Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T05:09:08.578Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of homofermentative and heterofermentative lactic acid bacteria for alfalfa silage: a meta-analysis

Published online by Cambridge University Press:  15 May 2020

J. E. Blajman Open the ORCID record for J. E. Blajman [Opens in a new window] ,
G. Vinderola ,
R. B. Páez  and
M. L. Signorini
J. E. Blajman*
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Instituto Nacional de Tecnología Agropecuaria EEA Rafaela, Ruta 34 Km. 227, 2300 Rafaela, Santa Fe, Argentina
G. Vinderola
Affiliation:
Instituto de Lactología Industrial (CONICET-UNL), Facultad de Ingeniería Química, Universidad Nacional del Litoral, Santiago del Estero 2829, 3000 Santa Fe, Argentina
R. B. Páez
Affiliation:
Instituto Nacional de Tecnología Agropecuaria EEA Rafaela, Ruta 34 Km. 227, 2300 Rafaela, Santa Fe, Argentina
M. L. Signorini
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Instituto Nacional de Tecnología Agropecuaria EEA Rafaela, Ruta 34 Km. 227, 2300 Rafaela, Santa Fe, Argentina
*
Author for correspondence: J. E. Blajman, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Lactic acid bacteria (LAB) are usually employed as alfalfa silage inoculants to obtain high-quality feed for animal husbandry. However, the effects of these inoculants are still unclear and need to be studied extensively. Therefore, the objective of this meta-analysis was to quantitatively summarize published research studies that assess the effects of homofermentative (HoLAB) and heterofermentative lactic acid bacteria (HeLAB) on fermentation parameters, nutritive value, microbiological composition and aerobic stability of alfalfa silage. PubMed, ScienceDirect and Scopus have been screened for articles published from 1980 to 2018. The criteria for inclusion were: randomized and controlled trials using alfalfa silage and published in peer-reviewed journals. It was found that inoculation with LAB decreased silage pH, neutral detergent fibre, acid detergent fibre and ammoniacal nitrogen, while it increased dry matter and crude protein compared to control in the pooled raw mean difference random-effect model. Additionally, LAB inoculation decreased acetate, propionate, ethanol and butyrate concentrations, whereas it increased lactate. In addition, inoculants reduced the counts of yeasts and moulds. Lastly, LAB inoculation improved aerobic stability. To the best of our knowledge, this is the first meta-analysis that aims at comparing the application of HoLAB and HeLAB for alfalfa silage. In the pool estimate, positive effects attributable to the application of microbial silage inoculants were found in most of the evaluated parameters; supporting the importance of applying both types of inoculants to improve forage preservation for the livestock industry.

Keywords

EnsilingEnterococcus faeciumLactobacillus buchneriLactobacillus plantarumLucernePediococcus acidilactici
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 158 , Issue 1-2 , March 2020 , pp. 107 - 118
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acosta Aragón, Y, Jatkauskas, J and Vrotniakienė, V (2012) The effect of a silage inoculant on silage quality, aerobic stability, and meat production on farm scale. International Scholarly Research Notices: Veterinary Science 2012, 1–6.Google ScholarPubMed
Adesogan, AT, Arriola, KG, Jiang, Y, Oyebade, A, Paula, EM, Pech-Cervantes, AA, Romero, JJ, Ferraretto, LF and Vyas, D (2019) Symposium review: technologies for improving fibre utilization. Journal of Dairy Science 102, 5726–5755.10.3168/jds.2018-15334CrossRefGoogle Scholar
