Regulation of growth performance and lipid metabolism in juvenile grass carp (Ctenopharyngodon idella) with honeysuckle (Lonicera japonica) extract

  • Xiao-Lin Meng
  • Zhen-Xiang Zhu
  • Rong-Hua Lu
  • Shuai Li
  • Wen-Pan Hu
  • Chao-Bin Qin
  • Xiao Yan
  • Guo-kun Yang
  • Guo-Xing NieEmail author


This study investigated the effects of honeysuckle extract (Lonicera japonica, HE) on the growth performance and lipid metabolism of juvenile grass carp (Ctenopharyngodon idella). HE at doses of 10 g kg−1 (LHE), 20 g kg−1 (MHE), and 40 g kg−1 (HHE) were individually mixed with the basal diet and fed to grass carp for 10 weeks, and ginseng extract (20 g kg−1, GSE) was used as a positive control. The results showed that HE administration exerted no effect on growth performance, but the hepatosomatic index (HSI) and muscle and liver lipid contents were significantly decreased in the LHE and MHE groups. The serum levels of LDL-c, total triglyceride (TG) and total cholesterol (TC) also declined in the HE-treated groups. Moreover, the disordered vacuolization and nucleus migration in the liver were alleviated in the MHE and HHE groups, and mRNA expressions of lipogenesis-related genes, such as acc1, fas, srebp1, and pparγ decreased. Similarly, the expression of genes related to lipolysis, such as cpt1, atgl, lpl, and pparα, was found to be significantly increased in the MHE and HHE groups compared with the control. Taken together, HE can effectively improve the lipid metabolism and ameliorate the lipid deposition of grass carp and thus may be a promising feed additive in aquaculture.


Lonicera japonica Ctenopharyngodon idella Growth performance Lipid metabolism 


Funding information

This work was financially supported by the Key Scientific and Technological Project of Henan Province (182102110007), Foundation for University Key Teachers from Henan Province (2018GGJS036), the Innovation Scientists and Technicians Troop Construction Projects of Henan Province (CXTD2016043) and the National Nature Science Foundation of China (31672671 and 31402311).

