A one-step in vitro continuous flow assessment of protein release from core-shell polymer microcapsules designed for therapeutic protein delivery

• Autorzy: Kupikowska-Stobba Barbara , Grzeczkowicz Marcin , Lewińska Dorota

Identyfikatory

DOI

10.1016/j.bbe.2021.05.003

• Języki publikacji: EN

Abstrakty

EN

Developing accurate methods for the assessment of therapeutic protein release from polymer drug delivery systems (microcapsules, microspheres, nanoparticles, 3D-printed systems) is of paramount importance for new formulation development. The most straightforward method for protein release assessment is spectrophotometric analysis of the release medium surrounding the formulation. However, direct spectrophotometric analysis is inapplicable to formulations releasing interfering compounds (coencapsulated drugs, additives) absorbing light in the same spectrum as proteins. Conventional protein release assays also require frequent release medium sampling and replacement, which reduces their accuracy. We propose a one-step method to assess protein release from core/shell microcapsules eliminating the need for sampling and allowing selective real-time protein quantitation in the release medium. To prevent spectral interferences, released protein is differentiated from interfering compounds by employing a colorimetric protein assay reagent, forming a colour complex selectively with the protein, as the release medium. To eliminate sampling, we employed a continuous flow closed loop set-up, where the release medium is constantly circulating between microcapsule-containing tank and spectrophotometer. A series of colorimetric protein assay reagents (bromocresol green, tetrabromophenol blue, eosin B, eosin Y, biuret) were evaluated in terms of their applicability as the release medium in described system. Only biuret reagent was found compatible with proposed method due to formation of color complex stable over extended period of time and low adsorption to microcapsules. Presented method allowed effective evaluation of albumin release from alginate-polyethersulfone microcapsules with accuracy equal to conventional ‘sample and separate’ technique. Albumin release followed first-order kinetics with plateau reached after 19 h.

Słowa kluczowe

EN

protein release; core shell microcapsule; continuous flow apparatus; colorimetric protein assay; mass transfer coefficient; albumin

PL

uwalnianie białka; współczynnik wnikania masy; albumina

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2021
• Tom: Vol. 41, no. 4
• Strony: 1347--1364
• Opis fizyczny: Bibliogr. 90 poz., rys., tab., wykr.

Twórcy

autor

Kupikowska-Stobba Barbara

• Laboratory of Electrostatic Methods of Bioencapsulation, Department of Biomaterials and Biotechnological Systems, Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland

autor

Grzeczkowicz Marcin

• Laboratory of Electrostatic Methods of Bioencapsulation, Department of Biomaterials and Biotechnological Systems, Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland

autor

Lewińska Dorota

• Laboratory of Electrostatic Methods of Bioencapsulation, Department of Biomaterials and Biotechnological Systems, Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Ks. Trojdena 4 St., 02-109 Warsaw, Poland

