Enteric Methane Emissions and Rumen Fermentation Profile Treated by Dietary Chitosan: A Meta-Analysis of In Vitro Experiments

R. P. Harahap, D. Setiawan, Nahrowi Nahrowi, S. Suharti, T. Obitsu, A. Jayanegara

Abstract

Chitosan is a natural compound obtained from deacetylation of chitin, which is a biopolymer present in the exoskeleton of crustaceans such as crabs and shrimp. The present study aimed to perform a meta-analysis from published studies regarding the effects of chitosan on methane emission and rumen fermentation profile of in vitro batch culture experiments. A total of 41 studies from 12 articles were integrated into a database. Parameters included were gas production, methane emission, rumen fermentation characteristics, microbial population, nutrient digestibility, and fatty acid profile. Data were analyzed according to mixed model methodology in which different studies were treated as random effects and chitosan addition levels were treated as fixed effects. Results showed that chitosan addition was able to reduce enteric methane emissions (p<0.001). Such methane decrease was accompanied by a decline in the protozoa population (p<0.05) and a tendency of methanogen reduction (p<0.1). The increasing chitosan level was associated with a decrease in total VFA and ammonia concentrations (both at p<0.001). Chitosan addition decreased acetate proportion (p<0.001) while elevated propionate proportion (p<0.001). Chitosan was associated with an increase of dry matter digestibility, crude protein digestibility, and neutral detergent fiber digestibility (p<0.001). Chitosan increased concentrations of C18:3n3 (p<0.05), conjugated linoleic acid (p<0.01) and polyunsaturated fatty acids (p<0.01) while decreased concentration of saturated fatty acids (p<0.001). It can be concluded that chitosan addition can mitigate enteric methane emission and alters rumen fermentation profiles in a favorable direction.

References

Aranaz, I., M. Mengibar, R. Harris, I. Panos, & B. Mirrales. 2009. Functional of characterization of chitin and chitosan. Curr. Chem. Biol. 3: 203-230. https://doi.org/10.2174/187231309788166415

Beier, S. & S. Bertilsson. 2011. Uncoupling of chitinase activity and uptake of hydrolyses products in freshwater bacterioplankton. Limnol. Oceanogr. 56:1179-1188. https://doi.org/10.4319/lo.2011.56.4.1179

Belanche, A., E. Ramos-Morales, & C. J. Newbold. 2016a. In vitro screening of natural feed additives from crustaceans, diatoms, seaweeds and plant extracts to manipulate rumen fermentation. J. Sci. Food Agric. 96: 3069-3078. https://doi.org/10.1002/jsfa.7481

Belanche, A., E. Pinloche, D. Preskett, & C. J. Newbold. 2016b. Effects and mode of action of chitosan and ivy fruit saponins on the microbiome, fermentation and methanogenesis in the rumen simulation technique. FEMS Microbiology Ecology. 92: fiv160. https://doi.org/10.1093/femsec/fiv160

Cazón, P., G. Velázquez, J. A. Ramirez, & M. Vázquez. 2017. Polysaccharide-based filmsand coatings for food packaging: a review. Food Hydrocoll. 68: 136-148. https://doi.org/10.1016/j.foodhyd.2016.09.009

Chiang, Y. W., T. H. Wang, & W. C. Lee. 2009. Chitosan coating for the protection of amino acids that were entrapped within hydrogenated fat. Food Hydrocoll. 23: 1057-1061. https://doi.org/10.1016/j.foodhyd.2008.04.007

Gandra, J. E., C. S. Takiya, E. R. Oliveira, P. G. Paiva, R. H. T. B. Goes, R. S. Gandra, & H. M. C. Araki. 2016. Nutrient digestion, microbial protein synthesis, and blood metabolites of Jersey heifers fed chitosan and whole raw soybeans. Rev. Bras. Zootec. 43: 130-137. https://doi.org/10.1590/S1806-92902016000300007

Gandra, J. R., E. R. Oliveira, C. S. Takiya, R. H. T. B. Goes, P. G. Paiva, K. M. P. Oliveira, E. R. S. Gandra, N. D. Orbach, & H. M. C. Haraki. 2016. Chitosan improves the chemical composition, microbiological quality, and aerobic stability of sugarcane silage. Anim. Feed Sci. Technol. 214: 44-52. https://doi.org/10.1016/j.anifeedsci.2016.02.020

Gandra, J. R., C. S. Takiya, T. A. Del Valle, E. R. Oliveira, R. H. T. B. de Goes, E. R. S. Gandra, J. D. O. Batista, & H. M. C. Araki. 2018. Soybean whole-plant ensiled with chitosan and lactic acid bacteria: Microorganism counts, fermentative profile, and total losses. J. Dairy Sci. 101: 7871-7880. https://doi.org/10.3168/jds.2017-14268

