药学学报, 2019, 54(12): 2240-2250
引用本文:
官娟, 陆伟跃, 占昌友. 血浆蛋白对脂质体体内性能的调控[J]. 药学学报, 2019, 54(12): 2240-2250.
GUAN Juan, LU Wei-yue, ZHAN Chang-you. Plasma proteins regulating in vivo performance of liposomes[J]. Acta Pharmaceutica Sinica, 2019, 54(12): 2240-2250.

血浆蛋白对脂质体体内性能的调控
官娟1,2, 陆伟跃2, 占昌友1,2
1. 复旦大学基础医学院, 上海 200032;
2. 复旦大学药学院, 智能化递药教育部和全军重点实验室, 上海 201203
摘要:
脂质体是在临床阶段应用最为广泛的纳米药物载体,进入血循环后迅速吸附血浆蛋白,其表面形成的蛋白冠可直接影响脂质体体内各项性能。深入研究脂质体自身性质、血浆蛋白组分与脂质体体内性能间相互关系,是加速新型脂质体药物临床开发和指导脂质体药物临床合理用药的必经之路。本文分别从影响脂质体蛋白冠的因素、蛋白冠对脂质体体内性能的影响和基于蛋白冠的脂质体药物设计三个方面进行综述,为脂质体药物相关研究提供参考。
关键词:    脂质体      蛋白冠      体内性能      临床转化      生物标记物     
Plasma proteins regulating in vivo performance of liposomes
GUAN Juan1,2, LU Wei-yue2, ZHAN Chang-you1,2
1. School of Basic Medical Sciences, Fudan University, Shanghai 200032, China;
2. Key Laboratory of Smart Drug Delivery, Ministry of Education and PLA, School of Pharmacy, Fudan University, Shanghai 201203, China
Abstract:
Liposomes have been widely exploited in clinics. After entry into blood stream, liposomes absorb a large number of plasma proteins to form protein corona, which severely regulates in vivo performance of liposomes. It is of high importance to study the relationships among liposome surface properties, plasma protein components and liposome in vivo performance for clinical translation. In this review, we will summarize the factors affecting liposome protein corona, the effects of protein corona on liposome performance and the rational design of liposomes, aiming to accelerate clinical translation of liposome-based therapeutics.
Key words:    liposome    protein corona    in vivo performance    clinical translation    biomarker   
收稿日期: 2019-07-30
DOI: 10.16438/j.0513-4870.2019-0611
基金项目: 国家自然科学基金资助项目(81673361,81973245);中国博士后创新人才支持计划(BX20190086);上海市科委“科技创新行动计划”(19431900300,18ZR1404800).
通讯作者: 占昌友,Tel:86-21-54237379,E-mail:cyzhan@fudan.edu.cn
Email: cyzhan@fudan.edu.cn
相关功能
PDF(1800KB) Free
打印本文
0
作者相关文章
官娟  在本刊中的所有文章
陆伟跃  在本刊中的所有文章
占昌友  在本刊中的所有文章

参考文献:
[1] Allen TM, Cullis PR. Liposomal drug delivery systems:from concept to clinical applications[J]. Adv Drug Deliv Rev, 2013, 65:36-48.
[2] Al-Jamal WT, Kostarelos K. Liposomes:from a clinically established drug delivery system to a nanoparticle platform for theranostic nanomedicine[J]. ACC Chem Res, 2011, 44:1094-1104.
[3] Bae YH, Park K. Targeted drug delivery to tumors:myths, reality and possibility[J]. J Control Release, 2011, 153:198-205.
[4] Nag OK, Yadav VR, Croft B, et al. Liposomes modified with superhydrophilic polymer linked to a nonphospholipid anchor exhibit reduced complement activation and enhanced circulation[J]. J Pharm Sci, 2015, 104:114-123.
[5] Nag OK, Awasthi V. Surface engineering of liposomes for stealth behavior[J]. Pharmaceutics, 2013, 5:542-569.
[6] Albanese A, Tang PS, Chan WC. The effect of nanoparticle size, shape, and surface chemistry on biological systems[J]. Annu Rev Biomed Eng, 2012, 14:1-16.
[7] Walkey CD, Olsen JB, Song F, et al. Protein corona fingerprin-ting predicts the cellular interaction of gold and silver nanoparticles[J]. ACS Nano, 2014, 8:2439-2455.
