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Aesthetic Plastic Surgery

, Volume 43, Issue 1, pp 233–242 | Cite as

Smooth Muscle Alpha Actin Immunoexpression (α-Sma) and CD-117 Antibody (C-Kit) in Capsules Formed by Polyurethane Foam-Coated Silicone Implants and with Textured Surface: A Study on Rats

  • Eduardo Nascimento SilvaEmail author
  • Jurandir Marcondes Ribas-Filho
  • Fernando Issamu Tabushi
  • Majenna Andrade Pachnicki Silva
  • Elisa Beatriz Dalledone Siqueira
  • Lucia de Noronha
  • Alfredo Benjamim Duarte da Silva
  • Leandro Cavalcante Lipinski
  • Isabelle Guth
  • Larissa Maria Vosgerau
Original Article Basic Science/Experimental
  • 98 Downloads

Abstract

Background

One of the undesirable complications that might occur after breast augmentation with silicone implants is capsular contracture. In its etiology, the relations between mast cells and myofibroblasts play an important role in collagen synthesis. Mast cells are able to activate fibroblasts into myofibroblasts, through paracrine secretions, inducing collagen production. The objectives of this study were to analyze the myofibroblast concentration through the α-SMA immunomarker and evaluate the intensity of mast cell expression against the C-Kit immunomarker.

Material and Method

Sixty-four Wistar rats were used, divided into two groups (polyurethane foam and textured surface) with 32 animals in each. The animals received silicone implants on the back, below the panniculus carnosus, and after the determined period, they were killed and the capsules formed around the implants were studied. The capsules were analyzed employing the immunohistochemical technique, with the α-SMA and C-Kit immunomarkers in subgroups of 30, 50, 70 and 90 days.

Results

The myofibroblast concentration was higher in the polyurethane group when compared to the textured group (30 days p = 0.105; 50 days p = 0.247; 70 days p = 0.014 and 90 days p = 0.536). The intensity of mast cell expression was more pronounced in the polyurethane group when compared to the textured group (30 days p = 0.798; 50 days p = 0.537; 70 days p = 0.094 and 90 days p = 0.536).

Conclusions

Polyurethane-coated implants induced higher concentrations of myofibroblasts and higher expression of mast cells, when compared to the textured surface implants.

No Level Assigned

This journal requires that authors assign a level of evidence to each article. For a full description of these Evidence-Based Medicine ratings, please refer to the Table of Contents or the online Instructions to Authors www.springer.com/00266.

Keywords

Implant capsular contracture Breast implants Mammaplasty Immunohistochemistry 

Notes

Authors’ Contributions

Eduardo Nascimento Silva contributed to conception, design, intellectual and scientific content of the study, technical procedures, and statistical analysis. Jurandir Marcondes Ribas-Filho involved in scientific and intellectual content of the study, interpretation of data, critical revision and final approval. Fernando Issamu Tabushi and Alfredo Benjamim Duarte da Silva helped in scientific and intellectual content of the study, interpretation of data and critical revision. Majenna Andrade Pachnicki Silva contributed to acquisition of data, technical procedures and manuscript preparation. Elisa Beatriz Dalledone Siqueira involved in conception, design, intellectual and scientific content of the study. Lucia de Noronha performed interpretation of data and histopathological examinations. Leandro Cavalcante Lipinski helped in scientific content of the study and technical procedures. Isabelle Guth and Larissa Maria Vosgerau contributed to acquisition of data and technical procedures.

Compliance with Ethical Standards

Ethics Committee Approval

State University of Ponta Grossa (UEPG).

