Changes in Bovine Colostrum Metabolites during Early Postpartum Period Revealed by 1H-NMR Metabolomics Approach

S. Settachaimongkon, N. Wannakajeepiboon, P. Arunpunporn, W. Mekboonsonglarp, D. Makarapong

Abstract

The objectives of this study were to characterize and compare non-volatile polar metabolite profiles of bovine colostrum, collected within 1 h and at 72 h after parturition, from crossbred Holstein cows raised in northeastern Thailand. The colostrum serum was characterized and compared using a non-targeted proton nuclear magnetic resonance (1H-NMR) technique combined with chemometric analysis. Results demonstrated that the main effect of post-parturition time provided a significant impact on the physical properties and major chemical constituents of colostrum, while the influence of farm origin and sampling month were likely undetectable. The 1H-NMR technique enabled to identify 45 non-volatile polar metabolites in the samples. Partial least-squares-discriminant analysis (PLS-DA) allowed discrimination of colostrum metabolome not only according to different times after parturition, but also the origins of the farm as well as sampling months. Differential metabolites were statistically identified as potential biomarkers accountable for the discrimination. Besides basic nutritive compounds (amino acids and sugars), several bioactive metabolites such as ascorbate, creatine, carnitine, choline, acetylcarnitine, N-acetylglucosamine, ornithine, orotate, and UPD-glucose could be successfully elucidated. Our finding reveals the application of non-targeted 1H-NMR metabolomics as an effective tool to assess the biomolecular profiles of bovine colostrum and their essential dynamics during the first three days after parturition.

