Abstract
Currently, one of the fastest growing industries in the world is the poultry industry; however, the increase in demand has generated the production of various byproducts, such as bones, and these byproducts have a negative impact on the environment. The aim of the present work was to evaluate the effect of glycation on the increase in antioxidant compounds and the formation of indicators of advanced glycation end products (AGE) in chicken bone hydrolysates; it also aimed to maximize the protein content, degree of hydrolysis and antioxidant content. Through analysis of variance, the content of AGE products (HMF and furfural) formed in the glycation process was analyzed. The chicken bone hydrolysate had a protein content of 1.42 g/l, a degree of hydrolysis of 17.2% and an antioxidant capacity of 8334 and 10,343 μmol ETrolox/l according to ABTS and ORAC evaluations, respectively. The glycation process increased the ORAC by 6.57%. The presence of hydroxymethylfurfural and furfural was determined in the glycated samples and detected at values between 0.05 and 0.22 and 0 and 0.26 ppm, respectively. In conclusion, hydrolysis and glycation are suitable alternatives that enable the use of chicken bones in producing food ingredients with higher added value.
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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
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The data were analyzed with Statgraphics Centurion XVI version 16.1.03 software.
References
Latin American Chicken Institute: Global chicken meat production.: 2000–2018. https://ilp-ala.org/producion-mundial-de-carne-de-pollo-2000-2018/#horizontalTab-5205 (2018). Accessed 04 February 2021
FAO.: World agriculture: towards 2015/2030: an FAO perspective. Earthscan, London (2003)
Martínez-Alvarez, O., Chamorro, S., Brenes, A.: Protein hydrolysates from animal processing by-products as a source of bioactive molecules with interest in animal feeding: a review. Food Res. Int. (2015). https://doi.org/10.1016/j.foodres.2015.04.005
Nascimento, C.D., Filho, R.A., Artur, A.G., Costa, M.: Application of poultry processing industry waste: a strategy for vegetation growth in degraded soil. Waste Manage. (2015). https://doi.org/10.1016/j.wasman.2014.11.001
Ferreira, A., Kunh, S.S., Cremonez, P.A., Dieter, J., Teleken, J.G., Sampaio, S.C., Kunh, P.D.: Brazilian poultry activity waste: Destinations and energetic potential. Renew. Sustain. Energy Rev. (2018). https://doi.org/10.1016/j.rser.2017.08.078
FIRA.: Agri-food panorama. Chicken meat 2019. https://www.inforural.com.mx/wp-content/uploads/2019/09/Panorama-Agroalimentario-Carne-de-pollo-2019.pdf (2019). Accessed 04 Feb 2021
FENAVI.: Report FENAVIQUÍN: Economic Studies Program-Fenavi-Fonav. https://www.solla.com/sites/default/files/productos/secciones/adjuntos/Fenaviquin_ed-295-oct-15-2019.pdf (2019). Accessed 04 Feb 2021
Özünlü, O., Ergezer, H., Gökçe, R.: Improving physicochemical, antioxidative and sensory quality of raw chicken meat by using acorn extracts. LWT Food Sci. Technol. (2018). https://doi.org/10.1016/j.lwt.2018.09.007
Dalle Zotte, A., Ricci, R., Cullere, M., Serva, L., Tenti, S., Marchesini, G.: Research note: effect of chicken genotype and white striping-wooden breast condition on breast meat proximate composition and amino acid profile. Poult. Sci. (2020). https://doi.org/10.1016/j.psj.2019.10.066