Supplementary material

Supplementary material 1 (MP4 73874 kb)

Supplementary material 2 (MP4 61689 kb)

References

  1. 1.
    Maxwell GP, Gabriel A (2014) The evolution of breast implants. Plast Reconstr Surg 134(1S):12S–17SGoogle Scholar
  2. 2.
    Mendes PRS, Bins-Ely J, Lima EAS, Vasconcellos ZAA, D’acampora AJ, Neves RE (2008) Histological study on acute inflammatory reaction to polyurethane-coated silicone implants in rats. Acta Cir Bras 23(1):93–101Google Scholar
  3. 3.
    Major MR, Wong VW, Longaker MT, Gurtner GC (2015) The foreign body response: at the interface of surgery and bioengineering. Plast Reconstr Surg 135(5):1489–1498Google Scholar
  4. 4.
    Poeppl N, Schreml S, Lichtenegger F, Lenich A, Eisenmann-Klein M, Prantl L (2007) Does the surface structure of implants have an impact on the formation of a capsular contracture? Aesthet Plast Surg 31(2):133–139Google Scholar
  5. 5.
    Araco A, Caruso R, Araco F, Gravante JOG (2009) Capsular contractures: a systematic review. Plast Reconstr Surg 124(6):1808–1819Google Scholar
  6. 6.
    Moyer KE, Ehrlich HP (2013) Capsular contracture after breast reconstruction: collagen fiber orientation and organization. Plast Reconstr Surg 131(4):680–685Google Scholar
  7. 7.
    Lu F, Gao J, Ogawa R, Hyakusoku H (2007) Variations in gap junctional intercellular communication and connexin expression in fibroblasts derived from keloid and hypertrophic scars. Plast Reconstr Surg 119(3):844–851Google Scholar
  8. 8.
    Wiener TC (2008) Relationship of incision choice to capsular contracture. Aesthet Plast Surg 32(2):303–306Google Scholar
  9. 9.
    Younan GJ, Heit YI, Dastouri P, Kekhia H, Xing W, Gurish MF, Orgill DP (2011) Mast cells are required in the proliferation and remodeling phases of microdeformational wound therapy. Plast Reconstr Surg 128(6):649e–658eGoogle Scholar
  10. 10.
    Arad E, Navon-Venezia S, Gur E, Kuzmenko B, Glick R, Frenkiel-Krispin D, Kramer E, Carmeli Y, Barnea Y (2013) Novel rat model of methicillin-resistant Staphylococcus aureus-infected silicone breast implants: a study of biofilm pathogenesis. Plast Reconstr Surg 131(2):205–214Google Scholar
  11. 11.
    Jacombs A, Tahir S, Hu H, Deva AK, Almatroudi A, Wessels WLF, Bradshaw DA, Vickery K (2014) In vitro and in vivo investigation of the influence of implant surface on the formation of bacterial biofilm in mammary implants. Plast Reconstr Surg 133(4):471e–480eGoogle Scholar
  12. 12.
    Bergmann PA, Tamouridis G, Lohmeyer JA, Mauss KL, Becker B, Knobloch J, Mailänder P, Siemers F (2014) The effect of a bacterial contamination on the formation of capsular contracture with polyurethane breast implants in comparison with textured silicone implants—an animal study. J Plast Reconstr Aesthet Surg 67(10):1364–1370Google Scholar
  13. 13.
    Kyle DJT, Bayat A (2015) Enhanced contraction of a normal breast-derived fibroblast-populated three-dimensional collagen lattice via contracted capsule fibroblast-derived paracrine factors: functional significance in capsular contracture formation. Plast Reconstr Surg 135(5):1413–1429Google Scholar
  14. 14.
    Frame J, Kamel D, Olivan M, Cintra H (2015) The in vivo pericapsular tissue response to modern polyurethane breast implants. Aesthet Plast Surg 39(5):713–723Google Scholar
  15. 15.
    Silva EN, Ribas-Filho JM, Czeczko NG, Pachnicki JPA, Montemor Netto MR, Lipinski LC, Noronha L, Colman J, Zeni JO, Carvalho CA (2016) Histological evaluation of capsules formed by silicon implants coated with polyurethane foam and with a textured surface in rats. Acta Cir Bras 31(12):774–782Google Scholar
  16. 16.
    Segreto F, Carotti S, Tosi D, Pendolino AL, Marangi GF, Morini S, Persichetti P (2016) Toll-like receptor 4 expression in human breast implant capsules: localization and correlation with estrogen receptors. Plast Reconstr Surg 137(3):792–798Google Scholar
  17. 17.
    Danino MA, Nizard N, Paek LS, Govshievich A, Giot JP (2017) Do bacteria and biofilm play a role in double-capsule formation around macrotextured implants? Plast Reconstr Surg 140(5):878–883Google Scholar
  18. 18.
