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Enzymatic hydrolysis improves digestibility of edible bird’s nest (EBN): combined effect of pretreatment and enzyme

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Abstract

Numerous studies proved the better health benefits of edible bird’s nest hydrolysate (EBNH) than edible bird’s nest (EBN). This study was conducted to investigate the effect of different pretreatments and enzymes on the chemical properties of EBNH. The degree of hydrolysis (DH), total soluble protein, UV–Vis absorption spectrum and FTIR spectrum of EBN and EBNH were determined. Besides, the digestibility of EBN and EBNH were also determined through simulated in vitro digestion. Initially, the 4% w/v EBN was treated with different pretreatments [boiling, combined boiling with ultrasound (40 kHz,250 W) and autoclave at 120 °C]. Then, the pretreated EBN was subjected to 2 h hydrolysis using pepsin, trypsin, papain and pancreatin, respectively. Besides, two-stages enzymatic hydrolysis using pepsin-papain, papain-trypsin and papain-pancreatin enzymes were also investigated. Results obtained propose that the combination of autoclave pretreatment and pancreatin hydrolysis produced EBNH with the highest DH (11.19 ± 0.18%). Heat treatment was crucial to unfold the glycoprotein, hence facilitate enzymatic hydrolysis. Two-stages enzymatic hydrolysis was proven less efficient than the process with heat pretreatment. Besides, papain was proven as the best enzyme to increase solubility of EBN glycoprotein. EBNH produced from boiled EBN using papain contained the highest total soluble protein content (459.63 ± 66.01 mg g−1). Results of UV–Vis absorption spectrum and FTIR spectrum reveal that efficiency of enzymatic hydrolysis of glycoprotein was strongly influenced by the extent of protein unfolding and aggregation. Among the EBNHs, EBNH produced from autoclaved EBN using pancreatin enzyme had the best digestibility. This study provides insight into the importance of pretreatment method and enzyme type in ensuring nutritional quality of EBNH.

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Data availability

The datasets of this study are available from the corresponding author upon reasonable request.

References

  1. M.C. Quek, N.L. Chin, Y.A. Yusof, S.W. Tan, C.L. Law, Preliminary nitrite, nitrate and color analysis of Malaysian edible bird’s nest. Infor Process. Agric. 2, 1–5 (2015)

    Google Scholar 

  2. S.N. Tan, D. Sani, C.W. Lim, A. Ideris, J. Stanslas, C.T.S. Lim, Proximate analysis and safety profile of farmed edible bird’s nest in Malaysia and its effect on cancer cells. Evid. Based Complement. Altern. Med. 2020, 8068797 (2020)

    Article  Google Scholar 

  3. Y. Dai, J. Cao, Y. Wang, Y. Chen, L. Jiang, A comprehensive review of edible bird’s nest. Food Res. Int. 140, 109875 (2021)

    Article  CAS  Google Scholar 

  4. T. Dobutr, W. Kantamala, S. Phimwapi, N. Jangpromma, P. Tippayawat, S. Boonlue, J. Daduang, S. Klaynongsruang, S. Poopornchai, S. Daduang, The effects of edible bird’s nest on T-lymphocyte proliferation, secondary lymphoid organs and interleukin-2 production. J. Funct. Foods 90, 104977 (2022)

    Article  CAS  Google Scholar 

  5. A.J.W. Ling, L.S. Chang, A.S. Babji, J. Latip, M. Koketsu, S.J. Lim, Review of sialic acid’s biochemistry, sources, extraction and functions with special reference to edible bird’s nest. Food Chem. 367, 130755 (2022)

    Article  CAS  Google Scholar 

  6. T.H. Lee, W.A. Wani, C.H. Lee, K.K. Cheng, S. Shreaz, S. Wong, N. Hamdan, N.A. Azmi, Edible bird’s nest: The functional values of the prized animal-based bioproduct from Southeast Asia—a review. Front. Pharmacol. (2021). https://doi.org/10.3389/fphar.2021.626233

    Article  Google Scholar 

  7. S.J. Lim, L.S. Chang, S. Fazry, W.A. Wan Mustapha, A.S. Babji, Functional food & ingredients from seaweed, edible bird’s nest and tropical fruits: a translational research. LWT 151, 112164 (2021)

