Antioxidant activities of plant extracts and essential oil-cyclodextrin complexes and their effect on lipid accumulation in porcine adipocytes in vitro https://doi.org/10.12982/VIS.2022.017

Main Article Content

Rakkiat Norkeaw
Chaiwat Arjin
Apinya Sartsook
Niraporn Chaiwang
Supamit Mekchay
Sarana Rose Sommano
Warintorn Ruksiriwanich
Korawan Sringarm

Abstract

Fat deposition is important for pig production because excessive fat decreases the economic value of meat production. Plant extracts have been used as feed additive in pig diets to improve oxidative stability of meat. However, only a few studies had investigated the effect of plant extracts on lipid accumulation of porcine adipocytes. Therefore, this study examined antioxidative potential of plant extracts and essential oil-cyclodextrin complexes and their effect on lipid accumulation in porcine adipocytes. Porcine preadipocytes were isolated from dorsal subcutaneous adipose tissue of a 5-month-old female pig. Preadipocytes were differentiated in the presence of extracts, then lipid accumulation was determined using oil red O staining. Results showed that green tea and grape seed extracts had the highest total phenolic and total flavonoid contents and also possessed the highest antioxidant activities. Among essential oil-cyclodextrin complexes, thyme oil had the highest antioxidant activities by all assays. With a regard to the lipid accumulation, all of plant extracts and essential oil-cyclodextrin complexes decreased lipid accumulation in adipocytes from 32.61 to 91.71% compared with the control. Green tea extract, thyme and galangal oil products decreased lipid accumulation about 60% lower than that of the control. In conclusion, green tea and grape seed extracts, and thyme oil powder illustrated high antioxidant potentials, while lipid accumulation in porcine adipocytes was greatly reduced by green tea extract, thyme and galangal oil products. The research finding is beneficial in the development of natural feed additives to improve oxidative stability and reduce excessive subcutaneous fat
in pig production.

Article Details

How to Cite
Norkeaw, R. ., Arjin, C. ., Sartsook, A. ., Chaiwang, N. ., Mekchay, S. ., Rose Sommano, S. ., Ruksiriwanich, W. ., & Sringarm, K. . (2022). Antioxidant activities of plant extracts and essential oil-cyclodextrin complexes and their effect on lipid accumulation in porcine adipocytes in vitro: https://doi.org/10.12982/VIS.2022.017. Veterinary Integrative Sciences, 20(1), 209–229. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/255943
Section
Research Articles

References

Aeschbach, R., Löliger, J., Scott, B.C., Murcia, A., Butler, J., Halliwell, B., Aruoma, O.I. 1994.Antioxidant actions of thymol, carvacrol, 6-gingerol, zingerone and hydroxytyrosol.Food Chem. Toxicol. 32, 31–36.

Al-Dalain, S.Y.A. 2020. Antioxidant properties flavonoids and phenolic content of grape seed extracts in Jordan. EurAsian J. Biosci. 14, 4571–4574.

Arjin, C., Hongsibsong, S., Pringproa, K., Seel-Audom, M., Ruksiriwanich, W., Sutan, K.,Sommano, S.R., Sringarm, K. 2021. Effect of ethanolic caesalpinia sappan fraction on in vitro antiviral activity against porcine reproductive and respiratory syndrome virus. Vet. Sci. 8, 1–14.

Arjin, C., Pringproa, K., Hongsibsong, S., Ruksiriwanich, W., Seel-Audom, M., Mekchay, S.,Sringarm, K. 2020. In vitro screening antiviral activity of Thai medicinal plants against porcine reproductive and respiratory syndrome virus. BMC Vet. Res. 16, 1–9.

Asbahani, A. El, Miladi, K., Badri, W., Sala, M., Addi, E.H.A., Casabianca, H., Mousadik, A.El, Hartmann, D., Jilale, A., Renaud, F.N.R., Elaissari, A. 2015. Essential oils: From extraction to encapsulation. Int. J. Pharm. 483, 220–243.

Bakkalbasi, E., Yemi, O., Aslanova, D., Art, N. 2005. Major flavan-3-ol composition and antioxidant activity of seeds from different grape cultivars grown in Turkey. Eur.Food Res. Technol. 221, 792–797.

Bandara, K.R.V., Padumadasa, C., Peiris, D.C. 2018. Potent antibacterial, antioxidant and toxic activities of extracts from Passiflora suberosa L. leaves. PeerJ 6, 1–16.

