Research Article
Gökkuşağı alabalığı rasyonuna eklenen astaksantinin kas dokusu siyalik asit miktarı üzerine etkisinin araştırılması
Abstract
Astaksantin, sucul hayvanlarda, pigmentasyondan, temel çoklu doymamış yağ asitlerinin oksidasyondan korunmasından, bağışıklık tepkisinden, iletişimden ve üremeden sorumlu oksitlenmiş bir karotenoid bileşenidir. Su ürünleri yetiştiriciliğinde astaksantin, Gökkuşağı alabalığına, etinin kendine özgü pembemsi rengini vermek için kullanılan bir pigmenttir. Siyalik asit, nöraminik asidin açillenmiş bir türevidir ve birçok glikoprotein ve glikolipidin oligosakkarit zincirlerinin terminal bileşeni olan dokuz karbonlu bir omurgaya sahip bir alfa-keto asit monosakarittir. Hücrelerin tanınmasında, iletişiminde, sinyalleşmesinde, kümelenmesinde ve gelişmesinde, enfeksiyonlarda, tümör büyümesinde ve metastazında, immunolojide, üreme biyolojisinde ve nörolojide önemli etkilere sahiptir. Sunulan çalışmada 40 adet dişi Gökkuşağı alabalığı kullanıldı. Balıklar iki gruba ayrılmış olup deney grubuna (n=20) 225 gün boyunca günlük 50 ppm/gün astaksantin verilirken, kontrol grubu (n=20) standart balık rasyonu ile beslendi. Balık kas dokusunda siyalik asit konnsantrasyonu enzim bağlı immünosorbent analiz (ELISA) yöntemi ile belirlendi. Normal balık rasyonu ile beslenmiş balıkların kas dokusu siyalik asit düzeyi 111,97 ± 4,56 µg/g ve rasyonuna astaksantin eklenmiş balık kas dokusunda siyalik asit düzeyi 110,33 ± 8,54 µg/g olarak bulundu. Araştırmamızda, balık diyetine astaksantin eklenmesinin, insan beslenmesinde çok önemli olan balıklardaki siyalik asit miktarında değişikliğe neden olmadığı belirlendi (p>0,05). Sonuç olarak rasyona eklenen astaksantinin balık kas dokusu siyalik asit miktarı üzerine bir etkisi olmadığı ortaya konuldu.
Keywords
Supporting Institution
Ondokuz Mayıs Üniversitesi Bilimsel Araştırma Projeleri birimi
Project Number
PYO.VET 1904.18.017
References
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- Aktaç T, Bakar E, Güner U. (2010) The effects of short-term exposure to cadmium and copper on sialic acid in carp (Cyprinus carpio) tissues. Fresenius Environ Bull. 19(3), 432-437.
- Angata T, Varki A. (2002) Chemical diversity in the sialic acids and related α-ketoacids: an evolutionary perspective. Chem Rev. 102(2), 439-470. doi: 10.1021/cr000407m.
- Azimzadeh K, Amniattalab A. (2017) Total sialic acid, oxidative stress and histopathological changes in rainbow trout saprolegniasis (Oncorhynchus mykiss). Kafkas Univ Vet Fak Derg, 23, 55-62. doi: 10.9775/kvfd.2016.15812
- Balami S, Sharma A, Karn R. (2019) Significance of nutritional value of fish for human health. Malaysian Journal of Halal Research, 2(2), 32-34. doi: 10.2478/mjhr-2019-0012
- Bork K, Reutter W, Gerardy-Schahn R, Horstkorte R. (2005). The intracellular concentration of sialic acid regulates the polysialylation of the neural cell adhesion molecule. FEBS Lett. 579(22), 5079-5083. doi: 10.1016/j.febslet.2005.08.013
- Bull C, Boltje TJ, vanDinther EA, Peters T, de Graaf AM, Leusen JH, Adema GJ. (2015) Targeted delivery of a sialic acid-blocking glycomimetic to cancer cells inhibits metastatic spread. ACS Nano. 9(1) 733-745. doi: 10.1021/nn5061964
- Chen X, Varki A. (2010) Advances in the biology and chemistry of sialic acids. ACS Chem Biol. 5(2), 163-176. doi: 10.1021/cb900266r