Bibliografia

• [1] Lyseng-Williamson KA. Elosulfase alfa: A review of its use in patients with mucopolysaccharidosis type IVA (Morquio A Syndrome). BioDrugs 2014;28(5):465–75. https://doi.org/ 10.1007/s40259-014-0108-z.
• [2] Landgraf W, Sandow J. Recombinant human insulins-clinical efficacy and safety in diabetes therapy. Eur Endocrinol 2016;12:12–7. https://doi.org/10.17925/EE.2016.12.01.12.
• [3] Morfini M, Coppola A, Franchini M, Di Minno G. Clinical use of factor VIII and factor IX concentrates. Blood Transfus 2013;11 (Suppl 4):55–63. https://doi.org/10.2450/2013.010s.
• [4] Mumcuoglu D, Siverino C, Tabisz B, Kluijtmans B, Nickel J. How to use BMP-2 for clinical applications? A review on pros and cons of existing delivery strategies. J Transl Sci 2017;3:1–11. https://doi.org/10.15761/jts.1000195.
• [5] Berraondo P, Sanmamed MF, Ochoa MC, Etxeberria I, Aznar MA, Pérez-Gracia JL, et al. Cytokines in clinical cancer immunotherapy. Br J Cancer 2019;120(1):6–15. https://doi.org/10.1038/s41416-018-0328-y.
• [6] Ghagane SC, Puranik SI, Gan SH, Hiremath MB, Nerli RB, Ravishankar MV. Frontiers of monoclonal antibodies: Applications in medical practices. Hum Antibodies 2018;26(3):135–42. https://doi.org/10.3233/HAB-170331.
• [7] Coats S, Williams M, Kebble B, Dixit R, Tseng L, Yao N-S, et al. Antibody-drug conjugates: Future directions in clinical and translational strategies to improve the therapeutic index. Clin Cancer Res 2019;25(18):5441–8. https://doi.org/10.1158/1078-0432.CCR-19-0272.
• [8] Jafari R, Zolbanin NM, Rafatpanah H, Majidi J, Kazemi T. Fc-fusion proteins in therapy: an updated view. Curr Med Chem 2017;24:1228–37. https://doi.org/10.2174/0929867324666170113112759.
• [9] Kintzing JR, Filsinger Interrante MV, Cochran JR. Emerging strategies for developing next-generation protein therapeutics for cancer treatment. Trends Pharmacol Sci 2016;37(12):993–1008. https://doi.org/10.1016/j.tips.2016.10.005.
• [10] Onwumeh J, Okwundu CI, Kredo T. Interleukin-2 as an adjunct to antiretroviral therapy for HIV-positive adults Art. No.: CD009818. Cochrane Database Syst Rev 2017;2017. https://doi.org/10.1002/14651858.CD009818.pub2.
• [11] Zhao L, Zhao Z, Chen X, Li J, Liu J, Li G. Safety and efficacy of prourokinase injection in patients with ST-elevation myocardial infarction: phase IV clinical trials of the prourokinase phase study. Heart Vessels 2018;33(5):507–12. https://doi.org/10.1007/s00380-017-1097-x.
• [12] Dinh ND, Kukumberg M, Nguyen AT, Keramati H, Guo S, Phan DT, et al. Functional reservoir microcapsules generated: via microfluidic fabrication for long-term cardiovascular therapeutics. Lab Chip 2020;20(15):2756–64. https://doi.org/10.1039/D0LC00296H.
• [13] Wang X, You S, Sato S, Yang J, Carcel C, Zheng D, et al. Current status of intravenous tissue plasminogen activator dosage for acute ischaemic stroke: An updated systematic review. Stroke Vasc Neurol 2018;3(1):28–33. https://doi.org/10.1136/svn-2017-00011210.1136/svn-2017-000112.supp1.
• [14] Sfikakis PP, Boletis JN, Tsokos GC. Rituximab anti-B-cell therapy in systemic lupus erythematosus: pointing to the future. Curr Opin Rheumatol 2005;17(5):550–7. https://doi.org/10.1097/01.bor.0000172798.26249.fc.
• [15] Vugmeyster Y, Xu X, Theil FP, Khawli LA, Leach MW. Pharmacokinetics and toxicology of therapeutic proteins: Advances and challenges. World J Biol Chem 2012;3:73–92. https://doi.org/10.4331/wjbc.v3.i4.73.
