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
Open accessAbstract
Forages are usually inoculated with homofermentative and facultative heterofermentative lactic acid bacteria (LAB) to enhance lactic acid fermentation of forages, but effects of such inoculants on silage quality and the performance of dairy cows are unclear. Therefore, we conducted a meta-analysis to examine the effects of LAB inoculation on silage quality and preservation and the performance of dairy cows. A second objective was to examine the factors affecting the response to silage inoculation with LAB. The studies that met the selection criteria included 130 articles that examined the effects of LAB inoculation on silage quality and 31 articles that investigated dairy cow performance responses. The magnitude of the effect (effect size) was evaluated using raw mean differences (RMD) between inoculated and uninoculated treatments. Heterogeneity was explored by meta-regression and subgroup analysis using forage type, LAB species, LAB application rate, and silo scale (laboratory or farm-scale) as covariates for the silage quality response and forage type, LAB species, diet type [total mixed ration (TMR) or non-TMR], and the level of milk yield of the control cows as covariates for the performance responses. Inoculation with LAB (≥10 5 cfu/g as fed) markedly increased silage fermentation and dry matter recovery in temperate and tropical grasses, alfalfa, and other legumes. However, inoculation did not improve the fermentation of corn, sorghum, or sugarcane silages. Inoculation with LAB reduced clostridia and mold growth, butyric acid production, and ammonia-nitrogen in all silages, but it had no effect on aerobic stability. Silage inoculation (≥10 5 cfu/g as fed) increased milk yield and the response had low heterogeneity. However, inoculation had no effect on diet digestibility and feed efficiency. Inoculation with LAB improved the fermentation of grass and legume silages and the performance of dairy cows but did not affect the fermentation of corn, sorghum, and sugar cane silages or the aerobic stability of any silage. Further research is needed to elucidate how silage inoculated with homofermentative and facultative heterofermentative LAB improves the performance of dairy cows.
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Compared with homofermentative lactic acid bacteria, heterofermentative lactic acid bacteria have half the lactate synthesis efficiency and produce more acetic acid and carbon dioxide, which leads to poor silage fermentation.
“Compared with homofermentative lactic acid bacteria, heterofermentative lactic acid bacteria have half the lactate synthesis efficiency and produce more acetic acid and carbon dioxide, which leads to poor silage fermentation [23,25].”
From Analysis on Fermentation Quality, Chemical Composition and Bacterial Communities of Corn Straw and Soybean Straw Mixed Silage (2023) · cites this paper as [23]
The Conclusions (page unavailable) say that inoculation with homofermentative or facultative heterofermentative LAB markedly enhanced fermentation in grass and legume silages, rather than leading to poor fermentation. The paper does not establish the claimed half-efficiency comparison or greater carbon dioxide production; its findings concern facultative heterofermentative LAB, not all heterofermentative LAB. (LLM, conf=0.78)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredThe addition of heterofermentative lactic acid bacteria can help to extend the storage and utilization time of silage.
“The addition of heterofermentative lactic acid bacteria can help to extend the storage and utilization time of silage [23].”
From Analysis on Fermentation Quality, Chemical Composition and Bacterial Communities of Corn Straw and Soybean Straw Mixed Silage (2023) · cites this paper as [23]
The Silage Quality results (page unavailable) report that inoculation with the homofermentative and facultative heterofermentative bacteria studied did not affect aerobic stability (P = 0.27). The paper finds improved fermentation for some forages, but not the longer usable life attributed to it. (LLM, conf=0.85)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredAfter the aerobic fermentation period, silage enters an anaerobic state, and lactic acid bacteria rapidly reproduce and produce a large amount of lactic acid, which inhibits the activity of harmful microorganisms such as Clostridium.
“After the aerobic fermentation period, silage enters an anaerobic state, and lactic acid bacteria rapidly reproduce and produce a large amount of lactic acid, which inhibits the activity of harmful microorganisms such as Clostridium [23].”
From Analysis on Fermentation Quality, Chemical Composition and Bacterial Communities of Corn Straw and Soybean Straw Mixed Silage (2023) · cites this paper as [23]
The Introduction (page unavailable) describes lactic-acid fermentation under anaerobic conditions and says the resulting low pH inhibits harmful microbes. Silage Quality (page unavailable) reports that LAB inoculation increased lactate and reduced clostridia in some forage types. The paper does not establish the claimed sequence in which an aerobic fermentation period ends before silage becomes anaerobic, and its inoculation findings do not apply to every forage type. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHomofermentative LAB inoculants are successful in reducing pH and shifting fermentation toward lactate in the majority of studies.
