Reducing agent can be omitted in the incubation medium of the batch in vitro fermentation model of the pig intestines
Open accessAbstract
Over the past decade, in vitro methods have been developed to study intestinal fermentation in pigs and its influence on the digestive physiology and health. In these methods, ingredients are fermented by a bacterial inoculum diluted in a mineral buffer solution. Generally, a reducing agent such as Na2S or cysteine-HCl generates the required anaerobic environment by releasing metabolites similar to those produced when protein is fermented, possibly inducing a dysbiosis. An experiment was conducted to study the impact of two reducing agents on results yielded by such in vitro fermentation models. Protein (soybean proteins, casein) and carbohydrate (potato starch, cellulose) ingredients were fermented in vitro by bacteria isolated from fresh feces obtained from three sows in three carbonate-based incubation media differing in reducing agent: (i) Na2S, (ii) cysteine-HCl and (iii) control with a mere saturation with CO2 and devoid of reducing agent. The gas production during fermentation was recorded over 72 h. Short-chain fatty acids (SCFA) production after 24 and 72 h and microbial composition of the fermentation broth after 24 h were compared between ingredients and between reducing agents. The fermentation residues after 24 h were also evaluated in terms of cytotoxicity using Caco-2 cell monolayers. Results showed that the effect of the ingredient induced higher differences than the reducing agent. Among the latter, cysteine-HCl induced the strongest differences compared with the control, whereas Na2S was similar to the control for most parameters. For all ingredients, final gas produced per g of substrate was similar (P>0.10) for the three reducing agents whereas the maximum rate of gas production (R max) was reduced (P0.10) after 24 h of fermentation with Na2S and in the control without reducing agent. Molar ratios of branched chain-fatty acids were higher (P<0.05) for protein (36.5% and 9.7% for casein and soybean proteins, respectively) than for carbohydrate (<4%) ingredients. Only fermentation residues of casein showed a possible cytotoxic effect regardless of the reducing agent (P<0.05). Concerning the microbial composition of the fermentation broth, most significant differences in phyla and in genera ascribable to the reducing agent were found with potato starch and casein. In conclusion, saturating the incubation media with CO2 seems sufficient to generate a suitable anaerobic environment for intestinal microbes and the use of a reducing agent can be omitted.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Reducing agents were not required to culture all rumen bacteria and their removal resulted in higher microbial diversity.
“A recent study by Poelaert et al. (2018) showed that reducing agents were not required to culture all rumen bacteria and that when removed they resulted in higher microbial diversity.”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Poelaert et al., 2018
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., et al. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01541-09 · Cited by 20,966 · see citing works
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., & Glöckner, F. O. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm864 · Cited by 6,682 · see citing works
A TWO‐STAGE TECHNIQUE FOR THE IN VITRO DIGESTION OF FORAGE CROPS
Tilley, J. M. A., & Terry, R. A. (1963) · Grass and Forage Science · doi:10.1111/j.1365-2494.1963.tb00335.x · Cited by 6,624 · see citing works
Kh, M. (1988) · Medical Entomology and Zoology · Cited by 2,422 · see citing works
Theodorou, M. K., Williams, B. A., Dhanoa, M. S., McAllan, A. B., & France, J. (1994) · Animal Feed Science and Technology · doi:10.1016/0377-8401(94)90171-6 · Cited by 1,809 · see citing works
Artursson, P., Palm, K., & Luthman, K. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(00)00128-9 · Cited by 1,549 · see citing works
Multiphasic analysis of gas production kinetics for in vitro fermentation of ruminant feeds
Groot, J. C. J., Cone, J. W., Williams, B. A., Debersaques, F., & Lantinga, E. A. (1996) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(96)01012-7 · Cited by 550 · see citing works
Guo, X., Xia, X., Tang, R., Zhou, J., Zhao, H., & Wang, K. (2008) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2008.02408.x · Cited by 502 · see citing works
An Ecological Network of Polysaccharide Utilization among Human Intestinal Symbionts
Rakoff-Nahoum, S., Coyne, M. J., & Comstock, L. E. (2013) · Current Biology · doi:10.1016/j.cub.2013.10.077 · Cited by 402 · see citing works
Evidence That Hydrogen Sulfide Is a Genotoxic Agent
Attene‐Ramos, M. S., Wagner, E. D., Plewa, M. J., & Gaskins, H. R. (2006) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-05-0126 · Cited by 363 · see citing works
Advances and perspectives in in vitro human gut fermentation modeling
Payne, A. N., Zihler, A., Chassard, C., & Lacroix, C. (2011) · Trends in biotechnology · doi:10.1016/j.tibtech.2011.06.011 · Cited by 340 · see citing works
Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs
Kim, H. B., Borewicz, K., White, B. A., Singer, R. S., Sreevatsan, S., Tu, Z. J., & Isaacson, R. E. (2011) · Veterinary Microbiology · doi:10.1016/j.vetmic.2011.05.021 · Cited by 335 · see citing works
Production, metabolism, and excretion of hydrogen in the large intestine
Christl, S. U., Murgatroyd, P. R., Gibson, G. R., & Cummings, J. H. (1992) · Gastroenterology · doi:10.1016/0016-5085(92)90765-q · Cited by 300 · see citing works
Caco-2 monolayers in experimental and theoretical predictions of drug transport
Artursson, P., Palm, K., & Luthman, K. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.09.005 · Cited by 280 · see citing works
Protein degradation in the large intestine: relevance to colorectal cancer.
