The Preparation, Anti-inflammatory, and Antioxidant Properties of Glucosamine Hydrochloride from the Waste of Litopenaeus vannamei Processing Plant

Document Type : Original Research

Authors
A. Jafari 1
M. Tabarsa 2
H. Naderimanesh 3
H. Ahmadi Gavlighi 4
S. You 5
1 Department of Seafood Processing, Faculty of Marine Sciences, Tarbiat Modares University
2 Department of Seafood Processing, Tarbiat Modares University
3 Department of Biophysics, Faculty of Biological Sciences, Tarbiat Modares University
4 Department of Food Science and Technology, Faculty of Agriculture, Tarbiat Modares University
5 Department of Marine Food Science and Technology, Gangneung-Wonju National University
10.22034/ECOPERSIA.12.2.6
Abstract
Aims: The purpose of the present study was to investigate the antioxidant and anti-inflammatory properties of glucosamine hydrochloride (G-HCl), glucosamine sulfate sodium chloride (GS-Na) and glucosamine sulfate potassium chloride (GS-K) isolated from the shells of Litopenaeus vannamei obtained from a shrimp processing plant.

Materials &Methods: G-HCl was synthesized via hydrolysis of chitin with concentrated HCl followed by several sequential decolorization, crystallization and washing steps. Using G-HCl as the precursor, addition of sodium and potassium sulfates at 40 ºC for 1 h resulted in production of GS-Na and GS-K.

Findings: The yield of chitin was found 19.9% and those of glucosamine products ranged between 75.5%-82.5%. The HPAEC-PAD indicated the presence of glucosamine monomers, as compared with commercial standard, with different elution time to that of glucose. The appearance of characteristic signals of O-H, N-H and C-O-C in the FT-IR spectra provided further support of glucosamine successful isolation. SEM images and EDX spectra of glucosamines confirmed the elemental compositions of samples and their polyhedral crystalline structures. DSC and TGA thermograms indicated endothermic and exothermic peaks specific to glucosamine products. Relatively low DPPH and ABTS radical scavenging activities and ferric reducing power was obtained for all glucosamine products. all the glucosamine derivatives indicated an anti-inflammatory effect on LPS-simulated RAW264.7 cells.

Conclusion: Glucosamine products showed no cytotoxicity and down-regulated the release of NO in RAW264.7 murine macrophage cells induced by LPS. Overall, the present results indicated the successful production of glucosamine from the waste of L. vannamei processing plant with antioxidant and anti-inflammatory properties.
Keywords
Litopenaeus vannamei
Shell
Chitin
Glucosamine
Antioxidant
Anti-inflammatory

Subjects

1. Olsen R.L., Toppe J., Karunasagar I. Challenges and realistic opportunities in the use of by-products from processing of fish and shellfish. Trends Food Sci. 2014; 1;36(2): 144-51. https://doi.org/10.1016/j.tifs.2014.01.007.
2. López-Pedrouso M., Lorenzo J.M, Cantalapiedra J., Zapata C., Franco J.M., Franco D. Aquaculture and by-products: Challenges and opportunities in the use of alternative protein sources and bioactive compounds. Adv. Food Nutr. Res. 2020; 1;92: 127-85. https://doi.org/10.1016/bs.afnr.2019.11.001.
3. Khodabandeh S., Hassan Sajedi R., Behmanesh M. Influence of Enzyme Type and Hydrolysis Time on Antioxidant Activity of Hydrolyzed Protein from Longtail Tuna (Thunnus tonggol) Dark Muscle. ECOPERSIA. 2023; 10;11(3): 187-95. https://ecopersia.modares.ac.ir/article-24-65190-en.html.
4. Ornum J.V. Shrimp waste-must it be wasted. INFOFISH Int. 1992; 6(92): 48-523.
5. Knorr D. Recovery and utilization of chitin and chitosan in food processing waste management. Food Technol, 1991; 26: 114–122. https://cir.nii.ac.jp/crid/1571135650706132352.
6. Nirmal N.P., Santivarangkna C., Rajput M.S., Benjakul S. Trends in shrimp processing waste utilization: An industrial prospective. Trends Food Sci. 2020 Sep 1;103: 20-35. https://doi.org/10.1016/j.tifs.2020.07.001.
7. IMARC. Shrimp market: Global industry trends, share, size, growth, opportunity and forecast 2020-2025. USA: IMARC group. https://www.imarcgroup.com/prefeasibility-report-shrimp-processing-plant.
8. FAO. 2023. Fishery and Aquaculture Statistics. Global aquaculture production 1950-2021 (FishstatJ); http://www.fao.org/fishery/en/statistics/software/fishstatj.