• [16] Kim BS, Oh JM, Kim KS, Seo KS, Cho JS, Khang G, et al. BSAFITC-loaded microcapsules for in vivo delivery. Biomaterials 2009;30(5):902–9. https://doi.org/10.1016/j.biomaterials.2008.10.030.
• [17] Yang Y, Opara EC, Liu Y, Atala A, ZhaoW. Microencapsulation of porcine thyroid cell organoids within a polymer microcapsule construct. Exp Biol Med (Maywood) 2017;242(3):286–96. https://doi.org/10.1177/1535370216673746.
• [18] Kupikowska-Stobba B, Lewińska D. Polymer microcapsules and microbeads as cell carriers for in vivo biomedical applications. Biomater Sci 2020;8(6):1536–74. https://doi.org/10.1039/C9BM01337G.
• [19] de Vos P, Bučko M, Gemeiner P, Navrátil M, Švitel J, Faas M, et al. Multiscale requirements for bioencapsulation in medicine and biotechnology. Biomaterials 2009;30(13):2559–70. https://doi.org/10.1016/j.biomaterials.2009.01.014.
• [20] Lagranha VL, Martinelli BZ, Baldo G, Testa GÁ, de Carvalho TG, Giugliani R, et al. Subcutaneous implantation of microencapsulated cells overexpressing α-L-iduronidase for mucopolysaccharidosis type I treatment. J Mater Sci Mater Med 2017;28:43. https://doi.org/10.1007/s10856-017-5844-4.
• [21] Zhi Z-l, Kerby A, King AJF, Jones PM, Pickup JC. Nano-scale encapsulation enhances allograft survival and function of islets transplanted in a mouse model of diabetes. Diabetologia 2012;55(4):1081–90. https://doi.org/10.1007/s00125-011-2431-y.
• [22] An D, Ma M. Robust, nanofiber-enabled hydrogel devices for islet encapsulation and delivery. In: Front. Bioeng. Biotechnol. Conf. Abstr. 10th World Biomater. Congr.. Frontiers Media SA; 2016. https://doi.org/10.3389/conf.fbioe.2016.01.02609.
• [23] Płończak M, Czubak J, Chwojnowski A, Kupikowska-Stobba B. Culture of human autologous chondrocytes on polysulphonic membrane - Preliminary studies. Biocybern Biomed Eng 2012;32(3):63–7.
• [24] Kim J, Shim IK, Hwang DG, Lee YN, Kim M, Kim H, et al. 3D cell printing of islet-laden pancreatic tissue-derived extracellular matrix bioink constructs for enhancing pancreatic functions. J Mater Chem B 2019;7(10):1773–81. https://doi.org/10.1039/C8TB02787K.
• [25] Saenz del Burgo L, Ciriza J, Espona-Noguera A, Illa X, Cabruja E, Orive G, et al. 3D Printed porous polyamide macrocapsule combined with alginate microcapsules for safer cell-based therapies. Sci Rep 2018;8(1):8512. https://doi.org/10.1038/s41598-018-26869-5.
• [26] Ashimova A, Yegorov S, Negmetzhanov B, Hortelano G. Cell Encapsulation Within Alginate Microcapsules: Immunological Challenges and Outlook. Front Bioeng Biotechnol 2019;7:380. https://doi.org/10.3389/fbioe.2019.00380.
• [27] Alvarado Y, Muro C, Illescas J, Díaz M del C, Riera F. Encapsulation of antihypertensive peptides from whey proteins and their releasing in gastrointestinal conditions. Biomolecules 2019;9(5):164. https://doi.org/10.3390/biom9050164.
• [28] Orive G, Santos E, Pedraz JL, Hernández RM. Application of cell encapsulation for controlled delivery of biological therapeutics. Adv Drug Deliv Rev 2014;67–68:3–14. https://doi.org/10.1016/j.addr.2013.07.009.
• [29] Liu Z, Hu W, He T, Dai Y, Hara H, Bottino R, et al. Pig-to-primate islet xenotransplantation: past, present, and future. Cell Transplant 2017;26(6):925–47. https://doi.org/10.3727/096368917X694859.
• [30] Read JE, Luo D, Chowdhury TT, Flower RJ, Poston RN, Sukhorukov GB, et al. Magnetically responsive layer-by-layer microcapsules can be retained in cells and under flow conditions to promote local drug release without triggering ROS production. Nanoscale 2020;12(14):7735–48. https://doi.org/10.1039/C9NR10329E.