References

Afshari, R., C. J. Pillidge, D. A. Dias, A. M. Osborn, & H. Gill. 2020. Cheesomics: The future pathway to understanding cheese flavour and quality. Crit. Rev. Food Sci. Nutr. 60:33-47. https://doi.org/10.1080/10408398.2018.1512471
Calderón, F., B. Chauveau-Duriot, B. Martin, B. Graulet, M. Doreau, & P. Nozière. 2007. Variations in carotenoids, vitamins A and E, and color in cow’s plasma and milk during late pregnancy and the first three months of lactation. J. Dairy Sci. 90:2335-2346. https://doi.org/10.3168/jds.2006-630
Ceniti, C., F. Froiio, D. Britti, D. Paolino, & N. Costanzo. 2019. Rheological characteristics of bovine colostrum and their correlation with immunoglobulin G. Int. J. Dairy Technol. 72:345-349. https://doi.org/10.1111/1471-0307.12593
Csapó, J., B. Béri, A. Süli, & E. Varga-Visi. 2012. Colostrum and milk of different cattle breeds as amino acid source. Acta Agric. Slov. 100:327-331.
Cui, J., D. Zhu, M. Su, D. Tan, X. Zhang, M. Jia, & G. Chen. 2019. The combined use of 1H and 2D NMR-based metabolomics and chemometrics for non-targeted screening of biomarkers and identification of reconstituted milk. J. Sci. Food Agric. 99:6455-6461. https://doi.org/10.1002/jsfa.9924
Cui, N., P. C. Wen, Q. Liang, H. N. Liu, W. B. Zhang, P. J. Wang, H. Y. Guo, & F. Z. Ren. 2015. Chemical composition of yak colostrum and transient milk. J. Anim. Physiol. Anim. Nutr. 99:825-833. https://doi.org/10.1111/jpn.12282
Denholm, K. S., S. McDougall, G. Chambers, & W. Clough. 2018. Factors associated with colostrum quality in individual cows from dairy herds in the Waikato region of New Zealand. N. Z. Vet. J. 66:115-120. https://doi.org/10.1080/00480169.2017.1418684
Dunn, A., A. Ashfield, B. Earley, M. Welsh, A. Gordon, & S. J. Morrison. 2017. Evaluation of factors associated with immunoglobulin G, fat, protein, and lactose concentrations in bovine colostrum and colostrum management practices in grassland-based dairy systems in Northern Ireland. J. Dairy Sci. 100:2068-2079. https://doi.org/10.3168/jds.2016-11724
Foroutan, A., A. C. Guo, R. Vazquez-Fresno, M. Lipfert, L. Zhang, J. Zheng, H. Badran, Z. Budinski, R. Mandal, B. N. Ametaj, & D. S. Wishart. 2019. Chemical composition of commercial cow’s milk. J. Agric. Food Chem. 67:4897-4914. https://doi.org/10.1021/acs.jafc.9b00204
Godhia, M. L. & N. Patel. 2013. Colostrum - Its composition, benefits as a nutraceutical: A review. Curr. Res. Nutr. Food Sci. 1:37-47. https://doi.org/10.12944/CRNFSJ.1.1.04
Goldansaz, S. A., A. C. Guo, T. Sajed, M. A. Steele, G. S. Plastow, & D. S. Wishart. 2017. Livestock metabolomics and the livestock metabolome: A systematic review. PLoS ONE. 12: e0177675. https://doi.org/10.1371/journal.pone.0177675
Górka, P., Z. M. Kowalski, R. Zabielski, & P. Guilloteau. 2018. Invited review: Use of butyrate to promote gastrointestinal tract development in calves. J. Dairy Sci. 101:4785-4800. https://doi.org/10.3168/jds.2017-14086
Gross, J. J., E. C. Kessler, & R. M. Bruckmaier. 2014. Colour measurement of colostrum for estimation of colostral IgG and colostrum composition in dairy cows. J. Dairy Res. 81:440-444. https://doi.org/10.1017/S0022029914000466
ISO/IDF. 2012. ISO/TS11869 - IDF/RM150:2012 - Fermented milks - determination of titratable acidity - potentiometric method. International Organization for Standardization, Geneva.
Kamal, A. M., O. A. Salama, & K. M. El-Saied. 2007. Changes in amino acids profile of camel milk protein during the early lactation. Int. J. Dairy Sci. 2:226-234. https://doi.org/10.3923/ijds.2007.226.234
Klein, M. S., N. Buttchereit, S. P. Miemczyk, A.-K. Immervoll, C. Louis, S. Wiedemann, W. Junge, G. Thaller, P. J. Oefner, & W. Gronwald. 2012. NMR metabolomic analysis of dairy cows reveals milk glycerophosphocholine to phosphocholine ratio as prognostic biomarker for risk of ketosis. J. Proteome Res. 11:1373-1381. https://doi.org/10.1021/pr201017n
Kráčmar, S., S. Gajdůšek, P. Jelínek, L. Zeman, V. Kozel, M. Kozlová, & E. Kráčmarová. 1999. Changes in amino acid composition of goat’s colostrum during the first 72 hours after birth. Czech J. Anim. Sci. 44:541-545.
Kráčmar, S., F. Buňka, I. Hoza, L. Čechová, & P. Valášek. 2007. Changes in amino acids composition of cows colostrum (during first 72 hours after parturition). Acta Univ. Agric. Silvic. Mendel. Brun. 55:81-94. https://doi.org/10.11118/actaun200755010081
Li, M., W. Li, F. Kong, S. Kang, X. Liang, H. Han, J. Wu, Y. Zheng, Q. Li, X. Yue, & M. Yang. 2020. Metabolomics methods to analyze full spectrum of amino acids in different domains of bovine colostrum and mature milk. Eur. Food Res. Technol. 246:213-224. https://doi.org/10.1007/s00217-019-03385-y
Luangwilai, M., K. Duangmal, N. Chantaprasarn & S. Settachaimongkon. 2021. Comparative metabolite profiling of raw milk from subclinical and clinical mastitis cows using ¹H-NMR combined with chemometric analysis. Int. J. Food Sci. Tech. 56: 493-503. https://doi.org/10.1111/ijfs.14665
Luise, D., G. Picone, A. Balzani, F. Capozzi, M. Bertocchi, C. Salvarani, P. Bosi, S. Edwards, & P. Trevisi. 2020. Investigation of the defatted colostrum1H-NMR metabolomics profile of gilts and multiparous sows and its relationship with litter performance. Animals. 10:154. https://doi.org/10.3390/ani10010154
Madsen, B. D., M. D. Rasmussen, M. O. Nielsen, L. Wiking, & L. B. Larsen. 2004. Physical properties of mammary secretions in relation to chemical changes during transition from colostrum to milk. J. Dairy Res. 71:263-272. https://doi.org/10.1017/S0022029904000263