Barizão, É.O., Visentainer, J.V., de Cinque Almeida, V., Ribeiro, D., Chisté, R.C., Fernandes,E. 2016. Citharexylum solanaceum fruit extracts: Profiles of phenolic compounds and carotenoids and their relation with ROS and RNS scavenging capacities. Food Res. Int. 86, 24–33.

Bilenler, T., Gokbulut, I., Sislioglu, K., Karabulut, I. 2015. Antioxidant and antimicrobial properties of thyme essential oil encapsulated in zein particles. Flavour Fragr. J. 30,392–398.

Binsan, W., Benjakul, S., Visessanguan, W., Roytrakul, S., Tanaka, M., Kishimura, H. 2008.Antioxidative activity of Mungoong, an extract paste, from the cephalothorax of white shrimp (Litopenaeus vannamei). Food Chem. 106, 185–193.

Bootyothee, K., Aunpromma, S., Artchayasawat, A., Pitaksakulrat, O., Boonjaraspinyo, S.,Boonmars, T., 2022. Screening of natural product extracts for fly repellent and larvicide. Vet. Integr. Sci. 20, 25–40.

Catillo, G., Zappaterra, M., Lo Fiego, D. Pietro, Steri, R., Davoli, R. 2021. Relationships between EUROP carcass grading and backfat fatty acid composition in Italian Large White heavy pigs. Meat Sci. 171, 108291.

Cheng, C., Liu, Z., Zhou, Y., Wei, H., Zhang, X., Xia, M., Deng, Z., Zou, Y., Jiang, S., Peng, J.2017. Effect of oregano essential oil supplementation to a reduced-protein, amino acid-supplemented diet on meat quality, fatty acid composition, and oxidative stability of Longissimus thoracis muscle in growing-finishing pigs. Meat Sci. 133, 103–109.

Choi, J.W., Lee, C.W., Lee, J., Choi, D.J., Sohng, J.K., Park, Y. Il 2016. 7,8-Dihydroxyflavone inhibits adipocyte differentiation via antioxidant activity and induces apoptosis in 3T3-L1 preadipocyte cells. Life Sci. 144, 103–112.

Choi, Y.-S., Choi, K.-D., Kim, S.-D., Phillip, O., Chung, C.-S. 2010. Extracts of Korean medicinal plant extracts alter lipogenesis of pig adipose tissue and differentiation of pig preadipocytes in vitro. J. Anim. Sci. Technol. 52, 383–388.

De Macêdo, D.G., Souza, M.M.A., Morais-Braga, M.F.B., Coutinho, H.D.M., Dos Santos, A.T.L., Da Cruz, R.P., Da Costa, J.G.M., Rodrigues, F.F.G., Quintans-Junior, L.J., Da Silva Almeida, J.R.G., De Menezes, I.R.A. 2018. Effect of seasonality on chemical profile and antifungal activity of essential oil isolated from leaves Psidium salutare (Kunth) O. Berg. PeerJ 6, 1–19.

Dunshea, F.R., Ostrowska, E., Luxford, B., Smits, R.J., Campbell, R.G., D’Souza, D.N.,Mullan, B.P. 2002. Dietary conjugated linoleic acid can decrease backfat in pigs housed under commercial conditions. Asian-Australasian J. Anim. Sci. 15, 1011–1017.

Efenberger-Szmechtyk, M., Nowak, A., Czyzowska, A. 2021. Plant extracts rich in polyphenols: antibacterial agents and natural preservatives for meat and meat products. Crit. Rev. Food Sci. Nutr. 61, 149–178.

Farooq, S., Sehgal, A. 2019. Synergistic antioxidant interactions between green tea and Ocimum gratissimum. Asian Pac. J. Trop. Biomed. 9, 333–338.

Ghasemzadeh, A., Jaafar, H.Z.E., Rahmat, A. 2015. Phytochemical constituents and biological activities of different extracts of Strobilanthes crispus (L.) Bremek leaves grown in different locations of Malaysia. BMC Complement. Altern. Med. 15, 1–10.

Hill, L.E., Gomes, C., Taylor, T.M. 2013. Characterization of beta-cyclodextrin inclusion complexes containing essential oils (trans-cinnamaldehyde, eugenol, cinnamon bark, and clove bud extracts) for antimicrobial delivery applications. LWT - Food Sci. Technol. 51, 86–93.