Hughes, R., Magee, E., & Bingham, S. A. (2000) · PubMed · Cited by 271 · see citing works
Colonic Sulfide in Pathogenesis and Treatment of Ulcerative Colitis
Roediger, W. E. W., Moore, J., & Babidge, W. (1997) · Digestive Diseases and Sciences · doi:10.1023/a:1018851723920 · Cited by 270 · see citing works
Leser, T. D., Lindecrona, R. H., Jensen, T. K., Jensen, B. B., & Møller, K. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.8.3290-3296.2000 · Cited by 206 · see citing works
Identification and Functional Analysis of Escherichia coli Cysteine Desulfhydrases
Awano, N., Wada, M., Mori, H., Nakamori, S., & Takagi, H. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.7.4149-4152.2005 · Cited by 164 · see citing works
Andriamihaja, M., Davila, A., Eklou-Lawson, M., Petit, N., Delpal, S., Allek, F., Blais, A., Delteil, C., Tomé, D., & Blachier, F. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00149.2010 · Cited by 145 · see citing works
Emerging role of hydrogen sulfide in colonic physiology and pathophysiology
Medani, M., Collins, D., Docherty, N. G., Baird, A. W., O’Connell, P. R., & Winter, D. C. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21528 · Cited by 142 · see citing works
Watanabe, Y., Suzuki, R., Koike, S., Nagashima, K., Mochizuki, M., Forster, R. J., & Kobayashi, Y. (2010) · Journal of Dairy Science · doi:10.3168/jds.2009-2754 · Cited by 120 · see citing works
Glucose and carbon dioxide metabolism by Succinivibrio dextrinosolvens
O'Herrin, S. M., & Kenealy, W. R. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.3.748-755.1993 · Cited by 90 · see citing works
Jha, R., Woyengo, T. A., Li, J., Bedford, M. R., Vasanthan, T., & Zijlstra, R. T. (2015) · Journal of Animal Science · doi:10.2527/jas.2014-7910 · Cited by 74 · see citing works
Pieper, R., Bindelle, J., Rossnagel, B. G., Kessel, A. V., & Leterme, P. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.01343-09 · Cited by 59 · see citing works
Self-citationBindelle, J., Pieper, R., Montoya, C. A., Kessel, A. G. V., & Leterme, P. (2011) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2011.01074.x · Cited by 50 · see citing works
Self-citationCremin, J. D., Fitch, M. D., & Fleming, S. E. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00437.2002 · Cited by 48 · see citing works
Koecher, K. J., Noack, J. A., Timm, D. A., Klosterbuer, A. S., Thomas, W., & Slavin, J. L. (2014) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf404688n · Cited by 47 · see citing works
Pieper, R., Janczyk, P., Urubschurov, V., Korn, U., Pieper, B., & Souffrant, W. B. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.01.026 · Cited by 45 · see citing works
Su, Y., Bian, G., Zhu, Z., Smidt, H., & Zhu, W. (2014) · Archaea · doi:10.1155/2014/547908 · Cited by 44 · see citing works
Rodriguez, C., Taminiau, B., Korsak, N., Avesani, V., Broeck, J. V., Brach, P., Delmée, M., & Daube, G. (2016) · BMC Microbiology · doi:10.1186/s12866-016-0848-7 · Cited by 44 · see citing works
Self-citationCloning and characterization of the l-cysteine desulfhydrase gene ofFusobacterium nucleatum
Fukamachi, H., Nakano, Y., Yoshimura, M., et al. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11373.x · Cited by 41 · see citing works
Fukushima, R. S., Weimer, P. J., & Kunz, D. A. (2003) · Brazilian Journal of Microbiology · doi:10.1590/s1517-83822003000100006 · Cited by 40 · see citing works