Kim, H.-J., Kim, H.-J., Jeon, J.J., Nam, K.-C., Shim, K.-S., Jung, J.-H., Kim, K., Choi, Y., Kim, S.-H., Jang, A.: Comparison of the quality characteristics of chicken breast meat from conventional and animal welfare farms under refrigerated storage. Poult. Sci. (2020). https://doi.org/10.1016/j.psj.2019.12.009
Kralik, G., Kralik, Z., Grčević, M., Hanžek, D.: Quality of chicken meat. In: Yücel, B., Taşkin, T. (eds.) Animal Husbandry and Nutrition. IntechOpen, London (2018)
Mehdizadeh, T., Langroodi, A.M.: Chitosan coatings incorporated with propolis extract and Zataria multiflora Boiss oil for active packaging of chicken breast meat. Int. J. Biol. Macromol. (2019). https://doi.org/10.1016/j.ijbiomac.2019.08.267
Brandelli, A., Sala, L., Juliano, S.: Microbial enzymes for bioconversion of poultry waste into added-value products. Food Res. Int. (2015). https://doi.org/10.1016/j.foodres.2015.01.015
Ding, G., Li, S., Wang, A., Chen, N.: Effect of chicken haemoglobin powder on growth, feed utilization, immunity and haematological index of largemouth bass (Micropterus salmoides). Aquacult. Fish. (2019). https://doi.org/10.1016/j.aaf.2019.04.003
Xia, Y., Wang, D.K., Kong, Y., Ungerfeld, E.M., Seviour, R., Massé, D.I.: Anaerobic digestibility of beef hooves with swine manure or slaughterhouse sludge. Waste Manage. (2015). https://doi.org/10.1016/j.wasman.2014.12.017
AlSharifi, M., Znad, H.: Development of a lithium based chicken bone (Li-Cb) composite as an efficient catalyst for biodiesel production. Renew. Energy (2019). https://doi.org/10.1016/j.renene.2019.01.052
Wang, J.Z., Dong, X.B., Yue, J.Y., Zhang, C.H., Jia, W., Li, X.: Preparation of substrate for flavorant from chicken bone residue with hot-pressure process. J. Food Sci. (2016). https://doi.org/10.1111/1750-3841.13211
Lasekan, A., Abu, F., Hashim, D.: Potential of chicken by-products as sources of useful biological resources. Waste Manage. (2013). https://doi.org/10.1016/j.wasman.2012.08.001
Dong, Z.Y., Li, M.Y., Tian, G., Zhang, T.H., Ren, H., Quek, S.Y.: Effects of ultrasonic pretreatment on the structure and functionality of chicken bone protein prepared by enzymatic method. Food Chem. (2019). https://doi.org/10.1016/j.foodchem.2019.125103
Karami, Z., Peighambardoust, S.H., Hesari, J., Akbari-Adergani, B., Andreu, D.: Antioxidant, anticancer and ACE-inhibitory activities of bioactive peptides from wheat germ protein hydrolysates. Food Biosci. (2019). https://doi.org/10.1016/j.fbio.2019.100450
Zheng, Z., Li, J., Li, J., Sun, H., Liu, Y.: Physicochemical and antioxidative characteristics of black bean protein hydrolysates obtained from different enzymes. Food Hydrocoll. (2019). https://doi.org/10.1016/j.foodhyd.2019.105222
Khiari, Z., Ndagijimana, M., Betti, M.: Low molecular weight bioactive peptides derived from the enzymatic hydrolysis of collagen after isoelectric solubilization/precipitation process of turkey by-products. Poult. Sci. (2014). https://doi.org/10.3382/ps.2014-03953
Neves, A.C., Harnedy, P.A., O’Keeffe, M.B., Alashi, M.A., Aluko, R.E., FitzGerald, R.J.: Peptide identification in a salmon gelatin hydrolysate with antihypertensive, dipeptidyl peptidase IV inhibitory and antioxidant activities. Food Res. Int. (2017). https://doi.org/10.1016/j.foodres.2017.06.065
Zheng, Z., Si, D., Ahmad, B., Li, Z., Zhang, R.: A novel antioxidative peptide derived from chicken blood corpuscle hydrolysate. Food Res. Int. (2018). https://doi.org/10.1016/j.foodres.2017.12.078
Udenigwe, C.C., Udechukwu, M.C., Yiridoe, C., Gibson, A., Gong, M.: Antioxidant mechanism of potato protein hydrolysates against in vitro oxidation of reduced glutathione. J. Funct. Foods (2016). https://doi.org/10.1016/j.jff.2015.11.004
