Advertisement

Inflammation

, Volume 42, Issue 2, pp 721–730 | Cite as

Breast Implant Texturization Does Not Affect the Crosstalk Between MSC and ALCL Cells

  • Monia OrcianiEmail author
  • Miriam Caffarini
  • Matteo Torresetti
  • Anna Campanati
  • Piercamillo Parodi
  • Giovanni Di Benedetto
  • Roberto Di Primio
ORIGINAL ARTICLE
  • 331 Downloads

Abstract

In the last decade, there has been a growing interest about the possible association between anaplastic large cell lymphoma (ALCL) and breast implants (BIA-ALCL). Many variables, such as breast implants texturization, have been investigated. Breast implants often lead to the formation of a periprosthetic capsule, characterized by inflammation. The presence of the inflamed capsule has been found in the majority of patients with BIA-ALCL. Inflammation may be sustained or counteracted by mesenchymal stem cells (MSCs) by the secretion of pro- or anti-inflammatory cytokines. MSCs were isolated from three capsules surrounding micro-textured (micro-MSCs) and from three capsules surrounding macro-textured (macro-MSCs) implants; after characterization, MSCs were co-cultured with KI-JK cells (a cell line derived from the cutaneous form of ALCL). The secretion of cytokines related to inflammation, the proliferation rate, and the expression of genes referred to pro-tumoral mechanisms were evaluated. Co-cultures of KI-JK cells with micro- or macro-MSCs gave the same results about the secretion of cytokines (increase of IL10, G-CSF, and TGF-β1 and decrease of IL4, IL5, IL12, IL13, IL17A, IFN-γ (p < 0.05) with respect to mock sample), expression of selected genes (increase for ACVR1, VEGF, TGF-βR2, CXCL12, and MKi67 (p < 0.05) with respect to control sample), and the proliferation rate (no variation between mock and co-cultured samples). Our results suggest that MSCs derived from capsules surrounding micro- and macro-textured implants display the same effects on the ALCL cells.

KEY WORDS

breast implants mesenchymal stem cells inflammation texturization ALCL 

Notes

Compliance with Ethical Standards

This study was approved by the Università Politecnica delle Marche Ethical Commitee and was conducted in accordance with the Declaration of Helsinki.

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10753_2018_930_Fig5_ESM.png (913 kb)
Supplementary Fig. 1

Flow cytometry results of micro-MSCs cells (a) and macro-MSCs (b). Representative FACScan analyses of cell-surface antigen expression, as indicated. Solid gray histograms refer to the negative control (IgG1 isotype control-FITC labeled). No significative differences were noted among the six cultures of MSCs. (PNG 912 kb)

10753_2018_930_MOESM1_ESM.tif (229 kb)
High resolution image (TIF 228 kb)
10753_2018_930_Fig6_ESM.png (3.5 mb)
Supplementary Fig. 2

Mesenchymal differentiation from micro-MSCs (a-b-c-d) and macro-MSCs (e-f-g-h). Representative images of osteogenic differentiation assessment by ALP staining (a, e) and identification of CaPO4 crystals by von Kossa reaction (b, f); adipocyte differentiation confirmed by Oil red staining (c, g); chondrogenic differentiation demonstrated by positive acid mucopolisaccarid coloration by Safranin-O (d, h). No differences were noted among micro- and macro-MSCs. Scale bar 50um (PNG 3615 kb)

10753_2018_930_MOESM2_ESM.tif (879 kb)
High resolution image (TIF 879 kb)

