Sains Malaysiana 53(2)(2024): 239-248

http://doi.org/10.17576/jsm-2024-5302-01

Evaluation of Encapsulated Astaxanthin from White Shrimp Shells (Litopenaeus vannamei) on Hepatotoxicity

(Penilaian Astaxantin Berkapsul daripada Kulit Udang Putih (Litopenaeus vannamei) terhadap Kehepatoksikan)

NIRACHA YANYIUM^1#, WANIDA SUKKETSIRI^1#, PENNAPA CHONPATHOMPIKUNLERT², WANWIMOL KLAYPRADIT³, JIRAWAT SAETAN¹, SEBASTIEN MARAIS⁴ & SUPITA TANASAWET^1,*

¹Division of Health and Applied Sciences, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

²Biodiversity Research Centre (BRC), Thailand Institute of Scientific and Technological Research (TISTR), Pathumthani, 12120, Thailand

³Department of Fishery Products, Faculty of Fisheries, Kasetsart University, Bangkok, 10900, Thailand

⁴Univ. Bordeaux, CNRS, INSERM, Bordeaux Imaging Center, BIC, UAR 3420, US 4, F-33000 Bordeaux, France

Diserahkan: 13 Jun 2023/Diterima: 1 Februari 2024

Abstract

Recent advances in astaxanthin encapsulation have been reported, but hepatotoxic effect remains unclear. The present investigation therefore aimed to examine the effects of encapsulated astaxanthin from white shrimp shells (Litopenaeus vannamei) on liver toxicity. Wistar rats were divided into 6 groups as control (C), and receiving vitamin E (VE), astaxanthin commercial (AC), astaxanthin extracted from white shrimp shells (AE), astaxanthin encapsulation into powder form (AP), and blank powder (BP). The evaluation of liver in response to astaxanthin administration was then assessed in terms of biochemical parameters and histopathological features. Liver enzymes, aspartate aminotransferase (AST) and alanine aminotransferase (ALT), showed no significant differences among all groups of treatment. Histopathological study showed no abnormal changes on liver tissue including hepatic inflammation. Our data demonstrated that astaxanthin encapsulation did not increase the expression of NF-ҡB nuclear translocation and CYP2E1 in comparison with the control group. Additionally, in this study, the consumption of astaxanthin and vitamin E resulted in a reduction in the oxidative stress index (OSI), while the levels of antioxidant enzymes, including glutathione peroxidase (GPx) and superoxide dismutase (SOD), were significantly increased compared to the control group. Our data suggested that astaxanthin encapsulation does not cause hepatic toxicity, contributing useful information in the applications of astaxanthin encapsulation technology.

Keywords: Astaxanthin; encapsulation; histopathology; liver; white shrimp shells

Abstrak

Perkembangan terkini dalam enkapsulasi astaxantin telah dilaporkan, namun kesan hepatotoksik masih tidak jelas. Oleh itu, penyelidikan ini bertujuan untuk mengkaji kesan astaxantin terkapsul daripada kulit udang putih (Litopenaeus vannamei) terhadap ketoksikan hati. Tikus Wistar dibahagikan kepada 6 kumpulan sebagai kawalan (C), serta menerima vitamin E (VE), astaxantin komersial (AC), astaxantin yang diekstrak daripada kulit udang putih (AE), astaxantin enkapsulasi dalam bentuk serbuk (AP) dan serbuk kosong (BP). Penilaian hati sebagai tindak balas kepada perlakuan astaxantin kemudiannya dinilai daripada segi parameter biokimia dan ciri histopatologi. Enzim hati, aspartat aminotransferase (AST) dan alanin aminotransferase (ALT), tidak menunjukkan perbezaan yang signifikan antara semua kumpulan rawatan. Kajian histopatologi mendedahkan tiada perubahan abnormal pada tisu hati termasuk keradangan hepatik. Data kami menunjukkan bahawa enkapsulasi astaxantin tidak meningkatkan pengekspresn translokasi nuklear NF-ҡB dan CYP2E1 berbanding kumpulan kawalan. Di samping itu, dalam kajian ini, penggunaan astaxantin dan vitamin E mengakibatkan pengurangan dalam indeks tekanan oksidatif (OSI), manakala tahap enzim antioksidan, termasuk glutation peroksidase (GPx) dan superoksida dismutase (SOD), meningkat dengan signifikan berbanding kumpulan kawalan. Data kami mencadangkan bahawa enkapsulasi astaxantin tidak menyebabkan ketoksikan hepatik, lantas menyumbang maklumat berguna dalam aplikasi teknologi pengkapsulan astaxantin.