Arriola, KG, Oliveira, AS, Ma, ZX, Lean, IJ, Giurcanu, MC and Adesogan, AT (2017) A meta-analysis on the effect of dietary application of exogenous fibrolytic enzymes on the performance of dairy cows. Journal of Dairy Science 100, 1–15.10.3168/jds.2016-12103CrossRefGoogle ScholarPubMed
Ashbell, G, Weinberg, ZG, Hen, Y and Filya, I (2002) The effects of temperature on the aerobic stability of wheat and corn silages. The Journal of Industrial Microbiology and Biotechnology 28, 261–263.10.1038/sj.jim.7000237CrossRefGoogle ScholarPubMed
Begg, CB and Mazumdar, M (1994) Operating characteristics of rank correlation test for publication bias. Biometrics 50, 1088–1101.CrossRefGoogle ScholarPubMed
Blajman, JE, Páez, RB, Vinderola, CG, Lingua, MS and Signorini, ML (2018) A meta-analysis on the effectiveness of lactic acid bacteria for corn silage. Journal of Applied Microbiology 125, 1655–1669.CrossRefGoogle Scholar
Borenstein, M, Hedges, LV, Higgins, JPT and Rothstein, HR (2009) Introduction to Meta-Analysis. Chichester, West Sussex, UK: John Wiley & Sons, Ltd.10.1002/9780470743386CrossRefGoogle Scholar
Borreani, G, Tabacco, E, Schmidt, RJ, Holmes, BJ and Muck, RE (2018) Silage review: factors affecting dry matter and quality losses in silages. Journal of Dairy Science 101, 3952–3979.CrossRefGoogle ScholarPubMed
Chen, L, Dong, Z, Li, J and Shao, T (2018) Ensiling characteristics, in Vitro rumen fermentation, microbial communities and aerobic stability of low-dry matter silages produced with sweet sorghum and alfalfa mixtures. Journal of the Science of Food and Agriculture 99, 2140–2151.10.1002/jsfa.9406CrossRefGoogle ScholarPubMed
Chilson, JM, Rezam, P, Drewnoski, M, Price, W and Hunt, CW (2016) Effect of homofermentative lactic acid bacteria and exogenous hydrolytic enzymes on the ensiling characteristics and rumen degradability of alfalfa and corn silages. The Professional Animal Scientist 32, 598–604.10.15232/pas.2015-01494CrossRefGoogle Scholar
Contreras-Govea, FE, Muck, RE, Mertens, DR and Weimer, PJ (2011) Microbial inoculant effects on silage and in vitro ruminal fermentation, and microbial biomass estimation for alfalfa, bmr corn, and corn silages. Animal Feed Science and Technology 163, 2–10.10.1016/j.anifeedsci.2010.09.015CrossRefGoogle Scholar
Danner, H, Holzer, M, Mayrhuber, E and Braun, R (2003) Acetic acid increases stability of silage under aerobic conditions. Applied and Environmental Microbiology 69, 562–570.10.1128/AEM.69.1.562-567.2003CrossRefGoogle ScholarPubMed
Dolci, P, Tabacco, E, Cocolin, L and Borreani, G (2011) Microbial dynamics during aerobic exposure of corn silage stored under oxygen barrier or polyethylene films. Applied and Environmental Microbiology 77, 7499–7507.10.1128/AEM.05050-11CrossRefGoogle ScholarPubMed
Dunière, L, Sindou, J, Chaucheyras-Durand, F, Chevallier, I and Thévenot-Sergentet, D (2013) Silage processing and strategies to prevent persistence of undesirable microorganisms. Animal Feed Science and Technology 182, 1–15.10.1016/j.anifeedsci.2013.04.006CrossRefGoogle Scholar
Duval, S and Tweedie, R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455–463.10.1111/j.0006-341X.2000.00455.xCrossRefGoogle ScholarPubMed
Egger, M, Davey Smith, G, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629–634.10.1136/bmj.315.7109.629CrossRefGoogle ScholarPubMed
