Effects of Lactobacillus Supplements on Growth Performance of Broilers: A Meta-Analysis
XING Shuang, FENG JingHai,Institute of Animal Science, Chinese Academy of Agricultural Sciences/State Key Laboratory of Animal Nutrition, Beijing 100193
Abstract Abstract: 【Objective】The purpose of present study was to analyze the effects of Lactobacillus supplements on the growth performance of broilers by meta-analysis. 【Method】A total of 24 articles, including 25 trials and 8 702 subjects, were retrieved from domestic and foreign databases. Reviewing Manager (version 5.3) was used to calculate the standardized mean difference (SMD)(the difference between Lactobacillus group and control group divided by the mean of standard deviation between the two groups). According to the number of samples used in different studies and the standard deviation determined by the indicators, the weights of different research results were determined, and several independent research results were summarized. According to I 2 statistics, the heterogeneity of growth performance data was tested, and the publication bias was analyzed by funnel plot and egger test. The random effect model was used to analyze the continuous data for the significant heterogeneity of each index in this analysis and subgroup analysis was carried out according to Lactobacillus strains to explore the effects of different Lactobacillus on the growth performance of broilers.【Result】The analysis showed that Lactobacillus significantly increased the ADG (SMD=1.53, P<0.001) and reduced the F/G (SMD= -1.50, P<0.001) of broilers during 0-6 week period of the experiment, and had no significant effect on feed intake (P=0.470). Lactobacillus significantly increased the ADG of broilers (SMD=1.05, P<0.001) in the growing period, and had a tendency to improve ADG (SMD=0.52, P=0.090) in the finishing period, significantly reduced the growing F/G (SMD= -1.31, P<0.001) and the finishing F/G (SMD= -0.94, P<0.001). The growth-promoting effect of Lactobacillus on broilers was better than that the finishing period according to the value of SMD. Funnel plot and egger analysis showed that the bias of F/G (P=0.012) and ADFI (P=0.006) in the early stage reached a significant level, while the biases of other indicators were not significant (P>0.05). Sensitivity analysis found that random deletion of arbitrary literature data had little effect on the analysis of daily gain and feed-to-weight ratio, indicating that the above results were stable and were not affected by one or several articles. The heterogeneity test found that there was significant heterogeneity in the analysis results of each growth index (P<0.001), indicating that the results of different literatures differed greatly, possibly due to differences in the Lactobacillus species or feeding doses used in different studies. Subgroup analysis based on Lactobacillus species could reduce the heterogeneity of the meta-analysis. Subgroup analysis showed that L. plantarum promoted the daily weight gain (1.98, P<0.001) and feed conversion efficiency (-1.66, P<0.001) on broiler 0-6 week period better than L. casei (0.51, -0.68, P≤0.02) and L. johnsonii (1.15, -0.16, P≤0.02). 