References

  1. 1.
    Ramos-Gallardo, G., J. Cuenca-Pardo, E. Rodríguez-Olivares, R. Iribarren-Moreno, L. Contreras-Bulnes, A. Vallarta-Rodríguez, M. Kalixto-Sanchez, C. Hernández, R. Ceja-Martinez, and C. Torres-Rivero. 2017. Breast implant and anaplastic large cell lymphoma meta-analysis. Journal of Investigative Surgery 30: 56–65.CrossRefGoogle Scholar
  2. 2.
    Brody, G.S., D. Deapen, C.R. Taylor, L. Pinter-Brown, S.R. House-Lightner, J.S. Andersen, G. Carlson, M.G. Lechner, and A.L. Epstein. 2015. Anaplastic large cell lymphoma occurring in women with breast implants: Analysis of 173 cases. Plastic and Reconstructive Surgery 135: 695–705.CrossRefGoogle Scholar
  3. 3.
    Gidengil, C.A., Z. Predmore, S. Mattke, K. van Busum, and B. Kim. 2015. Breast implant-associated anaplastic large cell lymphoma: A systematic review. Plastic and Reconstructive Surgery 135: 713–720.CrossRefGoogle Scholar
  4. 4.
    O'Neill, A.C., T. Zhong, and S.O.P. Hofer. 2017. Implications of breast implant-associated anaplastic large cell lymphoma (BIA-ALCL) for breast cancer reconstruction: An update for surgical oncologists. Annals of Surgical Oncology 24: 3174–3319.CrossRefGoogle Scholar
  5. 5.
    Richardson, K., T. Alrifai, K. Grant-Szymanski, G.J. Kouris, P. Venugopal, B. Mahon, and R. Karmali. 2017. Breast implant-associated anaplastic large-cell lymphoma and the role of brentuximab vedotin (SGN-35) therapy: A case report and review of the literature. Molecular and Clinical Oncology 6 (5): 39–542.Google Scholar
  6. 6.
    Kim, B., Z.S. Predmore, S. Mattke, K. van Busum, and C.A. Gidengil. 2015. Breast implant-associated anaplastic large cell lymphoma: Updated results from a structured expert consultation process. Plastic and Reconstructive Surgery Global Open 3: e296.CrossRefGoogle Scholar
  7. 7.
    Kadin, M.E., A. Deva, H. Xu, J. Morgan, P. Khare, R.A.F. MacLeod, B.W. van Natta, W.P. Adams Jr., G.S. Brody, and A.L. Epstein. 2016. Biomarkers provide clues to early events in the pathogenesis of breast implant-associated anaplastic large cell lymphoma. Aesthetic Surgery Journal 36: 773–781.CrossRefGoogle Scholar
  8. 8.
    Hu, H., A. Jacombs, K. Vickery, S.L. Merten, D.G. Pennington, and A.K. Deva. 2015. Chronic biofilm infection in breast implants is associated with an increased T-cell lymphocytic infiltrate: Implications for breast implant-associated lymphoma. Plastic and Reconstructive Surgery 135: 319–329.CrossRefGoogle Scholar
  9. 9.
    Thompson, P.A., and H.M. Prince. 2013. Breast implant-associated anaplastic large cell lymphoma: A systematic review of the literature and mini-meta analysis. Current Hematologic Malignancy Reports 8: 196–210.CrossRefGoogle Scholar
  10. 10.
    Headon, H., A. Kasem, and K. Mokbel. 2015. Capsular contracture after breast augmentation: An update for clinical practice. Plastic and Reconstructive Surgery Global Open 42: 532–543.Google Scholar
  11. 11.
    Loch-Wilkinson, A., K. Beath, R.J.W. Knight, W.L.F. Wessels, M. Magnusson, T. Papadopoulos, T. Connell, J. Lofts, M. Locke, I. Hopper, R. Cooter, K. Vickery, P.A. Joshi, H.M. Prince, and A.K. Deva. 2017. Breast implant associated anaplastic large cell lymphoma in Australia and New Zealand—High surface area textured implants are associated with increased risk. Plastic and Reconstructive Surgery Global Open 140: 645–654.CrossRefGoogle Scholar
  12. 12.
    U.S. Food and Drug Administration Center for Breast Implant-Associated Anaplastic Large Cell Lymphoma (BIA-ALCL). https://www.fda.gov/MedicalDevices/ProductsandMedicalProcedures/ImplantsandProsthetics/BreastImplants/ucm239995.htm. Accessed 10 Jan 2018.
  13. 13.
    Lacy, P., and J.L. Stow. 2011. Cytokine release from innate immune cells: Association with diverse membrane trafficking pathways. Blood 118: 9–18.CrossRefGoogle Scholar
  14. 14.
