Abstract
The aging of the world population is increasingly claimed as an alarming situation, since an ever-raising number of persons in advanced age but still physically active is expected to suffer from invalidating and degenerative diseases. The impairment of the endogenous healing potential provoked by the aging requires the development of more effective and personalized therapies, based on new biomaterials and devices able to direct the cell fate to stimulate and sustain the regrowth of damaged or diseased tissues. To obtain satisfactory results, also in cases where the cell senescence, typical of the elderly, makes the regeneration process harder and longer, the new solutions have to possess excellent ability to mimic the physiological extracellular environment and thus exert biomimetic stimuli on stem cells. To this purpose, the “biomimetic concept” is today recognized as elective to fabricate bioactive and bioresorbable devices such as hybrid osteochondral scaffolds and bioactive bone cements closely resembling the natural hard tissues and with enhanced regenerative ability. The review will illustrate some recent results related to these new biomimetic materials developed for application in different districts of the musculoskeletal system, namely bony, osteochondral and periodontal regions, and the spine. Further, it will be shown how new bioactive and superparamagnetic calcium phosphate nanoparticles can give enhanced results in cardiac regeneration and cancer therapy. Since tissue regeneration will be a major demand in the incoming decades, the high potential of biomimetic materials and devices is promising to significantly increase the healing rate and improve the clinical outcomes even in aged patients.
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Gibon E, Lu LY, Nathan K et al (2017) Inflammation, ageing, and bone regeneration. J Orthop Translat 10:28–35
Kenyon CJ (2010) The genetics of ageing (vol 464, pg 504, 2010). Nature 467:622
Conboy IM, Rando TA (2005) Aging, stem cells and tissue regeneration—lessons from muscle. Cell Cycle 4:407–410
Wolff JL, Starfield B, Anderson G (2002) Prevalence, expenditures, and complications of multiple chronic conditions in the elderly. Arch Intern Med 162:2269–2276
Freemont AJ, Hoyland JA (2007) Morphology, mechanisms and pathology of musculoskeletal ageing. J Pathol 211:252–259
Gheno R, Cepparo JM, Rosca CE et al (2012) Musculoskeletal disorders in the elderly. J Clin Imaging Sci 2:39
Xue QL (2011) The frailty syndrome: definition and natural history. Clin Geriatr Med 27:1–15
Sprio S, Campodoni E, Sandri M et al (2018) A graded multifunctional hybrid scaffold with superparamagnetic ability for periodontal regeneration. Int J Mol Sci 19:3604
Sprio S, Ruffini A, Dapporto M et al (2016) New strategies for regeneration of load bearing bones. In: Tampieri A, Sprio S (eds) Bio-inspired regenerative medicine: materials, processes and clinical applications. PAN Stanford Publishing, Singapore, pp 85–117
Tampieri A, Ruffini A, Ballardini A et al (2019) Heterogeneous chemistry in the 3-D state: an original approach to generate bioactive, mechanically-competent bone scaffolds. Biomater Sci 7:307–321
Tampieri A, Sandri M, Panseri S et al (2016) Biologically-inspired nanomaterials and nano-bio-magnetism: a synergy among new emerging concepts in regenerative medicine. In: Tampieri A, Sprio S (eds) Bio-inspired regenerative medicine: materials, processes and clinical applications. PAN Stanford Publishing, Singapore, pp 1–20
Iafisco M, Sandri M, Panseri S et al (2013) Magnetic bioactive and biodegradable hollow Fe-doped hydroxyapatite coated poly(l-lactic) acid micro-nanospheres. Chem Mater 25:2610–2617
Sprio S, Tampieri A, Landi E et al (2008) Physico-chemical properties and solubility behaviour of multi-substituted hydroxyapatite powders containing silicon. Mater Sci Eng C Biomimet Supramol Syst 28:179–187