• [31] Hajifathaliha F, Mahboubi A, Nematollahi L, Mohit E, Bolourchian N. Comparison of different cationic polymers efficacy in fabrication of alginate multilayer microcapsules. Asian J Pharm Sci 2020;15(1):95–103. https://doi.org/10.1016/j.ajps.2018.11.007.
• [32] Tsirigotis-Maniecka M, Szyk-Warszyńska L, Michna A, Warszyński P, Wilk KA. Colloidal characteristics and functionality of rationally designed esculin-loaded hydrogel microcapsules. J Colloid Interface Sci 2018;530:444–58. https://doi.org/10.1016/j.jcis.2018.07.006.
• [33] Feng C, Song R, Sun G, Kong M, Bao Z, Li Y, et al. Immobilization of coacervate microcapsules in multilayer sodium alginate beads for efficient oral anticancer drug delivery. Biomacromolecules 2014;15(3):985–96. https://doi.org/10.1021/bm401890x.
• [34] Kupikowska B, Lewińska D, Dudziński K, Jankowska-Śliwińska J, Grzeczkowicz M, Wojciechowski C, et al. Influence of changes in composition of the membrane-forming solution on the structure of alginate-polyethersulfone microcapsules. Biocybern Biomed Eng 2009;29(3):61–9. http://www.ibib.waw.pl/images/ibib/grupy/Wydawnictwa-Tomy/dokumenty/2009/BBE_29_3_061_FT.pdf.
• [35] Wei Yi, Wu Y, Wen K, Bazybek N, Ma G. Recent research and development of local anesthetic-loaded microspheres. J Mater Chem B 2020;8(30):6322–32. https://doi.org/10.1039/D0TB01129K.
• [36] Xia Y, Na X, Wu J, Ma G. The Horizon of the Emulsion Particulate Strategy: Engineering Hollow Particles for Biomedical Applications. Adv Mater 2019;31(38):1801159. https://doi.org/10.1002/adma.v31.3810.1002/adma.201801159.
• [37] Baek JS, Yeo EW, Lee YH, Tan NS, Loo SCJ. Controlled-release nanoencapsulating microcapsules to combat inflammatory diseases. Drug Des Devel Ther 2017;11:1707–17. https://doi.org/10.2147/DDDT.S133344.
• [38] Long Y, Liu C, Zhao B, Song K, Yang G, Tung CH. Bio-inspired controlled release through compression-relaxation cycles of microcapsules. NPG Asia Mater 2015;7. https://doi.org/10.1038/am.2014.114.
• [39] Pisani S, Dorati R, Genta I, Chiesa E, Modena T, Conti B. High efficiency vibrational technology (HEVT) for cell encapsulation in polymeric microcapsules. Pharmaceutics 2020;12(5):469. https://doi.org/10.3390/pharmaceutics12050469.
• [40] Verheyen CA, Morales L, Sussman J, Paunovska K, Manzoli V, Ziebarth NM, et al. Characterization of polyethylene glycol-reinforced alginate microcapsules for mechanically stable cell immunoisolation. Macromol Mater Eng 2019;304(4):1800679. https://doi.org/10.1002/mame.v304.410.1002/mame.201800679.
• [41] Nemati S, Alizadeh Sardroud H, Baradar Khoshfetrat A, Khaksar M, Ahmadi M, Amini H, et al. The effect of alginate-gelatin encapsulation on the maturation of human myelomonocytic cell line U937. J Tissue Eng Regen Med 2019;13(1):25–35. https://doi.org/10.1002/term.v13.110.1002/term.2765.
• [42] Lewińska D, Grzeczkowicz M, Kupikowska-Stobba B. Influence of electric parameters on the alginate-polyethersulfone microcapsule structure. Desalin Water Treat 2017;64:400–8. https://doi.org/10.5004/dwt.2017.11407.
• [43] Mohanraj B, Duan G, Peredo A, Kim M, Tu F, Lee D, et al. Mechanically activated microcapsules for ‘‘on-demand” drug delivery in dynamically loaded musculoskeletal tissues. Adv Funct Mater 2019;29(15):1807909. https://doi.org/10.1002/adfm.v29.1510.1002/adfm.201807909.
