Production performance of laying hens at peak lay, sulfur compounds in manure, and selected serum profiles: efficacy of Lactobacillus species as probiotics
K. Saksrithai A C , N. H. Willits B and A. J. King AA Department of Animal Science, University of California, Davis, CA 95616, USA.
B Department of Statistics, University of California, Davis, CA 95616, USA.
C Corresponding author. Email: ksaksrithai@ucdavis.edu
Animal Production Science 60(2) 296-304 https://doi.org/10.1071/AN18724
Submitted: 24 November 2018 Accepted: 3 May 2019 Published: 3 December 2019
Abstract
Context: Probiotics have potential to improve health of laying hens, thus improving the overall quality of eggs.
Aims: A study was conducted to evaluate the use of probiotics containing Lactobacillus species to improve egg quality and serum biochemistry, and to lower the concentration of sulfur-containing gas compounds from poultry manure.
Methods: Ninety-six White Leghorn W-36 laying hens (32 weeks old) were randomly assigned to two feeding treatments: Control and Control + Probiotics. A combination of probiotics (Lactobacillus paracasei, L. plantarum and L. rhamnosus totalling 1 × 1012 CFU/kg feed) was provided for 8 weeks. At Weeks 0, 4 and 8, eggs were analysed for weight, shell thickness, albumen height and Haugh unit. Faecal matter was analysed for total sulfur, sulfate-sulfur and 20 reduced sulfur compounds. Blood serum was analysed for amylase, calcium, phosphate, total cholesterol and triglycerides.
Key results: No significant differences were observed between the two treatments for any of the parameters. Five sulfide gases were detected in manure: hydrogen sulfide (H2S), dimethyl sulfide (CH3)2S, methyl mercaptan (CH3SH), carbonyl sulfide (COS) and carbon disulfide (CS2). Ratios of various detectable gases were computed. Trends for ratios H2S : (CH3)2S, H2S : CS2, and H2S : COS from manure for both treatments were >1, whereas the ratios H2S : CH3SH and (CH3)2S : CH3SH were <1.
Conclusion: Overall, probiotics did not enhance production, egg quality or the serum profile.
Implications: Possibly, the concentration of probiotics was too high, limiting bacterial colonisation and beneficial effects.
Additional keywords: volatile sulfur compounds.
References
Aghaei A, Tabatabaei S, Chaji M, Nazari M (2010) Effects of dried whey (prebiotics) and probiotics in laying hen’s performance and intestinal flora. Journal of Animal and Veterinary Advances 9, 1996–2000.| Effects of dried whey (prebiotics) and probiotics in laying hen’s performance and intestinal flora.Crossref | GoogleScholarGoogle Scholar |
Arslan C, Saatci M (2004) Effects of probiotic administration either as feed additive or by drinking water on performance and blood parameters of Japanese quail. Archiv für Geflügelkunde 68, 160–163.
Asli MM, Hosseini SA, Lotfollahian H, Shariatmadari F (2007) Effect of probiotics, yeast, vitamin E and vitamin C supplements on performance and immune response of laying hen during high environmental temperature. International Journal of Poultry Science 6, 895–900.
| Effect of probiotics, yeast, vitamin E and vitamin C supplements on performance and immune response of laying hen during high environmental temperature.Crossref | GoogleScholarGoogle Scholar |
Bageridizaj S, Pirmohammadi R, Bampidis V (2006) Effects of dietary probiotics on performance, egg quality, and yolk/serum cholesterol of laying hens. Journal of Animal and Veterinary Advances 5, 1175–1180.