- Crawford MA, Broadhurst CL. (2012) The role of docosahexaenoic and the marine food web as determinants of evolution and hominid brain development: the challenge for human sustainability. Nutr Health. 21(1), 17–39. doi: 10.1177/0260106012437550
- Deng, L., Chen, X., Varki, A. (2013) Exploration of sialic acid diversity and biology using sialoglycan micro arrays. Biopolymers. 99(10), 650-665. doi: 10.1002/bip.22314
- Di W, Fujita A, Hamaguchi K, Delannoy P, Sato C, Kitajima K. (2017) Diverse subcellular localizations of the insect CMP-sialic acid synthetases. Glycobiology. 27(4), 329-341. doi: 10.1093/glycob/cww128
- Elia AC, Prearo M, Dörr AJM, Pacini N, Magara G, Brizio P, Gasco L, Abete MC. (2019) Effects of astaxanthin and canthaxanthin on oxidative stress biomarkers in rainbow trout. J Toxicol Environ Health A. 82(13), 760-768. doi: 10.1080/15287394.2019.1648346
- Fakhri S, Abbaszadeh F, Dargahi L, Jorjani M. (2018) Astaxanthin: A mechanistic review on its biological activities and health benefits. Pharmacol Res. 136, 1-20. doi: 10.1016/j.phrs.2018.08.012
- Fang N, Wang C, Liu X, Zhao X, Liu Y, Liu X, Zhao X, Liu Y, Liu X, Du Y, Zhang Z, Zhang, H. (2019) De novo synthesis of astaxanthin: From organisms to genes. Trends Food Sci Technol. 92, 162-171.
- Fukuda M. (1996) Possible roles of tumor-associated carbohydrate antigens. Cancer research, 56(10), 2237-2244.
- Ghosh S. (2020) Sialic acids and sialoglycoconjugates in the biology of life, health and disease. Academic Press.
- Guerin M, Huntley ME, Olaizola M. (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 21, 5. doi: 10.1016/S0167-7799(03)00078-7.
- Guo CT, Takahashi T, Bukawa W, Takahashi N, Yagi H, Kato K, Suzuki Y. (2006) Edible bird's nest extract inhibits influenza virüs infection. Antiviral Res. 70(3), 140-146. doi: 10.1016/j.antiviral.2006.02.005
- Haghani A, Mehrbod P, Safi N, A’ini Abd Kadir F, Omar AR, Ideris A. (2017) Edible bird’s nest modulate intracellular molecular pathways of influenza A virüs infected cells. BMC Complement Altern Med. 17(1). 1-13. doi: 10.1186/s12906-016-1498-x
- Haghani A, Mehrbod P, Safi N, Aminuddin NA, Bahadoran A, Omar AR, Ideris A. (2016) Invitroandin vivomechanism of immunomodulatory and antiviral activity of Edible Bird'sNest (EBN) against influenza A virus (IAV) infection. J Ethnopharmacol. 185, 327-340. doi: 10.1016/j.jep.2016.03.020
- Harker M, Young AJ. (1995) Inhibition of astaxanthin synthesis in the green alga, Haematococcus pluvialis. Eur J Phycol. 30(3), 179-187.
- Heidarieh M, Moodi S, Safari O. (2019). Variations of kidney, liver and spleen total sialic acid levels in immunized rainbow trout (Oncorhynchus mykiss) against Ichthyophthirius multifiliis. Vet Arh. 89(2), 223-232.
- Huang X, Dong W, Milewska A, Golda A, Qi Y, Zhu QK, Sui J. (2015) Human coronavirus HKU1 spike protein uses O-acetylated sialicacid as an attachment receptor determinant and employs hemagglutinin-esterase protein as a receptor-destroying enzyme. J Virol. 89(14), 7202-7213. doi: 10.1128/JVI.00854-15
- Kaya İ, Karapehlivan M, Yilmaz M, Ersan Y, Koç E. (2012) Investigation of effects on plasma nitric oxide, malondialdehyde and total sialic acid levels of glyphosate in Kars creek transcaucasian barb (Capoeta capoeta [Guldenstaedt, 1773]) in Turkey. Fresenius Environ Bull. 21(1A), 123-6.
