Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Dietary supplementation of piperine improves innate immunity, growth performance, feed utilization and intestinal morphology of red seabream (Pagrus major)

  • Mirasha Hasanthi (Department of Marine Life Sciences, Jeju National University) ;
  • G.H.T. Malintha (Department of Marine Life Sciences, Jeju National University) ;
  • Kwan-Sik Yun (Synergen Inc.) ;
  • Kyeong-Jun Lee (Department of Marine Life Sciences, Jeju National University)
  • Received : 2023.04.21
  • Accepted : 2023.09.22
  • Published : 2023.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Piperine, the main bioactive component of black pepper (Piper nigrum Linn.), has anti-inflammatory, antifungal, and antibacterial properties. This study evaluated the supplemental effects of piperine or black pepper on innate immunity, growth, feed utilization efficiency, and intestinal morphology in red seabream (Pagrus major). Six experimental diets were formulated, supplementing piperine at 0.0, 0.25, 0.5, 1.0, and 2.0 g/kg levels (Con, P25, P50, P100, and P200) or 1.0 g/kg black pepper (BP100). Juvenile fish (7.6 ± 0.1 g) were randomly stocked into 18 circular tanks (220 L), including 30 fish per tank. Each diet was randomly assigned to triplicate groups, and the feeding trial was conducted for 8 weeks. The results showed that final body weight, specific growth rate, weight gain, and feed utilization efficiency were significantly improved (p < 0.05) when piperine was supplemented into diets at 0.25-2.0 g/kg levels compared to the Con group. Compared to the Con diet, condition factor was significantly increased (p < 0.05) in fish fed with dietary piperine at 0.25-2.0 g/kg or BP100 diet. Serum myeloperoxidase activity was increased (p < 0.05) in P25 and P100 groups and antiprotease activity was increased (p < 0.05) in P100 group compared to the Con group. Significantly higher (p < 0.05) lysozyme activity was observed in P50, P100, P200 and BP100 groups, while total immunoglobulin level was increased in P50, P100 and BP100 groups than Con group. Superoxide dismutase activity was increased (p < 0.05) by dietary piperine at 0.25-2.0 g/kg levels and BP100 diet compared to Con diet. Plasma cholesterol was significantly lower (p < 0.05) in fish fed with piperine (0.5-2.0 g/kg) or BP100 compared to the Con diet. Compared to the Con diet significantly longer (p < 0.05) intestinal villi were observed in fish fed with piperine at 0.25-1.0 g/kg levels, and higher goblet cell count was observed in P25 and BP100 groups. Dietary inclusion of piperine would be a potent immunostimulant in fish diet and the optimum supplementation level would be 0.25-1.0 g/kg.

Keywords

Acknowledgement

This study was supported by Synergen Inc., and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A03033553).

References

  1. Abd-Elaziz RA, Shukry M, Abdel-Latif HMR, Saleh RM. Growth-promoting and immunostimulatory effects of phytobiotics as dietary supplements for Pangasianodon hypophthalmus fingerlings. Fish Shellfish Immunol. 2023;133:108531.
  2. Abdel-Latif HMR, Yilmaz S, Kucharczyk D. Functionality and applications of phytochemicals in aquaculture nutrition. Front Vet Sci. 2023;10:1218542.
  3. Abdul Kari Z, Wee W, Mohamad Sukri SA, Che Harun H, Hanif Reduan MF, Irwan Khoo M, et al. Role of phytobiotics in relieving the impacts of Aeromonas hydrophila infection on aquatic animals: a mini-review. Front Vet Sci. 2022;9:1023784.
  4. Ahmad N, Fazal H, Abbasi BH, Farooq S, Ali M, Khan MA. Biological role of Piper nigrum L. (black pepper): a review. Asian Pac J Trop Biomed. 2012;2:1945-53. https://doi.org/10.1016/S2221-1691(12)60524-3
  5. Anderson DP, Moritomo T, de Grooth R. Neutrophil, glass-adherent, nitroblue tetrazolium assay gives early indication of immunization effectiveness in rainbow trout. Vet Immunol Immunopathol. 1992;30:419-29. https://doi.org/10.1016/0165-2427(92)90110-C
  6. Andrade KS, Ferreira SRS. Antioxidant activity of black pepper (Piper nigrum L.) oil obtained by super critical CO2. III Iberoamerican Conference on Super Critical Fluids; 2013; Cartagena de Indias, Colombia.
