In vivo monitoring of the inflammatory response in a stented mouse aorta model
Corresponding Author
Konstantinos K. Kapnisis
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Correspondence to: K. K. Kapnisis, Cyprus University of Technology, 45 Kitiou Kyprianou Str., Dorothea Bldg. 5th Floor, Lemesos 3041, Cyprus; e-mail: [email protected]Search for more papers by this authorCostas M. Pitsillides
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorGeorge Lapathitis
Neurology Clinic E, Cyprus Institute of Neurology and Genetics, Nicosia, 2370 Cyprus
Search for more papers by this authorChristos Karaiskos
Neurology Clinic E, Cyprus Institute of Neurology and Genetics, Nicosia, 2370 Cyprus
Search for more papers by this authorPolyvios C. Eleftheriou
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorBrigitta C. Brott
Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorPeter G. Anderson
Department of Pathology, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorJack E. Lemons
Department of Prosthodontics, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorAndreas S. Anayiotos
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorCorresponding Author
Konstantinos K. Kapnisis
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Correspondence to: K. K. Kapnisis, Cyprus University of Technology, 45 Kitiou Kyprianou Str., Dorothea Bldg. 5th Floor, Lemesos 3041, Cyprus; e-mail: [email protected]Search for more papers by this authorCostas M. Pitsillides
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorGeorge Lapathitis
Neurology Clinic E, Cyprus Institute of Neurology and Genetics, Nicosia, 2370 Cyprus
Search for more papers by this authorChristos Karaiskos
Neurology Clinic E, Cyprus Institute of Neurology and Genetics, Nicosia, 2370 Cyprus
Search for more papers by this authorPolyvios C. Eleftheriou
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorBrigitta C. Brott
Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorPeter G. Anderson
Department of Pathology, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorJack E. Lemons
Department of Prosthodontics, University of Alabama at Birmingham, Birmingham, Alabama, 35294-0111
Search for more papers by this authorAndreas S. Anayiotos
Department of Mechanical Engineering and Materials Science and Engineering, Cyprus University of Technology, Limassol, 3036 Cyprus
Search for more papers by this authorAbstract
The popularity of vascular stents continues to increase for a variety of applications, including coronary, lower limb, renal, carotid, and neurovascular disorders. However, their clinical effectiveness is hindered by numerous postdeployment complications, which may stimulate inflammatory and fibrotic reactions. The purpose of this study was to evaluate the vessel inflammatory response via in vivo imaging in a mouse stent implantation model. Corroded and noncorroded self-expanding miniature nitinol stents were implanted in mice abdominal aortas, and novel in vivo imaging techniques were used to assess trafficking and accumulation of fluorescent donor monocytes as well as cellular proliferation at the implantation site. Monocytes were quantitatively tracked in vivo and found to rapidly clear from circulation within hours after injection. Differences were found between the test groups with respect to the numbers of recruited monocytes and the intensity of the resulting fluorescent signal. Image analysis also revealed a subtle increase in matrix metalloproteinase activity in corroded compared with the normal stented aortas. In conclusion, this study has been successful in developing a murine stent inflammation model and applying novel in vivo imaging tools and methods to monitor the complex biological processes of the host vascular wall response. © 2015 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 227–238, 2016.
REFERENCES
- 1 Van Buuren F, Dahm JB, Horskotte D. Stent restenosis and thrombosis: Etiology, treatment, and outcomes. Minerva Med 2012; 103: 503–511.
- 2 Curcio A, Torella D, Indolfi C. Mechanisms of smooth muscle cell proliferation and endothelial regeneration after vascular injury and stenting. Circ J 2011; 75: 1287–1296.
- 3 Abe S, Yoneda S, Kanaya T, Oda K, Nishino S, Kageyama M, Taguchi I, Masawa N, Inoue T. Pathological features of in-stent restenosis after sirolimus-eluting stent versus bare metal stent placement. Cardiovasc Pathol 2012; 21: e19–e22.
- 4 Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation 2005; 111: 2257–2273.