[8] Bigdeli A, Palchetti S, Pozzi D, et al. Exploring cellular interactions of liposomes using protein corona fingerprints and physicochemical properties[J]. ACS Nano, 2016, 10:3723-3737.
[9] Bertrand N, Grenier P, Mahmoudi M, et al. Mechanistic understanding of in vivo protein corona formation on polymeric nanoparticles and impact on pharmacokinetics[J]. Nat Commun, 2017, 8:777.
[10] Karmali PP, Simberg D. Interactions of nanoparticles with plasma proteins:implication on clearance and toxicity of drug delivery systems[J]. Expert Opin Drug Deliv, 2011, 8:343-357.
[11] Saha K, Rahimi M, Yazdani M, et al. Regulation of macrophage recognition through the interplay of nanoparticle surface functionality and protein corona[J]. ACS Nano, 2016, 10:4421-4430.
[12] Chen D, Ganesh S, Wang W, et al. Plasma protein adsorption and biological identity of systemically administered nanoparticles[J]. Nanomedicine (Lond), 2017, 12:2113-2135.
[13] Soni S, Ruhela RK, Medhi B. Nanomedicine in central nervous system (CNS) disorders:a present and future prospective[J]. Adv Pharm Bull, 2016, 6:319-335.
[14] Tenzer S, Docter D, Kuharev J, et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology[J]. Nat Nanotechnol, 2013, 8:772-781.
[15] Yang ST, Liu Y, Wang YW, et al. Biosafety and bioapplication of nanomaterials by designing protein-nanoparticle interactions[J]. Small, 2013, 9:1635-1653.
[16] Milani S, Bombelli FB, Pitek AS, et al. Reversible versus irreversible binding of transferrin to polystyrene nanoparticles:soft and hard corona[J]. ACS Nano, 2012, 6:2532-2541.
[17] Walkey CD, Chan WC. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment[J]. Chem Soc Rev, 2012, 41:2780-2799.
[18] Hadjidemetriou M, Al-Ahmady Z, Buggio M, et al. A novel scavenging tool for cancer biomarker discovery based on the blood-circulating nanoparticle protein corona[J]. Biomaterials, 2019, 188:118-129.
[19] Caracciolo G. Liposome-protein corona in a physiological environment:challenges and opportunities for targeted delivery of nanomedicines[J]. Nanomedicine, 2015, 11:543-557.
[20] Mahmoudi M, Lynch I, Ejtehadi MR, et al. Protein-nanoparticle interactions:opportunities and challenges[J]. Chem Rev, 2011, 111:5610-5637.
[21] Roser M, Fischer D, Kissel T. Surface-modified biodegradable albumin nano-and microspheres. II:effect of surface charges on in vitro phagocytosis and biodistribution in rats[J]. Eur J Pharm Biopharm, 1998, 46:255-263.
[22] Capriotti AL, Caracciolo G, Caruso G, et al. Differential analysis of "protein corona" profile adsorbed onto different nonviral gene delivery systems[J]. Anal Biochem, 2011, 419:180-189.
[23] Caracciolo G, Pozzi D, Capriotti AL, et al. Evolution of the protein corona of lipid gene vectors as a function of plasma concentration[J]. Langmuir, 2011, 27:15048-15053.
[24] Capriotti AL, Caracciolo G, Cavaliere C, et al. Do plasma proteins distinguish between liposomes of varying charge density?[J]. J Proteomics, 2012, 75:1924-1932.
[25] Capriotti AL, Caracciolo G, Caruso G, et al. Label-free quantitative analysis for studying the interactions between nanoparticles and plasma proteins[J]. Anal Bioanal Chem, 2013, 405:635-645.
[26] Capriotti AL, Caracciolo G, Cavaliere C, et al. Shotgun proteomic analytical approach for studying proteins adsorbed onto liposome surface[J]. Anal Bioanal Chem, 2011, 401:1195-1202.
[27] Caracciolo G, Pozzi D, Capriotti AL, et al. Factors determining the superior performance of lipid/DNA/protammine nanoparticles over lipoplexes[J]. J Med Chem, 2011, 54:4160-4171.