    Kyurkchiev, D., I. Bochev, E. Ivanova-Todorova, M. Mourdjeva, T. Oreshkova, K. Belemezova, and S. Kyurkchiev. 2014. Secretion of immunoregulatory cytokines by mesenchymal stem cells. Plastic and Reconstructive Surgery Global Open 6: 552–570.Google Scholar
  15. 15.
    Paino, F., M. La Noce, D. Di Nucci, et al. 2017. Human adipose stem cell differentiation is highly affected by cancer cells both in vitro and in vivo: Implication for autologous fat grafting. Cell Death & Disease 8: e2568.CrossRefGoogle Scholar
  16. 16.
    La Noce, M., L. Mele, V. Tirino, et al. 2014. Neural crest stem cell population in craniomaxillofacial development and tissue repair. European Cells & Materials 28: 348–357.CrossRefGoogle Scholar
  17. 17.
    Sasser, A.K., B.L. Mundy, K.M. Smith, A.W. Studebaker, A.E. Axel, A.M. Haidet, S.A. Fernandez, and B.M. Hall. 2007. Human bone marrow stromal cells enhance breast cancer cell growth rates in a cell line-dependent manner when evaluated in 3D tumor environments. Cancer Lett 254:255–264.Google Scholar
  18. 18.
    Ma, S., N. Xie, W. Li, B. Yuan, Y. Shi, and Y. Wang. 2014. Immunobiology of mesenchymal stem cells. Cell Death and Differentiation 21: 216–225.CrossRefGoogle Scholar
  19. 19.
    Klopp, A.H., A. Gupta, E. Spaeth, M. Andreeff, and F. Marini III. 2011. Concise review: Dissecting a discrepancy in the literature: Do mesenchymal stem cells support or suppress tumor growth? Stem Cells 29: 11–19 Review.CrossRefGoogle Scholar
  20. 20.
    Orciani, M., R. Lazzarini, M. Scartozzi, E. Bolletta, M. Mattioli-Belmonte, A. Scalise, G. di Benedetto, and R. di Primio. 2013. The response of breast cancer cells to mesenchymal stem cells: A possible role of inflammation by breast implants. Plastic and Reconstructive Surgery 132: 899e–910e.CrossRefGoogle Scholar
  21. 21.
    Orciani, M., E. Bolletta, A. Campanati, G. Di Benedetto, and R. Di Primio. 2014. The response of breast cancer cells to mesenchymal stem cells: A possible role of inflammation by breast implants. Plastic and Reconstructive Surgery 134: 994e–996e.CrossRefGoogle Scholar
  22. 22.
    Orciani, M., G. Sorgentoni, M. Torresetti, R. Di Primio, and G. Di Benedetto. 2016. MSCs and inflammation: New insights into the potential association between ALCL and breast implants. Breast Cancer Research and Treatment 156: 65–72.CrossRefGoogle Scholar
  23. 23.
    Dominici, M., K. Le Blanc, I. Mueller, et al. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315–317.CrossRefGoogle Scholar
  24. 24.
    Halfon, S., N. Abramov, B. Grinblat, and I. Ginis. 2011. Markers distinguishing mesenchymal stem cells from fibroblasts are downregulated with passaging. Stem Cells and Development 20: 53–66.CrossRefGoogle Scholar
  25. 25.
    Lazzarini, R., F. Olivieri, C. Ferretti, M. Mattioli-Belmonte, R. Di Primio, and M. Orciani. 2014. mRNAs and miRNAs profiling of mesenchymal stem cells derived from amniotic fluid and skin: The double face of the coin. Cell and Tissue Research 355: 121–130.CrossRefGoogle Scholar
  26. 26.
    Keech, J.A., Jr., and B.J. Creech. 1997. Anaplastic T-cell lymphoma in proximity to a saline-filled breast implant. Plastic and Reconstructive Surgery 100: 554–555.CrossRefGoogle Scholar
  27. 27.
    U.S. Food and Drug Administration Center for Devices and Radiological Health. 2011. FDA medical device safety communication: Reports of anaplastic large cell lymphoma (ALCL) in women with breast implants. http://wayback.archive-it.org/7993/20170722214256/https://www.fda.gov/MedicalDevices/Safety/AlertsandNotices/ucm240000.htm. Accessed 10 Jan 2018.
  28. 28.
    Johnson, L., J.M. O'Donoghue, N. McLean, P. Turton, A.A. Khan, S.D. Turner, A. Lennard, N. Collis, M. Butterworth, G. Gui, J. Bristol, J. Hurren, S. Smith, K. Grover, G. Spyrou, K. Krupa, I.A. Azmy, I.E. Young, J.J. Staiano, H. Khalil, and F.A. MacNeill. 2017. Breast implant associated anaplastic large cell lymphoma: The UK experience. Recommendations on its management and implications for informed consent. European Journal of Surgical Oncology 43: 1393–1401.CrossRefGoogle Scholar