  7. AOAC. Official method of analysis of the Association of Official Analytical Chemists. 18th ed. Arlington, VA: Association of Official Analytical Chemists International; 2005.
  8. Bae GS, Kim MS, Jung WS, Seo SW, Yun SW, Kim SG, et al. Inhibition of lipopolysaccharide-induced inflammatory responses by piperine. Eur J Pharmacol. 2010;642:154-62. https://doi.org/10.1016/j.ejphar.2010.05.026
  9. Bajad S, Bedi KL, Singla AK, Johri RK. Piperine inhibits gastric emptying and gastrointestinal transit in rats and mice. Planta Med. 2001;67:176-9. https://doi.org/10.1055/s-2001-11505
  10. Blessy S, Gopinath P, Jayalakshmi. Antibacterial activity of ethanolic extract of black pepper against clinical isolates of Staphylococcus. J Pharm Sci Res. 2015;7:1015-6.
  11. Capasso R, Izzo AA, Borrelli F, Russo A, Sautebin L, Pinto A, et al. Effect of piperine, the active ingredient of black pepper, on intestinal secretion in mice. Life Sci. 2002;71:2311-7. https://doi.org/10.1016/S0024-3205(02)02019-2
  12. Chakraborty SB, Horn P, Hancz C. Application of phytochemicals as growth-promoters and endocrine modulators in fish culture. Rev Aquac. 2014;6:1-19. https://doi.org/10.1111/raq.12021
  13. de Rezende RAE, Soares MP, Sampaio FG, Cardoso IL, Ishikawa MM, Dallago BSL, et al. Phytobiotics blend as a dietary supplement for Nile tilapia health improvement. Fish Shellfish Immunol. 2021;114:293-300.
  14. Derosa G, Maffioli P, Sahebkar A. Piperine and its role in chronic diseases. In: Gupta SC, Prasad S, Aggarwal BB, editors. Anti-inflammatory nutraceuticals and chronic diseases. Cham: Springer International; 2016. p. 173-84.
  15. Dogra RKS, Khanna S, Shanker R. Immunotoxicological effects of piperine in mice. Toxicology. 2004;196:229-36. https://doi.org/10.1016/j.tox.2003.10.006
  16. Ellis AE. Serum antiproteases in fish. In Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB, editors. Techniques in fish immunology. Fair Haven, NJ: SOS Publications; 1990. p. 95-9.
  17. Ferraboschi P, Ciceri S, Grisenti P. Applications of lysozyme, an innate immune defense factor, as an alternative antibiotic. Antibiotics. 2021;10:1534.
  18. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
  19. Frangie C, Daher J. Role of myeloperoxidase in inflammation and atherosclerosis. Biomed Rep. 2022;16:1-11. https://doi.org/10.3892/br.2022.1536
  20. Ghosh R, Darin K, Nath P, Deb P. An overview of various Piper species for their biological activities. Int J Pharma Res Rev. 2014;3:67-75.
  21. Gorgani L, Mohammadi M, Najafpour GD, Nikzad M. Piperine-the bioactive compound of black pepper: from isolation to medicinal formulations. Compr Rev Food Sci Food Saf. 2017;16:124-40. https://doi.org/10.1111/1541-4337.12246
  22. Gupta A, Gupta M, Gupta S. Isolation of piperine and few sesquiterpenes from the cold petroleum ether extract of Piper nigrum (black pepper) and its antibacterial activity. Int J Pharmacogn Phytochem Res. 2013;5:101-5.
  23. Hasanthi M, Kim MG, Lim H, Lim J, Hur S, Lee S, et al. The dietary requirement for threonine in juvenile olive flounder (Paralichthys olivaceus). Fish Aquat Sci. 2023;26:58-68. https://doi.org/10.47853/FAS.2023.e5
  24. Hasanthi M, Lee KJ. Dietary niacin requirement of Pacific white shrimp (Litopenaeus vannamei). Aquaculture. 2023;566:739169.