[28] Caracciolo G, Cardarelli F, Pozzi D, et al. Selective targeting capability acquired with a protein corona adsorbed on the surface of 1,2-dioleoyl-3-trimethylammonium propane/DNA nanoparticles[J]. ACS Appl Mater Interfaces, 2013, 5:13171-13179.
[29] Pozzi D, Colapicchioni V, Caracciolo G, et al. Effect of polyethyleneglycol (PEG) chain length on the bio-nano-interactions between PEGylated lipid nanoparticles and biological fluids:from nanostructure to uptake in cancer cells[J]. Nanoscale, 2014, 6:2782-2792.
[30] Senior J, Gregoriadis G. Is half-life of circulating liposomes determined by changes in their permeability?[J]. Febs Lett, 1982, 145:109-114.
[31] Damen J, Regts J, Scherphof G. Transfer and exchange of phospholipid between small unilamellar liposomes and rat plasma high density lipoproteins. Dependence on cholesterol content and phospholipid composition[J]. Biochim Biophys Acta, 1981, 665:538-545.
[32] Gabizon A, Papahadjopoulos D. Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors[J]. Proc Natl Acad Sci U S A, 1988, 85:6949-6953.
[33] Allen TM, Chonn A. Large unilamellar liposomes with low uptake into the reticuloendothelial system[J]. Febs Lett, 1987, 223:42-46.
[34] Klibanov AL, Maruyama K, Torchilin VP, et al. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes[J]. Febs Lett, 1990, 268:235-237.
[35] Xiao W, Xiong J, Zhang S, et al. Influence of ligands property and particle size of gold nanoparticles on the protein adsorption and corresponding targeting ability[J]. Int J Pharm, 2018, 538:105-111.
[36] Mahmoudi M, Abdelmonem AM, Behzadi S, et al. Temperature:the "ignored" factor at the NanoBio interface[J]. ACS Nano, 2013, 7:6555-6562.
[37] Guan J, Shen Q, Zhang Z, et al. Enhanced immunocompatibility of ligand-targeted liposomes by attenuating natural IgM absorption[J]. Nat Commun, 2018, 9:2982.
[38] Yu K, Lai BF, Foley JH, et al. Modulation of complement activation and amplification on nanoparticle surfaces by glycopolymer conformation and chemistry[J]. ACS Nano, 2014, 8:7687-7703.
[39] Vu VP, Gifford GB, Chen F, et al. Immunoglobulin deposition on biomolecule corona determines complement opsonization efficiency of preclinical and clinical nanoparticles[J]. Nat Nanotechnol, 2019, 14:260-268.
[40] Tenzer S, Docter D, Kuharev J, et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology[J]. Nat Nanotechnol, 2013, 8:772-781.
[41] Palchetti S, Colapicchioni V, Digiacomo L, et al. The protein corona of circulating PEGylated liposomes[J]. Biochim Biophys Acta, 2016, 1858:189-196.
[42] Caracciolo G, Farokhzad OC, Mahmoudi M. Biological identity of nanoparticles in vivo:clinical implications of the protein corona[J]. Trends Biotechnol, 2017, 35:257-264.
[43] Xiao W, Gao H. The impact of protein corona on the behavior and targeting capability of nanoparticle-based delivery system[J]. Int J Pharm, 2018, 552:328-339.
[44] Caputo D, Papi M, Coppola R, et al. A protein corona-enabled blood test for early cancer detection[J]. Nanoscale, 2017, 9:349-354.
[45] Robson AL, Dastoor PC, Flynn J, et al. Advantages and limitations of current imaging techniques for characterizing liposome morphology[J]. Front Pharmacol, 2018, 9:80.
[46] Rideau E, Dimova R, Schwille P, et al. Liposomes and polymersomes:a comparative review towards cell mimicking[J]. Chem Soc Rev, 2018, 47:8572-8610.
[47] Corbo C, Molinaro R, Parodi A, et al. The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery[J]. Nanomedicine, 2016, 11:81-100.
[48] Nguyen VH, Lee BJ. Protein corona:a new approach for nanomedicine design[J]. Int J Nanomedicine, 2017, 12:3137-3151.
[49] Bouwens van der Vlis TAM, Kros JM, Mustafa D, et al. The complement system in glioblastoma multiforme[J]. Acta Neuropathol Commun, 2018, 6:91.