• [44] Esser-Kahn AP, Odom SA, Sottos NR, White SR, Moore JS. Triggered release from polymer capsules. Macromolecules 2011;44(14):5539–53. https://doi.org/10.1021/ma201014n.
• [45] Zernov AL, Ivanov EA, Makhina TK, Myshkina VL, Samsonova OV, Feofanov AV, et al. Microcapsules of poly(3-hydroxybutyrate) for sustained protein release. Sovrem Tehnol v Med 2015;7:50–6. https://doi.org/10.17691/stm2015.7.4.06.
• [46] Vandenberg GW, De La Noüe J. Evaluation of protein release from chitosan-aginate microcapsules produced using external or internal gelation. J Microencapsul 2001;18:433–41. https://doi.org/10.1080/02652040010019578.
• [47] Polk A, Amsden B, De Yao K, Peng T, Goosen MFA. Controlled release of albumin from chitosan-alginate microcapsules. J Pharm Sci 1994;83(2):178–85. https://doi.org/10.1002/jps.2600830213.
• [48] D’Souza SS, DeLuca PP. Methods to assess in vitro drug release from injectable polymeric particulate systems. Pharm Res 2006;23(3):460–74. https://doi.org/10.1007/s11095-005-9397-8.
• [49] Cipolla D, Wu H, Eastman S, Redelmeier T, Gonda I, Chan HK. Development and characterization of an in vitro release assay for liposomal ciprofloxacin for inhalation. J Pharm Sci 2014;103(1):314–27. https://doi.org/10.1002/jps.23795.
• [50] Voisine JM, Zolnik BS, Burgess DJ. In situ fiber optic method for long-term in vitro release testing of microspheres. Int J Pharm 2008;356(1-2):206–11. https://doi.org/10.1016/j.ijpharm.2008.01.017.
• [51] Zolnik BS, Raton JL, Burgess DJ. Application of USP apparatus 4 and in situ fiber optic analysis to microsphere release testing. Dissolution Technol 2005;12:11–4. https://doi.org/10.14227/DT120205P11.
• [52] David B, Doré E, Jaffrin MY, Legallais C. Mass transfers in a fluidized bed bioreactor using alginate beads for a future bioartificial liver. Int J Artif Organs 2004;27(4):284–93. https://doi.org/10.1177/039139880402700404.
• [53] D’Souza S. A review of in vitro drug release test methods for nano-sized dosage forms. Adv Pharm 2014;2014:1–12. https://doi.org/10.1155/2014/304757.
• [54] Tomic I, Vidis-Millward A, Mueller-Zsigmondy M, Cardot J-M. Setting accelerated dissolution test for PLGA microspheres containing peptide, investigation of critical parameters affecting drug release rate and mechanism. Int J Pharm 2016;505(1-2):42–51. https://doi.org/10.1016/j.ijpharm.2016.03.048.
• [55] Berkland C, Pollauf E, Raman C, Silverman R, Kim K, Pack DW. Macromolecule release from monodisperse PLG microspheres: Control of release rates and investigation of release mechanism. J Pharm Sci 2007;96(5):1176–91. https://doi.org/10.1002/jps.20948.
• [56] Musin EV, Kim AL, Tikhonenko SA. Destruction of polyelectrolyte microcapsules formed on CaCO3 microparticles and the release of a protein included by the adsorption method. Polymers (Basel) 2020;12(3):520. https://doi.org/10.3390/polym12030520.
• [57] She Z, Antipina MN, Li J, Sukhorukov GB. Mechanism of protein release from polyelectrolyte multilayer microcapsules. Biomacromolecules 2010;11(5):1241–7. https://doi.org/10.1021/bm901450r.
• [58] Formiga FR, Pelacho B, Garbayo E, Abizanda G, Gavira JJ, Simon-Yarza T, et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia-reperfusion model. J Control Release 2010;147(1):30–7. https://doi.org/10.1016/j.jconrel.2010.07.097.
• [59] Rasanayagam LJ, Lim KL, Beng CG, Lau KS. Measurement of urine albumin using bromocresol green. Clin Chim Acta 1973;44(1):53–7. https://doi.org/10.1016/0009-8981(73)90159-9.