Ferrero, F, Piano, S, Tabacco, E and Borreani, G (2019) Effects of conservation period and Lactobacillus hilgardii inoculum on the fermentation profile and aerobic stability of whole corn and sorghum silages. Journal of the Science of Food and Agriculture 99, 2530–2540.10.1002/jsfa.9463CrossRefGoogle ScholarPubMed
Filya, E and Sucu, I (2007) The effect of bacterial inoculants and a chemical preservative on the fermentation and aerobic stability of whole-crop cereal silages. Asian-Australasian Journal of Animal Sciences 20, 378–384.CrossRefGoogle Scholar
Heinl, S and Grabherr, R (2017) Systems biology of robustness and flexibility: Lactobacillus buchneri – a show case. Journal of Biotechnology 257, 61–69.10.1016/j.jbiotec.2017.01.007CrossRefGoogle ScholarPubMed
Higgins, JPT and Thompson, SG (2002) Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 1539–1558.10.1002/sim.1186CrossRefGoogle ScholarPubMed
Jatkauskas, J, Vrotniakiene, V, Ohlsson, C and Lund, B (2013) The effects of three silage inoculants on aerobic stability in grass, clover-grass, lucerne and maize silages. Agricultural and Food Science 22, 137–144.CrossRefGoogle Scholar
Kozelov, LK, Iliev, F, Hristov, AN, Zaman, S and McAllister, TA (2008) Effect of fibrolytic enzymes and an inoculant on in vitro degradability and gas production of low-dry matter alfalfa silage. Journal of the Science of Food and Agriculture 88, 2568–2575.CrossRefGoogle Scholar
Kung, L Jr (2010) Aerobic stability of silage. Univ. California, Davis.Google Scholar
Kung, L Jr and Ranjit, NK (2001) The effect of Lactobacillus buchneri and other additives on the fermentation and aerobic stability of barley silage. Journal of Dairy Science 84, 1149–1155.CrossRefGoogle ScholarPubMed
Kung, L Jr, Shaver, RD, Grant, RJ and Schmidt, RJ (2018) Silage review: interpretation of chemical, microbial, and organoleptic components of silages. Journal of Dairy Science 101, 4020–4033.CrossRefGoogle ScholarPubMed
Lean, IJ, Rabiee, AR, Duffield, TF and Dohoo, IR (2009) Invited review: use of meta-analysis in animal health and reproduction: methods and applications. Journal of Dairy Science 92, 3545–3565.CrossRefGoogle ScholarPubMed
Li, D, Wang, Y, Zhang, Y, Lin, Y and Yang, F (2018) Evaluation of lactic acid bacteria isolated from alfalfa for silage fermentation. Grass Science 64, 190–198.10.1111/grs.12198CrossRefGoogle Scholar
Liu, C, Lai, Y, Lu, X, Guo, P and Luo, H (2016) Effect of lactic acid bacteria inoculants on alfalfa (Medicago sativa L.) silage quality: assessment of degradation (in Situ) and gas production (in vitro). Journal of Integrative Agriculture 15, 2834–2841.CrossRefGoogle Scholar
Liu, QH, Dong, ZH and Shao, T (2018) Effect of additives on fatty acid profile of high moisture alfalfa silage during ensiling and after exposure to air. Animal Feed Science and Technology 236, 29–38.CrossRefGoogle Scholar
Lynch, JP, Baah, J and Beauchemin, KA (2015) Conservation, fibre digestibility, and nutritive value of corn harvested at 2 cutting heights and ensiled with fibrolytic enzymes, either alone or with a ferulic acid esterase-producing inoculant. Journal Dairy Science 98, 1214–1224.10.3168/jds.2014-8768CrossRefGoogle ScholarPubMed
McDonald, P, Henderson, AR and Heron, SJE (1991) The Biochemistry of Silage, 2nd Edn. Aberystwyth: Cambrian Printers Ltd, pp. 184–236.Google Scholar
McEniry, J, O'Kiely, P, Clipson, NJW, Forristal, PD and Doyle, EM (2006) The microbiological and chemical composition of baled and precision-chop silages on a sample of farms in County Meath. Irish Journal of Agricultural and Food Research 45, 73–83.Google Scholar