- Lorenz RT, Cysewski GR. (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol. 18, 160–167, 2000. doi: 10.1016/s0167-7799(00)01433-5
- Malykh YN, Krisch B, Gerardy-Schahn R, Lapina EB, Shaw L, Schauer R. (1999) The presence of N-acetylneuraminicacid in Malpighiantubules of larvae of the cicada Philaenusspumarius. Glycoconj J. 16(11), 731-739. doi: 10.1023/a:1007115627708
- Matsumoto A, Cabral H, Sato N, Kataoka K, Miyahara Y. (2010) Assessment of tumor metastasis by the direct determination of cell‐membrane sialic acid expression. Angew Chem. 122(32), 5626-5629. doi: 10.1002/anie.201001220
- Mishra SP. (2020) Significance of fish nutrients for human health. International Journal of Fisheries and Aquatic Research. 5(3), 47-49.
- Narayanan S. (1994) Sialic acid as a tumor marker. Ann Clin Lab Sci. 24(4), 376-384.
- Pongracz T, Wuhrer M, de Haan N. (2019) Expanding the reaction space of linkage-specific sialic acid derivatization. Molecules. 24(19), 3617. doi: 10.3390/molecules24193617
- Řehulka J. (2000) Influence of astaxanthin on growth rate, condition, and some blood indices of rainbow trout, Oncorhynchus mykiss. Aquaculture. 190(1-2), 27-47.
- Repnikova E, Koles K, Nakamura M, Pitts J, Li H, Ambavane A, Panin VM. (2010) Sialyl transferase regulates nervous system function in Drosophila. J Neurosci. 30(18), 6466-6476. doi: 10.1523/JNEUROSCI.5253-09.2010
- Roth J, Kempf A, Reuter G, Schauer R, Gehring WJ. (1992) Occurrence of sialic acids in Drosophila melanogaster. Science. 256(5057), 673-675. doi: 10.1126/science.1585182
- Sarojnalini C, Hei A. (2019) Fish as an important functional food for quality life. Functional foods,(Lagouri, V., ured.), IntechOpen, London, 77-97.
- Schauer R, Kelm S, Reuter G, Roggentin P, Shaw L. (1995) Biochemistry and role of sialic acids. In: Biology of theSialic Acids. Boston, MA: Springer; pp. 7-67.
- Schauer R. (2009) Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19(5), 507-514. doi: 10.1016/j.sbi.2009.06.003
- Schauer R, Kamerling JP. (2018) Kamerling Exploration of the Sialic Acid World. Advances in Carbohydrate Chemistry and Biochemistry. 1st ed., 75. Elsevier Inc.
- Schiedt K, Vecchi M, Glinz E. (1986) Astaxanthin and its metabolites in wild rainbow trout (Salrnogaivdneri R.). Comp Biochem Physid. 83B, 9-12.
- Schnaar RL, Gerardy-Schahn R, Hildebrandt H. (2014) Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 94(2), 461-518. doi: 10.1152/physrev.00033.2013
- Storebakken T, No HK. (1992) Pigmentation of rainbow trout. Aquaculture, 100(1-3), 209-229.
- Sun X, Zhang S, Ren J, Udenigwe CC. (2020) Sialic acid-based strategies for the prevention and treatment of Helicobacter pylori infection: Emerging trends in food industry. Crit Rev Food Sci Nutr. 1-12. doi: 10.1080/10408398.2020.1846157
- Wang CY, Cheng LJ, Shen B, Yuan ZL, Feng YQ, Lu SH. (2019) Anti hypertensive and antioxidant properties of sialic acid, the major component of edible bird's nests. Curr Top Nutraceutical Res. 17(4), 376-380.