Tampieri A, Sprio S, Sandri M et al (2011) Mimicking natural bio-mineralization processes: a new tool for osteochondral scaffold development. Trends Biotechnol 29:526–535
Tampieri A, Celotti G, Landi E et al (2003) Biologically inspired synthesis of bone-like composite: self-assembled collagen fibers/hydroxyapatite nanocrystals. J Biomed Mater Res A 67:618–625
Tampieri A, Sandri M, Landi E et al (2008) Design of graded biomimetic osteochondral composite scaffolds. Biomaterials 29:3539–3546
Sprio S, Ruffini A, Valentini F et al (2011) Biomimesis and biomorphic transformations: new concepts applied to bone regeneration. J Biotechnol 156:347–355
Sprio S, Sandri M, Iafisco M et al (2016) Bio-inspired assembling/mineralization process as a flexible approach to develop new smart scaffolds for the regeneration of complex anatomical regions. J Eur Ceram Soc 36:2857–2867
Murray CJ, Vos T, Lozano R et al (2012) Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2197–2223
Vos T, Flaxman AD, Naghavi M et al (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2163–2196
Kingsbury DJ, Bader-Meunier B, Patel G et al (2014) Safety, effectiveness, and pharmacokinetics of adalimumab in children with polyarticular juvenile idiopathic arthritis aged 2 to 4 years. Clin Rheumatol 33:1433–1441
Buckwalter JA, Woo SL, Goldberg VM et al (1993) Soft-tissue aging and musculoskeletal function. J Bone Joint Surg Am 75:1533–1548
Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials 21:2529–2543
Hutmacher D, Hutmacher D, Teoh S et al (2000) Design and fabrication of a 3D scaffold for tissue engineering bone. In: Agrawal C, Parr J, Lin S (eds) Synthetic bioabsorbable polymers for implants. ASTM International, West Conshohocken, PA, pp 152–167. https://doi.org/10.1520/stp15307s
Martin I, Obradovic B, Treppo S et al (2000) Modulation of the mechanical properties of tissue engineered cartilage. Biorheology 37:141–147
Barbour KE, Helmick CG, Boring M et al (2017) Vital Signs: prevalence of doctor-diagnosed arthritis and arthritis-attributable activity limitation—United States, 2013–2015. MMWR Morb Mortal Wkly Rep 66:246–253
Ethgen O, Reginster JY (2004) Degenerative musculoskeletal disease. Ann Rheum Dis 63:1–3
Hootman JM, Helmick CG, Barbour KE et al (2016) Updated projected prevalence of self-reported doctor-diagnosed arthritis and arthritis-attributable activity limitation among US adults, 2015–2040. Arthritis Rheumatol 68:1582–1587
Wang H, Bai J, He B et al (2016) Osteoarthritis and the risk of cardiovascular disease: a meta-analysis of observational studies. Sci Rep 6:39672
Veronese N, Stubbs B, Solmi M et al (2017) Association between lower limb osteoarthritis and incidence of depressive symptoms: data from the osteoarthritis initiative. Age Ageing 46:470–476
Cacciatore F, Della-Morte D, Basile C et al (2014) Long-term mortality in frail elderly subjects with osteoarthritis. Rheumatology (Oxford) 53:293–299
Castell MV, van der Pas S, Otero A et al (2015) Osteoarthritis and frailty in elderly individuals across six European countries: results from the European Project on OSteoArthritis (EPOSA). BMC Musculoskelet Disord 16:359
Henderson I, Lavigne P, Valenzuela H et al (2007) Autologous chondrocyte implantation: superior biologic properties of hyaline cartilage repairs. Clin Orthop Relat Res 455:253–261
Knutsen G, Engebretsen L, Ludvigsen TC et al (2004) Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J Bone Joint Surg Am 86-a:455–464
Kraeutler MJ, Belk JW, Purcell JM et al (2018) Microfracture versus autologous chondrocyte implantation for articular cartilage lesions in the knee: a systematic review of 5-year outcomes. Am J Sports Med 46:995–999
Niemeyer P, Albrecht D, Andereya S et al (2016) Autologous chondrocyte implantation (ACI) for cartilage defects of the knee: a guideline by the working group “Clinical Tissue Regeneration” of the German Society of Orthopaedics and Trauma (DGOU). Knee 23:426–435