    Article  CAS  Google Scholar 

  8. A.S. Babji, I.K. Etty Syarmila, D. Nur’ Aliah, M. Nurul Nadia, D. Hadi Akbar, A.S. Norrakiah, M. Ghassem, L. Najafian, M.Y. Salma, Assessment on bioactive components of hydrolysed edible bird nest. Int. Food Res. J. 25, 1936–1941 (2018)

    CAS  Google Scholar 

  9. K. Roh, J. Lee, Y. Kim, J. Park, J. Kim, J. Lee, D. Park, Mechanisms of edible bird’s nest extract-induced proliferation of human adipose-derived stem cells. Evid. Based Complement. Altern. Med. 2012, 797520 (2012)

    Article  Google Scholar 

  10. C. Guo, T. Takahashi, W. Bukawa, N. Takahashi, H. Yagi, K. Kato, K.I.P.J. Hidari, D. Miyamoto, T. Suzuki, Y. Suzuki, Edible bird’s nest extract inhibits influenza virus infection. Antivir. Res. 70, 140–146 (2006)

    Article  CAS  Google Scholar 

  11. M.Y. Yew, R.Y. Koh, S.M. Chye, S.A.Z. Abidin, I. Othman, K.Y. Ng, Neurotrophic properties and the de novo peptide sequencing of edible bird’s nest extracts. Food Biosci. 32, 100466 (2019)

    Article  CAS  Google Scholar 

  12. P.K. Chong, S.L. Mun, L.S. Chang, A.S. Babji, S.J. Lim, Fractionation of edible bird’s nest glycoprotein hydrolysates: characterisation and antioxidative activities of the fractions. Food Sci. Hum. Wellness 11, 886–894 (2022)

    Article  CAS  Google Scholar 

  13. H. Kong, K. Wong, S.C. Lo, Identification of peptides released from hot water insoluble fraction of edible bird’s nest under simulated gastro-intestinal conditions. Food Res. Int. 85, 19–25 (2016)

    Article  CAS  Google Scholar 

  14. B.M. Jain, M.P. Badve, A novel process for synthesis of soybean protein hydrolysates and study of its effectiveness as a biostimulant and emulsifier. Chem. Eng. Process.: Process. Intensif. 174, 108880 (2022)

    Article  CAS  Google Scholar 

  15. Y. Liu, Y. Huang, X. Deng, Z. Li, W. Lian, G. Zhang, Y. Zhu, X. Zhu, Effect of enzymatic hydrolysis followed after extrusion pretreatment on the structure and emulsibility of soybean protein. Process. Biochem. 116, 173–184 (2022)

    Article  CAS  Google Scholar 

  16. X. Pan, F. Fan, J. Ding, P. Li, X. Sun, L. Zhong, Y. Fang, Altering functional properties of rice protein hydrolysates by covalent conjugation with chlorogenic acid. Food Chem. 14, 100352 (2022)

    CAS  Google Scholar 

  17. X. Li, C. Feng, H. Hong, Y. Zhang, Z. Luo, Q. Wang, Y. Luo, Y. Tan, Novel ACE inhibitory peptides derived from whey protein hydrolysates: identification and molecular docking analysis. Food Biosci. 48, 101737 (2022)

    Article  CAS  Google Scholar 

  18. M. Kumar, P. Selvasekaran, S. Kapoor, M.D. Barbhai, J.M. Lorenzo, V. Saurabh, J. Potkule, S. Changan, A. ElKelish, S. Selim, A.A.S. Sayed, S. Radha, M. Singh, R. Senapathy, A. Pandiselvam, S. Dey, S. Dhumal, R. Natta, J.F. Amarowicz, Kennedy, Moringa oleifera Lam. seed proteins: extraction, preparation of protein hydrolysates, bioactivities, functional food properties and industrial application. Food Hydrocoll. 131, 107791 (2022)

    Article  CAS  Google Scholar 

  19. J.A. Vazquez, A. Pedreira, S. Duran, D. Cabanelas, P. Souto-Montero, P. Martinez, M. Mulet, R.I. Perez-Martin, J. Valcarcel, Biorefinery for tuna head wastes: production of protein hydrolysates, high-quality oils, minerals and bacterial peptones. J. Clean. Prod. 357, 131909 (2022)