- Yılmaz E, Aydın M, Yıldırım A, Şahin P. (2018) The importance of consumption of fish meat in early childhood period in terms of healthy development. Süleyman Demirel Üniversitesi Eğirdir Su Ürünleri Fakültesi Dergisi. 14(4), 357-364. doi: 10.22392/egirdir.405244
- Zhou, S., Zhang, T., Peng, B., Luo, X., Liu, X., Hu, L., Deng, Y. (2017) Targeted delivery of epirubic into tumor-associated macrophages by sialic acid cholesterol conjugate modified liposomes with improved anti tumor activity. Int J Pharm. 523(1), 203-216. doi: 10.1016/j.ijpharm.2017.03.034
Investigation of the effect of astaxanthin administration on the amount of sialic acid in muscle tissue in Rainbow trout
Abstract
Astaxanthin is an oxidized carotenoid component responsible for pigmentation, protecting essential polyunsaturated fatty acids from oxidation, immune response, communication, reproductive behavior, and improved reproduction in aquatic animals. In aquaculture, astaxanthin is a pigment used to give rainbow trout flesh its distinctive pinkish tint. Sialic acid is an alpha-keto acid monosaccharide with a nine-carbon backbone that is an acylated derivative of neuraminic acid and a terminal component of the oligosaccharide chains of many glycoproteins and glycolipids. It impacts cell recognition, communication, signaling, cellular aggregation and development, infections, tumor growth and metastasis, immunology, reproductive biology, and neurology. Forty female rainbow trout were used in the study. Fish were divided into two groups. The experimental group (n=20) received a daily dose of astaxanthin of 50 ppm/day for 225 days, whereas the control group (n=20) received a standard fish meal. The concentration of sialic acid in fish muscle tissue was evaluated using the enzyme-linked immunosorbent assay (ELISA) method. The sialic acid level in muscle tissue of fish fed a standard fish ration was 111.97 ± 4.56 µg/g, while the sialic acid level in muscle tissue of fish fed astaxanthin was 110.33 ± 8.54 µg/g. In our research, we found that adding astaxanthin to the fish diet had no effect on the amount of sialic acid in the fish, which is crucial in human nutrition. As a result, it was revealed that dietary astaxanthin did not influence the level of sialic acid in fish muscle tissue (p>0.05).
Keywords
Project Number
PYO.VET 1904.18.017
References
- Abdul Khalid SK, AbdRashed A, Abdul Aziz S, Ahmad H. (2019) Effects of sialic acid from edible bird nest on cell viability associated with brain cognitive performance in mice. World J Tradit Chin Med. 5(4), 214-219. doi: 10.4103/wjtcm.wjtcm_22_19
- Aktaç T, Bakar E, Güner U. (2010) The effects of short-term exposure to cadmium and copper on sialic acid in carp (Cyprinus carpio) tissues. Fresenius Environ Bull. 19(3), 432-437.
- Angata T, Varki A. (2002) Chemical diversity in the sialic acids and related α-ketoacids: an evolutionary perspective. Chem Rev. 102(2), 439-470. doi: 10.1021/cr000407m.
- Azimzadeh K, Amniattalab A. (2017) Total sialic acid, oxidative stress and histopathological changes in rainbow trout saprolegniasis (Oncorhynchus mykiss). Kafkas Univ Vet Fak Derg, 23, 55-62. doi: 10.9775/kvfd.2016.15812
- Balami S, Sharma A, Karn R. (2019) Significance of nutritional value of fish for human health. Malaysian Journal of Halal Research, 2(2), 32-34. doi: 10.2478/mjhr-2019-0012
- Bork K, Reutter W, Gerardy-Schahn R, Horstkorte R. (2005). The intracellular concentration of sialic acid regulates the polysialylation of the neural cell adhesion molecule. FEBS Lett. 579(22), 5079-5083. doi: 10.1016/j.febslet.2005.08.013
- Bull C, Boltje TJ, vanDinther EA, Peters T, de Graaf AM, Leusen JH, Adema GJ. (2015) Targeted delivery of a sialic acid-blocking glycomimetic to cancer cells inhibits metastatic spread. ACS Nano. 9(1) 733-745. doi: 10.1021/nn5061964
- Chen X, Varki A. (2010) Advances in the biology and chemistry of sialic acids. ACS Chem Biol. 5(2), 163-176. doi: 10.1021/cb900266r
- Crawford MA, Broadhurst CL. (2012) The role of docosahexaenoic and the marine food web as determinants of evolution and hominid brain development: the challenge for human sustainability. Nutr Health. 21(1), 17–39. doi: 10.1177/0260106012437550
- Deng, L., Chen, X., Varki, A. (2013) Exploration of sialic acid diversity and biology using sialoglycan micro arrays. Biopolymers. 99(10), 650-665. doi: 10.1002/bip.22314
- Di W, Fujita A, Hamaguchi K, Delannoy P, Sato C, Kitajima K. (2017) Diverse subcellular localizations of the insect CMP-sialic acid synthetases. Glycobiology. 27(4), 329-341. doi: 10.1093/glycob/cww128
- Elia AC, Prearo M, Dörr AJM, Pacini N, Magara G, Brizio P, Gasco L, Abete MC. (2019) Effects of astaxanthin and canthaxanthin on oxidative stress biomarkers in rainbow trout. J Toxicol Environ Health A. 82(13), 760-768. doi: 10.1080/15287394.2019.1648346
- Fakhri S, Abbaszadeh F, Dargahi L, Jorjani M. (2018) Astaxanthin: A mechanistic review on its biological activities and health benefits. Pharmacol Res. 136, 1-20. doi: 10.1016/j.phrs.2018.08.012
- Fang N, Wang C, Liu X, Zhao X, Liu Y, Liu X, Zhao X, Liu Y, Liu X, Du Y, Zhang Z, Zhang, H. (2019) De novo synthesis of astaxanthin: From organisms to genes. Trends Food Sci Technol. 92, 162-171.