【Conclusion】In conclusion, the meta-analysis showed that Lactobacillus could increase the daily weight gain and feed conversion efficiency of broilers at different period, and had no significant effect on feed intake. The promotion effect of Lactobacillus was different, among which L. plantarum was better. Keywords:Lactobacillus;broilers;growth performance;meta-analysis
PDF (585KB)元数据多维度评价相关文章导出EndNote|Ris|Bibtex收藏本文 本文引用格式 邢爽, 冯京海. 乳酸杆菌对肉鸡生长性能影响的Meta分析[J]. 中国农业科学, 2020, 53(1): 183-190 doi:10.3864/j.issn.0578-1752.2020.01.017 XING Shuang, FENG JingHai. Effects of Lactobacillus Supplements on Growth Performance of Broilers: A Meta-Analysis[J]. Scientia Acricultura Sinica, 2020, 53(1): 183-190 doi:10.3864/j.issn.0578-1752.2020.01.017
通过Web of Science、Science Direct、SpringerLink、Google学术、中国知网、维普和万方数据库筛选相关文献。检索方式为文章标题和关键词,英文检索词为:(lactobacillus or probiotics)and(broilers or poultry);中文检索词为:(乳酸杆菌或益生菌)和(肉鸡或家禽)。文献检索时间截止到2018年4月。
Table 1 表1 表1乳酸杆菌对肉鸡生长性能影响的Meta分析 Table 1Meta-analysis of the effect of Lactobacillus on growth performance in broiler chickens
指标 Index
效应量 Effect size
异质性检验 Heterogeneity
n
SMD
95%CI
实际值变化范围 Range of increase
P值 P value
I2
P值 P value
前期(1-21日龄)Early stage (1-21 d)
ADG
3614
1.05
0.69,1.42
1.69-3.15
P<0.001
98
P<0.001
ADFI
3482
-0.09
-0.47,0.28
-4.49-3.39
P=0.630
98
P<0.001
F/G
3614
-1.31
-1.86,-0.77
-0.26-0.02
P<0.001
99
P<0.001
后期(22-42日龄)Late stage (22-42 d)
ADG
3614
0.52
-0.08,1.12
-6.54-12.74
P=0.090
99
P<0.001
ADFI
3482
-0.32
-1.05,0.40
-14.96-12.83
P=0.380
99
P<0.001
F/G
3614
-0.94
-1.28,-0.59
-0.45-0.32
P<0.001
98
P<0.001
全期(1-42日龄)Entire stage (1-42 d)
ADG
4118
1.53
1.22,1.84
-0.74-8.58
P<0.001
97
P<0.001
ADFI
5706
-0.16
-0.16,0.28
-8.21-6.88
P=0.470
99
P<0.001
F/G
5918
-1.43
-1.83,-1.03
-0.38-1.03
P<0.001
99
P<0.001
n:肉鸡试验样本比较数,SMD:标准化均差,CI:置信区间,效应量为随机效应模型 n: Number of comparisons, SMD: Standardized mean difference, CI: Confidence interval, Effect sizes were estimated from a random effects model
Table 3 表3 表3不同乳酸杆菌对肉鸡全期生长性能影响的亚组分析 Table 3Subgroup analyses for the effects of different Lactobacillus species on the growth performance in broiler chickens
全期(1-42日龄) Entire stage (1-42 d)
效应量 Effect size
亚组分析异质性 Subgroup analysis for heterogeneity
n
SMD
95%CI
P值 P value
I2
P值 P value
总I2 Total I2
ADG
植物乳杆菌 L. plantarum
1550
1.98
1.46,2.50
P<0.001
97
P<0.001
87.4
嗜酸乳杆菌 L. acidophilus
1124
1.58
0.72,2.44
P<0.001
98
P<0.001
干酪乳杆菌 L. casei
364
0.51
0.19,0.83
P=0.002
79
P<0.001
约氏乳杆菌 L. johnsonii
440
1.15
0.42,1.87
P=0.002
96
P<0.001
ADFI
植物乳杆菌 L.plantarum
1550
0.29
-0.30,0.89
P=0.330
98
P<0.001
93.7
嗜酸乳杆菌 L. acidophilus
992
-0.41
-0.74,-0.09
P=0.010
89
P<0.001
干酪乳杆菌 L. casei
364
0.02
-0.13,0.17
P=0.780
1
P=0.400
约氏乳杆菌 L.johnsonii
440
0.72
-0.23,1.67
P=0.140
98
P<0.001
F/G
植物乳杆菌 L. plantarum
1550
-1.66
-2.14,-1.17
P<0.001
97
P<0.001
93.9
嗜酸乳杆菌 L. acidophilus
1124
-0.67
-1.23,-0.10
P=0.020
97
P<0.001
干酪乳杆菌 L. casei
364
-0.68
-0.95,-0.42
P<0.001
68
P=0.010
约氏乳杆菌 L. johnsonii
440
-0.16
-0.29,-0.02
P=0.020
0
P=0.650