Bindelle, J., Buldgen, A., Wavreille, J., Agneessens, R., Destain, J.-P., Wathelet, B., & Leterme, P. (2007) · animal · doi:10.1017/s1751731107000584 · Cited by 35 · see citing works
Self-citationCrystallization and properties of cysteine desulfhydrase from Aerobacter aerogenes
Kumagai, H., Sejima, S., Choi, Y.-J., Tanaka, H., & Yamada, H. (1975) · FEBS Letters · doi:10.1016/0014-5793(75)80831-3 · Cited by 35 · see citing works
Tran, T. H. T., Boudry, C., Everaert, N., Théwis, A., Portetelle, D., Daube, G., Nezer, C., Taminiau, B., & Bindelle, J. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv165 · Cited by 35 · see citing works
Self-citation1,4-Naphthoquinone and other nutrient requirements of Succinivibrio dextrinosolvens
Gomez-Alarcon, R. A., O'Dowd, C., Leedle, J. A. Z., & Bryant, M. P. (1982) · Applied and Environmental Microbiology · doi:10.1128/aem.44.2.346-350.1982 · Cited by 24 · see citing works
Cardarelli, H. R., Martinez, R. C. R., Albrecht, S., et al. (2015) · Beneficial Microbes · doi:10.3920/bm2014.0151 · Cited by 22 · see citing works
Sappok, M., Pellikaan, W. F., Verstegen, M. W. A., et al. (2009) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.3746 · Cited by 13 · see citing works
The use of a nitrogen free medium for in vitro fermentation studies
Morgan, R., Kliem, K. E., & Mould, F. L. (2004) · Proceedings of the British Society of Animal Science · doi:10.1017/s1752756200016355 · Cited by 3 · see citing works
Weiss, E., Rist, V. T. S., Rink, F., & Mosenthin, R. (2015) · Livestock Science · doi:10.1016/j.livsci.2015.03.009 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Huws, S. A., Creevey, C. J., Oyama, L. B., Mizrahi, I., Denman, S. E., Popova, M., Muñoz-Tamayo, R., Forano, E., Waters, S. M., Hess, M., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02161 · Cited by 487 · see citing works
- Authors
- Poelaert, C., Nollevaux, G., Boudry, C., Taminiau, B., Nezer, C., Daube, G., Schneider, Y.-J., Portetelle, D., Théwis, A., & Bindelle, J.
- Affiliations
- University of Liège (BE)
- UCLouvain (BE)
- Matériaux et santé (FR)
- Corresponding author
- Bindelle, J.
- Venue
- animal
- Publisher
- Elsevier BV
- Published
- 2018
- Volume
- 12
- Issue
- 6
- Pages
- 1154-1164
- ISSN
- 1751-7311 (ISSN-L)
- OpenAlex
- W2765284694
- Cited by
- 6
- References
- 41
- Citations by year
- 2026: 1 · 2024: 1 · 2020: 1 · 2019: 1 · 2018: 2
- FWCI
- 1.21
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- animal (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Open Repository and Bibliography (University of Liège) (submittedVersion, other-oa)
- Funders
- Fonds De La Recherche Scientifique - FNRS (1.5180.12)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
- Keywords
- reducing agents, anaerobic conditions, sodium sulfide, cysteine hydrochloride, short-chain fatty acids, branched-chain fatty acids, casein, soy protein, potato starch, cellulose, gas production, microbial community composition, fermentation residues, Caco-2 cytotoxicity, sows, fermentation medium optimization, dysbiosis
- MeSH terms
- Animals, Fatty Acids, Volatile, Feces, Female, Fermentation, Humans, Intestines, Swine, Caco-2 Cells, Reducing Agents
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review