- Fukuda M. (1996) Possible roles of tumor-associated carbohydrate antigens. Cancer research, 56(10), 2237-2244.
- Ghosh S. (2020) Sialic acids and sialoglycoconjugates in the biology of life, health and disease. Academic Press.
- Guerin M, Huntley ME, Olaizola M. (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol. 21, 5. doi: 10.1016/S0167-7799(03)00078-7.
- Guo CT, Takahashi T, Bukawa W, Takahashi N, Yagi H, Kato K, Suzuki Y. (2006) Edible bird's nest extract inhibits influenza virüs infection. Antiviral Res. 70(3), 140-146. doi: 10.1016/j.antiviral.2006.02.005
- Haghani A, Mehrbod P, Safi N, A’ini Abd Kadir F, Omar AR, Ideris A. (2017) Edible bird’s nest modulate intracellular molecular pathways of influenza A virüs infected cells. BMC Complement Altern Med. 17(1). 1-13. doi: 10.1186/s12906-016-1498-x
- Haghani A, Mehrbod P, Safi N, Aminuddin NA, Bahadoran A, Omar AR, Ideris A. (2016) Invitroandin vivomechanism of immunomodulatory and antiviral activity of Edible Bird'sNest (EBN) against influenza A virus (IAV) infection. J Ethnopharmacol. 185, 327-340. doi: 10.1016/j.jep.2016.03.020
- Harker M, Young AJ. (1995) Inhibition of astaxanthin synthesis in the green alga, Haematococcus pluvialis. Eur J Phycol. 30(3), 179-187.
- Heidarieh M, Moodi S, Safari O. (2019). Variations of kidney, liver and spleen total sialic acid levels in immunized rainbow trout (Oncorhynchus mykiss) against Ichthyophthirius multifiliis. Vet Arh. 89(2), 223-232.
- Huang X, Dong W, Milewska A, Golda A, Qi Y, Zhu QK, Sui J. (2015) Human coronavirus HKU1 spike protein uses O-acetylated sialicacid as an attachment receptor determinant and employs hemagglutinin-esterase protein as a receptor-destroying enzyme. J Virol. 89(14), 7202-7213. doi: 10.1128/JVI.00854-15
- Kaya İ, Karapehlivan M, Yilmaz M, Ersan Y, Koç E. (2012) Investigation of effects on plasma nitric oxide, malondialdehyde and total sialic acid levels of glyphosate in Kars creek transcaucasian barb (Capoeta capoeta [Guldenstaedt, 1773]) in Turkey. Fresenius Environ Bull. 21(1A), 123-6.
- Lorenz RT, Cysewski GR. (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol. 18, 160–167, 2000. doi: 10.1016/s0167-7799(00)01433-5
- Malykh YN, Krisch B, Gerardy-Schahn R, Lapina EB, Shaw L, Schauer R. (1999) The presence of N-acetylneuraminicacid in Malpighiantubules of larvae of the cicada Philaenusspumarius. Glycoconj J. 16(11), 731-739. doi: 10.1023/a:1007115627708
- Matsumoto A, Cabral H, Sato N, Kataoka K, Miyahara Y. (2010) Assessment of tumor metastasis by the direct determination of cell‐membrane sialic acid expression. Angew Chem. 122(32), 5626-5629. doi: 10.1002/anie.201001220
- Mishra SP. (2020) Significance of fish nutrients for human health. International Journal of Fisheries and Aquatic Research. 5(3), 47-49.