n:肉鸡试验样本数,SMD:标准化均差,Cl:置信区间。效应量为随机效应模型 n: Number of comparisons, SMD: Standardized mean difference, CI: Confidence interval. Effect sizes were estimated from a random effects model
LEE KW, HONG YH., LEE SH, JANG SI, PARK MS, BAUTISTA DA, RITTER GD, JEOUNG,HY, AN DJ, LILLEHOJ EP, LILLEHOJ HS . Effects of anticoccidial and antibiotic growth promoter programs on broiler performance and immune status Research in Veterinary Science, 2012,93(2):721-728. [本文引用: 1]
CHATTOPADHYAY MK . Use of antibiotics as feed additives: A burning question Frontiers in Microbiology, 2014,5:334. [本文引用: 1]
ECKERT NH, LEE JT, HYATTD, STEVENS SM, ANDERSONS, ANDERSON PN, BELTRANR, SCHATZMAYRG, MOHNLM, CALDWELL DJ . Influence of probiotic administration by feed or water on growth parameters of broilers reared on medicated and nonmedicated diets Journal of Applied Poultry Research, 2010,19(1):59-67. [本文引用: 1]
FORGETTAV, REMPELH, MALOUINF, VAILLANCOURT JR, TOPPE, DEWARK, DIARRA MS . Pathogenic and multidrug- resistant Escherichia fergusonii from broiler chicken Poultry Science, 2012,91(2):512-525. [本文引用: 1]
CARVALHO IT, SANTOSL . Antibiotics in the aquatic environments: A review of the European scenario Environment International, 2016,94:736-757. [本文引用: 1]
RONQUILLO MG, HERNANDEZ J CA . Antibiotic and synthetic growth promoters in animal diets: review of impact and analytical methods Food Control, 2017,72:255-267. [本文引用: 1]
ZORRIEHZAHRA MJ, DELSHAD ST, ADELM, TIWARIR, KARTHIKK, DHAMAK, LAZADO CC . Probiotics as beneficial microbes in aquaculture: An update on their multiple modes of action: A review Veterinary Quarterly, 2016,36(4):228-241. [本文引用: 1]
WANGH, NIX, QINGX, ZENGD, LUOM, LIUL, LIG, PANK, JINGB . Live probiotic Lactobacillus johnsonii BS15 promotes growth performance and lowers fat deposition by improving lipid metabolism, intestinal development, and gut microflora in broilers Frontiers in Microbiology, 2017,8:1073. [本文引用: 2]
FORTEC, MANUALIE, ABBATEY, PAPAP, VIECELIL, TENTELLINIM, TRABALZA-MARINUCCIM, MOSCATIL . Dietary Lactobacillus acidophilus positively influences growth performance, gut morphology, and gut microbiology in rurally reared chickens Poultry Science, 2017,97(3):930-936. [本文引用: 2]
APATA DF . Growth performance, nutrient digestibility and immune response of broiler chicks fed diets supplemented with a culture of Lactobacillus bulgaricus Journal of the Science of Food and Agriculture, 2008,88(7):1253-1258. [本文引用: 1]
PANDA AK, RAO S VR, RAJU M V LN, SHARMA SR . Dietary supplementation of Lactobacillus sporogenes on performance and serum biochemico-lipid profile of broiler chickens The Journal of Poultry Science, 2006,43(3):235-240. [本文引用: 2]
AWAD WA, GHAREEBK, ABDEL-RAHEEMS, B?HMJ . Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens Poultry Science, 2009,88(1):49-56. [本文引用: 1]
YUB, LIU JR, CHIOU MY, HSU YR, CHIOU P WS . The effects of probiotic Lactobacillus reuteri Pg4 strain on intestinal characteristics and performance in broilers. Asian Australasian Journal of Animal Sciences, 2007,20(8):1243-1251. [本文引用: 2]