- 5 Singh R, Dahotre NB. Corrosion degradation and prevention by surface modification of biometallic materials. J Mater Sci Mater Med 2007; 18: 725–751.
- 6 Thierry B, Tabrizian M. Biocompatibility and biostability of metallic endovascular implants: State of the art and perspectives. J Endovasc Ther 2003; 10: 807–824.
- 7 Keegan GM, Learmonth ID, Case CP. Orthopaedic metals and their potential toxicity in the arthroplasty patient: A review of current knowledge and future strategies. J Bone Joint Surg Br 2007; 89: 567–573.
- 8 Eliades T, Pratsinis H, Kletsas D, Eliades G, Makou M. Characterization and cytotoxicity of ions released from stainless steel and nickel-titanium orthodontic alloys. Am J Orthod Dentofacial Orthop 2004; 125: 24–29.
- 9 Santin M, Mikhalovska L, Lloyd AW, Mikhalovsky S, Sigfrid L, Denyer SP, Field S, Teer D. In vitro host response assessment of biomaterials for cardiovascular stent manufacture. J Mater Sci Mater Med 2004; 15: 473–477.
- 10 Voggenreiter G, Leiting S, Brauer H, Leiting P, Majetschak M, Bardenheuer M, Obertacke U. Immuno-inflammatory tissue reaction to stainless-steel and titanium plates used for internal fixation of long bones. Biomaterials 2003; 24: 247–254.
- 11 Wataha JC, O'Dell NL, Singh BB, Ghazi M, Whitford GM, Lockwood PE. Relating nickel-induced tissue inflammation to nickel release in vivo. J Biomed Mater Res 2001; 58: 537–544.
- 12 Halwani Dina O, Anderson Peter G, Brott Brigitta C, Anayiotos Andreas S, Lemons JE. Clinical device-related article surface characterization of explanted endovascular stents: Evidence of in vivo corrosion. J Biomed Mater Res B Appl Biomater 2010; 95: 225–238.
- 13 Nakano M, Otsuka F, Yahagi K, Sakakura K, Kutys R, Ladich ER, Finn AV, Kolodgie Frank D, Virmani R. Human autopsy study of drug-eluting stents restenosis: Histomorphological predictors and neointimal characteristics. Eur Heart J 2013; 34: 3304–3313.
- 14 Halwani DO, Anderson PG, Brott BC, Anayiotos AS, Lemons JE. The role of vascular calcification in inducing fatigue and fracture of coronary stents. J Biomed Mater Res B Appl Biomater 2012; 100: 292–304.
- 15 Halwani DO, Anderson PG, Lemons JE, Jordan WD, Anayiotos AS, Brott BC. In-vivo corrosion and local release of metallic ions from vascular stents into surrounding tissue. J Invasive Cardiol 2010; 22: 528–535.
- 16 Nakano M, Yahagi K, Otsuka F, Sakakura K, Finn AV, Kutys R, Ladich E, Fowler DR, Joner M, Virmani R. Causes of early stent thrombosis in patients presenting with acute coronary syndrome: An ex vivo human autopsy study. J Am Coll Cardiol 2014; 63: 2510–2520.
- 17 Lin J, Guidoin R, Wang L, Zhang Z, Paynter R, How T, Nutley M, Wei D, Douville Y, Samis G, Dionne G, Gilbert N. Long-term resistance to fracture and/or corrosion of the nitinol wires of the talent stent-graft: Observations from a series of explanted devices. J Long Term Eff Med Implants 2013; 23: 45–59.
- 18 Moore E Jr, James Berry JL. Fluid and solid mechanical implications of vascular stenting. Ann Biomed Eng 2002; 30: 498–508.
- 19 Caixeta AM, Brito FS, Costa MA, Serrano CV, Petriz JL, Da Luz PL. Enhanced inflammatory response to coronary stenting marks the development of clinically relevant restenosis. Catheter Cardiovasc Interv 2007; 69: 500–507.
- 20 Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007; 28: 521–574.
