Determination of selenium speciation in the muscle, kidney, and liver from different animals treated with different selenium supplements by HPLC-ICP-MS

Abstract

Dietary selenium (Se) deficiency is recognized as a global problem, and exogenous Se supplementation can effectively enrich its levels in animal bodies. Offal tissues are equally important as meat in Se enrichment. Varying properties among Se species require information beyond total Se concentration to fully evaluate health risk/benefits. In the present study, the reliable inductively coupled plasma mass spectrometry (ICP-MS) and HPLC-ICP-MS methods were optimized to analyze total Se content and Se speciation in the muscle and kidney of sheep, kidney and liver of pig, and liver of chicken after different Se supplementation treatments. The total Se contents in the liver and kidney were higher than in muscle. Five Se species were detected in the muscle, and selenourea was additionally detected in the liver and kidney. Sheep muscle and chicken liver mainly contained selenomethionine, and other tissues mainly contained selenocysteine. As the levels of selenomethionine or selenium-enriched yeast increased in the feed, the proportion of selenomethionine in the sample increased, as well as the proportion of selenocysteine decreased, and almost no inorganic selenium was detected in all tissues. This study has provided insights for analyzing the Se enrichment patterns in tissues, which is significant for understanding the Se metabolism, animal health, and enriching the dietary Se supplementation for humans.

Keywords

animal tissues / HPLC-ICP-MS / ICP-MS / selenium / selenium speciation

References

[1] Fan, S. J., Chen, J. Y., Tian, H. H., Yang, X. T., Zhou, L. Z., Zhao, Q. Y., Qin, Y. C., Zhang, J. M., & Tang, C. H. (2024). Selenium maintains intestinal epithelial cells to activate M2 macrophages against deoxynivalenol injury. Free Radical Biology and Medicine, 219, 215-230. https://doi.org/10.1016/j.freeradbiomed.2024.04.228

[2] Kieliszek, M., & Blazejak, S. (2013). Selenium: Significance, and outlook for supplementation. Nutrition, 29(5), 713-718. https://doi.org/10.1016/j.nut.2012.11.012

[3] Detopoulou, P., Letsiou, S., Nomikos, T. K. A., Sa, P., Pitsavos, C., Db, P., & Antonopoulou, S. (2023). Selenium, selenoproteins and 10-year cardiovascular risk: Results from the ATTICA Study. Current Vascular Pharmacology, 21(5), 346-355. https://doi.org/10.2174/1570161121666230731142023

[4] Tang, C. H., Li, S., Zhang, K., Li, J., Han, Y. S., Zhao, Q. Y., Guo, X. Q., Qin, Y. C., Yin, J. D., & Zhang, J. M. (2022). Selenium deficiency induces pathological cardiac lipid metabolic remodeling and inflammation. Molecular Nutrition and Food Research, 66(6), e2100644. https://doi.org/10.1002/mnfr.202100644

[5] EFSA Panel on Dietetic Products, Nutrition and Allergies NDA. (2014). Scientific opinion on dietary reference values for selenium. EFSA Journal, 12(10), 3846. European Food Safety Authority. https://doi.org/10.2903/j.efsa.2014.3846

[6] Oropeza-Moe, M., Wislff, H., & Bernhoft, A. (2015). Selenium deficiency associated porcine and human cardiomyopathies. Journal of Trace Elements in Medicine & Biology, 31, 148-156. https://doi.org/10.1016/j.jtemb.2014.09.011

[7] Chang, J. L., & Wang, Y. (2016). The monitoring reports of nutrition and health status of Chinese residents from 2010 to 2013 ( 1st ed.). Peking University Medical Press.