- Narayanan S. (1994) Sialic acid as a tumor marker. Ann Clin Lab Sci. 24(4), 376-384.
- Pongracz T, Wuhrer M, de Haan N. (2019) Expanding the reaction space of linkage-specific sialic acid derivatization. Molecules. 24(19), 3617. doi: 10.3390/molecules24193617
- Řehulka J. (2000) Influence of astaxanthin on growth rate, condition, and some blood indices of rainbow trout, Oncorhynchus mykiss. Aquaculture. 190(1-2), 27-47.
- Repnikova E, Koles K, Nakamura M, Pitts J, Li H, Ambavane A, Panin VM. (2010) Sialyl transferase regulates nervous system function in Drosophila. J Neurosci. 30(18), 6466-6476. doi: 10.1523/JNEUROSCI.5253-09.2010
- Roth J, Kempf A, Reuter G, Schauer R, Gehring WJ. (1992) Occurrence of sialic acids in Drosophila melanogaster. Science. 256(5057), 673-675. doi: 10.1126/science.1585182
- Sarojnalini C, Hei A. (2019) Fish as an important functional food for quality life. Functional foods,(Lagouri, V., ured.), IntechOpen, London, 77-97.
- Schauer R, Kelm S, Reuter G, Roggentin P, Shaw L. (1995) Biochemistry and role of sialic acids. In: Biology of theSialic Acids. Boston, MA: Springer; pp. 7-67.
- Schauer R. (2009) Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19(5), 507-514. doi: 10.1016/j.sbi.2009.06.003
- Schauer R, Kamerling JP. (2018) Kamerling Exploration of the Sialic Acid World. Advances in Carbohydrate Chemistry and Biochemistry. 1st ed., 75. Elsevier Inc.
- Schiedt K, Vecchi M, Glinz E. (1986) Astaxanthin and its metabolites in wild rainbow trout (Salrnogaivdneri R.). Comp Biochem Physid. 83B, 9-12.
- Schnaar RL, Gerardy-Schahn R, Hildebrandt H. (2014) Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 94(2), 461-518. doi: 10.1152/physrev.00033.2013
- Storebakken T, No HK. (1992) Pigmentation of rainbow trout. Aquaculture, 100(1-3), 209-229.
- Sun X, Zhang S, Ren J, Udenigwe CC. (2020) Sialic acid-based strategies for the prevention and treatment of Helicobacter pylori infection: Emerging trends in food industry. Crit Rev Food Sci Nutr. 1-12. doi: 10.1080/10408398.2020.1846157
- Wang CY, Cheng LJ, Shen B, Yuan ZL, Feng YQ, Lu SH. (2019) Anti hypertensive and antioxidant properties of sialic acid, the major component of edible bird's nests. Curr Top Nutraceutical Res. 17(4), 376-380.
- Yılmaz E, Aydın M, Yıldırım A, Şahin P. (2018) The importance of consumption of fish meat in early childhood period in terms of healthy development. Süleyman Demirel Üniversitesi Eğirdir Su Ürünleri Fakültesi Dergisi. 14(4), 357-364. doi: 10.22392/egirdir.405244
- Zhou, S., Zhang, T., Peng, B., Luo, X., Liu, X., Hu, L., Deng, Y. (2017) Targeted delivery of epirubic into tumor-associated macrophages by sialic acid cholesterol conjugate modified liposomes with improved anti tumor activity. Int J Pharm. 523(1), 203-216. doi: 10.1016/j.ijpharm.2017.03.034
There are 44 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Veterinary Sciences |
| Journal Section | Original Article |
| Authors | |
| Project Number | PYO.VET 1904.18.017 |
| Publication Date | December 23, 2022 |
| Submission Date | July 5, 2022 |
| Published in Issue | Year 2022 Volume: 33 Issue: 2 |