[50] Agrahari V, Burnouf PA, Burnouf T, et al. Nanoformulation properties, characterization, and behavior in complex biological matrices:challenges and opportunities for brain-targeted drug delivery applications and enhanced translational potential[J]. Adv Drug Deliv Rev, 2019. DOI:1016/j. addr. 2019.02.008.
[51] Patel HM, Moghimi SM. Serum-mediated recognition of liposomes by phagocytic cells of the reticuloendothelial system-the concept of tissue specificity[J]. Adv Drug Deliv Rev, 1998, 32:45-60.
[52] Ingen-Housz-Oro S, Pham-Ledard A, Brice P, et al. Immediate hypersensitivity reaction to pegylated liposomal doxorubicin:management and outcome in four patients[J]. Eur J Dermatol, 2017, 27:271-274.
[53] Alekseeva AA, Moiseeva EV, Onishchenko NR, et al. Liposomal formulation of a methotrexate lipophilic prodrug:assessment in tumor cells and mouse T-cell leukemic lymphoma[J]. Int J Nanomedicine, 2017, 12:3735-3749.
[54] Jiang Z, Guan J, Qian J, et al. Peptide ligand-mediated targeted drug delivery of nanomedicines[J]. Biomater Sci, 2019, 7:461-471.
[55] Corbo C, Molinaro R, Taraballi F, et al. Effects of the protein corona on liposome-liposome and liposome-cell interactions[J]. Int J Nanomedicine, 2016, 11:3049-3063.
[56] Kelly PM, Aberg C, Polo E, et al. Mapping protein binding sites on the biomolecular corona of nanoparticles[J]. Nat Nanotechnol, 2015, 10:472-479.
[57] Al-Ahmady ZS, Hadjidemetriou M, Gubbins J, et al. Formation of protein corona in vivo affects drug release from temperature-sensitive liposomes[J]. J Control Release, 2018, 276:157-167.
[58] Oh JY, Kim HS, Palanikumar L, et al. Cloaking nanoparticles with protein corona shield for targeted drug delivery[J]. Nat Commun, 2018, 9:4548.
[59] Garcia-Alvarez R, Hadjidemetriou M, Sanchez-Iglesias A, et al. In vivo formation of protein corona on gold nanoparticles. The effect of their size and shape[J]. Nanoscale, 2018, 10:1256-1264.
[60] Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery[J]. Nat Biotechnol, 2015, 33:941-951.
[61] Yuda T, Maruyama K, Iwatsuru M. Prolongation of liposome circulation time by various derivatives of polyethyleneglycols[J]. Biol Pharm Bull, 1996, 19:1347-1351.
[62] Rodriguez PL, Harada T, Christian DA, et al. Minimal "Self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles[J]. Science, 2013, 339:971-975.
[63] Parodi A, Quattrocchi N, van de Ven AL, et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions[J]. Nat Nanotechnol, 2013, 8:61-68.
[64] Arcella A, Palchetti S, Digiacomo L, et al. Brain targeting by liposome-biomolecular corona boosts anticancer efficacy of temozolomide in glioblastoma cells[J]. ACS Chem Neurosci, 2018, 9:3166-3174.
[65] Barran-Berdon AL, Pozzi D, Caracciolo G, et al. Time evolution of nanoparticle-protein corona in human plasma:relevance for targeted drug delivery[J]. Langmuir, 2013, 29:6485-6494.
[66] Surinova S, Schiess R, Huttenhain R, et al. On the development of plasma protein biomarkers[J]. J Proteome Res, 2011, 10:5-16.
[67] Kiddle SJ, Steves CJ, Mehta M, et al. Plasma protein biomarkers of Alzheimer's disease endophenotypes in asymptomatic older twins:early cognitive decline and regional brain volumes[J]. Transl Psychiatry, 2015, 5:e584.
[68] Schley G, Koberle C, Manuilova E, et al. Comparison of plasma and urine biomarker performance in acute kidney injury[J]. PLoS One, 2015, 10:e145042.
[69] Qiu Y, Patwa TH, Xu L, et al. Plasma glycoprotein profiling for colorectal cancer biomarker identification by lectin glycoarray and lectin blot[J]. J Proteome Res, 2008, 7:1693-1703.