- 21 Chamberlain J, Wheatcroft M, Arnold N, Lupton H, Crossman David C, Gunn J, Francis S. A novel mouse model of in situ stenting. Cardiovasc Res 2010; 85: 38–44.
- 22 Wang Y, Wang H, Piper MG, McMaken S, Mo X, Opalek J, Schmidt AM, Marsh CB. sRAGE induces human monocyte survival and differentiation. J Immunol 2010; 185: 1822–1835.
- 23 Pitsillides CM, Runnels JM, Spencer JA, Zhi L, Wu MX, Lin CP. Cell labeling approaches for fluorescence-based in vivo flow cytometry. Cytometry A 2011; 79: 758–765.
- 24 Fan Z, Spencer JA, Lu Y, Pitsillides CM, Singh G, Kim P, Yun SH, Toxavidis V, Strom TB, Lin CP, Koulmanda M. In vivo tracking of “color-coded” effector, natural and induced regulatory T cells in the allograft response. Nat Med 2010; 16: 718–722.
- 25 Novak J, Georgakoudi I, Wei X, Prossin A, Lin CP. In vivo flow cytometer for real-time detection and quantification of circulating cells. Opt Lett 2004; 29: 77.
- 26 Leblond F, Davis Scott C, Valdés Pablo A, Pogue BW. Pre-clinical whole-body fluorescence imaging: Review of instruments, methods and applications. J Photochem Photobiol B 2010; 98: 77–94.
- 27 Rodriguez-Menocal L, Wei Y, Pham Si M, St-Pierre M, Li S, Webster K, Goldschmidt-Clermont P, Vazquez-Padron RI. A novel mouse model of in-stent restenosis. Atherosclerosis 2010; 209: 359–366.
- 28 Mittal B, Mishra A, Srivastava A, Kumar S, Garg N. Matrix metalloproteinases in coronary artery disease. Adv Clin Chem 2014; 64: 1–72.
- 29 Ge J, Shen C, Liang C, Chen L, Qian J, Chen H. Elevated matrix metalloproteinase expression after stent implantation is associated with restenosis. Int J Cardiol 2006; 112: 85–90.
- 30 Shabalovskaya SA, Rondelli GC, Undisz AL, Anderegg JW, Burleigh TD, Rettenmayr ME. The electrochemical characteristics of native Nitinol surfaces. Biomaterials 2009; 30: 3662–3671.
- 31
Trépanier C,
Tabrizian M,
Yahia LH,
Bilodeau L,
Piron DL. Effect of modification of oxide layer on NiTi stent corrosion resistance. J Biomed Mater Res 1998; 43: 433–440.
10.1002/(SICI)1097-4636(199824)43:4<433::AID-JBM11>3.0.CO;2-# CAS PubMed Web of Science® Google Scholar
- 32 Ali ZA, Alp NJ, Lupton H, Arnold N, Bannister T, Hu Y, Mussa S, Wheatcroft M, Greaves DR, Gunn J, Channon KM. Increased in-stent stenosis in ApoE knockout mice: Insights from a novel mouse model of balloon angioplasty and stenting. Arterioscler Thromb Vasc Biol 2007; 27: 833–840.
- 33 Inoue T, Croce K, Morooka T, Sakuma M, Node K, Simon DI. Vascular inflammation and repair: implications for re-endothelialization, restenosis, and stent thrombosis. JACC Cardiovasc Interv 2011; 4: 1057–1066.
- 34 Ishikawa Y, Kirikae T, Hirata M, Yoshida M, Haishima Y, Kondo S, Hisatsune K. Local skin response in mice induced by a single intradermal injection of bacterial lipopolysaccharide and lipid A. Infect Immun 1991; 59: 1954–1960.
- 35 Ingersoll MA, Platt AM, Potteaux S, Randolph GJ. Monocyte trafficking in acute and chronic inflammation. Trends Immunol 2011; 32: 470–477.
- 36 Kircher MF, Grimm J, Swirski FK, Libby P, Gerszten RE, Allport JR, Weissleder R. Noninvasive in vivo imaging of monocyte trafficking to atherosclerotic lesions. Circulation 2008; 117: 388–395.