Sun, W., Zhao, M., Cui, C., Zhao, Q., Yang, B.: Effect of Maillard reaction products derived from the hydrolysate of mechanically deboned chicken residue on the antioxidant, textural and sensory properties of Cantonese sausages. Meat Sci. (2010). https://doi.org/10.1016/j.meatsci.2010.04.014
Siewe, F.B., Kudre, T.G., Bettadaiah, B.K., Narayan, B.: Effects of ultrasound-assisted heating on aroma profile, peptide structure, peptide molecular weight, antioxidant activities and sensory characteristics of natural fish flavouring. Ultrason. Sonochem. (2020). https://doi.org/10.1016/j.ultsonch.2020.105055
Liu, Q., Kong, B., Han, J., Sun, C., Li, P.: Structure and antioxidant activity of whey protein isolate conjugated with glucose via the Maillard reaction under dry-heating conditions. Food Struct. (2014). https://doi.org/10.1016/j.foostr.2013.11.004
Nooshkam, M., Madadlou, A.: Maillard conjugation of lactulose with potentially bioactive peptides. Food Chem. (2016). https://doi.org/10.1016/j.foodchem.2015.07.094
Han, W., Liu, Y., Xu, X., Huang, J., He, H., Chen, L., Hou, P.: Bioethanol production from waste hamburger by enzymatic hydrolysis and fermentation. J. Clean. Prod. (2020). https://doi.org/10.1016/j.jclepro.2020.121658
Novozymes.: Alcalase food grade. Product sheet. http://www.ebiosis.co.kr/Novozymes%20Product%20Sheet/Alcalase%202.4L.pdf (2002). Accessed 04 Feb 2021
Nie, X., Zhao, L., Regenstein, J.M., Xu, D., Meng, X.: Antioxidant capacity of Maillard reaction products’ fractions with different molecular weight distribution from chicken bone hydrolysate: galactose system. Int. J. Food Sci. Technol. (2017). https://doi.org/10.1111/ijfs.13445
AOAC.: Official Method of Analysis, 18th edn. AOAC, Gaithersburg, MD (2005)
Valencia, P., Pinto, M., Almonacid, S.: Identification of the key mechanisms involved in the hydrolysis of fish protein by Alcalase. Process Biochem. (2014). https://doi.org/10.1016/j.procbio.2013.11.012
Gbogouri, G., Linder, M., Fanni, J., Parmentier, M.: Influence of hydrolysis degree on the functional properties of salmon byproducts hydrolysates. J. Food Sci. (2004). https://doi.org/10.1111/j.1365-2621.2004.tb09909.x
Beaubier, S., Framboisier, X., Ioannou, I., Galet, O., Kapel, R.: Simultaneous quantification of the degree of hydrolysis, protein conversion rate and mean molar weight of peptides released in the course of enzymatic proteolysis. J. Chromatogr. B (2019). https://doi.org/10.1016/j.jchromb.2018.12.005
Samaranayaka, A.G.P.: Pacific hake (merluccius productus) fish protein hydrolysates with antioxidative properties. https://open.library.ubc.ca/cIRcle/collections/ubctheses/24/items/1.0069207 (2010). Accessed 04 Feb 2021
Khulal, U., Ghnimi, S., Stevanovic, N., Rajkovic, A., Velickovic, T.C.: Aggregability and digestibility study of fruit juice fortified camel milk powder proteins. Lwt 152, 112250 (2021). https://doi.org/10.1016/j.lwt.2021.112250
Xu, X., Qiao, Y., Shi, B., Dia, V.P.: Alcalase and bromelain hydrolysis affected physicochemical and functional properties and biological activities of legume proteins. Food Struct. 27, 100178 (2021). https://doi.org/10.1016/j.foostr.2021.100178
Li, Y., Lu, F., Luo, C., Chen, Z., Mao, J., Shoemaker, C., Zhong, F.: Functional properties of the Maillard reaction products of rice protein with sugar. Food Chem. (2009). https://doi.org/10.1016/j.foodchem.2009.03.078
Brescia, P.J.: Determination of antioxidant potential using an oxygen radical absorbance capacity (ORAC) assay with synergy TM H4. BioTek Application. https://www.biotek.com/assets/tech_resources/ORAC_App_Note.pdf (2012). Accessed 04 Feb 2021