• [60] Delanghe S, Van Biesen W, Van De Velde N, Eloot S, Pletinck A, Schepers E, et al. Binding of bromocresol green and bromocresol purple to albumin in hemodialysis patients. Clin Chem Lab Med 2018;56:436–40. https://doi.org/10.1515/cclm-2017-0444.
• [61] Wei Y, Li K, Tong S. The interaction of Bromophenol Blue with proteins in acidic solution. Talanta 1996;43(1):1–10. https://doi.org/10.1016/0039-9140(95)01683-X.
• [62] Waheed AA, Gupta PD. Application of an eosin B dye method for estimating a wide range of proteins. J Biochem Biophys Methods 1996;33(3):187–96. https://doi.org/10.1016/S0165-022X(96)00025-5.
• [63] Waheed AA, Gupta PD. Estimation of protein using eosin B dye. Anal Biochem 1996;233(2):249–52. https://doi.org/10.1006/abio.1996.0037.
• [64] Waheed AA, Gupta PD. Estimation of submicrogram quantities of protein using the dye eosin Y. J Biochem Biophys Methods 2000;42(3):125–32. https://doi.org/10.1016/S0165-022X(99)00055-X.
• [65] Xi X, Ye T, Wang S, Na X, Wang J, Qing S, et al. Self-healing microcapsules synergetically modulate immunization microenvironments for potent cancer vaccination. Sci Adv 2020;6(21):eaay7735. https://doi.org/10.1126/sciadv.aay7735.
• [66] Fine J. The biuret method of estimating albumin and globulin in serum and urine. Biochem J 1935;29:799–803. https://doi.org/10.1042/bj0290799.
• [67] Janairo G, Linley MS, Yap L, Llanos-Lazaro N, Robles J. Determination of the sensitivity range of biuret test for undergraduate biochemistry experiments. E -Journal Sci Technol 2015;5:77–83.
• [68] Bhatti MK, Hayat MM, Nasim F-U-H, Nasir R, Ashraf M, Hussain B, et al. Development and validation of spectrophotometric method for the determination of nimesulide in bulk and tablet dosage forms by biuret reagent method. J Chem Soc Pakistan 2012;34:713–6.
• [69] Zheng K, Wu L, He Z, Yang B, Yang Y. Measurement of the total protein in serum by biuret method with uncertainty evaluation. Meas J Int Meas Confed 2017;112:16–21. https://doi.org/10.1016/j.measurement.2017.08.013.
• [70] Alanezi AA, Neau SH, D’mello AP. Development and application of a modified method to determine the encapsulation efficiency of proteins in polymer matrices. AAPS PharmSciTech 2020;21(7):248. https://doi.org/10.1208/s12249-020-01789-8.
• [71] Lewińska D, Chwojnowski A, Wojciechowski C, Kupikowska-Stobba B, Grzeczkowicz M, Weryński† A. Electrostatic droplet generator with 3-coaxial-nozzle head for microencapsulation of living cells in hydrogel covered by synthetic polymer membranes. Sep Sci Technol 2012;47(3):463–9. https://doi.org/10.1080/01496395.2011.617350.
• [72] Przytulska M, Kulikowski JL, Lewińska D, Grzeczkowicz M, Kupikowska-Stobba B. Computer-aided image analysis for microcapsules’ quality assessment. Biocybern Biomed Eng 2015;35(4):342–50. https://doi.org/10.1016/j.bbe.2015.05.005.
• [73] Grzeczkowicz M, Lewińska D. A method for investigating transport properties of partly biodegradable spherical membranes using vitamin B12 as the marker. Desalin Water Treat 2018;128:170–8. https://doi.org/10.5004/dwt.2018.22631.
• [74] Lewińska D, Rosiński S, Hunkeler D, Poncelet D, Weryński A. Mass transfer coefficient in characterization of gel beads and microcapsules. J Memb Sci 2002;209(2):533–40. https://doi.org/10.1016/S0376-7388(02)00370-8.