Kata kunci: Astaxantin; enkapsulasi; hati; histopatologi; kulit udang putih

RUJUKAN

Al-kasmi, B., Alsirawan, B., Bashimam, M. & El-zein, H. 2017. Mechanical microencapsulation: The best technique in taste masking for the manufacturing scale- effect of polymer encapsulation on drug targeting. Journal of Controlled Release 260: 134-141.

Ambati, R.R., Phang, S.M., Ravi, S. & Aswathanarayana, R.G. 2014. Astaxanthin: Sources, extraction, stability, biological activities and its commercial application - A review. Marine Drugs 12: 128-152.

Arauz, J., Ramos-Tovar, E. & Muriel, P. 2016. Redox state and methods to evaluate oxidative stress in liver damage: From bench to bedside. Annals of Hepatology 15(2): 160-173.

Chen, Z., Tian, R., She, Z., Cai, J. & Li, H. 2020. Role of oxidative stress in the pathogenesis of nonalcoholic fatty liver disease. Free Radical Biology and Medicine 152: 116-141.

Chintong, S., Phatvej, W., Rerk-Am, U., Waiprib, Y. & Klaypradit, W. 2019. In vitro antioxidant, antityrosinase, and cytotoxic activities of astaxanthin from shrimp waste. Antioxidants 8: 128.

Cichoz-Lach, H. & Michalak, A. 2014. Oxidative stress as a crucial factor in liver disease. World Journal of Gastroenterology 20(25): 8082-8091.

Coelho, J.F., Ferreira, P.C., Alves, P., Cordeiro, R., Fonseca, A.C., Gois, J.R. & Gil, M.H. 2010. Drug delivery systems: Advanced technologies potentially applicable in personalized treatments. The EPMA Journal 1(1): 164-209.

Gasmi, B. & Kleiner, D.E. 2020. Liver histology: Diagnostic and prognostic features. Clinics in Liver Disease 24(1): 61-74.

Giannini, E.G., Testa, R. & Savarino, V. 2005. Liver enzyme alteration: A guide for clinicians. Canadian Medical Association Journal 172(3): 367-379.

Greuter, T. & Shah, V.H. 2016. Hepatic sinusoids in liver injury, inflammation, and fibrosis: New pathophysiological insights. Journal of Gastroenterology 51: 511-519.

Inglut, C.T., Sorrin, A.J., Kuruppu, T., Vig, S., Cicalo, J., Ahmad, H. & Huang, H.C. 2020. Immunological and toxicological considerations for the design of liposomes. Nanomaterials 10(2): 190.

Kuedo, Z., Sangsuriyawong, A., Klaypradit, W., Tipmanee, V. & Chonpathompikunlert, P. 2016. Effects of astaxanthin from Litopenaeus vannamei on carrageenan-induced edema and pain behavior in mice. Molecules 21: 382.

Kleiner, D.E. 2017. Histopathological challenges in suspected drug-induced liver injury. Liver International 38(2): 198-209.

Kobayashi, A., Suzuki, Y. & Sugai, S. 2020. Specificity of transaminase activities in the prediction of drug-induced hepatotoxicity. The Journal of Toxicological Sciences 45(9): 515-537.