Zhang W, Ouyang H, Dass CR et al (2016) Current research on pharmacologic and regenerative therapies for osteoarthritis. Bone Res 4:15040
Cao T, Ho KH, Teoh SH (2003) Scaffold design and in vitro study of osteochondral coculture in a three-dimensional porous polycaprolactone scaffold fabricated by fused deposition modeling. Tissue Eng 9:S103–S112
Chen J, Chen H, Li P et al (2011) Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials 32:4793–4805
Panseri S, Russo A, Giavaresi G et al (2012) Innovative magnetic scaffolds for orthopedic tissue engineering. J Biomed Mater Res A 100:2278–2286
Kon E, Delcogliano M, Filardo G et al (2010) Orderly osteochondral regeneration in a sheep model using a novel nano-composite multilayered biomaterial. J Orthop Res 28:116–124
Berruto M, Delcogliano M, de Caro F et al (2014) Treatment of large knee osteochondral lesions with a biomimetic scaffold: results of a multicenter study of 49 patients at 2-year follow-up. Am J Sports Med 42:1607–1617
Calabrese G, Gulino R, Giuffrida R et al (2017) In vivo evaluation of biocompatibility and chondrogenic potential of a cell-free collagen-based scaffold. Front Physiol 8:984
Di Martino A, Kon E, Perdisa F et al (2015) Surgical treatment of early knee osteoarthritis with a cell-free osteochondral scaffold: results at 24 months of follow-up. Injury 46:S33–S38
Filardo G, Kon E, Di Martino A et al (2013) Treatment of knee osteochondritis dissecans with a cell-free biomimetic osteochondral scaffold: clinical and imaging evaluation at 2-year follow-up. Am J Sports Med 41:1786–1793
Grigolo B, Cavallo C, Desando G et al (2015) Novel nano-composite biomimetic biomaterial allows chondrogenic and osteogenic differentiation of bone marrow concentrate derived cells. J Mater Sci Mater Med 26:173
Kon E, Filardo G (2018) A multilayer biomaterial for osteochondral regeneration shows superiority vs microfractures for the treatment of osteochondral lesions in a multicentre randomized trial at 2 years. Knee Surg 26:2704–2715
Kon E, Filardo G, Di Martino A et al (2014) Clinical results and MRI evolution of a nano-composite multilayered biomaterial for osteochondral regeneration at 5 years. Am J Sports Med 42:158–165
Kon E, Filardo G, Perdisa F et al (2014) A one-step treatment for chondral and osteochondral knee defects: clinical results of a biomimetic scaffold implantation at 2 years of follow-up. J Mater Sci Mater Med 25:2437–2444
Kon E, Filardo G, Venieri G et al (2014) Tibial plateau lesions. Surface reconstruction with a biomimetic osteochondral scaffold: results at 2 years of follow-up. Injury 45:S121–S125
Zhang Y, Pizzute T, Pei M (2014) Anti-inflammatory strategies in cartilage repair. Tissue Eng Part B Rev 20:655–668
Haumschild MS, Haumschild RJ (2009) The importance of oral health in long-term care. J Am Med Dir Assoc 10:667–671
Williams RC, Barnett AH, Claffey N et al (2008) The potential impact of periodontal disease on general health: a consensus view. Curr Med Res Opin 24:1635–1643
Dye BA (2012) Global periodontal disease epidemiology. Periodontol 58:10–25
Hajishengallis G (2010) Too old to fight? Aging and its toll on innate immunity. Mol Oral Microbiol 25:25–37
Bartold PM, McCulloch CA, Narayanan AS et al (2000) Tissue engineering: a new paradigm for periodontal regeneration based on molecular and cell biology. Periodontol 2000 24:253–269
Linde A, Goldberg M (1993) Dentinogenesis. Crit Rev Oral Biol Med 4:679–728
Maeda H, Tomokiyo A, Wada N et al (2014) Regeneration of the periodontium for preservation of the damaged tooth. Histol Histopathol 29:1249–1262
Bodineau A, Folliguet M, Seguier S (2009) Tissular senescence and modifications of oral ecosystem in the elderly: risk factors for mucosal pathologies. Curr Aging Sci 2:109–120