- 37 Ley K, Miller YI, Hedrick CC. Monocyte and macrophage dynamics during atherogenesis. Arterioscler Thromb Vasc Biol 2011; 31: 1506–1516.
- 38 ASTM International. ASTM F86-13. Standard Practice for Surface Preparation and Marking of Metallic Surgical Implants. West Conshohocken, PA: ASTM International; 2013. Available at: www.astm.org.
- 39 Mani G, Feldman MD, Patel D, Agrawal CM. Coronary stents: A materials perspective. Biomaterials 2007; 28: 1689–1710.
- 40 Riepe G, Heintz C, Kaiser E, Chakfé N, Morlock M, Delling M, Imig H. What can we learn from explanted endovascular devices? Eur J Vasc Endovasc Surg 2002; 24: 117–122.
- 41 Kapnisis KK, Halwani DO, Brott BC, Anderson PG, Lemons JE, Anayiotos AS. Stent overlapping and geometric curvature influence the structural integrity and surface characteristics of coronary nitinol stents. J Mech Behav Biomed Mater 2013; 20: 227–236.
- 42 Kapnisis K, Constantinides G, Georgiou H, Cristea DGC, Munteanu DBB, Anderson P, Lemons J, Anayiotos A. Multi-scale mechanical investigation of stainless steel and cobalt-chromium stents. J Mech Behav Biomed Mater 2014; 40C: 240–251.
- 43 Lüscher TF, Steffel J, Eberli FR, Joner M, Nakazawa G, Tanner FC, Virmani R. Drug-eluting stent and coronary thrombosis: Biological mechanisms and clinical implications. Circulation 2007; 115: 1051–1058.
- 44 Pallero MA, Talbert RM, Chen Y-F, Anderson PG, Lemons J, Brott BC, Murphy-Ullrich JE. Stainless steel ions stimulate increased thrombospondin-1-dependent TGF-beta activation by vascular smooth muscle cells: Implications for in-stent restenosis. J Vasc Res 2010; 47: 309–322.
- 45 Larsen K, Cheng C, Tempel D, Parker S, Yazdani S, den Dekker WK, Houtgraaf JH, de Jong R, Swager-Ten HS, Ligtenberg E, Hanson SR, Rowland S, Kolodgie F, Serruys PW, Virmani R, Duckers HJ. Capture of circulatory endothelial progenitor cells and accelerated re-endothelialization of a bio-engineered stent in human ex vivo shunt and rabbit denudation model. Eur Heart J 2012; 33: 120–128.
- 46 Langeveld B, Roks AJM, Tio RA, van Boven ADJ, van der Want JJL, Henning RH, van Beusekom HMM, van der Giessen WJ, Zijlstra F, van Gilst WH. Rat abdominal aorta stenting: A new and reliable small animal model for in-stent restenosis. J Vasc Res 2004; 41: 377–386.
- 47 Taylor AJ, Gorman PD, Kenwood B, Hudak C, Tashko G, Virmani R. A comparison of four stent designs on arterial injury, cellular proliferation, neointima formation, and arterial dimensions in an experimental porcine model. Catheter Cardiovasc Interv 2001; 53: 420–425.
- 48 Chaabane C, Otsuka F, Virmani R, Bochaton-Piallat M-L. Biological responses in stented arteries. Cardiovasc Res 2013; 99: 353–363.
- 49 Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation 2002; 105: 2974–2980.
- 50 Swirski FK, Pittet MJ, Kircher MF, Aikawa E, Jaffer FA, Libby P, Weissleder R. Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci. USA 2006; 103: 10340–10345.
- 51 Eisenblätter M, Ehrchen J, Varga G, Sunderkötter C, Heindel W, Roth J, Bremer C, Wall A. In vivo optical imaging of cellular inflammatory response in granuloma formation using fluorescence-labeled macrophages. J Nucl Med 2009; 50: 1676–1682.