Ivanović, M., Makoter, K., Razboršek, M.I. 2021. Comparative study of chemical composition and antioxidant activity of essential oils and crude extracts of four characteristic zingiberaceae herbs. Plants 10, 1–20.

Jiang, J., Tang, X., Xue, Y., Lin, G., Xiong, Y.L. 2017. Dietary linseed oil supplemented with organic selenium improved the fatty acid nutritional profile, muscular selenium deposition, water retention, and tenderness of fresh pork. Meat Sci. 131, 99–106.

Jung, C.H., Jang, S.J., Ahn, J., Gwon, S.Y., Jeon, T. Il, Kim, T.W., Ha, T.Y. 2012. Alpinia officinarum inhibits adipocyte differentiation and high-fat diet-induced obesity in mice through regulation of adipogenesis and lipogenesis. J. Med. Food 15, 959–967.

Kfoury, M., Auezova, L., Greige-Gerges, H., Fourmentin, S. 2019. Encapsulation in cyclodextrins to widen the applications of essential oils. Environ. Chem. Lett. 17, 129–143.

Khan, A.A., Amjad, M.S., Saboon, 2019. GC-MS analysis and biological activities of Thymus vulgaris and Mentha arvensis essential oil. Turkish J. Biochem. 44, 388–396.

Kim, G.C., Kim, J.S., Kim, G.M., Choi, S.Y. 2017. Anti-adipogenic effects of Tropaeolum majus (nasturtium) ethanol extract on 3T3-L1 cells. Food Nutr. Res. 61, 1–8.

Knecht, D., Duziński, K. 2016. The effect of sex, carcass mass, back fat thickness and lean meat conent on pork ham and loin characteristics. Arch. Anim. Breed. 59, 51–57.

Kulisic, T., Radonic, A., Katalinic, V., Milos, M. 2004. Use of different methods for testing antioxidative activity of oregano essential oil. Food Chem. 85, 633–640.

Lao, W., Tan, Y., Jin, X., Xiao, L., Kim, J.J.Y., Qu, X. 2015. Comparison of cytotoxicity and the anti-adipogenic effect of green tea polyphenols with epigallocatechin-3-gallate in 3T3-L1 preadipocytes. Am. J. Chin. Med. 43, 1177–1190.

Lee, H., Lee, Y.J., Choi, H., Ko, E.H., Kim, J.W. 2009. Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. J. Biol. Chem. 284, 10601–10609.

Lee, J., Kim, A.R., Lee, J.J. 2016. Ramie leaf extracts suppresses adipogenic differentiation in 3T3-L1 cells and pig preadipocytes. Asian-Australasian J. Anim. Sci. 29, 1338–1344.

Lee, L.S., Kim, S.H., Kim, Y.B., Kim, Y.C. 2014. Quantitative analysis of major constituents in green tea with different plucking periods and their antioxidant activity. Molecules. 19,9173–9186.

Lee, Y.J., Kim, D.B., Lee, J.S., Cho, J.H., Kim, B.K., Choi, H.S., Lee, B.Y., Lee, O.H. 2013. Antioxidant activity and anti-adipogenic effects of wild herbs mainly cultivated in Korea. Molecules. 18, 12937–12950.

Li, S.Y., Ru, Y.J., Liu, M., Xu, B., Péron, A., Shi, X.G. 2012. The effect of essential oils on performance, immunity and gut microbial population in weaner pigs. Livest. Sci. 145, 119–123.

Liang, C.-H., Lin, Y.-S., Chiang, S.-S. 2018. Regulation of adipogenesis and lipolysis by the rhizomes of Alpinia galanga in 3T3-L1 preadipocytes and high fat diet-induced obese BALB/c mice. Taiwan. J. Agric. Chem. & Food Sci. 56, 9–24.

Liu, Y., Che, T.M., Song, M., Lee, J.J., Almeida, J.A.S., Bravo, D., Van Alstine, W.G.,Pettigrew, J.E. 2013. Dietary plant extracts improve immune responses and growth efficiency of pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J. Anim. Sci. 91, 5668–5679.

Lucas, D., Brun, A., Gispert, M., Carabús, A., Soler, J., Tibau, J., Font-i-Furnols, M. 2017. Relationship between pig carcass characteristics measured in live pigs or carcasses with Piglog, Fat-o-Meat’er and computed tomography. Livest. Sci. 197, 88–95.