Lee CH, Hajibandeh J, Suzuki T et al (2014) Three-dimensional printed multiphase scaffolds for regeneration of periodontium complex. Tissue Eng Part A 20:1342–1351
Bortolomai I, Sandri M, Draghici E et al (2019) Gene modification and three-dimensional scaffolds as novel tools to allow the use of postnatal thymic epithelial cells for thymus regeneration approaches. Stem Cells Transl Med 8(10):1107–1122
Krishnakumar GS, Gostynska N, Dapporto M et al (2018) Evaluation of different crosslinking agents on hybrid biomimetic collagen-hydroxyapatite composites for regenerative medicine. Int J Biol Macromol 106:739–748
Sandri M, Filardo G, Kon E et al (2016) Fabrication and pilot in vivo study of a collagen-BDDGE-elastin core-shell scaffold for tendon regeneration. Front Bioeng Biotechnol 4:52
Goncalves PF, Sallum EA, Sallum AW et al (2005) Dental cementum reviewed: development, structure, composition, regeneration and potential functions. Braz J Oral Sci 4:651–658
Ho SP, Yu B, Yun W et al (2009) Structure, chemical composition and mechanical properties of human and rat cementum and its interface with root dentin. Acta Biomater 5:707–718
Valentijn AJ, Zouq N, Gilmore AP (2004) Anoikis. Biochem Soc Trans 32:421–425
Arora A, Kothari A, Katti DS (2015) Pore orientation mediated control of mechanical behavior of scaffolds and its application in cartilage-mimetic scaffold design. J Mech Behav Biomed Mater 51:169–183
Scarano A, Lorusso F, Staiti G et al (2017) Sinus augmentation with biomimetic nanostructured matrix: tomographic, radiological, histological and histomorphometrical results after 6 months in humans. Front Physiol 8:565
Panseri S, Russo A, Sartori M et al (2013) Modifying bone scaffold architecture in vivo with permanent magnets to facilitate fixation of magnetic scaffolds. Bone 56:432–439
Wright NC, Looker AC, Saag KG et al (2014) The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res 29:2520–2526
Willson T, Nelson SD, Newbold J et al (2015) The clinical epidemiology of male osteoporosis: a review of the recent literature. Clin Epidemiol 7:65–76
Foundation NO (2014) 54 Million Americans affected by osteoporosis and low bone mass. https://www.nof.org/news/54-million-americans-affected-by-osteoporosis-and-low-bone-mass/. Accessed 2 June 2014
Demontiero O, Vidal C, Duque G (2012) Aging and bone loss: new insights for the clinician. Therap Adv Musculoskelet Dis 4:61–76
Griffith JF (2015) Identifying osteoporotic vertebral fracture. Quant Imaging Med Surg 5:592–602
Tu KN, Lie JD, Wan CKV et al (2018) Osteoporosis: a review of treatment options. P & T 43:92–104
Denaro V, Longo UG, Maffulli N et al (2009) Vertebroplasty and kyphoplasty. Clin Cases Miner Bone Metabol 6:125–130
Movrin I, Vengust R, Komadina R (2010) Adjacent vertebral fractures after percutaneous vertebral augmentation of osteoporotic vertebral compression fracture: a comparison of balloon kyphoplasty and vertebroplasty. Arch Orthop Trauma Surg 130:1157–1166
Ginebra MP, Traykova T, Planell JA (2006) Calcium phosphate cements as bone drug delivery systems: a review. J Control Release 113:102–110
Horák P, Skácelová M, Kazi A (2017) Role of strontium ranelate in the therapy of osteoporosis. Curr Opin Pharmacol. https://doi.org/10.23937/2469-5726/1510050
Society NO (2017) Drug treatments for osteoporosis: strontium ranelate (Protelos). https://theros.org.uk/media/1596/drugtreatments-for-osteoporosis-strontium-ranelate-january-2016.pdf
Schumacher M, Gelinsky M (2015) Strontium modified calcium phosphate cements—approaches towards targeted stimulation of bone turnover. J Mater Chem B 3:4626–4640
Montesi M, Panseri S, Dapporto M et al (2017) Sr-substituted bone cements direct mesenchymal stem cells, osteoblasts and osteoclasts fate. PLoS One 12:e0172100
Perez RA, Kim H-W, Ginebra M-P (2012) Polymeric additives to enhance the functional properties of calcium phosphate cements. J Tissue Eng 3:2041731412439555