HANJ, WANGY, SONGD, LUZ, DONGZ, MIAOH, WANGW, HEJ, LIA . Effects of Clostridium butyricum and Lactobacillus plantarum on growth performance, immune function and volatile fatty acid level of caecal digesta in broilers Food and Agricultural Immunology, 2018,29(1):798-807. [本文引用: 1]
LIUL, NIX, ZENGD, WANGH, JINGB, YINZ, PANK . Effect of a dietary probiotic,Lactobacillus johnsonii BS15, on growth performance, quality traits, antioxidant ability, and nutritional and flavour substances of chicken meat Animal Production Science, 2017,57(5):920-926. [本文引用: 1]
LIY, CHANG WH, ZHANGS, ZHENG AJ, LIU GH, CAI HY, LIUW . Effects of dietary chitosan oligosaccharide and Lactobacillus casei on growth performance,meat quality and antioxidant function of broilers. Chinese Journal of Animal Nutrition, 2016,28(5):1450-1461. (in Chinese) [本文引用: 2]
ZOUX, XIAOR, LIH, LIUT, LIAOY, WANGY, WUS, LIZ . Effect of a novel strain of Lactobacillus brevis M8 and tea polyphenol diets on performance, meat quality and intestinal microbiota in broilers Italian Journal of Animal Science, 2018,17(2):396-407. [本文引用: 1]
LIZ, WANGW, LIUD, GUOY . Effects of Lactobacillus acidophilus on the growth performance and intestinal health of broilers challenged with Clostridium perfringens Journal of Animal Science and Biotechnology, 2018,9(1):25. [本文引用: 1]
SAUVANTD, SCHMIDELYP, DAUDIN JJ, ST-PIERRE NR . Meta-analyses of experimental data in animal nutrition Animal, 2008,2(8):1203-1214. [本文引用: 1]
HUANG MK, CHOI YJ, HOUDER, LEE JW, LEEB, ZHAOX . Effects of Lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens Poultry Science, 2004,83(5):788-795. [本文引用: 1]
SALARMOINIM, FOOLADI MH . Efficacy of Lactobacillus acidophilus as probiotic to improve broiler chicks performance Journal of Agricultural Science and Technology, 2010,13:165-172.
THANH NT, LOH TC, FOO HL, HAIR-BEJOM, AZHAR BK . Effects of feeding metabolite combinations produced by Lactobacillus plantarum on growth performance, faecal microbial population, small intestine villus height and faecal volatile fatty acids in broilers British Poultry Science, 2009,50(3):298-306.
LOH TC, THANH NT, FOO HL, HAIR-BEJOM, AZHAR BK . Feeding of different levels of metabolite combinations produced by Lactobacillus plantarum on growth performance, fecal microflora, volatile fatty acids and villi height in broilers Animal Science Journal, 2010,81(2):205-214.
PENGQ, ZENG XF, ZHU JL, WANGS, LIU XT, HOU CL, THACKER PA, QIAO SY . Effects of dietary Lactobacillus plantarum B1 on growth performance, intestinal microbiota, and short chain fatty acid profiles in broiler chickens Poultry Science, 2016,95(4):893-900.
SHENX, YID, NIX, ZENGD, JINGB, LEIM, BIANZ, ZENGY, LIT, XINJ . Effects of Lactobacillus plantarum on production performance, immune characteristics, antioxidant status, and intestinal microflora of bursin-immunized broilers Canadian Journal of Microbiology, 2014,60(4):193-202.
TAHERI HR, MORAVEJH, TABANDEHF, ZAGHARIM, SHIVAZADM . Efficacy of combined or single use of Lactobacillus crispatus LT116 and L.johnsonii LT171 on broiler performance British Poultry Science, 2010,51(5):580-585.