Balamuralikrishnan B, Lee SI, King IH (2017) Dietary inclusion of different multi-strain complex probiotics; effects on performance in broilers. British Poultry Science 58, 83–86.
| Dietary inclusion of different multi-strain complex probiotics; effects on performance in broilers.Crossref | GoogleScholarGoogle Scholar |
Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28, 799–808.
| The structure and synthesis of the fungal cell wall.Crossref | GoogleScholarGoogle Scholar |
Cao GT, Zhan XA, Zhang LL, Zeng XF, Chen AG, Yang CM (2018) Modulation of broilers’ caecal microflora and metabolites in response to a potential probiotic Bacillus amyloliquefaciens. Journal of Animal Physiology and Animal Nutrition 102, e909–e917.
| Modulation of broilers’ caecal microflora and metabolites in response to a potential probiotic Bacillus amyloliquefaciens.Crossref | GoogleScholarGoogle Scholar | 29314285PubMed |
Dizaji SB, Pirmohammadi R (2009) Effect of Saccharomyces cerevisiae and Bioplus 2B on performance of laying hens. International Journal of Agriculture and Biology 11, 495–497.
Eckert EH, Lee JT, Hyatt D, Stevens SM, Anderson S, Anderson PN, Beltran R, Schatzmayr G, Mohnl M, Caldwell DJ (2010) Influence of probiotic administration by feed or water on growth parameters of broilers reared on medicated and nonmedicated diets. Journal of Applied Poultry Research 19, 59–67.
| Influence of probiotic administration by feed or water on growth parameters of broilers reared on medicated and nonmedicated diets.Crossref | GoogleScholarGoogle Scholar |
Gallazzi D, Giardini A, Mangiagalli MG, Marelli S, Ferrazzi V, Orsi C, Cavalchini LG (2008) Effects of Lactobacillus acidophilus D2/CSL on laying hen performance. Italian Journal of Animal Science 7, 27–37.
| Effects of Lactobacillus acidophilus D2/CSL on laying hen performance.Crossref | GoogleScholarGoogle Scholar |
Haque I, Ahmad N, Miah MA (2017) Comparative analysis of body weight and serum biochemistry in broilers supplemented with some selected probiotics and antibiotic growth promoters. Journal of Advanced Veterinary and Animal Research 4, 288–294.
| Comparative analysis of body weight and serum biochemistry in broilers supplemented with some selected probiotics and antibiotic growth promoters.Crossref | GoogleScholarGoogle Scholar |
Hassanein S, Soliman N (2010) Effect of probiotic (Saccharomyces cerevisiae) adding to diets on intestinal microflora and performance of Hy-Line layers hens. American Journal of Science 6, 159–169.
Hatab MH, Elsayed MA, Ibrahim NS (2016) Effect of some biological supplementation on productive performance, physiological and immunological response of layer chicks. Journal of Radiation Research and Applied Science 9, 185–192.
| Effect of some biological supplementation on productive performance, physiological and immunological response of layer chicks.Crossref | GoogleScholarGoogle Scholar |
Haugh RR (1937) The Haugh unit for measuring egg quality. US Egg Poultry Magazine 43, 552–555.
Jasim MS, Taha AY (2017) Effect of supplementation of probiotic and citric acid to laying hens diet on egg quality traits. Iraqi Journal of Agricultural Science 48, 589–597.
Karimi Torshizi MA, Moghaddam AR, Rahimi SH, Mojgani N (2010) Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response. British Poultry Science 51, 178–184.
| Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response.Crossref | GoogleScholarGoogle Scholar | 20461578PubMed |
Khan SH, Atif M, Mukhtar N, Rehman A, Fareed G (2011) Effects of supplementation of multi-enzyme and multi-species probiotic on production performance, egg quality, cholesterol level and immune system in laying hens. Journal of Applied Animal Research 39, 386–398.
| Effects of supplementation of multi-enzyme and multi-species probiotic on production performance, egg quality, cholesterol level and immune system in laying hens.Crossref | GoogleScholarGoogle Scholar |
Le PD, Aarnink AJ, Jongbloed AW, Peet-Schwering CM, Ogink NW, Verstegen MW (2007) Effects of dietary crude protein level on odour from pig manure. Animal 1, 734–744.