[70] Bollineni RC, Fedorova M, Bluher M, et al. Carbonylated plasma proteins as potential biomarkers of obesity induced type 2 diabetes mellitus[J]. J Proteome Res, 2014, 13:5081-5093.
[71] Festa A, D'Agostino RJ, Tracy RP, et al. Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes:the insulin resistance atherosclerosis study[J]. Dlabetes, 2002, 51:1131-1137.
[72] Ridker PM, Hennekens CH, Buring JE, et al. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women[J]. N Engl J Med, 2000, 342:836-843.
[73] Don BR, Kaysen G. Serum albumin:relationship to inflammation and nutrition[J]. Semin Dial, 2004, 17:432-437.
[74] Song C, Dinan T, Leonard BE. Changes in immunoglobulin, complement and acute phase protein levels in the depressed patients and normal controls[J]. J Affect Disord, 1994, 30:283-288.
[75] Thambisetty M, Tripaldi R, Riddoch-Contreras J, et al. Proteome-based plasma markers of brain amyloid-beta deposition in non-demented older individuals[J]. J Alzheimers Dis, 2010, 22:1099-1109.
[76] Hye A, Lynham S, Thambisetty M, et al. Proteome-based plasma biomarkers for Alzheimer's disease[J]. Brain, 2006, 129:3042-3050.
[77] ManafiRad A, Farzadfar F, Habibi L, et al. Is amyloid-beta an innocent bystander and marker in Alzheimer's disease? Is the liability of multivalent cation homeostasis and its influence on amyloid-beta function the real mechanism?[J]. J Alzheimers Dis, 2014, 42:69-85.
[78] Corbo C, Molinaro R, Tabatabaei M, et al. Personalized protein corona on nanoparticles and its clinical implications[J]. Biomater Sci, 2017, 5:378-387.
[79] Colapicchioni V, Tilio M, Digiacomo L, et al. Personalized liposome-protein corona in the blood of breast, gastric and pancreatic cancer patients[J]. Int J Biochem Cell Biol, 2016, 75:180-187.
[80] Zhao Y, Alakhova DY, Kim JO, et al. A simple way to enhance Doxil® therapy:drug release from liposomes at the tumor site by amphiphilic block copolymer[J]. J Control Release, 2013, 168:61-69.
[81] Batist G, Barton J, Chaikin P, et al. Myocet (liposome-encapsulated doxorubicin citrate):a new approach in breast cancer therapy[J]. Expert Opin Pharmacother, 2002, 3:1739-1751.
[82] Ren S, Dai Y, Li C, et al. Pharmacokinetics and pharmacodynamics evaluation of a thermosensitive chitosan based hydrogel containing liposomal doxorubicin[J]. Eur J Pharm Sci, 2016, 92:137-145.
[83] No authors listed. FDA approves DaunoXome as first-line therapy for Kaposi's sarcoma. Food and Drug Administration[J]. J Int Assoc Physicians Aids Care, 1996, 2:50-51.
[84] Stone NR, Bicanic T, Salim R, et al. Liposomal amphotericin B (AmBisome®):a review of the pharmacokinetics, pharmacodynamics, clinical experience and future directions[J]. Drugs, 2016, 76:485-500.
[85] Adedoyin A, Bernardo JF, Swenson CE, et al. Pharmacokinetic profile of ABELCET (amphotericin B lipid complex injection):combined experience from phase I and phase II studies[J]. Antimicrob Agents Chemother, 1997, 41:2201-2208.
[86] Clemons KV, Stevens DA. Comparative efficacies of four amphotericin B formulations——fungizone, amphotec (Amphocil), AmBisome, and Abelcet——against systemic murine aspergillosis[J]. Antimicrob Agents Chemother, 2004, 48:1047-1050.
[87] Clemons KV, Stevens DA. Comparison of fungizone, Amphotec, AmBisome, and Abelcet for treatment of systemic murine cryptococcosis[J]. Antimicrob Agents Chemother, 1998, 42:899-902.
[88] Paterson DL, David K, Mrsic M, et al. Pre-medication practices and incidence of infusion-related reactions in patients receiving AMPHOTEC:data from the patient registry of amphotericin B cholesteryl sulfate complex for injection clinical tolerability (PRoACT) registry[J]. J Antimicrob Chemother, 2008, 62:1392-1400.