[8] Quang Toan, D., Cui, Z., Huang, J., Thi Anh Thu, T., Wang, D., Yang, W., Zhou, F., Wang, M., Yu, D., & Liang, D. (2018). Selenium distribution in the Chinese environment and its relationship with human health: A review. Environment International, 112, 294-309. https://doi.org/10.1016/j.envint.2017.12.035

[9] Montes-Bayón, M., Diaz Molet, M. J., Blanco González, E., & SanzMedel, A. (2006). Evaluation of different sample extraction strategies for selenium determination in selenium-enriched plants (Allium sativum and Brassica juncea) and Se speciation by HPLC-ICP-MS. Talanta, 68(4), 1287-1293. https://doi.org/10.1016/j.talanta.2005.07.040

[10] Wang, L., Huang, Q. H., Huang, Y. F., Xie, J. H., Qu, C., Chen, J. P., Zheng, L., Yi, T. G., Zeng, H. F., & Li, H. L. (2018). Comparison of protective effffect of ordinary Cordyceps militaris and selenium-enriched Cordyceps militaris on triptolide-induced acute hepatotoxicity and the potential mechanisms. Journal of Functional Foods, 46, 365-377. https://doi.org/10.1016/j.jff.2018.05.016

[11] Vicente-Zurdo, D., Gómez-Gómez, B., Pérez-Corona, M. T., & Madrid, Y. (2019). Impact of fish growing conditions and cooking methods on selenium species in swordfish and salmon fillets. Journal of Food Composition and Analysis, 83, 103275. https://doi.org/10.1016/j.jfca.2019.103275

[12] Davis, T. Z., Tiwary, A. K., Stegelmeier, B. L., Pfister, J. A., Panter, K. E., & Hall, J. (2017). Comparative oral dose toxicokinetics of sodium selenite and selenomethionine. Journal of Applied Toxicology, 37(2), 231-238. https://doi.org/10.1002/jat.3350

[13] Marschall, T. A., Bornhorst, J., Kuehnelt, D., & Schwerdtle, T. (2016). Differing cytotoxicity and bioavailability of selenite, methylselenocysteine, selenomethionine, selenosugar 1 and trimethylselenonium ion and their underlying metabolic transformations in human cells. Molecular Nutrition and Food Research, 60(12), 2622-2632. https://doi.org/10.1002/mnfr.201600422

[14] Kubachka, K. M., Hanley, T., Mantha, M., Wilson, R. A., Falconer, T. M., Kassa, Z., Oliveira, A., Landero, J., & Caruso, J. (2017). Evaluation of selenium in dietary supplements using elemental speciation. Food Chemistry, 218, 313-320. https://doi.org/10.1016/j.foodchem.2016.08.086

[15] Fernandes, A. P., & Gandin, V. (2015). Selenium compounds as therapeutic agents in cancer. Biochimica et Biophysica Acta (BBA) - General Subjects, 1850(8), 1642-1660. https://doi.org/10.1016/j.bbagen.2014.10.008

[16] Burk, R. F., & Hill, K. E. (2015). Regulation of selenium metabolism and transport. Annual Review of Nutrition, 35(1), 109-134. https://doi.org/10.1146/annurev-nutr-071714-034250

[17] Kryukov, G. V., Castellano, S., Novoselov, S. V., Lobanov, A. V., Zehtab, O., R. Guigó, R., & Gladyshev, V. N. (2003). Characterization of mammalian selenoproteomes. Science, 300(5624), 1439-1443. https://doi.org/10.1126/science.1083516

[18] Li, S., Gao, F., Huang, J., Wu, Y., Wu, S., & Lei, X. G. (2018). Regulation and function of avian selenogenome. Biochimica et Biophysica Acta (BBA) - General Subjects, 1862(11), 2473-2479. https://doi.org/10.1016/j.bbagen.2018.03.029

[19] Seremelis, I., Danezis, G. P., Pappas, A. C., Zoidis, E., & Fegeros, K. (2019). Avian stress-related transcriptome and selenotranscriptome: Role during exposure to heavy metals and heat stress. Antioxidants, 8(7), 216. https://doi.org/10.3390/antiox8070216

[20] Zhan, J. P., Qi, M., Wang, C., Wang, X. F., Wang, H. Z., & Dun, X. L. (2024). Precise determination of selenium forms and contents in selenium-enriched rapeseed seedlings and flowering stalks by HPLC-ICP-MS. Journal of Agricultural and Food Chemistry, 72(16), 9477-9486. https://doi.org/10.1021/acs.jafc.3c08416