  29. 29.
    Clemens, M.W., and S.M. Horwitz. 2017. NCCN consensus guidelines for the diagnosis and management of breast implant-associated anaplastic large cell lymphoma. Aesthetic Surgery Journal 37: 285–289.CrossRefGoogle Scholar
  30. 30.
    Lee, Y.S., A. Filie, D. Arthur, A.T. Fojo, and E.S. Jaffe. 2015. Breast-implant-associated anaplastic large cell lymphoma in a patient with Li-Fraumeni syndrome. Histopathology 67: 925–927.CrossRefGoogle Scholar
  31. 31.
    Hwang, M.J., H. Brown, R. Murrin, N. Momtahan, and G.D. Sterne. 2015. Breast implant-associated anaplastic large cell lymphoma: A case report and literature review. Aesthetic Plastic Surgery 39: 391–395.CrossRefGoogle Scholar
  32. 32.
    Xu, J., and S. Wei. 2014. Breast implant-associated anaplastic large cell lymphoma: Review of a distinct clinicopathologic entity. Archives of Pathology & Laboratory Medicine 138: 842–846.CrossRefGoogle Scholar
  33. 33.
    Meza Britez, M.E., C. Caballero Llano, and A. Chaux. 2012. Periprosthetic breast capsules and immunophenotypes of inflammatory cells. European Journal of Plastic Surgery 35: 647–651.CrossRefGoogle Scholar
  34. 34.
    Bizjak, M., C. Selmi, S. Praprotnik, O. Bruck, C. Perricone, M. Ehrenfeld, and Y. Shoenfeld. 2015. Silicone implants and lymphoma: The role of inflammation. Journal of Autoimmunity 65: 64–73.CrossRefGoogle Scholar
  35. 35.
    Barnsley, G.P., L.J. Sigurdson, and S.E. Barnsley. 2006. Textured surface breast implants in the prevention of capsular contracture among breast augmentation patients: A meta-analysis of randomized controlled trials. Plastic and Reconstructive Surgery 117: 2182–2190.CrossRefGoogle Scholar
  36. 36.
    Wong, C.H., M. Samuel, B.K. Tan, and C. Song. 2006. Capsular contracture in subglandular breast augmentation with textured versus smooth breast implants: A systematic review. Plastic and Reconstructive Surgery 118: 1224–1236.CrossRefGoogle Scholar
  37. 37.
    Liu, X., L. Zhou, F. Pan, Y. Gao, X. Yuan, and D. Fan. 2015. Comparison of the postoperative incidence rate of capsular contracture among different breast implants: A cumulative meta-analysis. PLoS One 10: e0116071.CrossRefGoogle Scholar
  38. 38.
    Stevens, W.G., M.Y. Nahabedian, M.B. Calobrace, J.L. Harrington, P.J. Capizzi, R. Cohen, R.C. d’Incelli, and M. Beckstrand. 2013. Risk factor analysis for capsular contracture: A 5-year Sientra study analysis using round, smooth, and textured implants for breast augmentation. Plastic and Reconstructive Surgery 132: 1115–1123.CrossRefGoogle Scholar
  39. 39.
    Boulland, M.L., V. Meignin, K. Leroy-Viard, C. Copie-Bergman, J. Brière, R. Touitou, P. Kanavaros, and P. Gaulard. 1998. Human interleukin-10 expression in T/natural killer-cell lymphomas association with anaplastic large cell lymphomas and nasal natural killer-cell lymphomas. The American Journal of Pathology 153: 1229–1237.CrossRefGoogle Scholar
  40. 40.
    Bianchi, A., S. Vallese, and O. Annibali. 2018. PD-L1/PD-1 check point in anaplastic large cell lymphoma, ALK+: A case report with Immunohistochemical and molecular study. Plastic and Reconstructive Surgery Global Open 3: 1.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Clinical and Molecular Sciences- HistologyUniversità Politecnica delle MarcheAnconaItaly
  2. 2.Department of Experimental and Clinical Medicine – Clinic of Plastic and Reconstructive SurgeryUniversità Politecnica delle MarcheAnconaItaly
  3. 3.Department of Clinical and Molecular Sciences- Clinic of DermatologyUniversità Politecnica delle MarcheAnconaItaly
  4. 4.Clinic of Plastic and Reconstructive Surgery of UdineUniversity of UdineUdineItaly

Personalised recommendations