| Effects of dietary crude protein level on odour from pig manure.Crossref | GoogleScholarGoogle Scholar | 22444473PubMed |
Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 70, 317–343.
| Cell wall assembly in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 16760306PubMed |
Leulier F, MacNeil LT, Lee WJ, Rawls JF, Cani PD, Schwazer M, Zhao L, Simpson SJ (2017) Integrative physiology: at the crossroads of nutrition, microbiota, animal physiology, and human health. Cell Metabolism 25, 522–534.
| Integrative physiology: at the crossroads of nutrition, microbiota, animal physiology, and human health.Crossref | GoogleScholarGoogle Scholar | 28273475PubMed |
Line JE, Bailey JS, Cox NA, Stern NJ, Tompkins T (1998) Effect of yeast-supplemented feed on Salmonella and Campylobacter populations in broilers. Poultry Science 77, 405–410.
| Effect of yeast-supplemented feed on Salmonella and Campylobacter populations in broilers.Crossref | GoogleScholarGoogle Scholar | 9521452PubMed |
Lokapirnasari WP, Dewi AR, Fathinah A, Hidanah S, Harijani N, Soeharsono S, Karimah B, Andriani AD (2017) Effect of probiotic supplementation on organic feed to alternative antibiotic growth promoter on production performance and economics analysis of quail. Veterinary World 10, 1508–1514.
| Effect of probiotic supplementation on organic feed to alternative antibiotic growth promoter on production performance and economics analysis of quail.Crossref | GoogleScholarGoogle Scholar | 29391694PubMed |
Lye HS, Rahmat-Ali GR, Liong MT (2010) Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. International Dairy Journal 20, 169–175.
| Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract.Crossref | GoogleScholarGoogle Scholar |
Mansoub NH (2010) Effect of probiotic bacteria utilization on serum cholesterol and triglycerides contents and performance of broiler chickens. Global Veterinaria 5, 184–186.
Mikulski D, Jankowski J, Naczmanski J, Mikulska M, Demey V (2012) Effects of dietary probiotic (Pediococcus acidilactici) supplementation on performance, nutrient digestibility, egg traits, egg yolk cholesterol, and fatty acid profile in laying hens. Poultry Science 91, 2691–2700.
| Effects of dietary probiotic (Pediococcus acidilactici) supplementation on performance, nutrient digestibility, egg traits, egg yolk cholesterol, and fatty acid profile in laying hens.Crossref | GoogleScholarGoogle Scholar | 22991559PubMed |
Muyyarikkandy MS, Amalaradjou MA (2017) Lactobacillus bulgaricus, Lactobacillus rhamnosus and Lactobacillus paracasei attenuate Salmonella Enteritidis, Salmonella Heidelberg and Salmonella Typhimurium colonization and virulence gene expression in vitro. International Journal of Molecular Sciences 18, 2381
| Lactobacillus bulgaricus, Lactobacillus rhamnosus and Lactobacillus paracasei attenuate Salmonella Enteritidis, Salmonella Heidelberg and Salmonella Typhimurium colonization and virulence gene expression in vitro.Crossref | GoogleScholarGoogle Scholar |
Naidu A, Xie X, Leumer D, Harrison S, Burrill M, Fonda E (2002) Reduction of sulfide, ammonia compounds, and adhesion properties of Lactobacillus casei strain KE99 in vitro. Current Microbiology 44, 196–205.
| Reduction of sulfide, ammonia compounds, and adhesion properties of Lactobacillus casei strain KE99 in vitro.Crossref | GoogleScholarGoogle Scholar | 11821928PubMed |
Naqvi ZH, Hassan MM, Xhaudry Z, Akram M, Ahmad R (2000) Effect of Effective Microorganisms (EM4) on health of layers. Pakistan Journal of Biological Sciences 3, 1516–1518.
| Effect of Effective Microorganisms (EM4) on health of layers.Crossref | GoogleScholarGoogle Scholar |
Nguyen TDT, Kang JH, Lee MS (2007) Chaaracterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. International Journal of Food Microbiology 113, 358–361.
| Chaaracterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects.Crossref | GoogleScholarGoogle Scholar |
Nosrati M, Javandel F, Camacho LM, Khusro A, Cipriano M, Seidavi A, Salem AZM (2017) The effects of antibiotic, probiotic, organic acid, vitamin C, and Echinacea purpurea extract on performance, carcass characteristics, blood chemistry, microbiota, and immunity of broiler chickens. Journal of Applied Poultry Research 26, 295–306.