Mallavarapu, G.R., Rao, L., Ramesh, S., Dimri, B., Rajeswara Rao, B., Kaul, P.N.,Bhattacharya, A.K. 2002. Composition of the volatile oils of Alpinia galanga rhizomes and leaves from India. J. Essent. Oil Res. 14, 397–399.

Malsawmtluangi, L., Nautiyal, B.P., Hazarika, T., Chauhan, R.S., Tava, A. 2016. Essential oil composition of bark and leaves of Cinammoum verum Bertch. & Presl from Mizoram, North East India. J. Essent. Oil Res. 28, 551–556.

Mandic, A.I., Dilas, S.M., Ćetković, G.S., Čanadanović-Brunet, J.M., Tumbas, V.T. 2008.Polyphenolic composition and antioxidant activities of grape seed extract. Int. J. Food Prop. 11, 713–726.

Mighri, H., Akrout, A., Bennour, N., Eljeni, H., Zammouri, T., Neffati, M. 2019. LC/MS method development for the determination of the phenolic compounds of Tunisian Ephedra alata hydro-methanolic extract and its fractions and evaluation of their antioxidant activities. South African J. Bot. 124, 102–110.

Nantitanon, W., Yotsawimonwat, S., Okonogi, S. 2010. Factors in fluencing antioxidant activities and total phenolic content of guava leaf extract. LWT - Food Sci. Technol.43, 1095–1103.

Ogawa, T., Tabata, H., Katsube, T., Ohta, Y., Yamasaki, Y., Yamasaki, M., Shiwaku, K. 2010. Suppressive effect of hot water extract of wasabi (Wasabia japonica Matsum.) leaves on the differentiation of 3T3-L1 preadipocytes. Food Chem. 118, 239–244.

Omonijo, F.A., Ni, L., Gong, J., Wang, Q., Lahaye, L., Yang, C. 2018. Essential oils as alternatives to antibiotics in swine production. Anim. Nutr. 4, 126–136.

Ozkan, G., Baydar, H., Erbas, S. 2010. The influence of harvest time on essential oil composition, phenolic constituents and antioxidant properties of Turkish oregano (Origanum onites L.). J. Sci. Food Agric. 90, 205–209.

Popovich, D.G., Li, L., Zhang, W. 2010. Bitter melon (Momordica charantia) triterpenoid extract reduces preadipocyte viability, lipid accumulation and adiponectin expression in 3T3-L1 cells. Food Chem. Toxicol. 48, 1619–1626.

Rababah, T.M., Hettiarachchy, N.S., Horax, R. 2004. Total phenolics and antioxidant activities of fenugreek, green tea, black tea, grape seed, ginger, rosemary, gotu kola, and ginkgo extracts, vitamin E, and tert-butylhydroquinone. J. Agric. Food Chem. 52, 5183–5186.

Ravi Kiran, C., Chakka, A.K., Padmakumari Amma, K.P., Nirmala Menon, A., Sree Kumar,M.M., Venugopalan, V.V. 2013. Essential oil composition of fresh ginger cultivars from North-East India. J. Essent. Oil Res. 25, 380–387.

Rossi, R., Pastorelli, G., Cannata, S., Tavaniello, S., Maiorano, G., Corino, C. 2013. Effect of long term dietary supplementation with plant extract on carcass characteristics meat quality and oxidative stability in pork. Meat Sci. 95, 542–548.

Ruamrungsri, N., Siengdee, P., Sringarm, K., Chomdej, S., Ongchai, S., Nganvongpanit, K.2016. In vitro cytotoxic screening of 31 crude extracts of Thai herbs on a chondrosarcoma cell line and primary chondrocytes and apoptotic effects of selected extracts. In vitro Cell. Dev. Biol. - Anim. 52, 434–444.

Ruberto, G., Baratta, M.T. 2000. Antioxidant activity of selected essential oil components in two lipid model systems. Food Chem. 69, 167–174.

Sampath, V., Shangmugam, S., Park, J.H., Kim, I.H. 2020. The effect of black pepper (Piperine) extract supplementation on growth performance, nutrient digestibility, fecal microbial, fecal gas mission and meat quality of finishing pigs. Animals. 10, 1–11.

Saravanan, S., Pari, L. 2016. Protective effect of thymol on high fat diet induced diabetic nephropathy in C57BL/6J mice. Chem. Biol. Interact. 245, 1–11.