LIUL, ZHU LX . Effects of Sporolactobacillus on performance, intestinal development and microflora of broilers. Chinese Journal of Animal Nutrition, 2011,23(12):2136-2142. (in Chinese)
LIANG HW, ZHU HY, ZHANGL, BAI MM, ZHANG JY, QIN GX, ZHEN YG . Effect of Lactobacillus plantarum on growth performance and serum biochemical indices of broilers. China Animal Husbandry & Veterinary Medicine, 2015,42(3):589-596.(in Chinese)
LIN XH, LI CF, WANGJ, WANGF, GUW . Effects ofLactobacillus plantarum on growth performance and protein digestibility of broilers. Feed China, 2013(14):28-30.(in Chinese)
FU GH . Effects of Lactobacillus fermentum f-6 on growth performance and digestive function of broiler chickens [D]. Huhhot: Inner Mongolia Agricultural University, 2010.(in Chinese)
SHOKRYAZDANP, FASELEH JM, LIANG JB, RAMASAMYK, SIEO CC, HO YW . Effects of a Lactobacillus salivarius mixture on performance, intestinal health and serum lipids of broiler chickens PLoS One, 2017,12(5):e0175959.
DE CA, SIRRIF, MANFREDAG, MONIACIP, GIARDINIA, ZAMPIGAM, MELUZZIA . Effect of dietary supplementation with Lactobacillus acidophilus D2/CSL (CECT 4529) on caecum microbioma and productive performance in broiler chickens PLoS ONE, 2017,12(5):e0176309.
VANTSAWA PA, UMART, BULUST . Effects of probiotic Lactobacillus acidophilus on performance of broiler chickens Research Journal, 2017,5(8):302-306.
LIU NZ, CHENJ, CUI SF, YAN FH, GUW . Effects of supplementing different levels of Lactobacillus plantarum on growth performance and immunity of Broilers Acta Agriculturae Jiangxi, 2012,24(6):108-111.(in Chinese) [本文引用: 1]
AIBAY, SUZUKIN, KABIR AM, TAKAGIA, KOGAY . Lactic acid-mediated suppression of Helicobacter pylori by the oral administration of Lactobacillus salivarius as a probiotic in a gnotobiotic murine model American Journal of Gastroenterology, 1998,93(11):2097-2101. [本文引用: 1]
DERAZ SF, KARLSSON ENHEDSTR?MM, ANDERSSONM M, MATTIASSONB. Purification and characterisation of acidocin D20079, a bacteriocin produced by Lactobacillus acidophilus DSM 20079 Journal of Biotechnology, 2005,117(4):343-354. [本文引用: 1]
AOX, ZHANGX, SHIL, ZHAOK, YUJ, DONGL, CAOY, CAIY . Identification of lactic acid bacteria in traditional fermented yak milk and evaluation of their application in fermented milk products Journal of Dairy Science, 2012,95(3):1073-1084. [本文引用: 1]
HUSSEIN AR, KHALAF ZZ, SAMIRZ, SAMIRR . Antibacterial activity of crud Bacteriocin-like substance against food borne bacterial pathogens Iraqi Journal of Science, 2018,59(1A):16-24. [本文引用: 1]
ZHAO HX, ZHANY, XU ZR . Research and application of Lactobacillus Jiangxi Feed, 2003,1:9-12.(in Chinese) [本文引用: 1]
WILSONS, NORTONP, HAVERSONK, LEIGHJ, BAILEYM . Development of the palatine tonsil in conventional and germ-free piglets Developmental & Comparative Immunology, 2005,29(11):977-987. [本文引用: 1]
VON MOLLENDORFF JW, TODOROV SD, DICKS L MT . Comparison of bacteriocins produced by lactic-acid bacteria isolated from boza, a cereal-based fermented beverage from the Balkan Peninsula Current Microbiology, 2006,53(3):209-216. [本文引用: 1]
BUJALANCEC, MORENOE, JIMENEZ-VALERAM, RUIZ- BRAVOA . A probiotic strain of Lactobacillus plantarum stimulates lymphocyte responses in immunologically intact and immunocompromised mice International Journal of Food Microbiology, 2007,113(1):28-34. [本文引用: 1]