Supplementary material

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  1. Abdel-Tawwab M (2015) The use of American ginseng (Panax quinquefolium) in practical diets for Nile tilapia (Oreochromis niloticus): resistance to waterborne copper toxicity. Aquac Res 46:1001–1006CrossRefGoogle Scholar
  2. Bilen S, Unal S, Guvensoy H (2016) Effects of oyster mushroom (Pleurotus ostreatus) and nettle (Urtica dioica) methanolic extracts on immune responses and resistance to Aeromonas hydrophila in rainbow trout (Oncorhynchus mykiss). Aquaculture 454:90–94CrossRefGoogle Scholar
  3. Bonarska-Kujawa D, Pruchnik H, Cyboran S, Zylka R, Oszmianski J, Kleszczynska H (2014) Biophysical mechanism of the protective effect of blue honeysuckle (Lonicera caerulea L. var. kamtschatica Sevast.) polyphenols extracts against lipid peroxidation of erythrocyte and lipid membranes. J Membr Biol 247:611–625CrossRefGoogle Scholar
  4. Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70CrossRefGoogle Scholar
  5. Cho AS, Jeon SM, Kim MJ, Yeo J, Seo KI, Choi MS, Lee MK (2010) Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food Chem Toxicol 48:937–943CrossRefGoogle Scholar
  6. Dong H, Lu FE, Zhao L (2012) Chinese herbal medicine in the treatment of nonalcoholic fatty liver disease. Chin J Integr Med 18:152–160CrossRefGoogle Scholar
  7. Dong GF, Yang YO, Yao F, Wan Q, Yu L, Zhou JC, Li Y (2013) Responses of yellow catfish (Pelteobagrus fulvidraco Richardson) to low-protein diets and subsequent recovery. Aquac Nutr 19:430–439CrossRefGoogle Scholar
  8. Dong GF, Zou Q, Wang H, Huang F, Liu XC, Chen L, Yang CY, Yang YO (2014) Conjugated linoleic acid differentially modulates growth, tissue lipid deposition, and gene expression involved in the lipid metabolism of grass carp. Aquaculture 432:181–191CrossRefGoogle Scholar
  9. Du ZY, Liu YJ, Tian LX, Wang JT, Wang Y, Liang GY (2005) Effect of dietary lipid level on growth, feed utilization and body composition by juvenile grass carp (Ctenopharyngodon idella). Aquac Nutr 11:139–146CrossRefGoogle Scholar
  10. Du ZY, Clouet P, Zheng WH, Degrace P, Tian LX, Liu YJ (2006) Biochemical hepatic alterations and body lipid composition in the herbivorous grass carp (Ctenopharyngodon idella) fed high-fat diets. Br J Nutr 95:905–915CrossRefGoogle Scholar
  11. Fielding BA, Frayn KN (1998) Lipoprotein lipase and the disposition of dietary fatty acids. Br J Nutr 80:495–502CrossRefGoogle Scholar
  12. Gabriel NN, Qiang J, Ma XY, He J, Xu P, Liu K (2015) Dietary Aloe vera improves plasma lipid profile, antioxidant, and hepatoprotective enzyme activities in GIFT-tilapia (Oreochromis niloticus) after Streptococcus iniae challenge. Fish Physiol Biochem 41:1321–1332CrossRefGoogle Scholar
  13. Gao W, Liu YJ, Tian LX, Mai KS, Liang GY, Yang HJ, Huai MY, Luo WJ (2011) Protein-sparing capability of dietary lipid in herbivorous and omnivorous freshwater finfish: a comparative case study on grass carp (Ctenopharyngodon idella) and tilapia (Oreochromis niloticus× O. aureus). Aquac Nutr 17:2–12CrossRefGoogle Scholar
  14. Goto T, Hirazawa N, Takaishi Y, Kashiwada Y (2015) Antiparasitic effects of Sophora flavescens root extracts on the ciliate, Cryptocaryon irritans. Aquaculture 435:173–177CrossRefGoogle Scholar
  15. Hirata T, Kobayashi T, Wada A, Ueda T, Fujikawa T, Miyashita H, Ikeda T, Tsukamoto S, Nohara T (2011) Anti-obesity compounds in green leaves of Eucommia ulmoides. Bioorg Med Chem Lett 21:1786–1791CrossRefGoogle Scholar
  16. Hoseinifar SH, Zou HK, Van Doan H, Miandare HK, Hoseini SM (2018) Evaluation of some intestinal cytokines genes expression and serum innate immune parameters in common carp (Cyprinus carpio) fed dietary loquat (Eriobotrya japonica) leaf extract. Aquac Res 49:120–127CrossRefGoogle Scholar
  17. Ji R, Li Y, Li X, Xiang X, Li Y, Zhu S, Yang B, Zhang Y, Mai K, Ai Q (2017) Effects of dietary tea polyphenols on growth, biochemical and antioxidant responses, fatty acid composition and expression of lipid metabolism related genes of large yellow croaker (Larimichthys crocea). Aquac Res 00:1–9Google Scholar
  18. Jin Y, Tian LX, Zeng SL, Xie SW, Yang HJ, Liang GY, Liu YJ (2013) Dietary lipid requirement on non-specific immune responses in juvenile grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 34:1202–1208CrossRefGoogle Scholar
  19. Jin SS, Chang CQ, Zhang LT, Liu Y, Huang XR, Chen ZM (2015) Chlorogenic acid improves late diabetes through adiponectin receptor signaling pathways in db/db mice. PLoS One 10:e0120842. CrossRefGoogle Scholar
  20. Johnsen F, Hillestad M, Austreng E (1993) High energy diets for Atlantic salmon. Effects of pollution. In: Fish nutrition in practice. Proceedings of the international symposium on fish nutrition and feeding. INRA, Paris, pp 391–401 [SJ Kaushik and P Luquet, editors]Google Scholar
  21. Jurgonski A, Juskiewicz J, Zdunczyk Z (2013) An anthocyanin-rich extract from Kamchatka honeysuckle increases enzymatic activity within the gut and ameliorates abnormal lipid and glucose metabolism in rats. Nutrition 29:898–902CrossRefGoogle Scholar