[21] Hu, T., Li, L., Hui, G. F., Zhang, J. J., Li, H. F., Wu, W. L., Wei, X. H., & Guo, Y. B. (2019). Selenium biofortification and its effect on multi-element change in Auricularia auricular. Food Chemistry. Food Chemistry, 295, 206-213. https://doi.org/10.1016/j.foodchem.2019.05.101

[22] Uden, P. C., Boakye, H. T., Kahakachchi, C., Hafezi, R., Nolibos, P., Block, E., Johnson, S., & Tyson, J. F. (2004). Element selective characterization of stability and reactivity of selenium species in selenized yeast. Journal of Analytical Atomic Spectrometry, 19(1), 65-73. https://doi.org/10.1016/S0039-9140(01)00398-8

[23] Dernovics, M., Garcıa-Barrera, T., Bierla, K., Preud'homme, H., & Lobinski, R. (2007). Standardless identification of selenocystathionine and its γ-glutamyl derivatives in monkeypot nuts by 3D liquid chromatography with ICP-MS detection followed by nano HPLC-Q-TOF-MS/MS. Analyst, 132(5), 439-449. https://doi.org/10.1039/b618637h

[24] Pedrero, Z., & Madrid, Y. (2009). Novel approaches for selenium speciation in foodstuffs and biological specimens: A review. Analytica Chimica Acta, 634(2), 135-152. https://doi.org/10.1016/j.aca.2008.12.026

[25] Roberge, M. T., Borgerding, A. J., & Finley, J. W. (2003). Speciation of selenium compounds from high selenium broccoli is affected by the extracting solution. Journal of Agricultural and Food Chemistry, 51(15), 4191-4197. https://doi.org/10.1021/jf021247d

[26] Bakirdere, S., Volkan, M., & Ataman, O. Y. (2015). Speciation of selenium in supplements by high performance liquid chromatography-inductively coupled plasma-mass spectrometry. Analytical Letters, 48(9), 1511-1523. https://doi.org/10.1080/00032719.2014.986679

[27] Oliveira, A. F., Landero, J., Kubachka, K., Nogueira, A. R. A., Zanetti, M. A., & Caruso, J. (2016). Development and application of a selenium speciation method in cattle feedand beef samples using HPLC-ICP-MS: Evaluating the selenium metabolic process in cattle. Journal of Analytical Atomic Spectrometry, 31(4), 1034-1040. https://doi.org/10.1039/C5JA00330J

[28] Cao, J., Guo, F. C., Zhang, L. Y., Dong, B., & Gong, L. M. (2014). Effects of dietary Selenomethionine supplementation on growth performance, antioxidant status, plasma selenium concentration, and immune function in weaning pigs. Journal of Animal Science and Biotechnology, 5(1), 46. https://doi.org/10.1186/2049-1891-5-46

[29] Zhang, H. Q., Zhao, Z. Q., Zhang, X., Zhang, W., Huang, L. Q., Zhang, Z., Yuan, L., & Liu, X. Y. (2019). Effects of foliar application of selenate and selenite at different growth stages on Selenium accumulation and speciation in potato (Solanum tuberosum L.). Food Chemistry, 286, 550-556. https://doi.org/10.1016/j.foodchem.2019.01.185

[30] Tangjaidee, P., Swedlund, P., Xiang, J., Yin, H., & Quek, S. Y. (2023). Lenium-enriched plant foods: Selenium accumulation, speciation, and health functionality. Frontiers in Nutrition, 9, 962312. https://doi.org/10.1016/10.3389/fnut.2022.962312

[31] Hu, J., Wang, Z., Zhang, L., Peng, J., Huang, T., Yang, X., Jeong, B. R., & Yang, Q. (2022). Seleno-amino acids in vegetables: A review of their forms and metabolism. Frontiers in Plant Science, 13, 804368. https://doi.org/10.1016/10.3389/fpls.2022.804368