McGrath, B. A., P. F. Fox, P. L. H. McSweeney, & A. L. Kelly. 2016. Composition and properties of bovine colostrum: a review. Dairy Sci. Technol. 96:133-158. https://doi.org/10.1007/s13594-015-0258-x
Meklati, F. R., A. Meribai, N. Yezli, & T. Benabdelaziz. 2019. Colostrum and milk fatty acids profiles from imported prim’Holstein cows. Pertanika J. Trop. Agric. Sci. 42:595-607.
O’Callaghan, T. F., M. O’Donovan, J. P. Murphy, K. Sugrue, D. Mannion, W. P. McCarthy, M. Timlin, K. N. Kilcawley, R. M. Hickey, & J. T. Tobin. 2020. Evolution of the bovine milk fatty acid profile – From colostrum to milk five days post parturition. Int. Dairy J. 104:104655. https://doi.org/10.1016/j.idairyj.2020.104655
Penchev Georgiev, I. 2008. Differences in chemical composition between cow colostrum and milk. Bulg. J. Vet. Med. 1:3-12.
Picone, G., M. Zappaterra, D. Luise, A. Trimigno, F. Capozzi, V. Motta, R. Davoli, L. Nanni Costa, P. Bosi, & P. Trevisi. 2018. Metabolomics characterization of colostrum in three sow breeds and its influences on piglets’ survival and litter growth rates. J. Anim. Sci. Biotechnol. 9:23. https://doi.org/10.1186/s40104-018-0237-1
Potts, D. M. & D. G. Peterson. 2019. Identification of small molecule flavor compounds that contribute to the somatosensory attributes of bovine milk products. Food Chem. 294:27-34. https://doi.org/10.1016/j.foodchem.2019.05.010
Promket, D., W. Kenchaiwong, & K. Ruangwittayanusorn. 2020. Effects of climate change on milk yield and milk composition in thai crossbred holstein cows. International Journal of GEOMATE 18:108-113. https://doi.org/10.21660/2020.67.5807
Puppel, K., M. Gołębiewski, G. Grodkowski, J. Slósarz, M. Kunowska-Slósarz, P. Solarczyk, M. Łukasiewicz, M. Balcerak, & T. Przysucha. 2019. Composition and factors affecting quality of bovine colostrum: A review. Animals. 9:1070. https://doi.org/10.3390/ani9121070
Qi, Y., X. Zhao, D. Huang, X. Pan, Y. Yang, H. Zhao, H. Hu, & G. Cheng. 2018. Exploration of the Relationship between Intestinal Colostrum or Milk, and Serum Metabolites in Neonatal Calves by Metabolomics Analysis. J. Agric. Food Chem. 66:7200-7208. https://doi.org/10.1021/acs.jafc.8b01621
Robinson, J. L. 1980. Bovine milk orotic acid: Variability and significance for human nutrition. J. Dairy Sci. 63:865-871. https://doi.org/10.3168/jds.S0022-0302(80)83017-7
Scano, P., E. Cusano, P. Caboni, & R. Consonni. 2019. NMR metabolite profiles of dairy: A review. Int. Dairy J. 90:56-67. https://doi.org/10.1016/j.idairyj.2018.11.004
Settachaimongkon, S., M. J. R. Nout, E. C. Antunes Fernandes, K. A. Hettinga, J. M. Vervoort, T. C. M. van Hooijdonk, M. H. Zwietering, E. J. Smid, & H. J. F. van Valenberg. 2014. Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt. Int. J. Food Microbiol. 177: 29-36. https://doi.org/10.1016/j.ijfoodmicro.2014.02.008
Settachaimongkon, S., H. J. F. van Valenberg, & E. J. Smid. 2017. Metabolomics as an emerging strategy for the investigation of yogurt components, in: N. P. Shah (Ed.), Yogurt in Health and Disease Prevention. Academic Press, London, pp. 427-449. https://doi.org/10.1016/B978-0-12-805134-4.00025-0
Sundekilde, U. K., F. Gustavsson, N. A. Poulsen, M. Glantz, M. Paulsson, L. B. Larsen, & H.C. Bertram. 2014. Association between the bovine milk metabolome and rennet-induced coagulation properties of milk. J. Dairy Sci. 97: 6076-6084. https://doi.org/10.3168/jds.2014-8304
Tsioulpas, A., A. S. Grandison, & M. J. Lewis. 2007. Changes in physical properties of bovine milk from the colostrum period to early lactation. J. Dairy Sci. 90:5012-5017. https://doi.org/10.3168/jds.2007-0192
Wu, J., M. Domellöf, A. M. Zivkovic, G. Larsson, A. Öhman, & M. L. Nording. 2016. NMR-based metabolite profiling of human milk: A pilot study of methods for investigating compositional changes during lactation. Biochem. Biophys. Res. Commun. 469:626-632. https://doi.org/10.1016/j.bbrc.2015.11.114
Zándoki, R., J. Csapó, Z. Csapó-Kiss, I. Tábori, Z. Domokos, E. Szucs, & J. Tozsér. 2006. Change of amino acid profile in Charolais cows’ colostrum and transient milk during the first week post partum. Czech J. Anim. Sci. 51:375-382. https://doi.org/10.17221/3954-CJAS
Zhang, S., X. Zeng, M. Ren, X. Mau, & S. Qiao. 2017. Novel metabolic and physiological functions of branched chain amino acids: A review. J. Anim. Sci. Biotechnol. 8:10. https://doi.org/10.1186/s40104-016-0139-z
Zhang, Z., A. S. Adelman, D. Rai, J. Boettcher, & B. Lonnerdal. 2013. Amino acid profiles in term and preterm human milk through lactation: A systematic review. Nutrients. 5:4800-4821. https://doi.org/10.3390/nu5124800
Zhao, X. W., Y. X. Qi, D. W. Huang, X. C. Pan, G. L. Cheng, H. L. Zhao, & Y. X. Yang. 2018. Changes in serum metabolites in response to ingested colostrum and milk in neonatal calves, measured by nuclear magnetic resonance-based metabolomics analysis. J. Dairy Sci. 101:7168-7181. https://doi.org/10.3168/jds.2017-14287

Authors

S. Settachaimongkon
sarn.s@chula.ac.th (Primary Contact)
N. Wannakajeepiboon
P. Arunpunporn
W. Mekboonsonglarp
D. Makarapong
SettachaimongkonS., WannakajeepiboonN., ArunpunpornP., MekboonsonglarpW., & MakarapongD. (2021). Changes in Bovine Colostrum Metabolites during Early Postpartum Period Revealed by 1H-NMR Metabolomics Approach. Tropical Animal Science Journal, 44(2), 229-239. https://doi.org/10.5398/tasj.2021.44.2.229

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