Goiri, I., A. Garcia-Rodriguez, & L. M. Oregui. 2009a. Effect of chitosans on in vitro rumen digestion and fermentation of maize silage. Anim. Feed Sci. Technol. 148: 276-287. https://doi.org/10.1016/j.anifeedsci.2008.04.007

Goiri, I., L. M. Oregui, & A. Garcia-Rodriguez. 2009b. Dose-response effects of chitosans on in vitro rumen digestion and fermentation of mixtures differing in forage-to-concentrate ratios. Anim. Feed Sci. Technol. 151: 215-227. https://doi.org/10.1016/j.anifeedsci.2009.01.016

Goiri, I., G. Indurain, K. Insausti, V. Sarries, & A. Garcia-Rodriguez. 2010. Ruminal biohydrogenation of unsaturated fatty acids in vitro as affected by chitosan. Anim. Feed Sci. Technol. 159: 35-40. https://doi.org/10.1016/j.anifeedsci.2010.05.007

Goiri, I. & L. M. Oregui. 2014. Use of chitosans to modulate ruminal fermentation of a 50 : 50 forage-to-concentrate diet in sheep. J. Anim. Sci. 88: 749-755. https://doi.org/10.2527/jas.2009-2377

Haryati, R. P., A. Jayanegara, E. B. Laconi, M. Ridla, & P. Suptijah. 2019. Evaluation of chitin and chitosan from insect as feed additives to mitigate ruminal methane emission. In AIP Con. Proc. 2120, 040008. https://doi.org/10.1063/1.5115646

Henry, D. D., F. M. Ciriaco, & M. Kohmann. 2015. Effects of chitosan on nutrient digestibility, CH4 emissions, and in vitro. J. Anim. Sci. 93: 3539-3550. https://doi.org/10.2527/jas.2014-8844

Hristov, A. N., T. Ott, J. Tricarico, A. Rotz, G. Waghorn, A. Adesogan, J. Dijkstra, F. Montes, J. Oh, & E. Kebreab. 2013. Mitigation of methane and nitrous oxide emissions from animal operations: III. A review of animal management mitigation options. J. Anim. Sci. 91: 5095-5113. https://doi.org/10.2527/jas.2013-6585

Janssen, P. H. 2010. Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim. Feed Sci. Technol. 160: 1-22. https://doi.org/10.1016/j.anifeedsci.2010.07.002

Jayanegara, A., K. A. Sarwono, M. Kondo, H. Matsui, M. Ridla, E. B. Laconi, & Nahrowi. 2018a. Use of 3-nitrooxypropanol as feed additive for mitigating enteric methane emissions from ruminants: a meta-analysis. Ital. J. Anim. Sci. 17: 650-656. https://doi.org/10.1080/1828051X.2017.1404945

Jayanegara, A., R. P. Harahap, R. F. Rozi, & Nahrowi. 2018b. Effects of lipid extraction on nutritive composition of winged bean (Psophocarpus tetragonolobus), rubber seed (Hevea brasiliensis), and tropical almond (Terminalia catappa). Vet. World. 11: 446-451. https://doi.org/10.14202/vetworld.2018.446-451

Jenkins, T. C., R. J. Wallace, P. J. Moate, & E. E. Mosley. 2008. Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J. Anim. Sci. 86: 397-412. https://doi.org/10.2527/jas.2007-0588

Kaharabata, S. K., P. H. Schuepp, & R. L. Desjardins. 2015. Estimating methane emissions from dairy cattle housed in a barn and feedlot using an atmospheric tracer. Environ. Sci. Technol. 34: 3296-3302. https://doi.org/10.1021/es990578c

Kondo, M., Y. Hirano, N. Ikai, K. Kita, A. Jayanegara, & H. O. Yokota. 2014. Assessment of anti-nutritive activity of tannins in tea by-products based on in vitro rumen fermentation. Asian Australas. J. Anim. Sci. 27: 1571-1576. https://doi.org/10.5713/ajas.2014.14204

Kong, M., X. G. Chen, K. Xing, & H. J. Park. 2010. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int. J. Food Microbiol. 144: 51-63. https://doi.org/10.1016/j.ijfoodmicro.2010.09.012

Krehbiel, C. R. 2014. Invited Review: Applied nutrition of ruminants: Fermentation and digestive physiology. Professional Animal Scientist. 30: 129-139. https://doi.org/10.15232/S1080-7446(15)30100-5

Leng, R. 2014. Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation. Anim. Prod. Sci. 54: 519-543. https://doi.org/10.1071/AN13381

Li, C., X. Zhao, Y. Cao, Y. Lei, C. Liu, H. Wang, & J. Yao. 2013. Effects of chitosan on in vitro ruminal fermentation in diets with different forage to concentrate ratios. J. Anim. Vet. Adv. 12: 839-845.