Duarte-Correa, Y., Díaz-Osorio, A., Osorio-Arias, J., Sobral, P.J.A., Vega-Castro, O.: Development of fortified low-fat potato chips through vacuum impregnation and microwave vacuum drying. Innov. Food Sci. Emerg. Technol. (2020). https://doi.org/10.1016/j.ifset.2020.102437
Contreras-Calderón, J., Guerra-Hernández, E., García-Villanova, B.: Indicators of non-enzymatic browning in the evaluation of heat damage of ingredient proteins used in manufactured infant formulas. Eur. Food Res. Technol. (2008). https://doi.org/10.1007/s00217-007-0700-2
Gómez-Narváez, F., Contreras-Calderón, J., Pérez-Martínez, L.: Usefulness of some Maillard reaction indicators for monitoring the heat damage of whey powder under conditions applicable to spray drying. Int. Dairy J. (2019). https://doi.org/10.1016/j.idairyj.2019.104553
Abilmazhinova, N., Vlahova-Vangelova, D., Dragoev, S., Abzhanova, S., Balev, D.: Optimization of the oxidative stability of horse minced meat enriched with dihydroquercetin and Vitamin C as a new functional food. Compt. Rend. Acad. Bulgare Sci. (2020). https://doi.org/10.7546/CRABS.2020.07.18
Sheibani, A., Ghaziaskar, H.S.: Pressurized fluid extraction of pistachio oil using a modified supercritical fluid extractor and factorial design for optimization. LWT Food Sci. Technol. (2008). https://doi.org/10.1016/j.lwt.2007.09.002
Silveira, S.T., Daroit, D.J., Brandelli, A.: Pigment production by Monascus purpureus in grape waste using factorial design. LWT Food Sci. Technol. (2008). https://doi.org/10.1016/j.lwt.2007.01.013
Uniyal, S., Sharma, R.K., Kondakal, V.: New insights into the biodegradation of chlorpyrifos by a novel bacterial consortium: process optimization using general factorial experimental design. Ecotoxicol. Environ. Saf. (2021). https://doi.org/10.1016/j.ecoenv.2020.111799
Spanish Foundation for the Development of Animal Nutrition. FEDNA.: Meat meal, 50/14/26. http://www.fundacionfedna.org/ingredientes_para_piensos/harina-de-carne-501426. Accessed 04 Feb 2021
ChileMink.: Ingredients for animal consumption: technical data sheet meat and bone meal. https://irp-cdn.multiscreensite.com/9a7951af/files/uploaded/Ficha%20Tecnica%20Harina%20Rev3%20sept%2015%202020.pdf (2018). Accessed 04 Feb 2021
RAMGRAS S.A.C.I.A.: Meat and bone meal specifications 40/45% proteins. http://ramgras.com.ar/es-ficha-tecnica-harina-de-carne-y-huesos.pdf. Accessed 04 Feb 2021
Protidos.: Raw materials for animal nutrition. http://dianuro.com/FICHASPROTIDOS.pdf (2017). Accessed 04 Feb 2021
Hamzeh, A., Wongngam, W., Kiatsongchai, R., Yongsawatdigul, J.: Cellular and chemical antioxidant activities of chicken blood hydrolysates as affected by in vitro gastrointestinal digestion. Poult. Sci. (2019). https://doi.org/10.3382/ps/pez283
dos Santos Aguilar, J.G., de Souza, A.K.S., de Castro, R.J.S.: Enzymatic hydrolysis of chicken viscera to obtain added-value protein hydrolysates with antioxidant and antihypertensive properties. Int. J. Pept. Res. Ther. (2020). https://doi.org/10.1007/s10989-019-09879-3
Dhakal, D., Koomsap, P., Lamichhane, A., Sadiq, M.B., Anal, A.K.: Optimization of collagen extraction from chicken feet by papain hydrolysis and synthesis of chicken feet collagen based biopolymeric fibres. Food Biosci. (2018). https://doi.org/10.1016/j.fbio.2018.03.003
Bao, Z., Zhao, Y., Wang, X., Chi, Y.J.: Effects of degree of hydrolysis (DH) on the functional properties of egg yolk hydrolysate with alcalase. J. Food Sci. Technol (2017). https://doi.org/10.1007/s13197-017-2504-0