9. Suryawanshi N., Eswari J.S. Chitin from seafood waste: particle swarm optimization and neural network study for the improved chitinase production. J. Chem. Technol. Biotechnol. 2022; 97(2): 509-19. https://doi.org/10.1002/jctb.6656.
10. Coward-Kelly G., Agbogbo F.K., Holtzapple MT. Lime treatment of shrimp head waste for the generation of highly digestible animal feed. Bioresour. Technol. 2006; 1;97(13):1515-20. https://doi.org/10.1016/j.biortech.2005.06.014.
11. Sachindra N.M., Bhaskar N. In vitro antioxidant activity of liquor from fermented shrimp biowaste. Bioresour. Technol. 2008; 99(18): 9013-6. https://doi.org/10.1016/j.biortech.2008.04.036.
12. Díaz‐Rojas E.I., Argüelles‐Monal W.M., Higuera‐Ciapara I., Hernández J., Lizardi‐Mendoza J., Goycoolea F.M. Determination of chitin and protein contents during the isolation of chitin from shrimp waste. Macromol. Biosci. 2006; 23;6(5): 340-7. https://doi.org/10.1002/mabi.200500233.
13. Jayakumar R., Prabaharan M., Kumar P.S., Nair S.V., Tamura H.J., Biomaterials based on chitin and chitosan in wound dressing applications. Biotechnol. Adv. 2011; 1;29(3): 322-37. https://doi.org/10.1016/j.biotechadv.2011.01.005.
14. Soni T., Zhuang M., Kumar M., Balan V., Ubanwa B., Vivekanand V., Pareek N. Multifaceted production strategies and applications of glucosamine: a comprehensive review. Crit. Rev. Biotechnol. 2023; 2;43(1): 100-20. https://doi.org/10.1080/07388551.2021.2003750.
15. Anderson J.W., Nicolosi R.J., Borzelleca J.F. Glucosamine effects in humans: a review of effects on glucose metabolism, side effects, safety considerations and efficacy. Food Chem. Toxicol. 2005; 1;43(2): 187-201. https://doi.org/10.1016/j.fct.2004.11.006.
16. Houpt J.B., McMillan R., Wein C., Paget-Dellio S.D. Effect of glucosamine hydrochloride in the treatment of pain of osteoarthritis of the knee. J. Rheumat. 1999; 1;26(11):2423-30. https://europepmc.org/article/med/10555905.
17. Luo J., Hu Y., Wu Y., Fan W. Effect of glucosamine hydrochloride in ameliorating knee osteoarthritis. Chinese J. Clinical Rehab. 2005; 9: 70-72. https://doi.org/10.1155/2022/8120458.
18. Vangsness C.T., Spiker W., Erickson J. A review of evidence-based medicine for glucosamine and chondroitin sulfate use in knee osteoarthritis. Arthroscopy: J. Arthrosc. Relat. Surg. 2009; 1;25(1):86-94. https://doi.org/10.1016/j.arthro.2008.07.020.
19. Bissett D.L. Glucosamine: an ingredient with skin and other benefits. J. Cosmetic Dermatol. 2006; 5(4): 309-15. https://doi.org/10.1111/j.1473-2165.2006.00277.x.
20. Piperno M., Reboul P., Le Graverand M.H., Peschard M.J., Annefeld M., Richard M., Vignon E. Glucosamine sulfate modulates dysregulated activities of human osteoarthritic chondrocytes in vitro. Osteoarthritis and Cartilage. 2000; 1;8(3): 207-12. https://doi.org/10.1053/joca.1999.0291.
21. Shikhman A.R., Kuhn K., Alaaeddine N., Lotz M. N-acetylglucosamine prevents IL-1β-mediated activation of human chondrocytes. J. Immunol. 2001; 15;166(8): 5155-60. https://doi.org/10.4049/jimmunol.166.8.5155.
22. Li Y., Chen L., Liu Y., Zhang Y., Liang Y., Mei Y. Anti-inflammatory effects in a mouse osteoarthritis model of a mixture of glucosamine and chitooligosaccharides produced by bi-enzyme single-step hydrolysis. Sci. Rep. 2018; 4;8(1): 5624. https://doi.org/10.1038/s41598-018-24050-6.
23. Cheng D.W., Jiang Y., Shalev A., Kowluru R., Crook E.D., Singh L.P. An analysis of high glucose and glucosamine-induced gene expression and oxidative stress in renal mesangial cells. Arch. Physiol. Biochem. 2006; 1;112(4-5): 189-218. https://doi.org/10.1080/13813450601093518.