Sprio S, Dapporto M, Montesi M et al (2016) Novel osteointegrative Sr-substituted apatitic cements enriched with alginate. Materials (Basel) 9:763
Xu HHK, Wang P, Wang L et al (2017) Calcium phosphate cements for bone engineering and their biological properties. Bone Res 5:17056
Yun MH (2015) Changes in regenerative capacity through lifespan. Int J Mol Sci 16:25392–25432
Maredziak M, Marycz K, Tomaszewski KA et al (2016) The influence of aging on the regenerative potential of human adipose derived mesenchymal stem cells. Stem Cells Int 2016, Article ID 2152435
Yun YR, Jang JH, Jeon E et al (2012) Administration of growth factors for bone regeneration. Regen Med 7:369–385
Wang Z, Wang Z, Lu WW et al (2017) Novel biomaterial strategies for controlled growth factor delivery for biomedical applications. Npg Asia Mater 9:e435
Hou R, Zhang G, Du G et al (2013) Magnetic nanohydroxyapatite/PVA composite hydrogels for promoted osteoblast adhesion and proliferation. Colloids Surf B Biointerfaces 103:318–325
Meng J, Xiao B, Zhang Y et al (2013) Super-paramagnetic responsive nanofibrous scaffolds under static magnetic field enhance osteogenesis for bone repair in vivo. Sci Rep 3:2655
Meng J, Zhang Y, Qi X et al (2010) Paramagnetic nanofibrous composite films enhance the osteogenic responses of pre-osteoblast cells. Nanoscale 2:2565–2569
Mertens ME, Hermann A, Buhren A et al (2014) Iron oxide-labeled collagen scaffolds for non-invasive MR imaging in tissue engineering. Adv Funct Mater 24:754–762
Shan D, Shi Y, Duan S et al (2013) Electrospun magnetic poly(L-lactide) (PLLA) nanofibers by incorporating PLLA-stabilized Fe3O4 nanoparticles. Mater Sci Eng C Mater Biol Appl 33:3498–3505
Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–49
Singh N, Jenkins GJ, Asadi R et al (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev 1:5358
Tampieri A, D’Alessandro T, Sandri M et al (2012) Intrinsic magnetism and hyperthermia in bioactive Fe-doped hydroxyapatite. Acta Biomater 8:843–851
Panseri S, Cunha C, D’Alessandro T et al (2012) Intrinsically superparamagnetic Fe-hydroxyapatite nanoparticles positively influence osteoblast-like cell behaviour. J Nanobiotechnol 10:32
Clavijo-Jordan V, Kodibagkar VD, Beeman SC et al (2012) Principles and emerging applications of nanomagnetic materials in medicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4:345–365
Assiotis A, Sachinis NP, Chalidis BE (2012) Pulsed electromagnetic fields for the treatment of tibial delayed unions and nonunions. A prospective clinical study and review of the literature. J Orthop Surg Res 7:24
Chalidis B, Sachinis N, Assiotis A et al (2011) Stimulation of bone formation and fracture healing with pulsed electromagnetic fields: biologic responses and clinical implications. Int J Immunopathol Pharmacol 24:17–20
Glazer PA, Heilmann MR, Lotz JC et al (1997) Use of electromagnetic fields in a spinal fusion. A rabbit model. Spine (Phila Pa 1976) 22:2351–2356
Grace KL, Revell WJ, Brookes M (1998) The effects of pulsed electromagnetism on fresh fracture healing: osteochondral repair in the rat femoral groove. Orthopedics 21:297–302
Yan QC, Tomita N, Ikada Y (1998) Effects of static magnetic field on bone formation of rat femurs. Med Eng Phys 20:397–402
Sprio S, Panseri S, Adamiano A et al (2017) Porous hydroxyapatite-magnetite composites as carriers for guided bone regeneration. Front Nanosci Nanotechnol 3:1–9
Russo A, Bianchi M, Sartori M et al (2018) Bone regeneration in a rabbit critical femoral defect by means of magnetic hydroxyapatite macroporous scaffolds. J Biomed Mater Res B Appl Biomater 106:546–554
Tampieri A, Iafisco M, Sandri M et al (2014) Magnetic bioinspired hybrid nanostructured collagen-hydroxyapatite scaffolds supporting cell proliferation and tuning regenerative process. ACS Appl Mater Interfaces 6:15697–15707
Banobre-Lopez M, Pineiro-Redondo Y, De Santis R et al (2011) Poly(caprolactone) based magnetic scaffolds for bone tissue engineering. J Appl Phys 109:07