    Calobrace MB, Capizzi PJ (2014) The biology and evolution of cohesive gel and shaped implants. Plast Reconstr Surg 134(1S):6S–11SGoogle Scholar
  19. 19.
    Duxbury PJ, Harvey JR (2016) Systematic review of the effectiveness of polyurethane-coated compared with textured silicone implants in breast surgery. J Plast Reconstr Aesthet Surg 69(4):452–460Google Scholar
  20. 20.
    Adams WP, Culbertson EJ, Deva AK, Magnusson MR, Layt C, Jewell ML, Mallucci P, Héden P (2017) Macrotextured breast implants with defined steps to minize bacterial contamination around the device: experience in 42.000 implants. Plast Reconstr Surg 140(3):427–431Google Scholar
  21. 21.
    Barr S, Hill EW, Bayat A (2017) Functional biocompatibility testing of silicone breast implants and a novel classification system based on surface roughness. J Mech Behav Biomed Mater 75:75–81Google Scholar
  22. 22.
    Vieira JV, D’Acampora AJ, Marcos ABW, di Giunta G, Vasconcellos ZAA, Ely JB, Neves RE, Figueiredo CP (2010) Vascular endothelial growth factor overexpression positively modulates the characteristics of periprosthetic tissue of polyurethane-coated silicone breast implant in rats. Plast Reconstr Surg 126(6):1899–1910Google Scholar
  23. 23.
    Abramo AC, de Oliveira VR, Ledo-Silva MC, de Oliveira EL (2010) How texture-inducing contraction vectors affect the fibrous capsule shrinkage around breasts implants? Aesthet Plast Surg 34(5):555–560Google Scholar
  24. 24.
    Minami E, Koh IHJ, Ferreira JCR, Waitzberg AFL, Chifferi V, Rosewick TF, Pereira MD, Saldiva PHN, Figueiredo LFP (2006) The composition and behavior of capsules around smooth and textured breast implants in pigs. Plast Reconstr Surg 118(4):874–884Google Scholar
  25. 25.
    Balderrama CMSR, Ribas-Filho JM, Malafaia O, Czeczko NG, Dietz UA, Sakamoto DG, Bittencourt LPM (2009) Healing reaction to mammary prostheses covered by textured silicone and silicone foam in rats. Acta Cir Bras 24(5):367–376Google Scholar
  26. 26.
    Loch-Wilkinson A, Knight KJBRJW, Wessels WLF, Magnusson M, Papadopoulos T, Connell T, Lofts J, Locke M, Hopper I, Cooter R, Vickery K, Prince HM, Deva AK (2017) Breast implant-associated anaplastic large cell lymphoma in Australia and New Zealand: high-surface-area textured implants are associated with increased risk. Plast. Reconstr. Surg. 140(4):645–654Google Scholar
  27. 27.
    Foley TT, Saggers GC, Moyer KE, Ehrlich HP (2011) Rat mast cells enhance fibroblast proliferation and fibroblast-populated collagen lattice contraction trough gap junctional intercellular communications. Plast Reconstr Surg 127(4):1478–1486Google Scholar
  28. 28.
    Foley TT, Ehrlich HP (2013) Through gap junction communications, co-cultured mast cells and fibroblasts generate fibroblasts activities allied with hypertrophic scarring. Plast Reconstr Surg 133(5):1036–1044Google Scholar
  29. 29.
    Foley TT, Ehrlich HP (2014) Mast cells prevent dexamethasone-induced cell death of cultured fibroblasts: relationship to gap junctional intercellular communications. Plast Reconstr Surg 133(5):638e–644eGoogle Scholar
  30. 30.
    Brazin J, Malliaris S, Groh B, Mehrara B, Hidalgo D, Otterburn D, Silver RB, Spector JA (2014) Mast cells in the periprosthetic breast capsule. Aesthet Plast Surg 38(3):592–601Google Scholar
  31. 31.
    Isenberg JS (2014) Time spent before the mast: an emerging role for mast cells in prosthetic breast implant capsule formation. Aesthet Plast Surg 38(4):815–816Google Scholar
  32. 32.
    Bresnick SD (2017) Prophylactic leukotriene inhibitor therapy for the reduction of capsular contracture in primary silicone breast augmentation: experience with over 1100 cases. Plast Reconstr Surg 139(2):379e–385eGoogle Scholar
  33. 33.
    Chen H, Xu Y, Yang G, Zhang Q, Huang X, Yu L, Dong X (2017) Mast cell chymase promotes hypertrophic scar fibroblast proliferation and collagen synthesis by activating TGF-β1/ Smads signaling pathway. Exp Ther Med 14(5):4438–4442Google Scholar
  34. 34.
    Moreira M, Fagundes DJ, Simões MJ, Oliveira MCBM, Previdelli ITS, Moreira AC (2009) Zafirlukast pocket delivery impairs the capsule healing around textured implants in rats. Aesthet Plast Surg 33(1):90–97Google Scholar
  35. 35.