24. Chen Y.J., Huang Y.S., Chen J.T., Chen Y.H., Tai M.C., Chen C.L., Liang C.M. Protective effects of glucosamine on oxidative-stress and ischemia/reperfusion-induced retinal injury. Invest. Ophthalmol. Visual Sci. 2015; 1;56(3): 1506-16. https://doi.org/10.1167/iovs.14-15726.
25. Mendis E., Kim M.M., Rajapakse N., Kim S.K. Sulfated glucosamine inhibits oxidation of biomolecules in cells via a mechanism involving intracellular free radical scavenging. Eur. J. Pharmacol. 2008; 28;579(1-3): 74-85. https://doi.org/10.1016/j.ejphar.2007.10.027.
26. Valvason C., Musacchio E., Pozzuoli A., Ramonda R., Aldegheri R., Punzi L.. Influence of glucosamine sulphate on oxidative stress in human osteoarthritic chondrocytes: effects on HO-1, p22 Phox and iNOS expression. Rheumatol. 2008; 1;47(1): 31-5. https://doi.org/10.1093/rheumatology/kem289.
27. Stadler J.O., Stefanovic-Racic M.A., Billiar T.R., Curran R.D., McIntyre L.A., Georgescu H.I., Simmons R.L., Evans C.H. Articular chondrocytes synthesize nitric oxide in response to cytokines and lipopolysaccharide. J. Immunol. (Baltimore, Md.: 1950). 1991; 1;147(11): 3915-20. https://doi.org/10.4049/jimmunol.147.11.3915.
28. Yan Y., Wanshun L., Baoqin H., Changhong W., Chenwei F., Bing L., Liehuan C. The antioxidative and immunostimulating properties of D-glucosamine. Int. Immunopharmacol. 2007; 1;7(1): 29-35. https://doi.org/10.1016/j.intimp.2006.06.003.
29. Xing R., Liu S., Guo Z., Yu H., Li C., Ji X., Feng J., Li P. The antioxidant activity of glucosamine hydrochloride in vitro. Bioorganic Med. Chem. 2006; 15;14(6): 1706-9. https://doi.org/10.1016/j.bmc.2005.10.018.
30. Xing R., Liu S., Wang L., Cai S., Yu H., Feng J., Li P. The preparation and antioxidant activity of glucosamine sulfate. Chin. J. Oceanol. Limnol. 2009; 27: 283-7. https://doi.org/10.1007/s00343-009-9135-x.
31. Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., Tannenbaum S.R. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal. Biochem. 1982; 1;126(1): 131-8. https://doi.org/10.1016/0003-2697(82)90118-X.
32. Brand-Williams W., Cuvelier ME., Berset C.L. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol. 1995; 1;28(1): 25-30.
33. Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 1999; 1;26(9-10): 1231-7. https://doi.org/10.1016/S0891-5849(98)00315-3.
34. Re R., Pellegrini N., Proteggente A., Pannala A., Yang M., Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 1999; 1;26(9-10): 1231-7. https://doi.org/10.1016/S0891-5849(98)00315-3.
35. Oyaizu M. Studies on products of browning reaction prepared from glucose amine products derived from bees. J. Pharm. Biomed. Anal. 1986; 41: 1220-34. https://doi.org/10.5264/eiyogakuzashi.44.307.
36. Zhang Z., Khan N.M., Nunez K.M., Chess E.K., Szabo C.M. Complete monosaccharide analysis by high-performance anion-exchange chromatography with pulsed amperometric detection. Anal. Chem. 2012; 84(9): 4104-10. https://doi.org/10.1021/ac300176z.
37. Bertuzzi D.L., Becher T.B., Capreti N.M., Amorim J., Jurberg I.D., Megiatto J.D., Ornelas C. General Protocol to Obtain D‐Glucosamine from Biomass Residues: Shrimp Shells, Cicada Sloughs and Cockroaches. Global Challenges. 2018; 2(11): 1800046. https://doi.org/10.1002/gch2.201800046.
38. Zaeni A., Safitri E., Fuadah B., Sudiana I.N. Microwave-assisted hydrolysis of chitosan from shrimp shell waste for glucosammine hydrochlorid production. Journal of Physics: Conference Series. 2017; 1 (846): 012011. IOP Publishing.
39. Yu S., Zang H., Chen S., Jiang Y., Yan B., Cheng B. Efficient conversion of chitin biomass into 5-hydroxymethylfurfural over metal salts catalysts in dimethyl sulfoxide-water mixture under hydrothermal conditions. Polym. Degrad. Stab. 2016; 1(134): 105-14. https://doi.org/10.1016/j.polymdegradstab.2016.09.035.