[32] Fang, G., Lv, Q., Liu, C., Huo, M. M., & Wang, S. (2015). An ionic liquid improved HPLC-ICP-MS method for simultaneous determination of arsenic and selenium species in animal/plant-derived foodstuffs. Analytical Methods, 7(20), 8617-8625. https://doi.org/10.1039/C5AY02021B

[33] Juniper, D. T., Phipps, R. H., & Bertin, G. (2011). Effect of dietary supplementation with selenium-enriched yeast or sodium selenite on selenium tissue distribution and meat quality in commercial-line turkeys. Anima, 5(11), 1751-1760. https://doi.org/10.1017/S1751731111000796

[34] Mattioli, S., Dal Bosco, A., Duarte, J. M. M., D’Amato, R., Castellini, C., Beone, G. M., Fontanella, M. C., Beghelli, D., Regni, L., Businelli, D., Trabalza-Marinucci, M., & Proietti, P. (2019). Use of Selenium-enriched olive leaves in the feed of growing rabbits: Effect on oxidative status, mineral profile and Selenium speciation of Longissimus dorsi meat. Journal of Trace Elements in Medicine & Biology, 51, 98-105. https://doi.org/10.1016/j.jtemb.2018.10.004

[35] Lipiec, E., Siara, G., Bierla, K., Ouerdane, L., & Szpunar, J. (2010). Determination of selenomethionine, selenocysteine, and inorganic selenium in eggs by HPLC–inductively coupled plasma mass spectrometry. Analytical and Bioanalytical Chemistry, 397(2), 731-741. https://doi.org/10.1007/s00216-010-3544-8

[36] Juniper, D. T., Phipps, R. H., Ramos-Morales, E., & Bertin, G. (2009). Effect of high dose selenium enriched yeast diets on the distribution of total selenium and selenium species within lamb tissues. Livestock Science, 122(1), 63-67. https://doi.org/10.1016/j.livsci.2008.07.025

[37] Zhang, K., Guo, X. Q., Zhao, Q. Y., Han, Y. S., Zhan, T. F., Li, Y., Tang, C. H., & Zhang, J. M. (2020). Development and application of a HPLC-ICP-MS method to determine selenium speciation in muscle of pigs treated with different selenium supplements. Food Chemistry, 302, 125371. https://doi.org/10.1016/j.foodchem.2019.125371

[38] Jia, X. T., Guo, X. Q., Han, Y. S., Li, J., Zhao, Q. Y., Zhang, K., Tang, C. H., Ma, Q., Wang, J., Zhao, Z. W., Zhang, J. M., & Qin, Y. C. (2021). Evaluation of biological safety of selenium yeast for tan sheep: Growth performance, blood routine parameters, selenoprotein gene expression and enrichment regularity. Chinese Journal of Animal Nutrition, 33(9), 2-12.

[39] Si, X. Y., Wang, H., Guo, X. Q., Zhao, Q. Y., Tang, C. H., Qin, Y. C., & Zhang, J. M. (2020). Effects of different supplemental levels of yeast selenium in flaxseed diets on liver antioxidant capacity, yolk fatty acid composition and egg selenium content of laying hens. Chinese Journal of Animal Nutrtion, 32(5), 2138-2147.

[40] National Standards of the People's Republic of China. Welfare criteria for animals to be slaughtered GB/T 42304-2023.

[41] Zhang, K., Zhao, Q. Y., Zhan, T. F., Han, Y. S., Tang, C. H., & Zhang, J. M. (2020). Effect of different selenium sources on growth performance, tissue selenium content, meat quality, and selenoprotein gene expression in finishing pigs. Biological Trace Element Research, 196(2), 463-471. https://doi.org/10.1007/s12011-019-01949-3

[42] European Parliament (EU). (2003). EC No 1831/2003 (European parliament): Addi-tives for use in animal nutrition. Retrieved from https://irmm.jrc.ec.europa.eu/SiteCollectionDocuments/EC-1831-2003.pdf