    Article  CAS  Google Scholar 

  20. K.O. Lima, A. Aleman, M.E. Lopez-Caballero, M.C. Gomez-Guillen, M.P. Montero, C. Prentice, A.J.T. Huisa, J.M. Monserrat, Characterization, stability and in vivo effects in Caenorhabditis elegans of microencapsulated protein hydrolysates from stripped weakfish (Cynoscion guatucupa) industrial byproducts. Food Chem. 364, 130380 (2021)

    Article  Google Scholar 

  21. Y. Yao, M. Wang, Y. Liu, L. Han, X. Liu, Insights into the improvement of the enzymatic hydrolysis of bovine bone protein using lipase pretreatment. Food Chem. 302, 125199 (2020)

    Article  CAS  Google Scholar 

  22. Y. Wu, Y. Zhang, W. Duan, Q. Wang, F. An, P. Luo, Q. Huang, Ball-milling is an effective pretreatment of glycosylation modified the foaming and gel properties of egg white protein. J. Food Eng. 319, 110908 (2022)

    Article  CAS  Google Scholar 

  23. R.M. Gonzalez-Balderas, S.B. Velasquez-Orta, M. Felix, C. Bengoechea, I.Y. Noguez, M.T.O. Ledesma, Identification and effect of ozone and ultrasound pretreatments on Desmodesmus sp. and Tetradesmus obliquus proteins. Algal Res. 60, 102514 (2021)

    Article  Google Scholar 

  24. S. Huang, Y. Li, C. Li, S. Ruan, S.M.R. Azam, N. Ou Yang, X. Ye, Y. Wang, H. Ma, Effects of ultrasound-assisted sodium bisulfite pretreatment on the preparation of cholesterol-lowering peptide precursors from soybean protein. Int. J. Biol. Macromol. 183, 295–304 (2021)

    Article  CAS  Google Scholar 

  25. H. Daliri, R. Ahmadi, A. Pezeshki, H. Hamishehkar, M. Mohammadi, H. Beyrami, M.K. Heshmati, M. Ghorbani, Quinoa bioactive protein hydrolysate produced by pancreatin enzyme: functional and antioxidant properties. LWT 150, 111853 (2021)

    Article  CAS  Google Scholar 

  26. V.G. Tacias-Pascacio, D. Castaneda-Valbuena, R. Morellon-Sterling, O. Tavano, A. Berenguer-Murcia, G. Vela-Gutierrez, I.A. Rather, R. Fernandez-Lafuente, Bioactive peptides from fisheries residues: a review of use of papain in proteolysis reactions. Int. J. Biol. Macromol. 184, 415–428 (2021)

    Article  CAS  Google Scholar 

  27. X. Mao, X. Cheng, X. Wang, S. Wu, Free-radical-scavenging and anti-inflammatory effect of yak milk casein before and after enzymatic hydrolysis. Food Chem. 126, 484–490 (2011)

    Article  CAS  Google Scholar 

  28. C. Megias, J. Pedroche, M.M. Yust, J. Giron-Calle, M. Alaiz, F. Millan, J. Vioque, Production of copper-chelating peptides after hydrolysis of sunflower proteins with pepsin and pancreatin. LWT 41, 1973–1977 (2008)

    Article  CAS  Google Scholar 

  29. G. Moraes, L.C. Almeida, in Biology and Physiology of Freshwater Neotropical Fish. ed. by B.B. Baldisserotto, E.C. Urbinati, J.E.P. Cyrino (Elsevier, Netherlands, 2020)

    Google Scholar 

  30. T.H. Yan, S.J. Lim, A.S. Babji, M.H. Rawi, S.R. Sarbini, Enzymatic hydrolysis: sialylated mucin (SiaMuc) glycoprotein of edible swiftlet’s nest (ESN) and its molecular weight distribution as bioactive ESN SiaMuc-glycopeptide hydrolysate. Int. J. Biol. Macromol. 175, 422–431 (2021)

    Article  Google Scholar 

  31. P. Fathi, M. Moosavi-Nasab, A. Mirzapour-Kouhdasht, M. Khalesi, Generation of hydrolysates from rice bran proteins using a combined ultrasonication-Alcalase hydrolysis treatment. Food Biosci. 42, 101110 (2021)

    Article  CAS  Google Scholar 

  32. M. Araya, S. Garcia, J. Rengel, S. Pizarro, G. Alvarez, Determination of free and protein amino acid content in microalgae by HPLC-DAD with pre-column derivatization and pressure hydrolysis. Mar. Chem. 234, 103999 (2021)

