8	284	+	1.23	0.54
7.	ADFI	G	L	77	121	22.4	0.5	0.4	0.2	2.55	750	+	0.67	0.21
8.	RBC	cell/μL	L	22	53.1	10.7	0.46	0.31	0.1	1.41	175	+	0.56	0.21
9.	WBC	cell/μL	L	26	19	9.6	0.15	0.11	0.18	1.16	173	+	0.64	0.12
10.	Lymphocyte	%	L	17	62	6.47	0.23	0.73	0.75	1.24	141	+	0.32	0.33
11.	Hemoglobin	mg/dL	L	23	12	1.15	0.023	0.03	0.47	1.08	87.6	+	0.21	0.21
12.	Total protein	mg/dL	L	44	33.1	7.78	0.1	0.04	0.05	1.40	253	+	0.33	0.11
13.	Glucose	mg/dL	L	26.	61.9	21.9	0.03	0.43	0.93	1.55	221	+	0.32	0.32
14.	Cholesterol	mg/dL	L	35	62.9	12.7	−0.9	0.4	0.03	1.1	302	–	0.21	0.23
15.	Triglyceride	mg/dL	L	27	80	19.4	−0.82	0.4	0.05	1.3	231	–	0.44	0.11
16.	Albumin	mg/dL	L	34	6.11	3.72	0.39	0.22	0.01	2	243	+	0.47	0.32
17.	HDL	mmol/L	L	7	32.4	5.75	−0.47	0.63	0.49	0.82	48.7	–	0.32	0.33
18.	LDL	mmol/L	L	7	18.7	3.07	−0.22	0.41	0.61	0.87	43.8	–	0.21	0.54
19.	IgG	no unit	L	10	20.4	17.4	0.24	0.14	0.14	0.93	59.1	+	0.35	0.32
21.	IgY	no unit	L	7	8.02	8.22	0.03	0.02	0.26	0.8	23.2	+	0.76	0.21
23.	Carcase	%	L	23	55.4	2.55	0.1	0.08	0.03	1.09	125	+	0.23	0.33
24.	SW	G	L	32	1939	252	6.55	6.03	0.28	1.57	441	+	0.12	0.33
25.	Kidney	g/Kg	L	23	0.5	0.11	0.0002	0.0008	0.76	1.3	−51.3	+	0.34	0.56
26.	Liver	g/Kg	L	23	10	6.06	0.032	0.02	0.22	1.08	97.3	+	0.54	0.57
27.	Heart	g/Kg	L	23	2.6	1.06	0.05	0.019	0.01	1.36	69.2	+	0.34	0.21
28.	Lightness	No unit	L	12	52.3	1.87	0.12	0.15	0.45	0.88	63	+	0.23	0.32
29.	Redness	No unit	L	12	2.84	1.47	−0.02	0.03	0.6	0.87	42.1	–	0.23	0.72
30.	Yellowness	No unit	L	12	5.6	1.11	0.02	0.04	0.63	0.91	43.6	+	0.53	0.33
31.	DM	% of fresh	L	30	60.2	5.73	−0.03	0.11	0.73	1.43	186	–	0.53	0.34
32.	OM	% of DM	L	19	54.5	7.45	0.11	0.08	0.18	1.25	107	+	0.44	0.34
33.	CP	% of DM	L	27	56.6	8.35	0.033	0.12	0.78	1.1	173	+	0.33	0.21
34.	EE	% of DM	L	27	56.1	12.55	0.08	0.06	0.20	1.16	157	+	0.23	0.32
35.	NDF	% of DM	L	13	31.9	4.95	0.2	0.28	0.48	1.02	86.5	+	0.23	0.45
36.	ADF	% of DM	L	9	19	5.12	−0.2	0.2	0.34	0.73	54.9	–	0.11	0.32

IBW: initial body weight; FBW: final body weight; BWG: body weight gain; FCR: feed conversion ratio; ADG: average daily gain; ADFI: average daily feed intake; RBC: red blood cell; WBC: white blood cell; HDL: High-density lipoprotein; LDL: Low-density lipoprotein; DM: Dry matter; OM: organic matter; CP: crude protein; EE: ether extract; NDF: neutral detergent fibre; ADF: Acid detergent fibre; M: model; N: number of data; SE – standard error; RMSE – root mean square errors; AIC – akaike information criterion; L – linear; P: powder; L: liquid; LAB: lactic acid bacteria; Y: yeast; +: positive; -: negative

Rotolo L, Gai F, Peiretti PG, Ortoffi M, Zoccarato I, Gasco L. 2014. Live yeast (Saccharomyces cerevisiae var. boulardii) supplementation in fattening rabbit diet: effect on productive performance and meat quality. Livest Sci. 162:178–184.