“Reviews (e.g., Muck and Kung, 1997; Oliveira et al., 2017) indicate homofermentative inoculants are successful in reducing pH and shifting fermentation toward lactate in the majority of studies.”
From Silage review: Factors affecting dry matter and quality losses in silages (2018) · cites this paper as Oliveira et al., 2017
The Silage Quality results (page unavailable) report that LAB inoculation reduced pH and increased lactate overall. The paper also says these fermentation improvements occurred in grasses and legumes but not in corn, sorghum, or sugarcane; it does not establish that they occurred in a majority of individual studies. (LLM, conf=0.86)
Experimental — accuracy not yet measuredA meta-analysis indicated no reduction in pH in corn, sorghum, and sugarcane silages relative to untreated silages.
“although a meta-analysis indicated no reduction in pH in corn, sorghum, and sugarcane silages relative to untreated silages.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
The Silage Quality results (page not supplied) report no pH effect for corn and sorghum silages, supporting that part of the claim. They also report that inoculation significantly reduced pH in sugarcane silage, contrary to the claim for sugarcane. (LLM, conf=0.91)
Experimental — accuracy not yet measured
Inoculation reduced pH of silages in temperate and tropical grasses and in alfalfa and other legumes, but not in corn, sorghum, and sugarcane.
“Inoculation reduced the pH of silages in temperate and tropical grasses and in alfalfa and other legumes, but not in corn, sorghum, and sugarcane.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
The Silage Quality results report reduced pH in temperate and tropical grasses and alfalfa, and no pH effect in corn and sorghum. But they also explicitly report reduced pH in sugarcane silage, contrary to that part of the claim. The broader discussion says sugarcane fermentation was not improved; that does not establish that its pH was unchanged. (LLM, conf=0.90)
Experimental — accuracy not yet measuredDry matter recovery was 2.8 percentage units higher in grass silages compared with untreated, unaffected in corn and sorghum silages, and reduced by 2.4 percentage units in sugarcane silage.
“Dry matter recovery was 2.8 percentage units higher in grass silages compared with untreated, unaffected corn and sorghum silages, and reduced by 2.4 percentage units in sugarcane silage.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
The Silage Quality section reports that LAB inoculation increased dry matter recovery in temperate and tropical grass silages, had no effect in corn and sorghum silages, and reduced it in sugarcane silage. The passages available from our copy do not give the claimed forage-specific magnitudes of 2.8 and 2.4 percentage units; they refer instead to Figure 3 (page not provided). (LLM, conf=0.84)
Experimental — accuracy not yet measuredSilage fermentation is a complex biochemical process mainly dominated by anaerobic lactic acid bacteria.
“Silage fermentation is a complex biochemical process mainly dominated by anaerobic lactic acid bacteria [23].”
From Analysis on Fermentation Quality, Chemical Composition and Bacterial Communities of Corn Straw and Soybean Straw Mixed Silage (2023) · cites this paper as [23]
Homofermentative LAB additives resulted in higher milk production according to a meta-analysis.
“These additives resulted in higher milk production according to the meta-analysis by mechanisms that are still unclear.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Milk production increases by inoculation were not affected by forage type, inoculant species, or level of milk production.
“Milk production increases by inoculation were not affected by forage type, inoculant species, or level of milk production.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Aerobic stability was not affected by inoculation with homofermentative or facultative heterofermentative LAB nor was there any effect by crop.
“The recent meta-analysis, Oliveira et al. (2017) found that aerobic stability was not affected by inoculation nor was there any effect by crop.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Inoculation with homofermentative or facultative heterofermentative LAB had only a trend for increased DMI and no effect on feed efficiency in lactating dairy cattle.
“with only a trend for increased DMI and no effect on feed efficiency”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Yeast count was higher in inoculated silages than in untreated silages.
“However, yeast count was higher in inoculated silages than in untreated silages.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Effects of homofermentative or facultative heterofermentative inoculants on silage vary by crop.
“A recent meta-analysis of 130 articles revealed that the effects of these inoculants varied by crop”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Trends were observed for increased milk fat and milk protein concentrations for cows fed inoculated silage.
“Trends were observed for increased milk fat and milk protein concentrations for cows fed inoculated silage.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
The reduction in acetic acid by inoculation was significant for all crops except alfalfa and other legumes.