    Article  CAS  Google Scholar 

  33. P.L. Tang, H.S. Goh, S.S. Sia, Combined enzymatic hydrolysis and herbal extracts fortification to boost in vitro antioxidant activity of edible bird’s nest solution. Chin. Herb. Med. 13, 549–555 (2021)

    Article  Google Scholar 

  34. S. Ehnert, J. Seehase, C. Muller-Renno, M. Hannig, C. Ziegler, Simultaneous quantification of total carbohydrate and protein amounts from aqueous solutions by the sulfuric acid ultraviolet absorption method (SA-UV method). Anal. Chim. Acta 1174, 338712 (2021)

    Article  CAS  Google Scholar 

  35. G. Ma, Q. Xu, H. Du, B.M. Kimatu, A. Su, W. Yang, Q. Hu, H. Xiao, Characterization of polysaccharide from Pleurotus eryngii during simulated gastrointestinal digestion and fermentation. Food Chem. 370, 131303 (2022)

    Article  CAS  Google Scholar 

  36. L.S. Chua, S.N. Zukefli, A comprehensive review of edible bird nests and swiftlet farming. J. Integr. Med. 14, 415–428 (2016)

    Article  Google Scholar 

  37. A. Salhi, S. Amara, P. Mansuelle, R. Puppo, R. Lebrun, B. Gontero, A. Aloulou, F. Carriere, Characterization of all the lipolytic activities in pancreatin and comparison with porcine and human pancreatic juices. Biochimie 169, 106–120 (2020)

    Article  CAS  Google Scholar 

  38. Y. Luo, K. Pan, Q. Zhong, Physical, chemical and biochemical properties of casein hydrolyzed by three proteases: partial characterizations. Food Chem. 155, 146–154 (2014)

    Article  CAS  Google Scholar 

  39. Z. Shahi, S.Z. Sayyed-Alangi, L. Najafian, Effects of enzyme type and process time on hydrolysis degree, electrophoresis bands and antioxidant properties of hydrolyzed proteins derived from defatted Bunium persicum Bioss. press cake. Heliyon 6, e03365 (2020)

    Article  Google Scholar 

  40. E.E. Quist, R.D. Philips, F.K. Saalia, The effect of enzyme systems and processing on the hydrolysis of peanut (Arachis hypogaes L.) protein. LWT 42, 1717–1721 (2009)

    Article  CAS  Google Scholar 

  41. L. You, M. Zhao, C. Cui, H. Zhao, B. Yang, Effect of degree of hydrolysis on the antioxidant activity of loach (Misgurnus anguilicaudatus) protein hydrolysates. IFSET 10, 235–240 (2009)

    CAS  Google Scholar 

  42. V. Polzonetti, P. Natalini, S. Vincenzetti, A. Vita, S. Pucciarelli, in Olives and Olive Oil in Health and Disease Prevention. ed. by V.R. Preedy, R.R. Watson (Elsevier, Netherlands, 2010)

    Google Scholar 

  43. W. He, K. He, F. Sun, L. Mu, S. Liao, Q. Li, J. Yi, Z. Liu, X. Wu, Effect of heat, enzymatic hydrolysis and acid-alkali treatment on the allergenicity of silkworm pupa protein extract. Food Chem. 343, 128461 (2021)

    Article  CAS  Google Scholar 

  44. Y. Zhang, H.M. Romero, Exploring the structure-function relationship of Great Northern and navy bean (Phaseolus vulgaris L.) protein hydrolysates: a study on the effect of enzymatic hydrolysis. Int. J. Biol. Macromol. 162, 1516–1525 (2020)

    Article  CAS  Google Scholar 

  45. S.J. Gaspard, A.V. Sunds, L.B. Larsen, N.A. Poulsen, J.A. O’Mahony, A.L. Kelly, A. Brodkorb, Influence of desialylation of caseinomacropeptide on the denaturation and aggregation of whey proteins. J. Dairy Sci. 103, 4975–4990 (2020)

    Article  CAS  Google Scholar 

  46. N. Wang, X. Zhou, W. Wang, L. Wang, L. Jiang, T. Liu, D. Yu, Effect of high intensity ultrasound on the structure and solubility of soy protein isolate-pectin complex. Ultrason. Sonochem 80, 105808 (2021)