  22. Kim SH, Park KS (2003) Effects of Panax ginseng extract on lipid metabolism in humans. Pharmacol Res 48:511–513CrossRefGoogle Scholar
  23. Leung HWC, Hour MJ, Chang WT, Wu YC, Lai MY, Wang MY, Lee HZ (2008) P38-associated pathway involvement in apoptosis induced by photodynamic therapy with Lonicera japonica in human lung squamous carcinoma CH27 cells. Food Chem Toxicol 46:3389–3400CrossRefGoogle Scholar
  24. Lin D, Mao YQ, Cai FS (1990) Nutritional lipid liver disease of grass carp Ctenopharyngodon idullus (C. et V.). Chin J Oceanol Limnol 8:363–373CrossRefGoogle Scholar
  25. Luo L, Ai LC, Liang XF, Hu HX, Xue M, Wu XF (2017) N-3 long-chain polyunsaturated fatty acids improve the sperm, egg, and offspring quality of Siberian sturgeon (Acipenser baerii). Aquaculture 473:266–271CrossRefGoogle Scholar
  26. Minghetti M, Leaver MJ, Tocher DR (2011) Transcriptional control mechanisms of genes of lipid and fatty acid metabolism in the Atlantic salmon (Salmo salar L.) established cell line, SHK-1. Biochim Biophys Acta 1811:194–202CrossRefGoogle Scholar
  27. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45. CrossRefGoogle Scholar
  28. Sargent JR, Bell JG, McEvoy L, Tocher DR, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199CrossRefGoogle Scholar
  29. Sheikhlar A, Goh YM, Alimon R, Ebrahimi M (2017) Antioxidative effects of mulberry foliage extract in African catfish diet. Aquac Res 48:4409–4419CrossRefGoogle Scholar
  30. Smirnova E, Goldberg EB, Makarova KS, Lin L, Brown WJ, Jackson CL (2006) ATGL has a key role in lipid droplet/adiposome degradation in mammalian cells. EMBO Rep 7:106–113CrossRefGoogle Scholar
  31. Sun J, Ji H, Li XX, Shi XC, Du ZY, Chen LQ (2016) Lipolytic enzymes involving lipolysis in teleost: synteny, structure, tissue distribution and expression in grass carp (Ctenopharyngodon idella). Comp Biochem Physiol B: Biochem Mol Biol 198:110–118CrossRefGoogle Scholar
  32. Sun WT, Li XQ, Xu HB, Chen JN, Xu XY, Leng XJ (2017) Effects of dietary chlorogenic acid on growth, flesh quality and serum biochemical indices of grass carp (Ctenopharyngodon idella). Aquac Nutr 23:1254–1263CrossRefGoogle Scholar
  33. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  34. Wang Y, Li Z, Li J, Duan YF, Niu J, Wang J, Huang Z, Lin HZ (2015a) Effects of dietary chlorogenic acid on growth performance, antioxidant capacity of white shrimp Litopenaeus vannamei under normal condition and combined stress of low-salinity and nitrite. Fish Shellfish Immunol 43:337–345CrossRefGoogle Scholar
  35. Wang JL, Meng XL, Lu RH, Wu C, Luo YT, Yan X, Li XJ, Kong XH, Nie GX (2015b) Effects of Rehmannia glutinosa on growth performance, immunological parameters and disease resistance to Aeromonas hydrophila in common carp (Cyprinus carpio L.). Aquaculture 435:293–300CrossRefGoogle Scholar
  36. Wang Y, Liang JP, Duan YF, Niu J, Wang J, Huang Z, Lin HZ (2017) Effects of dietary Rhodiola rosea on growth, body composition and antioxidant capacity of white shrimp Litopenaeus vannamei under normal conditions and combined stress of low-salinity and nitrite. Aquac Nutr 23:548–559CrossRefGoogle Scholar
  37. Watt MJ, Steinberg GR (2008) Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem J 414:313–325CrossRefGoogle Scholar
  38. Wu T, Yu ZP, Tang Q, Song HZ, Gao ZC, Chen W, Zheng XD (2013) Honeysuckle anthocyanin supplementation prevents diet-induced obesity in C57BL/6 mice. Food Funct 4:1654–1661CrossRefGoogle Scholar
  39. Xiang Z, Ning ZX (2008) Scavenging and antioxidant properties of compound derived from chlorogenic acid in South-China honeysuckle. LWT-Food Sci Technol 41:1189–1203CrossRefGoogle Scholar
  40. Yan L, Meng Q, Kim I (2012) Effect of an herb extract mixture on growth performance, nutrient digestibility, blood characteristics, and fecal microbial shedding in weanling pigs. Livest Sci 145:189–195CrossRefGoogle Scholar
  41. Yessoufou A, Attakpa E, Ategbo JM, Moutairou K, Simonin AM, Dramane K, Hichami A, Khan NA (2009) Peroxisome proliferator-activated receptor-alpha modulates insulin gene transcription factors and inflammation in adipose tissues in mice. Mol Cell Biochem 323:101–111CrossRefGoogle Scholar
  42. Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C, Li M, Zhang C, Zhang Z, Zhang Y (2012) Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One 7:e42529CrossRefGoogle Scholar
  43. Zhou JS, Lin YQ, Ji H, Yu HB (2016) The effect of green tea waste on growth and health of grass carp (Ctenopharyngodon idellus). Turk J Fish Aquat Sci 16:679–689CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of FisheriesHenan Normal UniversityXinxiangPeople’s Republic of China
  2. 2.Engineering Technology Research Center of Henan Province for Aquatic Animal CultivationHenan Normal UniversityXinxiangPeople’s Republic of China

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