NRC (1994) ‘Nutrient requirements of poultry.’ 9th revised edn. (The National Academy Press: Washington, DC)
Ofek I, Mirelman D, Sharon N (1977) Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature 265, 623–625.
| Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors.Crossref | GoogleScholarGoogle Scholar | 323718PubMed |
Onderci M, Sahin N, Sahin K, Cikim G, Aydin A, Ozercan I, Aydin S (2006) Efficacy of supplementation of α-amylase-producing bacterial culture on the performance, nutrient use, and gut morphology of broiler chickens fed a corn-based diet. Poultry Science 85, 505–510.
| Efficacy of supplementation of α-amylase-producing bacterial culture on the performance, nutrient use, and gut morphology of broiler chickens fed a corn-based diet.Crossref | GoogleScholarGoogle Scholar | 16553283PubMed |
Oyofo BA, Droleskey RE, Norman JO, Mollenhauer HH, Ziprin RL, Corrier DE, DeLoach JR (1989) Inhibition by mannose of in vitro colonization of chicken small intestine by Salmonella typhimurium. Poultry Science 68, 1351–1356.
| Inhibition by mannose of in vitro colonization of chicken small intestine by Salmonella typhimurium.Crossref | GoogleScholarGoogle Scholar | 2685796PubMed |
Panda AK, Reddy MR, Rama Rao SV, Praharaj NK (2003) Production performance, serum/yolk cholesterol and immune competence of White Leghorn layers as influenced by dietary supplementation with probiotic. Tropical Animal Health and Production 35, 85–94.
| Production performance, serum/yolk cholesterol and immune competence of White Leghorn layers as influenced by dietary supplementation with probiotic.Crossref | GoogleScholarGoogle Scholar | 12636363PubMed |
Parvaneh K, Jamaluddin R, Karimi G, Erfani R (2014) Effect of probiotics supplementation on bone mineral content and bone mass density. The Scientific World Journal 2014, 595962
Rajput IR, Li YL, Xu X, Huang Y, Zhi WC, Yu DY, Li W (2013) Supplementary effects of Saccharomyces boulardii and Bacillus subtilis B10 on digestive enzyme activities, antioxidation capacity and blood homeostasis in broiler. International Journal of Agriculture and Biology 15, 231–237.
Ramasamy K, Abdullah N, Jalaludin S, Wang M, Ho YW (2009) Effects of Lactobacillus cultures on performance of laying hens, and total cholesterol, lipid and fatty acid composition of egg yolk. Journal of the Science of Food and Agriculture 89, 482–486.
| Effects of Lactobacillus cultures on performance of laying hens, and total cholesterol, lipid and fatty acid composition of egg yolk.Crossref | GoogleScholarGoogle Scholar |
Saksrithai K, King AJ (2019) Lactobacillus and dietary sunflower meal supplementation in layer diets: effects on specific serum content and hydrogen sulfide concentration in layer manure. Research in Veterinary Science 122, 64–71.
| Lactobacillus and dietary sunflower meal supplementation in layer diets: effects on specific serum content and hydrogen sulfide concentration in layer manure.Crossref | GoogleScholarGoogle Scholar | 30463030PubMed |
Schostera A, Kokotovicb B, Perminc A, Pedersend P, Dal Bellod F, Guardabassia L (2013) In vitro inhibition of Clostridium difficile and Clostridium perfringens by commercial probiotic strains. Clinical Microbiology (Los Angeles, Calif.) 20, 36–41.