Cumby, N., Zhong, Y., Naczk, M.: Antioxidant activity and water-holding capacity of canola protein hydrolysates. Food Chem. (2008). https://doi.org/10.1016/j.foodchem.2007.12.039
Ahn, C.B., Jeon, Y.J., Kim, Y.T., Je, J.Y.: Angiotensin i converting enzyme (ACE) inhibitory peptides from salmon byproduct protein hydrolysate by Alcalase hydrolysis. Process Biochem. (2012). https://doi.org/10.1016/j.procbio.2012.08.019
Vv, R., Ghaly, A., Brooks, M., Budge, S.: Extraction of proteins from mackerel fish processing waste using Alcalase enzyme. J. Bioprocess. Biotech. (2013). https://doi.org/10.4172/2155-9821.1000130
Gutiérrez Pulido, H., Vara Salazar, R.D.L.: Análisis y diseño de experimentos, 2nd edn., pp. 418–420. McGrawHill, México, DF (2008)
Yu, L., Sun, J., Liu, S., Bi, J., Zhang, C., Yang, Q.: Ultrasonic-assisted enzymolysis to improve the antioxidant activities of peanut (Arachin conarachin L.) antioxidant hydrolysate. Int. J. Mol. Sci. (2012). https://doi.org/10.3390/ijms13079051
Bhaskar, N., Benila, T., Radha, C., Lalitha, R.G.: Optimization of enzymatic hydrolysis of visceral waste proteins of Catla (Catla catla) for preparing protein hydrolysate using a commercial protease. Biores. Technol. (2008). https://doi.org/10.1016/j.biortech.2006.12.015
Londoño, M.B.Z., Chaparro, D., Rojano, B.A., Arbelaez, A.F.A., Betancur, L.F.R., Celis, M.E.M.: Effect of storage time on physicochemical, sensorial, and antioxidant characteristics, and composition of mango (cv. Azúcar) juice. Emirat. J. Food Agric. (2017). https://doi.org/10.9755/ejfa.2016-09-1256
Seeram, N.P., Aviram, M., Zhang, Y., Henning, S.M., Feng, L., Dreher, M., Heber, D.: Comparison of antioxidant potency of commonly consumed polyphenol-rich beverages in the United States. J. Agric. Food Chem. (2008). https://doi.org/10.1021/jf073035s
Wannenmacher, J., Cotterchio, C., Schlumberger, M., Reuber, V., Gastl, M., Becker, T.: Technological influence on sensory stability and antioxidant activity of beers measured by ORAC and FRAP. J. Sci. Food Agric. (2019). https://doi.org/10.1002/jsfa.9979
Shu, G., Zhang, B., Zhang, Q., Wan, H., Li, H.: Effect of temperature, pH, enzyme to substrate ratio, substrate concentration and time on the antioxidative activity of hydrolysates from goat milk casein by alcalase. Acta Univ. Cibinien. Ser. E (2016). https://doi.org/10.1515/aucft-2016-0013
Dey, S.S., Dora, K.C.: Antioxidative activity of protein hydrolysate produced by alcalase hydrolysis from shrimp waste (Penaeus monodon and Penaeus indicus). J. Food Sci. Technol. (2014). https://doi.org/10.1007/s13197-011-0512-z
Zhang, Y., Olsen, K., Grossi, A., Otte, J.: Effect of pretreatment on enzymatic hydrolysis of bovine collagen and formation of ACE-inhibitory peptides. Food Chem. (2013). https://doi.org/10.1016/j.foodchem.2013.05.058
Anzani, C., Prandi, B., Tedeschi, T., Baldinelli, C., Sorlini, G., Wierenga, P.A., et al.: Degradation of collagen increases nitrogen solubilisation during enzymatic hydrolysis of fleshing meat. Waste Biomass Valoriz. (2018). https://doi.org/10.1007/s12649-017-9866-4
Yim, H.S., Chye, F.Y., Rao, V., Low, J.Y., Matanjun, P., How, S.E., Ho, C.W.: Optimization of extraction time and temperature on antioxidant activity of Schizophyllum commune aqueous extract using response surface methodology. J. Food Sci. Technol. (2013). https://doi.org/10.1007/s13197-011-0349-5
Sun, Y., Hayakawa, S., Ogawa, M., Izumori, K.: Evaluation of the site specific protein glycation and antioxidant capacity of rare sugar-protein/peptide conjugates. J. Agric. Food Chem. (2005). https://doi.org/10.1021/jf051565n