[43] Kuricova, S., Boldizarova, K., Gresekova, L., Bobcek, R., Levkut, M., & Leng, L. (2003). Chicken selenium status when fed a diet supplemented with Se-yeast. Acta Veterinaria Brno, 72(3), 339-346. https://doi.org/10.2754/avb200372030339

[44] Lu, J., & Holmgren, A. (2009). Selenoproteins. Journal of Biological Chemistry, 284(2), 723-727. https://doi.org/10.1074/jbc.R800045200

[45] Weekley, C. M., & Harris, H. H. (2013). Which form is that? The importance of selenium speciation and metabolism in the prevention and treatment of disease. Chemical Society Reviews, 42(23), 8870-8894. https://doi.org/10.1039/c3cs60272a

[46] Björnstedt, M., Kumar, S., & Holmgren, A. (1992). Selenodiglutathione is a highly efficient oxidant of reduced thioredoxin and a substrate for mammalian thioredoxin reductase. Journal of Biological Chemistry, 267(12), 8030-8034. https://doi.org/10.1016/0014-5793(92)80267-K

[47] Fernández-Bautista, T., Gomez-Gomez, B., Palacin-Garcia, R., Gracia-Lor, E., Perez-Corona, T., & Madrid, Y. (2022). Analysis of Se and Hg biomolecules distribution and Se speciation in poorly studied protein fractions of muscle tissues of highly consumed fishes by SEC-UV-ICP-MS and HPLC-ESI-MS/MS. Talanta, 15(237), 122922. https://doi.org/10.1016/j.talanta.2021.122922

[48] Suzuki, K. T., Doi, C., & Suzuki, N. (2006). Metabolism of ⁷⁶Se-methylselenocysteine compared with that of ⁷⁷Se-selenomethionine and ⁸²Se-selenite. Toxicology and Applied Pharmacology, 217(2), 185-195. https://doi.org/10.1016/j.taap.2006.09.006

[49] Kantorova´, V., Kanˇa, A., Krausov´a, G., & Mestek, O. (2022). Effect of protease XXIII on selenium species interconversion during their extraction from biological samples. Journal of Food Composition and Analysis, 105, 104260. https://doi.org/10.1016/j.jfca.2021.104260

[50] Callejón-Leblic, B., Rodríguez-Moro, G., Arias-Borrego, A., Pereira-Vega, A., Gómez-Ariza, J. L., & García-Barrera, T. (2020). Absolute quantification of selenoproteins and selenometabolites in lung cancer human serum by column switching coupled to triple quadrupole inductively coupled plasma mass spectrometry. Journal of Chromatography A, 1619, 460919. https://doi.org/10.1016/j.chroma.2020.460919002

[51] Schomburg, L. (2011). Selenium, selenoproteins and the thyroid gland: Interactions in health and disease. Nature Reviews Endocrinology, 8(3), 160-171. https://doi.org/10.1038/nrendo.2011.174

[52] Gammelgaard, B., Rasmussen, L. H., Gabel-Jensen, C., & Steffansen, B. (2012). Steffansen. Estimating intestinal absorption of inorganic and organic selenium compounds by in vitro flux and biotransformation studies in Caco-2 cells and ICP-MS detection. Biological Trace Element Research, 145(2), 248-256. https://doi.org/10.1007/s12011-011-9174-y

[53] Thiry, C., Ruttens, A., Pussemier, L., & Schneider, Y. L. (2013). An in vitro investigation of species-dependent intestinal transport of selenium and the impact of this process on selenium bioavailability. British Journal of Nutrition, 109(12), 2126-2134. https://doi.org/10.1017/S0007114512004412

[54] Schrauzer, G. N. (2000). Selenomethionine: A review of its nutritional significance, metabolism and toxicity. The Journal of Nutrition, 130(7), 1653-1656. https://doi.org/10.1093/jn/130.7.1653

[55] Bierla, K., Szpunar, J., Yiannikouris, A., & Lobinski, R. (2012). Comprehensive speciation of selenium in selenium-rich yeast. TrAC, Trends in Analytical Chemistry, 41, 122-132. https://doi.org/10.1016/j.trac.2012.08.006