Gloria A, Russo T, D’Amora U et al (2013) Magnetic poly(epsilon-caprolactone)/iron-doped hydroxyapatite nanocomposite substrates for advanced bone tissue engineering. J R Soc Interface 10:20120833
Nappini S, Bonini M, Bombelli FB et al (2011) Controlled drug release under a low frequency magnetic field: effect of the citrate coating on magnetoliposomes stability. Soft Matter 7:1025–1037
Liu D, Yang F, Xiong F, Gu N (2016) The smart drug delivery system and its clinical potential. Theranostics 6:1306–1323
Plouffe BD, Murthy SK, Lewis LH (2015) Fundamentals and application of magnetic particles in cell isolation and enrichment: a review. Rep Progress Phys Phys Soc (Great Britain) 78:016601
Sprio S, Sandri M, Iafisco M et al (2014) 9—composite biomedical foams for engineering bone tissue. In: Netti PA (ed) Biomedical foams for tissue engineering applications. Woodhead, Sawston, pp 249–280. https://doi.org/10.1533/9780857097033.2.249
Ganguly R, Puri IK (2010) Microfluidic transport in magnetic MEMS and bioMEMS. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:382–399
Amer MH, Rose FRAJ, Shakesheff KM et al (2017) Translational considerations in injectable cell-based therapeutics for neurological applications: concepts, progress and challenges. NPJ Regener Med 2:23
Yohan D, Chithrani BD (2014) Applications of nanoparticles in nanomedicine. J Biomed Nanotechnol 10:2371–2392
Wu K, Su D, Liu J et al (2018) Magnetic nanoparticles in nanomedicine. arXiv e-prints
Dilnawaz F, Singh A, Mohanty C et al (2010) Dual drug loaded superparamagnetic iron oxide nanoparticles for targeted cancer therapy. Biomaterials 31:3694–3706
Schellenberger E, Schnorr J, Reutelingsperger C et al (2008) Linking proteins with anionic nanoparticles via protamine: ultrasmall protein-coupled probes for magnetic resonance imaging of apoptosis. Small 4:225–230
Veiseh O, Gunn JW, Zhang M (2010) Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. Adv Drug Deliv Rev 62:284–304
Yiu HH, McBain SC, Lethbridge ZA et al (2010) Preparation and characterization of polyethylenimine-coated Fe3O4-MCM-48 nanocomposite particles as a novel agent for magnet-assisted transfection. J Biomed Mater Res A 92:386–392
Yu MK, Jeong YY, Park J et al (2008) Drug-loaded superparamagnetic iron oxide nanoparticles for combined cancer imaging and therapy in vivo. Angew Chem Int Ed Engl 47:5362–5365
Patil RM, Thorat ND, Shete PB et al (2018) Comprehensive cytotoxicity studies of superparamagnetic iron oxide nanoparticles. Biochem Biophys Rep 13:63–72
Iannotti V, Adamiano A, Ausanio G et al (2017) Fe-doping-induced magnetism in nano-hydroxyapatites. Inorg Chem 56:4446–4458
Adamiano A, Wu VM, Carella F et al (2019) Magnetic calcium phosphates nanocomposites for the intracellular hyperthermia of cancers of bone and brain. Nanomedicine (Lond) 14:1267–1289
Marrella A, Iafisco M, Adamiano A et al (2018) A combined low-frequency electromagnetic and fluidic stimulation for a controlled drug release from superparamagnetic calcium phosphate nanoparticles: potential application for cardiovascular diseases. J R Soc Interface 15:20180236
Organization WH (2018) Global strategy for women’s, children’s and adolescents’ health (2016–2030): Data portal
Lelieveld J, Klingmuller K, Pozzer A et al (2019) Cardiovascular disease burden from ambient air pollution in Europe reassessed using novel hazard ratio functions. Eur Heart J 40:1590–1596
Yazdanyar A, Newman AB (2009) The burden of cardiovascular disease in the elderly: morbidity, mortality, and costs. Clin Geriatr Med 25:563–577
Zhang YJ, Yang SH, Li MH et al (2014) Berberine attenuates adverse left ventricular remodeling and cardiac dysfunction after acute myocardial infarction in rats: role of autophagy. Clin Exp Pharmacol Physiol 41:995–1002
Huang Z, Han Z, Ye B et al (2015) Berberine alleviates cardiac ischemia/reperfusion injury by inhibiting excessive autophagy in cardiomyocytes. Eur J Pharmacol 762:1–10