“The reduction in acetic acid by inoculation was significant for all crops except for alfalfa and other legumes.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
Inoculation with homofermentative or facultative heterofermentative LAB increased raw milk production (0.37 kg/d; P < 0.01) in lactating dairy cattle.
“A recent metaanalysis of 31 lactating dairy cattle studies indicated that inoculation with homofermentative or facultative heterofermentative LAB increased raw milk production (0.37 kg/d; P < 0.01)”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
The reduction in butyric acid and ammonia-N and the increase in lactic acid from inoculation were unaffected by forage type.
“In contrast, the reduction in butyric acid and ammonia-N and the increase in lactic acid from inoculation were unaffected by forage type.”
From Silage review: Recent advances and future uses of silage additives (2018) · cites this paper as Oliveira et al., 2017
A recent meta-analysis confirmed benefits of homofermentative and facultative heterofermentative LAB inoculants and proposed limitations and benefits.
“A recent meta-analysis of the impacts of homofermentative and facultative heterofermentative lactic acid bacteria (LAB) inoculants [5] confirmed these results and proposed some limitations and benefits to be gained by inoculation.”
Lactic acid bacteria used as silage additives improve several fermentation parameters, including aerobic stability.
“Lactic acid bacteria (LAB) used as silage additives have been shown to improve several fermentation parameters, including aerobic stability.”
Acetic acid in Control after 64 days was 17.5 ± 1.6 g/kg DM, in the range of published reports.
“The concentration of acetic acid in the Control samples after 64 days of fermentation was 17.5 ± 1.6 g·kg−1 DM, i.e., in the range of published reports [5].”
Inoculating at doses as high as 107 CFU/g is economically not feasible.
“Considering that significant differences compared to control were observed for all strains for a dose of 105 CFU/g, and that inoculating at doses as high as 107 CFU/g is economically not feasible (Oliveira et al., 2017), the dose of 106 CFU/g was chosen for further studies.”
From Potential of Lactic Acid Bacteria Isolated From Different Forages as Silage Inoculants for Improving Fermentation Quality and Aerobic Stability (2020) · cites this paper as Oliveira et al., 2017
Heterofermentative LAB was able to inhibit the growth of undesirable microorganisms.
“heterofermentative LAB was able to inhibit the growth of undesirable microorganisms, which was consistent with previous reports [6,44].”
From Succession of Microbial Communities of Corn Silage Inoculated with Heterofermentative Lactic Acid Bacteria from Ensiling to Aerobic Exposure (2021) · cites this paper as [44]
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- Authors
- Oliveira, A. S., Weinberg, Z. G., Ogunade, I. M., Cervantes, A. A. P., Arriola, K. G., Jiang, Y., Kim, D., Li, X., Gonçalves, M. C. M., Vyas, D., & Adesogan, A. T.
- Affiliations
- Universidade Federal de Mato Grosso (BR)
- University of Florida (US)
- Instituto Federal Goiano (BR)
- Corresponding author
- Adesogan, Adegbola T.
- ORCID
- Venue
- Journal of Dairy Science
- Publisher
- American Dairy Science Association
- Published
- 2017-06
- Volume
- 100
- Issue
- 6
- Pages
- 4587-4603
- ISSN
- 0022-0302 (ISSN-L)
- OpenAlex
- W2600083889
- Cited by
- 409
- References
- 45
- Citations by year
- 2026: 36 · 2025: 46 · 2024: 47 · 2023: 69 · 2022: 56 · 2021: 52 · 2020: 48 · 2019: 28 · 2018: 23 · 2017: 2
- FWCI
- 4.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Dairy Science (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Funders
- United States - Israel Binational Agricultural Research and Development Fund (IS-4704-14)
- University of Florida
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (2013-1)
- Fundação de Amparo à Pesquisa do Estado de Mato Grosso (483724/2011)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycotoxins in Agriculture and Food
- Keywords
- lactic acid bacteria inoculation, homofermentative lactic acid bacteria, silage fermentation, silage quality, aerobic stability, dairy cow performance, milk yield, dry matter recovery, mold growth, butyrate, ammonia nitrogen, grass silage, legume silage, corn silage, sorghum silage, sugarcane silage, total mixed ration, feed efficiency
- MeSH terms
- Aerobiosis, Medicago sativa, Animals, Cattle, Zea mays, Digestion, Female, Fermentation, Poaceae, Lactation, Lactobacillus, Fabaceae, Silage, Lactic Acid, Saccharum, Sorghum
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