Gómez-Ruiz, J.Á., Ames, J.M., Leake, D.S.: Antioxidant activity and protective effects of green and dark coffee components against human low density lipoprotein oxidation. Eur. Food Res. Technol. (2008). https://doi.org/10.1007/s00217-007-0815-5
Gülcan, Ü., Candal Uslu, C., Mutlu, C., Arslan-Tontul, S., Erbaş, M.: Impact of inert and inhibitor baking atmosphere on HMF and acrylamide formation in bread. Food Chem. (2020). https://doi.org/10.1016/j.foodchem.2020.127434
Arribas-Lorenzo, G., Morales, F.J.: Estimation of dietary intake of 5-hydroxymethylfurfural and related substances from coffee to Spanish population. Food Chem. Toxicol. (2010). https://doi.org/10.1016/j.fct.2009.11.046
EFSA.: Opinion of the Scientific Panel on food additives, flavourings, processing aids and materials in contact with food (AFC) related to Flavouring Group Evaluation 13 (FGE.13); Furfuryl and furan derivatives with and without additional side-chain substituents. EFSA J. (2005). https://doi.org/10.2903/j.efsa.2005.215
Council Directive. Official Journal of the European Communities.: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32001L0110&from=ES (2002). Accessed 04 Feb 2021
Yuan, J.P., Chen, F.: Separation and identification of furanic compounds in fruit juices and drinks by high-performance liquid chromatography photodiode array detection. J. Agric. Food Chem. (1998). https://doi.org/10.1021/jf970894f
Theobald, A., Müller, A., Anklam, E.: Determination of 5-hydroxymethylfurfural in vinegar samples by HPLC. J. Agric. Food Chem. (1998). https://doi.org/10.1021/jf970912t
Ortu, E., Caboni, P.: Levels of 5-hydroxymethylfurfural, furfural, 2-furoic acid in sapa syrup, Marsala wine and bakery products. Int. J. Food Prop. (2018). https://doi.org/10.1080/10942912.2017.1373668
Purlis, E., Salvadori, V.O.: Modelling the browning of bread during baking. Food Res. Int. (2009). https://doi.org/10.1016/j.foodres.2009.03.007
Eskin, N.A.M., Ho, C.T., Shahidi, F.: Browning reactions in foods. Biochem. Foods (2012). https://doi.org/10.1016/B978-0-08-091809-9.00006-6
Peleteiro, S., Garrote, G., Santos, V., Parajó, J.C.: Conversion of hexoses and pentoses into furans in an ionic liquid. Afinidad 71, 202–206 (2014)
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The authors would like to thank the BIOALI (Food Biotechnology Research Group), NUTEC (Food and Nutrition Technology Research Group) and GEMCA (Drug, Cosmetic and Food Stability Group), Faculty of Pharmaceutical and Food Sciences, Universidad de Antioquia, for their support in the development of this project.
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All authors had readen and agree with the published version of the manuscript. Conceptualization, methodology, formal analysis, experimental research, writing: preparation of the original draft, Luisa Londoño, Sara Franco and Sandra Restrepo; accompaniment of the experimental phase and resources, Lina Suárez, Fáver Gómez; writing: proofreading and editing, Óscar Vega, Pedro Valencia; visualization, Helena Núñez, Ricardo Simpson.
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Londoño-Zapata, L., Franco-Cardona, S., Restrepo-Manotas, S. et al. Valorization of the By-products of Poultry Industry (Bones) by Enzymatic Hydrolysis and Glycation to Obtain Antioxidants Compounds. Waste Biomass Valor 13, 4469–4480 (2022). https://doi.org/10.1007/s12649-022-01801-1
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DOI: https://doi.org/10.1007/s12649-022-01801-1