Allijn IE, Czarny BMS, Wang X et al (2017) Liposome encapsulated berberine treatment attenuates cardiac dysfunction after myocardial infarction. J Control Rel 247:127–133
Zhuge Y, Zheng ZF, Xie MQ et al (2016) Preparation of liposomal amiodarone and investigation of its cardiomyocyte-targeting ability in cardiac radiofrequency ablation rat model. Int J Nanomed 11:2359–2367
Somasuntharam I, Boopathy AV, Khan RS et al (2013) Delivery of Nox2-NADPH oxidase siRNA with polyketal nanoparticles for improving cardiac function following myocardial infarction. Biomaterials 34:7790–7798
Di Mauro V, Iafisco M, Salvarani N et al (2016) Bioinspired negatively charged calcium phosphate nanocarriers for cardiac delivery of MicroRNAs. Nanomedicine (Lond) 11:891–906
Miragoli M, Ceriotti P, Iafisco M et al (2018) Inhalation of peptide-loaded nanoparticles improves heart failure. Sci Transl Med 10:eaan6205
Group. USCSW (2013) US cancer statistics: 1999–2009 incidence and mortality web-based report. https://www.cdc.gov/cancer/uscs/index.htm
Pedersen JK, Engholm G, Skytthe A et al (2016) Cancer and aging: epidemiology and methodological challenges. Acta Oncol 55:7–12
White MC, Holman DM, Boehm JE et al (2014) Age and cancer risk a potentially modifiable relationship. Am J Prev Med 46:S7–S15
Al-Kattan A, Girod-Fullana S, Charvillat C et al (2012) Biomimetic nanocrystalline apatites: emerging perspectives in cancer diagnosis and treatment. Int J Pharm 423:26–36
Zheng C, Xu J, Yao XP et al (2011) Polyphosphazene nanoparticles for cytoplasmic release of doxorubicin with improved cytotoxicity against Dox-resistant tumor cells. J Colloid Interface Sci 355:374–382
Farbod K, Sariibrahimoglu K, Curci A et al (2016) Controlled release of chemotherapeutic platinum-bisphosphonate complexes from injectable calcium phosphate cements. Tissue Eng Part A 22:788–800
Palazzo B, Iafisco M, Laforgia M et al (2007) Biomimetic hydroxyapatite-drug nanocrystals as potential bone substitutes with antitumor drug delivery properties. Adv Func Mater 17:2180–2188
Iafisco M, Palazzo B, Marchetti M et al (2009) Smart delivery of antitumoral platinum complexes from biomimetic hydroxyapatite nanocrystals. J Mater Chem 19:8385–8392
Iafisco M, Palazzo B, Martra G et al (2012) Nanocrystalline carbonate-apatites: role of Ca/P ratio on the upload and release of anticancer platinum bisphosphonates. Nanoscale 4:206–217
Rodriguez-Ruiz I, Delgado-Lopez JM, Duran-Olivencia MA et al (2013) pH-responsive delivery of doxorubicin from citrate-apatite nanocrystals with tailored carbonate content. Langmuir 29:8213–8221
Iafisco M, Drouet C, Adamiano A et al (2016) Superparamagnetic iron-doped nanocrystalline apatite as a delivery system for doxorubicin. J Mater Chem B 4:57–70
Sarda S, Iafisco M, Pascaud-Mathieu P et al (2018) Interaction of folic acid with nanocrystalline apatites and extension to methotrexate (antifolate) in view of anticancer applications. Langmuir 34:12036–12048
Iafisco M, Delgado-Lopez JM, Varoni EM et al (2013) Cell surface receptor targeted biomimetic apatite nanocrystals for cancer therapy. Small 9:3834–3844
Funding
The work has received funding from the EU’s H2020 Research and Innovation Programme under the Grant Agreement no. 720834, and from the National Research Council of Italy (CNR), Research Project “Aging: molecular and technological innovations for improving the health of the elderly population” (Prot. MIUR 2867 25.11.2011).
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Tampieri, A., Sandri, M., Iafisco, M. et al. Nanotechnological approach and bio-inspired materials to face degenerative diseases in aging. Aging Clin Exp Res 33, 805–821 (2021). https://doi.org/10.1007/s40520-019-01365-6
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DOI: https://doi.org/10.1007/s40520-019-01365-6