Shah, M.A., Bosco, S.J.D., Mir, S.A. 2014. Plant extracts as natural antioxidants in meat and meat products. Meat Sci. 98, 21–33.

Sittisart, P., Chitsomboon, B. 2014. Intracellular ROS scavenging activity and downregulation of inflammatory mediators in RAW264.7 macrophage by fresh leaf extracts of pseuderanthemum palatiferum. Evidence-based Complement. Altern. Med. 2014,1–11.

Sobeh, M., Mahmoud, M.F., Hasan, R.A., Abdelfattah, M.A.O., Osman, S., Rashid, H.O.,El-Shazly, A.M., Wink, M. 2019. Chemical composition, antioxidant and hepatoprotective activities of methanol extracts from leaves of Terminalia bellirica and Terminalia sericea (Combretaceae). PeerJ 7, 1–22.

Sunanta, P., Chung, H.H., Kunasakdakul, K., Ruksiriwanich, W., Jantrawut, P., Hongsibsong,S., Sommano, S.R. 2020. Genomic relationship and physiochemical properties among raw materials used for Thai black garlic processing. Food Sci. Nutr. 8, 4534–4545.

Suzuki, S., Suzuki, M., Sembon, S., Fuchimoto, D., Onishi, A. 2013. Characterization of actions of octanoate on porcine preadipocytes and adipocytes differentiated in vitro.Biochem. Biophys. Res. Commun. 432, 92–98.

Tepe, B., Sokmen, M., Akpulat, H.A., Daferera, D., Polissiou, M., Sokmen, A. 2005.Antioxidative activity of the essential oils of Thymus sipyleus subsp. sipyleus var.sipyleus and Thymus sipyleus subsp. sipyleus var. rosulans. J. Food Eng. 66, 447–454.

Wadhwa, G., Kumar, S., Chhabra, L., Mahant, S., Rao, R. 2017. Essential oil–cyclodextrin complexes: an updated review. J. Incl. Phenom. Macrocycl. Chem. 89, 39–58.

Weerawatanakorn, M., Rojsuntornkitti, K., Pan, M.-H., Wongwaiwech, D. 2018. Some Phytochemicals and Anti-inflammation Effect of Juice from Tiliacora triandra Leaves.J. Food Nutr. Res. 6, 32–38.

Wiegand, B.R., Parrishx, F.C., Swan, J.E., Larsen, S.T., Baas, T.J. 2001. Conjugated linoleic acid improves feed efficiency, decreases subcutaneous fat, and improves certain aspects of meat quality in Stress-Genotype pigs. J. Anim. Sci. 79, 2187–2195.

Wood, J.D., Enser, M., Fisher, A. V., Nute, G.R., Sheard, P.R., Richardson, R.I., Hughes, S.I.,Whittington, F.M. 2008. Fat deposition, fatty acid composition and meat quality: A review. Meat Sci. 78, 343–358.

Yahyaoui, A., Arfaoui, M.O., Rigane, G., Hkir, A., Amari, K., Ben Salem, R., Ammari, Y. 2019.Investigation on the chemical composition and antioxidant capacity of extracts from Crataegus azarolus L.: Effect of growing location of an important tunisian medicinal plant. Chem. Africa 2, 361–365.

Yan, L., Wang, J.P., Kim, H.J., Meng, Q.W., Ao, X., Hong, S.M., Kim, I.H. 2010. Influence of essential oil supplementation and diets with different nutrient densities on growth performance, nutrient digestibility, blood characteristics, meat quality and fecal noxious gas content in grower-finisher pigs. Livest. Sci. 128, 115–122.

Youdim, K.A., Deans, S.G., Finlayson, H.J. 2002. The antioxidant properties of thyme (Thymus zygis L.) essential oil: An inhibitor of lipid peroxidation and a free radical scavenger. J. Essent. Oil Res. 14, 210–215.

Zengin, G., Llorent-Martínez, E.J., Córdova, M.L.F. de, Bahadori, M.B., Mocan, A., Locatelli, M., Aktumsek, A. 2018. Chemical composition and biological activities of extracts from three Salvia species: S. blepharochlaena, S. euphratica var. leiocalycina, and S.verticillata subsp. amasiaca. Ind. Crops Prod. 111, 11–21.

Zhou, M., Lin, Y., Fang, S., Liu, Y., Shang, X. 2019. Phytochemical content and antioxidant activity in aqueous extracts of Cyclocarya paliurus leaves collected from different populations. PeerJ 7, 1–18.