    Pistorio AL, Ehrlich HP (2011) Modulatory effects of connexin-43 expression on gap junction intercellular communications with mast cells and fibroblasts. J Cell Biochem 112(5):1441–1449Google Scholar
  36. 36.
    Prantl L, Schreml S, Fichtner-Feigl S, Pöppl N, Eisenmann-Klein M, Schwarze H, Füchtmeier B (2007) Clinical and morphological conditions in capsular contracture formed around silicone breast implants. Plast Reconstr Surg 120(1):275–284Google Scholar
  37. 37.
    Graf R, Ascenço ASK, Freitas R, Balbinot P, Peressutti C, Costa DFB, Santos FHCR, Ratti MAS, Kulchetscki RM (2015) Prevention of capsular contracture using leukotriene antagonists. Plast Reconstr Surg 136(5):592e–596eGoogle Scholar
  38. 38.
    Ceua-Fiocruz (2008) Manual de Utilização de Animais/FIOCRUZ. 1ª Ed. Ministério da Saúde, Rio de Janeiro: FIOCRUZGoogle Scholar
  39. 39.
    Avninder S, Ylaya K, Hewitt SM (2008) Tissue microarray: a simple technology that has revolutionized research in pathology. J Postgrad Med 54(2):158–162Google Scholar
  40. 40.
    Zwieten A (2013) Tissue microarray technology and findings for diagnostic immunohistochemistry. Pathology 45(1):71–79Google Scholar
  41. 41.
    Lee SG, Lee SD, Kim MK, Ryu WS, Jung SP, Kim S, Kim HY, Yoon ES, Kim CH, Nam SJ, Bae JW (2015) Effect of antiadhesion barrier solution and fibrin on capsular formation after silicone implant insertion in a white rat model. Aesthet Plast Surg 39(1):162–170Google Scholar
  42. 42.
    Unlu RE, Yilmaz AD, Orbay H, Can B, Tekdemir I, Sensoz O (2007) Influence of rifampin on capsule formation around silicone implants in a rat model. Aesthet Plast Surg 31(4):358–364Google Scholar
  43. 43.
    Bastos EM, Neto MS, Garcia EB, Veiga DF, Han YA, Denadai R, Santos RA, Ferreira LM (2007) Effect of zafirlukast on capsular contracture around silicone implants in rats. Aesthet Plast Surg 31(5):559–565Google Scholar
  44. 44.
    Vieira JV, D’Acampora A, Neves FS, Mendes PR, Vasconcellos ZAA, Ely JB, Neves RE, Figueiredo CP (2016) Capsular contracture in silicone breast implants: insights from rat models. An Acad Bras Cienc 88(3):1459–1470Google Scholar
  45. 45.
    Boyko TV, Longaker MT, Yang GP (2017) Laboratory models for the study of normal and pathologic wound healing. Plast Reconstr Surg 139(3):654–662Google Scholar
  46. 46.
    Wagenführ Júnior J (2007) Comparative histopathological analysis of coverings from silicone and polyurethane foams implanted in mice. ReSoc Bras Cir Plast 22(1):19–23Google Scholar
  47. 47.
    Haddad Filho D, Zveibel DK, Alonso N, Gemperli R (2007) Comparison between textured silicone implants and those bonded with expanded polytetrafluoroethylene in rats. Acta Cir Bras 22(3):187–194Google Scholar
  48. 48.
    Gancedo M, Ruiz-Corro L, Salazar-Montes A, Rincón AR, Armendáriz-Borunda J (2008) Pirfenidone prevents capsular contracture after mammary implantation. Aesthet Plast Surg 32(1):32–40Google Scholar
  49. 49.
    Wagenführ Júnior J, Ribas-Filho JM, Nascimento MM, Ribas FM, Wanka MV, Godoi AL (2012) Histopathological reaction over prosthesis surface covered with silicone and polyurethane foam implanted in rats. Acta Cir Bras 27(12):866–873Google Scholar
  50. 50.
    Bui JM, Perry TA, Ren CD, Nofrey B, Teitelbaum S, Epps DE (2015) Histological characterization of human breast implant capsules. Aesthet Plast Surg 39(3):306–315Google Scholar
  51. 51.
    Thevenot T, Baker DW, Weng H, Sun M, Tang L (2011) The pivotal role of fibrocytes and mast cells in mediating fibrotic reactions to biomaterials. Biomaterials 32(33):8394–8403Google Scholar
  52. 52.
    Hwang K, Sim HB, Huan F, Kim DJ (2010) Myofibroblasts and capsular tissue tension in breast capsular contracture. Aesthet Plast Surg 34(6):716–721Google Scholar
  53. 53.
    Rocha-De-souza CM, Berent-Maoz B, Mankuta D, Moses AE, Levi-Schaffer F (2008) Human mast cell activation by Staphylococcus aureus: interleukin-8 and tumor necrosis factor alpha release and the role of toll-like receptor 2 and CD48 molecules. Infect Immun 76(10):4489–4497Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature and International Society of Aesthetic Plastic Surgery 2018