[89] Benesch M, Siegler N, Hoff K, et al. Safety and toxicity of intrathecal liposomal cytarabine (Depocyte) in children and adolescents with recurrent or refractory brain tumors:a multi-institutional retrospective study[J]. Anticancer Drugs, 2009, 20:794-799.
[90] Rueda DA, Olmos HD, Viciana GR, et al. Liposomal cytarabine (DepoCyte) for the treatment of neoplastic meningitis[J]. Clin Transl Oncol, 2005, 7:232-238.
[91] Gambling D, Hughes T, Martin G, et al. A comparison of depodur, a novel, single-dose extended-release epidural morphine, with standard epidural morphine for pain relief after lower abdominal surgery[J]. Anesth Analg, 2005, 100:1065-1074.
[92] Peravali R, Brock R, Bright E, et al. Enhancing the enhanced recovery program in colorectal surgery-use of extended-release epidural morphine (DepoDur®)[J]. Ann Coloproctol, 2014, 30:186-191.
[93] Pasero C, McCaffery M. Extended-release epidural morphine (DepoDur)[J]. J Perlanesth Nurs, 2005, 20:345-350.
[94] Keck S, Glennon C, Ginsberg B. DepoDur extended-release epidural morphine:reshaping postoperative care[J]. Orthop Nurs, 2007, 26:86-93.
[95] Alam M, Hartrick CT. Extended-release epidural morphine (DepoDur):an old drug with a new profile[J]. Pain Pract, 2005, 5:349-353.
[96] Burbridge M, Jaffe RA. Exparel®:a new local anesthetic with special safety concerns[J]. Anesth Analg, 2015, 121:1113-1114.
[97] Oppenheimer AJ, Fiala T, Oppenheimer DC. Direct transversus abdominis plane blocks with exparel during abdominoplasty[J]. Ann Plast Surg, 2016, 77:499-500.
[98] Ketonis C, Kim N, Liss F, et al. Wide awake trigger finger release surgery:prospective comparison of lidocaine, marcaine, and exparel[J]. Hand (N Y), 2016, 11:177-183.
[99] Richard BM, Rickert DE, Doolittle D, et al. Pharmacokinetic compatibility study of lidocaine with EXPAREL in Yucatan miniature pigs[J]. ISRN Pharm, 2011, 2011:582351.
[100] Surdam JW, Licini DJ, Baynes NT, et al. The use of exparel (liposomal bupivacaine) to manage postoperative pain in unilateral total knee arthroplasty patients[J]. J Arthroplasty, 2015, 30:325-329.
[101] Soberon JJ, Sisco-Wise LE, Dunbar RM. Compartment syndrome in a patient treated with perineural liposomal bupivacaine (Exparel)[J]. J Clin Anesth, 2016, 31:1-4.
[102] Day KM, Nair NM, Sargent LA. Extended release liposomal bupivacaine injection (Exparel) for early postoperative pain control following palatoplasty[J]. J Craniofac Surg, 2018, 29:e525-e528.
[103] Day KM, Nair NM, Griner D, et al. Extended release liposomal bupivacaine injection (Exparel) for early postoperative pain control following pharyngoplasty[J]. J Craniofac Surg, 2018, 29:726-730.
[104] Richard BM, Newton P, Ott LR, et al. The safety of EXPAREL® (bupivacaine liposome injectable suspension) administered by peripheral nerve block in rabbits and dogs[J]. J Drug Deliv, 2012, 2012:962101.
[105] Richard BM, Rickert DE, Newton PE, et al. Safety evaluation of EXPAREL (DepoFoam bupivacaine) administered by repeated subcutaneous injection in rabbits and dogs:species comparison[J]. J Drug Deliv, 2011, 2011:467429.
[106] Glenn B, Drum M, Reader A, et al. Does liposomal bupivacaine (Exparel) significantly reduce postoperative pain/numbness in symptomatic teeth with a diagnosis of necrosis? a prospective, randomized, double-blind trial[J]. J Endod, 2016, 42:1301-1306.
[107] Vogel JD. Liposome bupivacaine (EXPAREL®) for extended pain relief in patients undergoing ileostomy reversal at a single institution with a fast-track discharge protocol:an IMPROVE Phase IV health economics trial[J]. J Pain Res, 2013, 6:605-610.