 Web of Science ®Google Scholar

Seyidoglu N, Galip N, Sonat FA. 2014. Effect of yeast culture on growth performance, haematological and biochemical indices of New Zealand white rabbits. Uludağ Üniv. Vet. Fak. Dergisi. 32(2):11–18.

 Google Scholar

Phuoc TL, Jamikorn U. 2017. Effects of probiotic supplement (Bacillus subtilis and Lactobacillus acidophilus) on feed efficiency, growth performance, and microbial population of weaning rabbits. Asian-Australas J Anim Sci. 30(2):198–205.

 PubMed Web of Science ®Google Scholar

Fathi M, Abdelsalam M, Al‐Homidan I, Ebeid T, El‐Zarei M, Abou‐Emera O. 2017. Effect of probiotic supplementation and genotype on growth performance, carcass traits, hematological parameters and immunity of growing rabbits under hot environmental conditions. Anim Sci J. 88(10):1644–1650.

 PubMed Web of Science ®Google Scholar

Attia YA, Abd El Hamid EA, Ismaiel AM, El-Nagar A. 2013. The detoxication of nitrate by two antioxidants or a probiotic, and the effects on blood and seminal plasma profiles and reproductive function of New Zealand White rabbit bucks. Animal. 7(4):591–601.

 PubMed Web of Science ®Google Scholar

El-Shafei AER, Younis T, Al-Gamal M, Hesham A. 2019. Impact of probiotic (Lactobacillus planterium) supplementation on productive and physiological performance of growing rabbits under egyptian conditions. Egyptian J Rabbit Sci. 29(1):125–148.

 Google Scholar

El-Sagheer M, Hassanein HHM. 2014. Effect of enzymes and probiotic mixture supplementation to the diet of growing female rabbits on performance and carcass criteria. Egyptian Poult Sci J. 34(1):259–272.

 Google Scholar

Ezema C, Eze DC. 2012. Determination of the effect of probiotic (Saccharomyces cerevisiae) on growth performance and hematological parameters of rabbits. Comp Clin Pathol. 21(1):73–76.

 Google Scholar

Wang C, Zhu Y, Li F, Huang L. 2017. The effect of Lactobacillus isolates on growth performance, immune response, intestinal bacterial community composition of growing Rex Rabbits. J Anim Physiol Anim Nutr. 101(5):e1–e13.

 PubMed Web of Science ®Google Scholar

Wallace PA, Osei DY, Aseidu P, Amoah KO, Asafu-Adjaye A. 2012. Influence of the probiotic, RE 3 on nutritional performance, hematological, immune status and carcass characteristics of rabbit reared under tropical conditions. J Anim Feed Res. 2:450–456.

 Google Scholar

Simonová MP, Lauková A, Chrastinová L, Plachá I, Strompfová V, Čobanová K, Formelová Z, Chrenková M. 2013. Combined administration of bacteriocin-producing, probiotic strain Enterococcus faecium CCM7420 with Eleutherococcus senticosus and their effect in rabbits. Polish J Vet Sci. 16(4):619–627.

 PubMed Web of Science ®Google Scholar

Trocino A, Xiccato G, Carraro L, Jimenez G. 2005. Effect of diet supplementation with Toyocerin®(Bacillus cereus var. toyoi) on performance and health of growing rabbits. World Rabbit Sci. 13(1):17–28.

 Web of Science ®Google Scholar

Liu L, Zeng D, Yang M, Wen B, Lai J, Zhou Y, Hao S, Xiong L, Lin Y, Pan K, et al. 2019. Probiotic Clostridium butyricum improves the growth performance, immune function, and gut microbiota of weaning Rex Rabbits. Probiotics & Antimicro Prot. 11(4):1278–1292.

 PubMed Web of Science ®Google Scholar

El‐Deep MH, Dawood MA, Assar MH, Ahamad Paray B. 2021. Aspergillus awamori positively impacts the growth performance, nutrient digestibility, antioxidative activity and immune responses of growing rabbits. Vet Med Sci. 7(1):226–235.

 PubMed Web of Science ®Google Scholar

Nicodemus N, Carabaño R, Garcia J, De Blas JC. 2004. Performance response of doe rabbits to Toyocerin (R) (Bacillus cereus var. Toyoi) supplementation. World Rabbit Sci. 12:109–118.

 Web of Science ®Google Scholar

Pogány Simonová M, Lauková A, Chrastinová Ľ, Plachá I, Szabóová R, Kandričáková A, Žitňan R, Chrenková M, Ondruška Ľ, Bónai A, et al. 2020. Beneficial effects of Enterococcus faecium EF9a administration in rabbit diet. World Rabbit Sci. 28(4):169–179.