Authors and Affiliations

  • Eduardo Nascimento Silva
    • 1
    • 2
    Email author
  • Jurandir Marcondes Ribas-Filho
    • 1
  • Fernando Issamu Tabushi
    • 1
  • Majenna Andrade Pachnicki Silva
    • 3
  • Elisa Beatriz Dalledone Siqueira
    • 1
  • Lucia de Noronha
    • 4
  • Alfredo Benjamim Duarte da Silva
    • 2
    • 5
  • Leandro Cavalcante Lipinski
    • 6
  • Isabelle Guth
    • 1
  • Larissa Maria Vosgerau
    • 1
  1. 1.Evangelical Faculty of Medicine of Paraná (FEPAR)Evangelical University Hospital of Curitiba (HUEC) and Institute for Medical Research (IPEM)CuritibaBrazil
  2. 2.Plastic Surgery and AnatomyState University of Ponta Grossa (UEPG)Ponta GrossaBrazil
  3. 3.Ponta GrossaBrazil
  4. 4.Anatomical PathologyPontifical Catholic University of Paraná (PUC-PR)CuritibaBrazil
  5. 5.Operative TechniqueFederal University of Paraná (UFPR)CuritibaBrazil
  6. 6.Operative TechniqueState University of Ponta Grossa (UEPG)Ponta GrossaBrazil

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