  25. Hassan S, Hassan M, Soliman F, Safwat A. Influence of hot red pepper oil in broiler diets on blood, antioxidant, immunological parameters and intestinal bacteria counts. Anim Biotechnol. 2023;1295-304.
  26. Hu X, Wu D, Tang L, Zhang J, Zeng Z, Geng F, et al. Binding mechanism and antioxidant activity of piperine to hemoglobin. Food Chem. 2022;394:133558.
  27. Jana P, Karmakar S, Roy U, Paul M, Singh AK, Bera KK. Phytobiotics in aquaculture health management: a review. J Entomol Zool Stud. 2018;6:1422-9.
  28. Karsha PV, Lakshmi OB. Antibacterial activity of black pepper (Piper nigrum Linn.) with special reference to its mode of action on bacteria. Indian J Nat Prod Resour. 2010;1:213-5.
  29. Khajuria A, Johri RK, Zutshi U. Piperine mediated alterations in lipid peroxidation and cellular thiol status of rat intestinal mucosa and epithelial cells. Phytomedicine. 1999;6:351-5. https://doi.org/10.1016/S0944-7113(99)80058-0
  30. Khajuria A, Thusu N, Zutshi U. Piperine modulates permeability characteristics of intestine by inducing alterations in membrane dynamics: influence on brush border membrane fluidity, ultrastructure and enzyme kinetics. Phytomedicine. 2002;9:224-31. https://doi.org/10.1078/0944-7113-00114
  31. Kumar A, Raman RP, Kumar K, Pandey PK, Kumar V, Mohanty S, et al. Antiparasitic efficacy of piperine against Argulus spp. on Carassius auratus (Linn. 1758): in vitro and in vivo study. Parasitol Res. 2012;111:2071-6. https://doi.org/10.1007/s00436-012-3054-z
  32. Matiullah FR, Bhatti EM, Khan N, Parveen S. Use of black pepper seed as growth enhancer in Labeo rohita. Int J Biosci. 2016;8:1-9. https://doi.org/10.12692/ijb/8.3.1-9
  33. Medagoda N, Lee KJ. Effects of dietary arachidonic acid supplementation in high plant protein diets on growth, feed utilization, and immunity of olive flounder, Paralichthys olivaceus. Aquaculture. 2023;571:739431.
  34. Murlidhar M, Goswami TK. Nutritional constituent of black pepper as medicinal molecules: a review. Open Access Sci Rep. 2012;1:1-7.
  35. Meghwal M, Goswami TK. Piper nigrum and piperine: an update. Phytother Res. 2013;27:1121-30. https://doi.org/10.1002/ptr.4972
  36. Meyer M, Jaspers I. Respiratory protease/antiprotease balance determines susceptibility to viral infection and can be modified by nutritional antioxidants. Am J Physiol Lung Cell Mol Physiol. 2015;308:L1189-201. https://doi.org/10.1152/ajplung.00028.2015
  37. Mohammed GJ, Omran AM, Hussein HM. Antibacterial and phytochemical analysis of Piper nigrum using gas chromatography - mass spectrum and Fourier-transform infrared spectroscopy. Int J Pharmacogn Phytochem Res. 2016;8:977-96.
  38. Nahak G, Sahu RK. Phytochemical evaluation and antioxidant activity of Piper cubeba and Piper nigrum. J Appl Pharm Sci. 2011;1:153-7.
  39. Nilavan ES, Raman RP, Srivastava PP, Basha KA, Kumar K, Kumar A, et al. Dietary piperine improves haemato-immunological parameters, growth profiles and resistance against Aeromonas hydrophila in Labeo rohita (Hamilton, 1822). J Aquac Trop. 2017;32:189-203.
  40. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
  41. Platel K, Srinivasan K. Influence of dietary spices and their active principles on pancreatic digestive enzymes in albino rats. Food/Nahrung. 2000;44:42-6. https://doi.org/10.1002/(SICI)1521-3803(20000101)44:1<42::AID-FOOD42>3.0.CO;2-D
  42. Pundir RK, Jain P. Comparative studies on the antimicrobial activity of black pepper (Piper nigrum) and turmeric (Curcuma longa) extracts. Int J Appl Biol Pharm Technol. 2010;1:492-500.