Lourenço, M., E. Ramos-Morales, & R. J. Wallace. 2010. The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Anim. 4: 1008-1023. https://doi.org/10.1017/S175173111000042X

Morgavi, D. P., E. Forano, C. Martin, & C. J. Newbold. 2010. Microbial ecosystem and methanogenesis in ruminants. Anim. 4: 1024-1036. https://doi.org/10.1017/S1751731110000546

Muxika, A., A. Etxabide, J. Uranga, P. Guerrero, & K. de la Caba. 2017. Chitosan as a bioactive polymer: Processing, properties and applications. Int. J. Biol. Macromol. 105: 1358-1368. https://doi.org/10.1016/j.ijbiomac.2017.07.087

Newbold, C. J., G. de la Fuente, A. Belanche, E. Ramos-Morales, & N. R. McEwan. 2015. The role of ciliate protozoa in the rumen. Front. Microbiol. 6: 1-14. https://doi.org/10.3389/fmicb.2015.01313

Patra, A. K. & J. Saxena. 2011. Exploitation of dietary tannins to improve rumenmetabolism and ruminant nutrition. J. Sci. Food. Agric. 91: 24-37. https://doi.org/10.1002/jsfa.4152

Pereira, D. C., R. H. T. B. Goes, A. C. Martinez, J. R. Gandra, E. Presendo, M. V. Santos, R. T. Oliveira, N. G. Silva, M. G. Ribeiro, & J. L. R. Alvez. 2019. In vitro evaluation of the association of chitosan and cashew nut shell liquid as additives for ruminants. Rev. Bras. Saúde Prod. Anim. 20: 1-12. https://doi.org/10.1590/s1519-994005102019

Seankamsorn, A., A. Cherdthong & M. Wanapat. 2019. Combining crude glycerin with chitosan can manipulate in vitro ruminal efficiency and inhibit methane synthesis. Anim. 10: 30. https://doi.org/10.3390/ani10010037

St-Pierre, N. 2001. Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84: 741-755. https://doi.org/10.3168/jds.S0022-0302(01)74530-4

Toral, P. G., F. J. Monahan, G. Hervas, P. Frutos, & A. P. Moloney. 2018. Modulating ruminal lipid metabolism to improve the fatty acid composition of meat and milk challenges and opportunities. Anim. 12: S272-S281. https://doi.org/10.1017/S1751731118001994

Vasta, V., M. Daghio, A. Cappucci, A. Buccioni, A. Serra, C. Viti, & M. Mele. 2019. Plant polyphenols and rumen microbiota responsible for fatty acid biohydrogenation, fiber digestion, and methane emission: Experimental evidence and methodological approaches. J. Dairy Sci. 102: 3781-3804. https://doi.org/10.3168/jds.2018-14985

Vendramini, T. H. A., C. S. Takiya, T. H. Silva, F. Zanferari, M. F. Rentas, C. E. C. Consentini, R. Gardinal, T. S. Acedo, & F. P. Rennó. 2016. Effects of a blend of essential oils, chitosan or monensin on nutrient intake and digestibility of lactating dairy cows. Anim. Feed Sci. Technol. 214: 12-21. https://doi.org/10.1016/j.anifeedsci.2016.01.015

Wencelová, M., Z. Váradyová, K. Mihaliková, S. Kišidayová, & D. Jalč. 2013. Evaluating the effects of chitosan, plant oils, and different diets on rumen metabolism and protozoan population in sheep. Turk. J. Vet. Anim. Sci. 38: 26-33. https://doi.org/10.3906/vet-1307-19

Wina, E., S. Muetzel, & K. Becker. 2005. The impact of saponins or saponin-containing plant materials on ruminant production - a review. J. Agric. Food Chem. 53: 8093-8105. https://doi.org/10.1021/jf048053d

Zanferari, F., T. H. A. Vendramini, M. F. Rentas, R. Gardinal, G. D. Calomeni, L. G. Mesquita, C. S. Takiya, & F. P. Rennó. 2018. Effects of chitosan and whole raw soybeans on ruminal fermentation and bacterial populations, and milk fatty acid profile in dairy cows. J. Dairy Sci. 101: 10939-10952. https://doi.org/10.3168/jds.2018-14675

Authors

R. P. Harahap
D. Setiawan
Nahrowi Nahrowi
S. Suharti
T. Obitsu
A. Jayanegara
anu_jayanegara@yahoo.com (Primary Contact)
Author Biography

A. Jayanegara, Department of Nutrition and Feed Technology, Faculty of Animal Science, Bogor Agricultural University

Field of interest: ruminant feed and nutrition

Email: anu_jayanegara@yahoo.com

HarahapR. P., SetiawanD., NahrowiN., SuhartiS., ObitsuT., & JayanegaraA. (2020). Enteric Methane Emissions and Rumen Fermentation Profile Treated by Dietary Chitosan: A Meta-Analysis of In Vitro Experiments. Tropical Animal Science Journal, 43(3), 233-239. https://doi.org/10.5398/tasj.2020.43.3.233

Article Details

List of Cited By :

Crossref logo