40. Kim H.S., Kim S.K., Jeong G.T. Efficient conversion of glucosamine to levulinic acid in a sulfamic acid-catalyzed hydrothermal reaction. RSC advances. 2018; 8(6): 3198-205. https://doi.org/10.1039/C7RA12980G.
41. Wahab A., Khan G.M., Sharifi M., Khan A., Khan A., Khan N. Preparation, solid state characterization and evaluation of ketoprofen-glucosamine HCl solid dispersions. Arch. Pharm. Pharmaceutic. Sci. 2018; 26;2(1): 010-9. https://doi.org/10.29328/journal.apps.1001007.
42. Al-Hamidi H., Edwards A.A., Mohammad M.A., Nokhodchi A. To enhance dissolution rate of poorly water-soluble drugs: glucosamine hydrochloride as a potential carrier in solid dispersion formulations. Colloids Surf., B. 2010; 76(1): 170-8. https://doi.org/10.1016/j.colsurfb.2009.10.030.
43. Asare-Addo K., Šupuk E., Al-Hamidi H., Owusu-Ware S., Nokhodchi A., Conway B.R. Triboelectrification and dissolution property enhancements of solid dispersions. Int. J. Pharm. 2015; 15;485(1-2): 306-16. https://doi.org/10.1016/j.ijpharm.2015.03.013.
44. El-Houssiny A., Ward A., Mostafa D., Abd-El-Messieh S., Abdel-Nour K., Darwish M., Khalil W. Drug–polymer interaction between glucosamine sulfate and alginate nanoparticles: FTIR, DSC and dielectric spectroscopy studies. Advances in Adv. Nat. Sci.: Nanosci. 2016; 7(2): 025014. https://doi.org/10.1088/2043-6262/7/2/025014.
45. Scherer R., Godoy H.T. Antioxidant activity index (AAI) by the 2, 2-diphenyl-1-picrylhydrazyl method. Food Chem. 2009; 112(3): 654-8. https://doi.org/10.1016/j.foodchem.2008.06.026.
46. Kamala K., Sivaperumal P., Rajaram R. Extraction and characterization of water soluble chitosan from Parapeneopsis stylifera shrimp shell waste and its antibacterial activity. Inter. J. Sci. Res. Public. 2013; 3(4): 1-8. https://doi.org/10.29322.
47. Benavente M., Arias S., Moreno L., Martínez J. Production of glucosamine hydrochloride from crustacean shell. J. Pharm. Pharmacol. 2015; 3(1): 20-26. doi: 10.17265/2328-2150/2015.01.003.
48. Brugnerotto J., Lizardi J., Goycoolea F., Argüelles-Monal W., Desbrieres J., Rinaudo M. An infrared investigation in relation with chitin and chitosan characterization. Polymer, 2001; 42(8): 3569-3580. https://doi.org/10.1016/S0032-3861(00)00713-8.
49. Chen H., Zhang M., Qu Z., Xie B. Antioxidant activities of different fractions of polysaccharide conjugates from green tea (Camellia Sinensis). Food Chem. 2008; 106(2): 559-563. https://doi.org/10.1016/j.foodchem.2007.06.040.
50. Díaz‐Rojas E.I., Argüelles‐Monal W.M., Higuera‐Ciapara I., Hernández J., Lizardi‐Mendoza J., Goycoolea F.M. Determination of chitin and protein contents during the isolation of chitin from shrimp waste. Macromol. Biosci. 2006; 6(5): 340-347. https://doi.org/10.1002/mabi.200500233.
51. Drovanti A., Bignamini A., Rovati A. Therapeutic activity of oral glucosamine sulfate in osteoarthrosis: a placebo-controlled double-blind investigation. Clin. Ther. 1980; 3(4): 260-272. https://www.altmetric.com/details/2789010.
52. Gottardi, D., Hong, P. K., Ndagijimana, M., & Betti, M. Conjugation of gluten hydrolysates with glucosamine at mild temperatures enhances antioxidant and antimicrobial properties. LWT-Food Sci. Technol. 2014; 57(1): 181-187. https://doi.org/10.1016/j.lwt.2014.01.013.
53. Jamialahmadi K., Arasteh O., Riahi M.M., Mehri S., Riahi-Zanjani B., Karimi G. Protective effects of glucosamine hydrochloride against free radical-induced erythrocytes damage. Environ. Toxicol. Pharmacol. 2014; 38(1): 212-219. https://doi.org/10.1016/j.etap.2014.05.018.