  43. Punitha SMJ, Babu MM, Sivaram V, Shankar VS, Dhas SA, Mahesh TC, et al. Immunostimulating influence of herbal biomedicines on nonspecific immunity in Grouper Epinephelus tauvina juvenile against Vibrio harveyi infection. Aquac Int. 2008;16:511-23. https://doi.org/10.1007/s10499-007-9162-6
  44. Sabina EP, Souriyan ADH, Jackline D, Rasool MK. Piperine, an active ingredient of black pepper attenuates acetaminophen-induced hepatotoxicity in mice. Asian Pac J Trop Med. 2010;3:971-6. https://doi.org/10.1016/S1995-7645(11)60011-4
  45. Shin J, Yun KS, Gunathilaka BE, Hasanthi M, Ko D, Lim H, et al. Piperine supplementation in diet improves growth, feed efficiency, innate immunity, digestibility and disease resistance of Pacific white shrimp (Litopenaeus vannamei). Aquac Rep. 2023;29:101490.
  46. Singh A, Duggal S. Piperine-review of advances in pharmacology. Int J Pharm Sci Nanotechnol. 2009;2:615-20. https://doi.org/10.37285/ijpsn.2009.2.3.4
  47. Siwicki AK, Anderson DP, Rumsey GL. Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Vet Immunol Immunopathol. 1994;41:125-39. https://doi.org/10.1016/0165-2427(94)90062-0
  48. Srinivasan K. Black pepper and its pungent principle-piperine: a review of diverse physiological effects. Crit Rev Food Sci Nutr. 2007;47:735-48. https://doi.org/10.1080/10408390601062054
  49. Srinivasan K. 1034 Metabolic effects of dietary pungent spices on the gut in animal models. J Anim Sci. 2016;94:495-6. https://doi.org/10.2527/jam2016-1034
  50. Srinivasan K, Sambaiah K. The effect of spices on cholesterol 7 alpha-hydroxylase activity and on serum and hepatic cholesterol levels in the rat. Int J Vitam Nutr Res. 1991;61:364-9.
  51. Swathy JS, Mishra P, Thomas J, Mukherjee A, Chandrasekaran N. Antimicrobial potency of high-energy emulsified black pepper oil nanoemulsion against aquaculture pathogen. Aquaculture. 2018;491:210-20. https://doi.org/10.1016/j.aquaculture.2018.03.045
  52. Ullah A, Azmat H, Masood Z, Arooj F, Hussain SM, Malik A. Impact of dietary leaf extracts of black pepper Piper nigrum L. on the growth, hematological and immunological parameters of Labeo rohita (Hamilton, 1822) cultured in glass aquaria. Braz J Biol. 2021;83.
  53. Vijayakumar RS, Nalini N. Lipid-lowering efficacy of piperine from Piper nigrum L. in high-fat diet and antithyroid drug-induced hypercholesterolemic rats. J Food Biochem. 2006;30:405-21. https://doi.org/10.1111/j.1745-4514.2006.00074.x
  54. Vijayakumar RS, Surya D, Nalini N. Antioxidant efficacy of black pepper (Piper nigrum L.) and piperine in rats with high fat diet induced oxidative stress. Redox Rep. 2004;9:105-10. https://doi.org/10.1179/135100004225004742
  55. Woof JM, Kerr MA. The function of immunoglobulin A in immunity. J Pathol Soc Great Br Ireland. 2006;208:270-82.
  56. Yilmaz S, Celik ES, Ergun S, Ahmadifar E, Abdel-Latif HMR. Effects of dietary walnut (Juglans regia) leaves extract on immunity, gene expression responses, and disease resistance in Oreochromis niloticus. Fish Shellfish Immunol. 2023;135:108656.
  57. Zarai Z, Boujelbene E, Salem NB, Gargouri Y, Sayari A. Antioxidant and antimicrobial activities of various solvent extracts, piperine and piperic acid from Piper nigrum. LWT Food Sci Technol. 2013;50:634-41.  https://doi.org/10.1016/j.lwt.2012.07.036