McKersie, BD and Buchanan-Smith, J (1982) Changes in the levels of proteolytic enzymes in ensiled alfalfa forage. Canadian Journal of Plant Science 62, 111–116.CrossRefGoogle Scholar
Muck, RE (2010) Silage microbiology and its control through additives. Revista Brasileira de Zootecnia 39, 183–191.CrossRefGoogle Scholar
Muck, RE, Nadeau, EMG, McAllister, TA, Contreras-Govea, FE, Santos, MC and Kung, L Jr (2018) Silage review: recent advances and future uses of silage additives. Journal of Dairy Science 101, 3980–4000.10.3168/jds.2017-13839CrossRefGoogle ScholarPubMed
Nascimento Agarussi, MC, Gomes Pereira, O, de Paula, RA, da Silva, VP, Santos Roseira, JP and Fonseca e Silva, F (2019) Novel lactic acid bacteria strains as inoculants on alfalfa silage fermentation. Scientific Reports 9, 8007.CrossRefGoogle ScholarPubMed
Ni, K, Wang, Y, Cai, Y and Pang, H (2015) Natural lactic acid bacteria population and silage fermentation of whole-crop wheat. Asian-Australasian Journal of Animal Sciences 28, 1123–1132.CrossRefGoogle ScholarPubMed
Nishino, N, Yoshida, M, Shiota, H and Sakaguchi, E (2003) Accumulation of 1,2-propanediol and enhancement of aerobic stability in whole crop maize silage inoculated with Lactobacillus buchneri. Journal of Applied Microbiology 94, 800–807.10.1046/j.1365-2672.2003.01810.xCrossRefGoogle ScholarPubMed
Ogunade, IM, Kim, DH, Jiang, Y, Weinberg, ZG, Jeong, KC and Adesogan, AT (2016) Control of Escherichia coli O157:H7 in contaminated alfalfa silage: effects of silage additives. Journal of Dairy Science 99, 4427–4436.CrossRefGoogle ScholarPubMed
Oliveira, AS, Weinberg, ZG, Ogunade, IM, Cervantes, AAP, Arriola, KG, Jiang, Y, Kim, D, Li, X, Gonçalves, MCM, Vyas, D and Adesogan, AT (2017) Meta-analysis of effects of inoculation with homofermentative and facultative heterofermentative lactic acid bacteria on silage fermentation, aerobic stability, and the performance of dairy cows. Journal of Dairy Science 100, 4587–4603.CrossRefGoogle ScholarPubMed
Oude Elferink, SJWH, Krooneman, J, Gottschal, JC, Spoelstra, SF, Faber, F and Driehuis, F (2001) Anaerobic conversion of lactic acid to acetic acid and 1,2-propanediol by Lactobacillus buchneri. Applied and Environmental Microbiology 67, 125–132.CrossRefGoogle ScholarPubMed
Ozduven, ML and Celebicam, A (2017) The effects of bacterial inoculants and/or enzymes on the fermentation characteristics and aerobic stability of alfalfa ensiled at different stages of maturity. International Journal of Current Research 9, 45983–45988.Google Scholar
Pahlow, G, Muck, RE, Driehuis, F, Oude Elferink, SJWH and Spoelstra, SF (2003) Microbiology of ensiling. In Buxton, DR, Muck, RE and Harrison, HJ (eds), Silage Science and Technology (Agronomy Series No. 42). Madison, WI: American Society of Agronomy, pp. 31–93.Google Scholar
Rabelo, CHS, Mari, LJ and Reis, RA (2016) Survey about the use of bacterial inoculants in Brazil: effects on silage quality and animal performance. In Silva, T and Santos, EM (eds), Advances in Silage Production and Utilization. Rijeka, Croatia: IntechOpen, pp. 3–37.Google Scholar
Rabelo, CHS, Lara, EC, Basso, FC, Härter, CJ and Reis, RA (2018) Growth performance of finishing feedlot lambs fed maize silage inoculated with Bacillus subtilis and lactic acid bacteria. The Journal of Agricultural Science, Cambridge 156, 839–847.10.1017/S0021859618000679CrossRefGoogle Scholar