54. Kraisangsri J., Nalinanon S., Riebroy S., Yarnpakdee S., Ganesan P. Physicochemical characteristics of glucosamine from blue swimming crab (Portunus pelagicus) shell prepared by acid hydrolysis. Walailak Journal of Science and Technology (WJST), 2018; 15(12): 869-877. https://doi.org/10.48048/wjst.2018.3666.
55. Li X., Li X., Zhou A. Evaluation of antioxidant activity of the polysaccharides extracted from Lycium barbarum fruits in vitro. Euro. Polymer J. 2007; 43(2): 488-497. https://doi.org/10.1016/j.eurpolymj.2006.10.025.
56. Trung T.S., Phuong P.T. Bioactive compounds from by-products of shrimp processing industry in Vietnam. J. Food Drug Anal. 2012; 20(1): 64. https://doi.org/10.38212/2224-6614.2130.
57. Mohan K., Muralisankar T., Jayakumar R., Rajeevgandhi C.A. Study on structural comparisons of α-chitin extracted from marine crustacean shell waste. Carbohydr. Polym. Technol. Appl. 2021; 25(2): 100037. https://doi.org/10.1016/j.carpta.2021.100037.
58. Synowiecki J., Al-Khateeb N.A. Production, properties, and some new applications of chitin and its derivatives. 2003; 145-171. https://doi.org/10.1080/10408690390826473.
59. Mojarrad J.S., Nemati M., Valizadeh H., Ansarin M., Bourbour S. Preparation of glucosamine from exoskeleton of shrimp and predicting production yield by response surface methodology. J. Agric. Food. Chem. 2007; 55(6): 2246-50. https://doi.org/10.1021/jf062983a.
60. Wang X., Liu B., Li X., Sun R. Novel glucosamine hydrochloride–rectorite nanocomposites with antioxidant and anti-ultraviolet activity. Nanotechnol. 2012; 23(49): 495706. https://doi.org/ 10.1088/0957-4484/23/49/495706.
61. Miao Q., Li Q., Tan W., Mi Y., Ma B., Zhang J., Guo Z. Preparation, Anticoagulant and Antioxidant Properties of Glucosamine-Heparin Salt. Mar. Drug. 2022; 20(10): 646. https://doi.org/10.3390/md20100646.
62. Rao R.S., Muralikrishna G. Water soluble feruloyl arabinoxylans from rice and ragi: Changes upon malting and their consequence on antioxidant activity. Phytochem. 2006; 67(1): 91-9. https://doi.org/10.1016/j.phytochem.2005.09.036.
63. Meng L., Sun S., Li R., Shen Z., Wang P., Jiang X. Antioxidant activity of polysaccharides produced by Hirsutella sp. and relation with their chemical characteristics. Carbohydr. Polymer. 2015; 117: 452-7. https://doi.org/10.1016/j.carbpol.2014.09.076.
64. Liew F.Y., Xu D., Brint E.K., O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 2005; 5(6): 446-58. https://doi.org/10.1038/nri1630.
65. Azuma K., Osaki T., Kurozumi S., Kiyose M., Tsuka T., Murahata Y., Imagawa T., Itoh N., Minami S., Sato K., Okamoto Y. Anti-inflammatory effects of orally administered glucosamine oligomer in an experimental model of inflammatory bowel disease. Carbohydr. Polymer. 2015; 115: 448-56. https://doi.org/10.1016/j.carbpol.2014.09.012.
66. Chiu H.W., Li L.H., Hsieh C.Y., Rao Y.K., Chen F.H., Chen A., Ka S.M., Hua K.F. Glucosamine inhibits IL-1β expression by preserving mitochondrial integrity and disrupting assembly of the NLRP3 inflammasome. Sci. Rep. 2019; 9(1): 5603. https://doi.org/10.1038/s41598-019-42130-z.
67. Hwang S.Y., Shin J.H., Hwang J.S., Kim S.Y., Shin J.A., Oh E.S., Oh S., Kim J.B., Lee J.K., Han IO. Glucosamine exerts a neuroprotective effect via suppression of inflammation in rat brain ischemia/reperfusion injury. Glia. 2010; 58(15): 1881-92. https://doi.org/10.1002/glia.21058.
68. Wu Y.L., Lin A.H., Chen C.H., Huang W.C., Wang H.Y., Liu M.H., Lee T.S., Kou Y.R. Glucosamine attenuates cigarette smoke-induced lung inflammation by inhibiting ROS-sensitive inflammatory signaling. Free Radical Biol. Med. 2014; 1(69): 208-18. https://doi.org/10.1016/j.freeradbiomed.2014.01.026