[56] Ma, S., Caprioli, R. M., Hill, K. E., & Burk, R. F. (2003). Loss of selenium from selenoproteins: Conversion of selenocysteine to dehydroalanine in vitro. Journal of the American Society for Mass Spectrometry, 14(6), 593-600. https://doi.org/10.1016/S1044-0305(03)00141-7

[57] Zhan, X. A., Wang, M., Zhao, R. Q., Li, W. F., & Xu, Z. R. (2007). Effects of different selenium source on selenium distribution, loin quality and antioxidant status in finishing pigs. Animal Feed Science and Technology, 132(3–4), 202-211. https://doi.org/10.1016/j.anifeedsci.2006.03.020

[58] Juniper, D. T., Phipps, R. H., Ramos-Morales, E., & Bertin, G. (2008). Selenium persistency and speciation in the tissues of lambs following the withdrawal of dietary high-dose selenium-enriched yeast. Animal, 2(3), 375-380. https://doi.org/10.1017/S1751731107001395

[59] Lei, X. G., Dann, H. M., Ross, D. A., Cheng, W. H., Combs, G. F., & Roneker, K. R. (1998). Dietary selenium supplementation is required to support full expression of three selenium-dependent glutathione peroxidases in various tissues of weanling pigs. The Journal of Nutrition, 128(1), 130-135. https://doi.org/10.1038/sj.ijo.0800548

[60] Bryszewska, M. A., & Mågeb, A. (2015). Determination of selenium and its compounds in marine organisms. Journal of Trace Elements in Medicine & Biology, 29, 91-98. https://doi.org/10.1016/j.jtemb.2014.10.004

[61] Bakırdere, S., Volkan, M., & Ataman, O. Y. (2018). Selenium speciation in chicken breast samples from inorganic and organic selenium fed chickens using high performance liquid chromatography-inductively coupled plasma-mass spectrometry. Journal of Food Composition and Analysis, 17, 28-35. https://doi.org/10.1016/j.jfca.2018.05.005

[62] Evenson, J. K., & Sunde, R. A. (2021). Metabolism of tracer ⁷⁵Se selenium from inorganic and organic selenocompounds into selenoproteins in rats, and the missing ⁷⁵Se metabolites. Frontiers in Nutrition, 8, 699652. https://doi.org/10.3389/fnut.2021.699652

[63] Bierla, K., Taylor, R. M., Szpunar, J., Lobinski, R., & Sunde, R. A. (2020). Identification and determination of selenocysteine, selenosugar, and other selenometabolites in Turkey liver. Metallomics, 12(5), 758-766. https://doi.org/10.1039/d0mt00040j

[64] Capelo, J. L., Fernandez, C., Pedras, B., Santos, P., Gonzalez, P., & Vazb, C. (2006). Trends in selenium determination/speciation by hyphenated techniques based on AAS or AFS. Talanta, 68(5), 1442-1447. https://doi.org/10.1016/j.talanta.2005.08.027

[65] Jagtap, R., & Maher, W. (2016). Determination of selenium species in biota with an emphasis on animal tissues by HPLC-ICP-MS. Microchemical Journal, 124, 422-529. https://doi.org/10.1016/j.microc.2015.07.014

[66] Spears, J. W. (2003). Trace mineral bioavailability in ruminants. Journal of Nutrition, 133(5), 1506S-1509S. https://doi.org/10.1093/jn/133.5.1506S

[67] Gresakova, L., Cobanova, K., & Faix, S. (2013). Selenium retention in lambs fed diets supplemented with selenium from inorganic or organic sources. Small Ruminant Research, 111(1–3), 76-82. https://doi.org/10.1016/j.smallrumres.2012.10.009

[68] Katarzyna, B., Joanna, S., Alexandros, Y., & Lobinski, R. (2012). Comprehensive speciation of selenium in selenium-rich yeast. Trends in Analytical Chemistry, 41, 201-210. https://doi.org/10.1016/j.trac.2012.08.006

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