Luedde, T. & Schwabe, R.F. 2011. NF-kB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nature Reviews Gastroenterology & Hepatology 8(2): 108-118.

Martinez-Alvarez, O., Calvo, M.M. & Gomez-Estaca, J. 2020. Recent advances in astaxanthin micro/nanoencapsulation to improve its stability and functionality as a food ingredient. Marine Drugs 18(8): 406.

Meunier, L. & Larrey, D. 2019. Drug-induced liver injury: Biomarkers, requirements, candidates, and validation. Frontier in Pharmacology 10: 1482.

Qin, J.D., Cao, Z.H., Li, X.F., Kang, X.L., Xue, Y., Li, Y.L., Zhang, D., Liu, X.Y. & Xue, Y.Z. 2014. Effect of ammonium pyrrolidine dithhiocarbamate (PDTC) on NF-kB activation and CYP2E1 content of rats with immunological liver injury. Pharmaceutical Biology 52(11): 1460-1466.

Qin, L., Kang, X., Li, X., Wang, T., Liu, F., Jia, J., Jin, Z. & Xue, Y. 2019. NF-kB-mediated regulation of rat CYP2E1 by two independent signaling pathways. PLoS ONE 14(12): e0225531.

Sangsuriyawong, A., Limpawattana, M., Siriwan, D. & Klaypradit, W. 2019. Properties and bioavailability assessment of shrimp astaxanthin loaded liposomes. Food Science and Biotechnology 28(2): 529-537.

Sukketsiri, W., Chonpathompikunlert, P., Tanasawet, S., Choosri, N. & Wongtawatchai, T. 2016. Effects of Apium graveolens extract on the oxidative stress in the liver of adjuvant-induced arthritic rats. Preventive Nutrition and Food Science 21(2): 79-84.

Sun, T., Kang, Y., Liu, J., Zhang, Y., Ou, L., Liu, X., Lai, R. & Shao, L. 2021. Nanomaterials and hepatic diseases: Toxicokinetics, disease types, intrinsic mechanisms, liver susceptibility, and influencing factors. Journal of Nanobiotechnology 19(1): 108.

Takasima, T., Chonpathompikunlert, P., Sroyraya, M., Hutamekalin, P., Limpawattana, M. & Klaypradit, W. 2019. Effects of astaxanthin from shrimp sell on oxidative stress and behavior in animal model of Alzheimer’s disease. Marine Drugs 17(11): 628.

Takasima, T., Limpawattana, M. & Klaypradit, W. 2015. Astaxanthin encapsulated in beads using ultrasonic atomizer and application in yogurt as evaluated by consumer sensory profile. LWT-Food Science and Technology 62: 431-437.

Tanasawet, S., Sukketsiri, W., Chonpathompikunlert, P., Klaypradit, W., Sroyraya, M. & Hutamekalin, P. 2020. Apoptotic effect of astaxanthin from white shrimp shells on lung cancer A549 cells. Tropical Journal of Pharmaceutical Research 19(9): 1835-1842.

Xiong, F. & Chang, M.X. 2020. Astaxanthin and its effects in inflammatory responses and inflammation-associated diseases: Recent advances and future directions. Molecules 25(22): 5342.

Xu, L., Yu, Y., Sang, R., Li, J., Ge, B. & Zhang, X. 2018. Protective effects of taraxasterol against ethanol-induced liver injury by regulating CYP2E1.Nrf2/HO-1 and NF-kB signaling pathways in mice. Oxidative Medicine and Cellular Longevity 2018: 8284107.

Yao, Y., Zang, Y., Qu, J., Tang, M. & Zhang, T. 2019. The toxicity of metallic nanoparticles on liver: The subcellular damages, mechanisms, and outcomes. International Journal of Nanomedicine 14: 8787-8804.

*Pengarang untuk surat-menyurat; email: supita.t@psu.ac.th