 Web of Science ®Google Scholar

Chrastinová LU, Chrenková M, Lauková A, Poláčiková M, Simonová M, Szabóová R, Strompfová V, Ondruška L, Chlebec I, Parkányi V, et al. 2010. Influence of selected phytoadditives and probiotics on zootechnical performance, caecal parameters and meet quality of rabbits. Arch Zootech. 13(2):30–35.

 Google Scholar

Kritas SK, Petridou EI, Fortomaris P, Tzika E, Arsenos G, Koptopoulos G. 2008. The effect of probiotics on microbiology, health and performance of fattening rabbits. Asian-Australas J Anim Sci. 21(9):1312–1317.

 Web of Science ®Google Scholar

Kurchaeva EE, Vostroilov AV, Artemov ES, Maksimov IV. 2019. Improvement of rabbit productivity using probiotics and herbal supplements. IOP Conference Series Earth and Environmental Science. 341:012–051.

 Google Scholar

Simonová MP, Chrastinová Ľ, Lauková A. 2020. Effect of beneficial strain Enterococcus faecium EF9a isolated from Pannon White rabbit on growth performance and meat quality of rabbits. Ital J Anim Sci. 19(1):650–655.

 Web of Science ®Google Scholar

Kalma RP, Chauhan HD, Srivastava AK, Pawar MM. 2018. Growth and blood profile of broiler rabbits on probiotic supplementation. Indian J Small Rumin. 24(1):66–69.

 Google Scholar

Helal F, El-Badawi A, El-Naggar S, Shourrap M, Aboelazab O, Hafsa SA. 2021. Probiotics role of Saccharomyces cerevisiae and Bacillus subtilis in improving the health status of rabbits’ gastrointestinal tract. Bull Nat Res Centr. 45(66):1–9.

 Google Scholar

El Dimerdash MZ, Dalia MH, Hanan FA, Doaa SA. 2011. Studies on the effect of some probiotics in Rabbits. SCVMJ. 16:151–168. 2011

 Google Scholar

Oso AO, Idowu OMO, Haastrup AS, Ajibade AJ, Olowonefa KO, Aluko AO, Ogunade IM, Osho SO, Bamgbose AM. 2013. Growth performance, apparent nutrient digestibility, caecal fermentation, ileal morphology and caecal microflora of growing rabbits fed diets containing probiotics and prebiotics. Livest Sci. 2013 157(1):184–190.

 Web of Science ®Google Scholar

Seyidoğlu N, Galip N. 2014. Effects of Saccharomyces cerevisiae and Spirulina platensis on growth performances and biochemical parameters in rabbits. Kafkas Univ Vet Fak Derg. 20(3):331–336.

 Web of Science ®Google Scholar

Shah AA, Liu Z, Qian C, Wu J, Sultana N, Zhong X. 2020. Potential effect of the microbial fermented feed utilization on physicochemical traits, antioxidant enzyme and trace mineral analysis in rabbit meat. J Anim Physiol Anim Nutr. 104(3):767–775.

 PubMed Web of Science ®Google Scholar

Shehu BM, Ayo JO, Ayanwale BA, Jiya EZ, Tsado DN. 2014. Growth performance and nutrient digestibility of weaned rabbits fed diets supplemented with varying levels of baker’s yeast (Saccharomyces cerevisiae). Int Agr Rural Dev. 17(1):1619–1627.

 Google Scholar

Emmanuel DC, Amaka AE, Okezie ES, Sunday UP, Ethelbert OC. 2019. Epididymal sperm characteristics, testicular morphometric traits and growth parameters of rabbit bucks fed dietary saccharomyces cerevisiae and/or zinc oxide. Brazilian Poult Sci. 21(01):001–010.

 Google Scholar

Ahmed KD, Omar AA, Saad TJA, Abdul RYA, Mahmud DA, Naif NL, Odeh AA. 2019. Effect of using the saccharomyces cerevisiae on some production traits and carcass characters of the local rabbits. Plant Arc. 19(2):895–897.

 Google Scholar

Abd El-Aziz AH, Mahrose KM, El-Kasrawy NI, Alsenosy AEWA. 2021. Yeast as growth promoter in two breeds of growing rabbits with special reference to its economic implications. Anais da Acad Brasileira de Ciências. 93(2):1–13. 2021

 Web of Science ®Google Scholar

Chowdhury R, Rahman MA, Al Mamun M. 2022. Influence of dietary organic acid, probiotic and antioxidant on the growth performance and nutrient digestibility in growing rabbit. Bang J Anim Sci. 51(2):55–61.

 Google Scholar