    Article  CAS  Google Scholar 

  47. P. Khramtsov, T. Kalashnikova, M. Bochkova, M. Kropaneva, V. Timganova, S. Zamorina, M. Rayev, Measuring the concentration of protein nanoparticles synthesized by desolvation method: comparison of bradford assay, BCA assay, hydrolysis/UV spectroscopy and gravimetric analysis. Int. J. Pharm. 599, 120422 (2021)

    Article  CAS  Google Scholar 

  48. S. Chutipongtanate, K. Watcharatanyatip, T. Homvises, K. Jaturongkakul, V. Thongboonkerd, Systematic comparisons of various spectrophotometric and colorimetric methods to measure concentrations of protein, peptide and amino acid: Detectable limits, linear dynamic ranges, interferences, practicality and unit costs. Talanta 98, 123–129 (2012)

    Article  CAS  Google Scholar 

  49. F. Schmid, eLS (2001). https://doi.org/10.1038/npg.els.0003142

    Article  Google Scholar 

  50. N. Zhang, F. Liu, X. Dong, Y. Sun, Equilibrium and kinetic studies of the counteraction of trehalose on acid-induced protein unfolding. Biochem. Eng. J. 70, 188–195 (2013)

    Article  CAS  Google Scholar 

  51. A. Mazzini, E. Polverini, M. Parisi, R.T. Sorbi, R. Favilla, Dissociation and unfolding of bovine odorant binding protein at acidic pH. J. Struct. Biol. 159, 82–91 (2007)

    Article  CAS  Google Scholar 

  52. R. Herman, Y. Gao, N. Storer, Acid-induced unfolding kinetics in simulated gastric digestion of proteins. Regul. Toxicol. Pharmacol. 46, 93–99 (2006)

    Article  CAS  Google Scholar 

  53. L. Guo, Y. Wu, M. Liu, B. Wang, Y. Ge, Y. Chen, Determination of edible bird’s nests by FTIR and SDS-PAGE coupled with multivariate analysis. Food Control. 80, 259–266 (2017)

    Article  CAS  Google Scholar 

  54. J.Y. Gan, L.S. Chang, N.A.M. Nasir, A.S. Babji, S.J. Lim, Evaluation of physicochemical properties, amino acid profile and bioactivities of edible bird’s nest hydrolysate as affected by drying methods. LWT 131, 109777 (2020)

    Article  CAS  Google Scholar 

  55. B.R. Singh, in Infrared Analysis of Peptides and Protein: Principles and Applications. ed. by B.R. Singh (American Chemical Society, Washington, 1999). https://doi.org/10.1021/bk-2000-0750.ch001

    Chapter  Google Scholar 

  56. J. Grdadolnik, A FTIR investigation of protein conformation. Bull. Chem. Technol. Macedonia 21, 23–34 (2002)

    CAS  Google Scholar 

  57. P.B. Stathopulos, G.A. Scholz, Y. Hwang, J.A.O. Rumfeldt, J.R. Lepock, E.M. Meiering, Sonication of proteins causes formation of aggregates that resemble amyloid. Protein Sci. 13, 3017–3027 (2008)

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the assistances and supports provided by Ms. Ravina Saravanan, intern in food analysis laboratory and Mr. Booi Chin Hai, laboratory assistant in food science laboratory. Besides, the authors also appreciate the generosity of Nestlin Malaysia Sdn. Bhd. for providing financial support to this project under project vote number 76030.

Funding

Findings reported in this study are funded by Nestlin Malaysia Sdn. Bhd. under Grant agreement No. 76030.

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  1. Department of Bioscience, Faculty of Applied Sciences, Tunku Abdul Rahman University College, Setapak, 53300, Kuala Lumpur, Malaysia

    Chin Huan Ng, Pei Ling Tang & Yien Yien Ong

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Contributions

Study conception and design were contributed by PLT and YYO. Material preparation, data collection and analysis were performed by PLT. The first draft of the manuscript was written by PLT and CHN. Second review and editing were carried out by YYO. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Pei Ling Tang.

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Ng, C.H., Tang, P.L. & Ong, Y.Y. Enzymatic hydrolysis improves digestibility of edible bird’s nest (EBN): combined effect of pretreatment and enzyme. Food Measure 17, 549–563 (2023). https://doi.org/10.1007/s11694-022-01648-z

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