Randby, AT, Weisbjerg, MR, Nørgaard, P and Heringstad, B (2012) Early lactation feed intake and milk yield responses of dairy cows offered grass silages harvested at early maturity stages. Journal of Dairy Science 95, 304–317.CrossRefGoogle ScholarPubMed
Santos, MC and Kung, L Jr (2016) Short communication: the effects of dry matter and length of storage on the composition and nutritive value of alfalfa silage. Journal of Dairy Science 99, 5466–5469.10.3168/jds.2016-10866CrossRefGoogle ScholarPubMed
Sariçiçek, BZ, Yildirim, B, Kocabaş, Z and Özgümüş Demir, E (2016) The effects of storage time on nutrient composition and silage quality parameters of corn silage made in plastic mini silo in laboratory conditions. Igdir University Journal of the Institute of Science and Technology 6, 177–183.10.21597/jist.2016321853CrossRefGoogle Scholar
Schmidt, RJ, Hu, W, Mills, JA and Kung, L Jr (2009) The development of lactic acid bacteria and Lactobacillus buchneri. Journal of Dairy Science 92, 5005–5010.CrossRefGoogle ScholarPubMed
Shelby, LB and Vaske, JJ (2008). Understanding meta-analysis: a review of the methodological literature. Leisure Sciences 30, 96–110.CrossRefGoogle Scholar
Twarużek, M, Dorszewski, P, Grabowicz, M, Szterk, P, Grajewski, J and Kaszkowiak, J (2016) Effect of additives on the fermentation profile, microbial colonization and oxygen stress of alfalfa silages. Journal of Elementology 21, 1161–1172.Google Scholar
Wang, J, Wang, JQ, Zhou, H and Feng, T (2009) Effects of addition of previously fermented juice prepared from alfalfa on fermentation quality and protein degradation of alfalfa silage. Animal Feed Science and Technology 151, 280–290.CrossRefGoogle Scholar
Wang, S, Guo, G, Li, J, Chen, L, Dong, Z and Shao, T (2019) Improvement of fermentation profile and structural carbohydrate compositions in mixed silages ensiled with fibrolytic enzymes, molasses and Lactobacillus plantarum MTD-1. Italian Journal of Animal Science 18, 328–335.CrossRefGoogle Scholar
Weinberg, ZG, Khanal, P, Yildiz, C, Chen, Y and Arieli, A (2010) Effects of stage of maturity at harvest, wilting and LAB inoculant on aerobic stability of wheat silages. Animal Feed Science and Technology 158, 29–35.10.1016/j.anifeedsci.2010.03.006CrossRefGoogle Scholar
Xu, Z, He, H, Zhang, S and Kong, J (2017) Effects of inoculants Lactobacillus brevis and Lactobacillus parafarraginis on the fermentation characteristics and microbial communities of corn stover silage. Scientific Reports 7, 13614.CrossRefGoogle ScholarPubMed
Yuan, XJ, Wen, AY, Wang, J, Desta, ST, Dong, ZH and Shao, T (2018) Effects of four short-chain fatty acids or salts on fermentation characteristics and aerobic stability of alfalfa (Medicago sativa L.) silage. Journal of the Science of Food and Agriculture 98, 328–335.CrossRefGoogle ScholarPubMed
Zhang, T, Li, L, Wang, X, Zeng, Z, Hu, Y and Cui, Z (2009) Effects of Lactobacillus buchneri and Lactobacillus plantarum on fermentation, aerobic stability, bacteria diversity and ruminal degradability of alfalfa silage. World Journal of Microbiology and Biotechnology 25, 965–971.CrossRefGoogle Scholar
Zhang, W, Grimi, N, Jaffrin, MY, Ding, L and Tang, B (2017) A short review on the research progress in alfalfa leaf protein separation technology. Journal of the Society of Chemical Industry 92, 2894–2900.Google Scholar
Zielińska, K, Fabiszewska, A and Stefańska, I (2015) Different aspects of Lactobacillus inoculants on the improvement of quality and safety of alfalfa silage. Chilean Journal of Agricultural Research 75, 298–306.10.4067/S0718-58392015000400005CrossRefGoogle Scholar