Shalaei M, Hosseini SM, Zergani E (2014) Effect of different supplements on eggshell quality, some characteristics of gastrointestinal tract and performance of laying hens. Veterinary Research Forum : An International Quarterly Journal 5, 277–286.
Slover CM, Danzijer L (2008) Lactobacillus: a review. Clinical Microbiology Newsletter 30, 23–27.
| Lactobacillus: a review.Crossref | GoogleScholarGoogle Scholar |
Sobczak A, Kozlowski K (2015) The effect of probiotic preparation containing Bacillus subtilis ATCC PTA-6737 on egg production and physiological parameters of laying hens. Annals of Animal Science 15, 711–723.
| The effect of probiotic preparation containing Bacillus subtilis ATCC PTA-6737 on egg production and physiological parameters of laying hens.Crossref | GoogleScholarGoogle Scholar |
Tapingkae W, Panyachai K, Yachai M, Doan HV (2018) Effects of dietary red yeast (Sporidiobolus pararoseus) on production performance and egg quality of laying hens. Journal of Animal Physiology and Animal Nutrition 102, e337–e344.
| Effects of dietary red yeast (Sporidiobolus pararoseus) on production performance and egg quality of laying hens.Crossref | GoogleScholarGoogle Scholar | 28608538PubMed |
Torrallardona D, Harris CI, Fuller MF (1996) Microbial amino acid synthesis and utilization in rats: the role of coprophagy. British Journal of Nutrition 76, 701–709.
| Microbial amino acid synthesis and utilization in rats: the role of coprophagy.Crossref | GoogleScholarGoogle Scholar | 8958004PubMed |
Verdenelli M, Ghelfi F, Silvi S, Orpianesi C, Cecchini C, Cresci A (2009) Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. European Journal of Nutrition 48, 355–363.
| Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces.Crossref | GoogleScholarGoogle Scholar | 19365593PubMed |
Wang H, Ni X, Qing X, Zeng D, Luo M, Liu L, Li G, Pan K, Jing B (2017) 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 8, 1073
| Live probiotic Lactobacillus johnsonii BS15 promotes growth performance and lowers fat deposition by improving lipid metabolism, intestinal development, and gut microflora in broilers.Crossref | GoogleScholarGoogle Scholar | 28659893PubMed |
Youssef AW, Hassan HMA, Ali HM, Moamed MA (2013) Effect of probiotics, prebiotics and organic acids on layer performance and egg quality. Asian Journal of Political Science 7, 1–10.
Yun W, Lee DH, Choi YI, Kim IH, Cho JH (2017) Effects of supplementation of probiotics and prebiotics on growth performance, nutrient digestibility, organ weight, fecal microbiota, blood profile, and excreta noxious gas emissions in broilers. Journal of Applied Poultry Research 26, 584–592.
| Effects of supplementation of probiotics and prebiotics on growth performance, nutrient digestibility, organ weight, fecal microbiota, blood profile, and excreta noxious gas emissions in broilers.Crossref | GoogleScholarGoogle Scholar |
Zarei M, Ehsani M, Torki M (2011) Dietary inclusion of probiotics, prebiotics and synbiotic and evaluating performance of laying hens. American Journal of Agricultural and Biological Sciences 6, 249–255.
| Dietary inclusion of probiotics, prebiotics and synbiotic and evaluating performance of laying hens.Crossref | GoogleScholarGoogle Scholar |
Zhi-gang T, Naeem M, Chao W, Tian W, Yan-min Z (2014) Effect of dietary probiotics supplementation with different nutrient density on growth performance, nutrient retention and digestive enzyme activities in broilers. Journal of Animal and Plant Science 24, 1309–1315.
Zhu J (2000) A review of microbiology in swine manure odor control. Agriculture, Ecosystems & Environment 78, 93–106.
| A review of microbiology in swine manure odor control.Crossref | GoogleScholarGoogle Scholar |