• [75] Takada S, Yamagata Y, Misaki M, Taira K, Kurokawa T. Sustained release of human growth hormone from microcapsules prepared by a solvent evaporation technique. J Control Release 2003;88(2):229–42. https://doi.org/10.1016/S0168-3659(02)00494-7.
• [76] Rhee YS, Sohn M, Woo BH, Thanoo BC,DeLuca PP, Mansour HM. Sustained-release delivery of octreotide from biodegradable polymeric microspheres. AAPS PharmSciTech 2011;12(4):1293–301. https://doi.org/10.1208/s12249-011-9693-z.
• [77] Rawat A, Burgess DJ. USP apparatus 4 method for in vitro release testing of protein loaded microspheres. Int J Pharm 2011;409(1-2):178–84. https://doi.org/10.1016/j.ijpharm.2011.02.057.
• [78] Cao WG, Jiao QC, Fu Y, Chen L, Liu Q. Mechanism of the interaction between Bromophenol Blue and Bovine Serum Albumin. Spectrosc Lett 2003;36(3):197–209. https://doi.org/10.1081/SL-120024351.
• [79] Krohn RI. The colorimetric detection and quantitation of total protein. Handb Food Anal Chem 2005;1–2:77–104. https://doi.org/10.1002/0471709085.ch3.
• [80] Liu D, Yuan J, Li J, Zhang G. Preparation of chitosan poly (methacrylate) composites for adsorption of bromocresol green. ACS Omega 2019;4(7):12680–6. https://doi.org/10.1021/acsomega.9b01576.
• [81] Homaeigohar S. The nanosized dye adsorbents for water treatment. Nanomaterials 2020;10(2):295. https://doi.org/10.3390/nano10020295.
• [82] Elvers B, editor. Ullmann’s Encyclopedia of Industrial Chemistry. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA; 2000. https://doi.org/10.1002/14356007.a21_449.
• [83] Rosiński S, Lewińska D,Wójcik M, Orive G, Pedraz J, Weryński A. Mass transfer characteristics of poly-lysine, poly-ornithine and poly-methylene-co-guanidine membrane coated alginate microcapsules. J Memb Sci 2005;254(1-2):249–57. https://doi.org/10.1016/j.memsci.2004.12.046.
• [84] Yang Y-Y, Chia H-H, Chung T-S. Effect of preparation temperature on the characteristics and release profiles of PLGA microspheres containing protein fabricated by double-emulsion solvent extraction/evaporation method. J Control Release 2000;69(1):81–96. https://doi.org/10.1016/S0168-3659(00)00291-1.
• [85] Habibi S, Rabiller-Baudry M, Lopes F, Bellet F, Goyeau B, Rakib M, et al. New insights into the structure of membrane fouling by biomolecules using comparison with isotherms and ATRFTIR local quantification. Environ Technol (United Kingdom) 2020:1–18. https://doi.org/10.1080/09593330.2020.1783370.
• [86] Akamatsu K, Kagami Y, Nakao S-I. Effect of BSA and sodium alginate adsorption on decline of filtrate flux through polyethylene microfiltration membranes. J Memb Sci 2020;594:117469. https://doi.org/10.1016/j.memsci.2019.117469.
• [87] Mahdavinia GR, Mousanezhad S, Hosseinzadeh H, Darvishi F, Sabzi M. Magnetic hydrogel beads based on PVA/sodium alginate/laponite RD and studying their BSA adsorption. Carbohydr Polym 2016;147:379–91. https://doi.org/10.1016/j.carbpol.2016.04.024.
• [88] Guillaume YC, Guinchard C, Robert JF, Berthelot A. Ionic binding of human serum albumin - Dependence on pH and ionic strength: A chromatographic approach. Chromatographia 2000;52(9-10):575–8. https://doi.org/10.1007/BF02789753.
• [89] Fogh-Andersen N, Bjerrum PJ, Siggaard-Andersen O. Ionic binding, net charge, and Donnan effect of human serum albumin as a function of pH. Clin Chem 1993;39:48–52. https://doi.org/10.1093/clinchem/39.1.48.
• [90] Araya S, Kobayashi M. Protein denaturation and biuret reaction. J Biochem 1951;38(1):7–18. https://doi.org/10.1093/oxfordjournals.jbchem.a126227.