[108] Marcet JE, Nfonsam VN, Larach S. An extended pain relief trial utilizing the infiltration of a long-acting multivesicular liPosome foRmulation of bupiVacaine, EXPAREL (IMPROVE):a phase IV health economic trial in adult patients undergoing ileostomy reversal[J]. J Pain Res, 2013, 6:549-555.
[109] Cohen SM. Extended pain relief trial utilizing infiltration of Exparel®, a long-acting multivesicular liposome formulation of bupivacaine:a phase IV health economic trial in adult patients undergoing open colectomy[J]. J Pain Res, 2012, 5:567-572.
[110] Bupivacaine liposomal injection (Exparel) for post surgical pain[J]. Med Lett Drugs Ther, 2012, 54:26-27.
[111] Ang MJ, Silkiss RZ. The use of long-acting liposomal bupivacaine (Exparel) for postoperative pain control following enucleation or evisceration[J]. Ophthalmic Plast Reconstr Surg, 2018, 34:599.
[112] Butz DR, Shenaq DS, Rundell VL, et al. Postoperative pain and length of stay lowered by use of exparel in immediate, implant-based breast reconstruction[J]. Plast Reconstr Surg Glob Open, 2015, 3:e391.
[113] Ilfeld BM, Viscusi ER, Hadzic A, et al. Safety and side effect profile of liposome bupivacaine (Exparel) in peripheral nerve blocks[J]. Reg Anesth Pain Med, 2015, 40:572-582.
[114] Ichikawa K, Takeuchi Y, Yonezawa S, et al. Antiangiogenic photodynamic therapy (PDT) using visudyne causes effective suppression of tumor growth[J]. Cancer Lett, 2004, 205:39-48.
[115] Gluck R, Walti E. Biophysical validation of Epaxal Berna, a hepatitis A vaccine adjuvanted with immunopotentiating reconstituted influenza virosomes (IRIV)[J]. Dev Biol (Basel), 2000, 103:189-197.
[116] Bovier PA. Epaxal:a virosomal vaccine to prevent hepatitis A infection[J]. Expert Rev Vaccines, 2008, 7:1141-1150.
[117] Kursteiner O, Moser C, Lazar H, et al. Inflexal V-the influenza vaccine with the lowest ovalbumin content[J]. Vaccines, 2006, 24:6632-6635.
[118] Herzog C, Hartmann K, Kunzi V, et al. Eleven years of inflexal V-a virosomal adjuvanted influenza vaccine[J]. Vaccine, 2009, 27:4381-4387.
[119] Mischler R, Metcalfe IC. Inflexal V a trivalent virosome subunit influenza vaccine:production[J]. Vaccine, 2002, Suppl 5:B17-B23.
[120] Rodriguez MA, Pytlik R, Kozak T, et al. Vincristine sulfate liposomes injection (Marqibo) in heavily pretreated patients with refractory aggressive non-Hodgkin lymphoma:report of the pivotal phase 2 study[J]. Cancer, 2009, 115:3475-3482.
[121] Cohen MR, Smetzer JL. New connectors coming for enteral feeding tubes; marqibo and risk of errors; angeliq is not a birth control pill[J]. Hosp Pharm, 2014, 49:596-598.
[122] Bedikian AY, Silverman JA, Papadopoulos NE, et al. Pharmacokinetics and safety of Marqibo (vincristine sulfate liposomes injection) in cancer patients with impaired liver function[J]. J Clin Pharmacol, 2011, 51:1205-1212.
[123] No authors listed. FDA approves liposomal vincristine (Marqibo) for rare leukemia[J]. Oncology (Williston Park), 2012, 26:841.
[124] Passero FJ, Grapsa D, Syrigos KN, et al. The safety and efficacy of Onivyde (irinotecan liposome injection) for the treatment of metastatic pancreatic cancer following gemcitabine-based therapy[J]. Expert Rev Anticancer Ther, 2016, 16:697-703.
[125] No authors listed. In brief:liposomal irinotecan (Onivyde) for pancreatic cancer[J]. Med Lett Drugs Ther, 2016, 58:e76.
[126] Zhang H. Onivyde for the therapy of multiple solid tumors[J]. Onco Targets Ther, 2016, 9:3001-3007.