Skip to main content
SpringerLink
Log in

Histomorphometric analysis of implant osseointegration using hydrophilic implants in diabetic rats

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

To evaluate peri-implant bone formation of titanium implants using an in vivo rat model with and without uncontrolled diabetes mellitus (DM) to evaluate osseointegration of hydrophobic (Neoporos®) and hydrophilic (Acqua®) surfaces.

Materials and methods

54 rats were divided into two groups: DM group (DMG) (streptozotocin-induced diabetes) and a control group (CG). Implants with hydrophobic (Neoporos®) and hydrophilic surfaces (Acqua®) were placed in the left or right tibia of animals. Animals were further divided into three groups (n = 9) euthanized after 7, 14, or 28 days. Bone-to-implant contact (BIC) and bone area fraction occupancy (BAFO) were assessed in total, cortical, and medullary areas.

Results

The DMG group, after a 7-day healing period, yielded with the Acqua implants presented significantly higher total BIC (+37.9%; p=0.03) and trabecular BIC (%) (+46.3%; p=0.02) values in comparison to the Neoporos implants. After 28 days of healing, the CG yielded that the cortical BAFO of Acqua implants to be significantly, 14%, higher (p=0.04) than Neoporos implants.

Conclusion

The positive effects of the Acqua surface were able to counteract the adverse impact of uncontrolled DM at early osseointegration periods. After 28 days in vivo, the metabolic systemic impairment caused by DM overcame the surface treatment effect, leading to impaired osseointegration in both hydrophilic and hydrophobic implants.

Clinical relevance

The adverse effects of diabetes mellitus with respect to bone healing may be minimized by deploying implants with strategically modified surfaces. This study evaluated the effects of implants with Acqua® and Neoporos® surfaces in both diabetic and healthy animals. During the initial healing period in diabetic animals, the hydrophilic surface was demonstrated to have beneficial effect on osseointegration in comparison to the hydrophobic surface. The results provide an insight into early healing, but the authors suggest that a future short-term and long-term clinical study is needed to assess the possible benefit of the Acqua® implant as well as in increasing the predictability of implant osseointegration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Association AD (2013) Diagnosis and classification of diabetes mellitus. Diabetes Care 36:S67–S74. https://doi.org/10.2337/dc13-S067

    Article  Google Scholar 

  2. Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, Guariguata L, Motala AA, Ogurtsova K, Shaw JE, Bright D, Williams R, IDF Diabetes Atlas Committee (2019) Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract 157:107843. https://doi.org/10.1016/j.diabres.2019.107843

    Article  PubMed  Google Scholar 

  3. World Health Organization Diabetes. Retrivied from https://www.who.int/news-room/fact-sheets/detail/diabetes

  4. Care D, Suppl SS (2020) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2020. Diabetes Care 43:S14–S31. https://doi.org/10.2337/dc20-S002

    Article  Google Scholar 

  5. Kasperk C, Georgescu C, Nawroth P (2017) Diabetes mellitus and bone metabolism. Exp Clin Endocrinol Diabetes 125:213–217. https://doi.org/10.1055/s-0042-123036

    Article  PubMed  Google Scholar 

  6. Murray CE, Coleman CM (2019) Impact of diabetes mellitus on bone health. Int J Mol Sci 20:4873. https://doi.org/10.3390/ijms20194873

    Article  PubMed Central  Google Scholar 

  7. Monje A, Catena A, Borgnakke WS (2017) Association between diabetes mellitus/hyperglycaemia and peri-implant diseases: systematic review and meta-analysis. J Clin Periodontol 44:636–648. https://doi.org/10.1111/jcpe.12724

    Article  PubMed  Google Scholar 

  8. Katyayan PA, Katyayan M, Shah RJ (2013) Rehabilitative considerations for dental implants in the diabetic patient. J Indian Prosthodont Soc 13:175–183. https://doi.org/10.1007/s13191-012-0207-9

    Article  PubMed  Google Scholar 

  9. Jiao H, Xiao E, Graves DT (2015) Diabetes and its effect on bone and fracture healing. Curr Osteoporos Rep 13:327–335. https://doi.org/10.1007/s11914-015-0286-8

    Article  PubMed  PubMed Central  Google Scholar 

  10. Oates TW, Dowell S, Robinson M, McMahan CA (2009) Glycemic control and implant stabilization in type 2 diabetes mellitus. J Dent Res 88:367–371. https://doi.org/10.1177/0022034509334203

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kanazawa I, Sugimoto T (2018) Diabetes mellitus-induced bone fragility. Intern Med 57:2773–2785. https://doi.org/10.2169/internalmedicine.0905-18

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chrcanovic BR, Albrektsson T, Wennerberg A (2014) Reasons for failures of oral implants. J Oral Rehabil 41:443–476. https://doi.org/10.1111/joor.12157

    Article  PubMed  Google Scholar 

  13. De Molon RS, Morais-Camilo JAND, Verzola MHA et al (2013) Impact of diabetes mellitus and metabolic control on bone healing around osseointegrated implants: removal torque and histomorphometric analysis in rats. Clin Oral Implants Res 24:831–837. https://doi.org/10.1111/j.1600-0501.2012.02467.x

    Article  PubMed  Google Scholar 

  14. Naujokat H, Kunzendorf B, Wiltfang J (2016) Dental implants and diabetes mellitus—a systematic review. Int J Implant Dent 2:5. https://doi.org/10.1186/s40729-016-0038-2

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hasegawa H, Hashimoto K, Takeichi T et al (2008) Type 2 diabetes impairs implant osseointegration capacity in rats. Int J Oral Maxillofac Implants 23:237–246

    PubMed  Google Scholar 

  16. NemŢoi A, Trandafir V, Paşca AS, Şindilar EV, Drăgan E, Odri GA, NemŢoi A, Haba D, Şapte E (2017) Osseointegration of chemically modified sandblasted and acid-etched titanium implant surface in diabetic rats: a histological and scanning electron microscopy study. Romanian J Morphol Embryol 58:881–886

    Google Scholar 

  17. Wennerberg A, Albrektsson T (2009) Effects of titanium surface topography on bone integration: A systematic review. Clin Oral Implants Res 20:172–184. https://doi.org/10.1111/j.1600-0501.2009.01775.x

    Article  PubMed  Google Scholar 

  18. Rasouli R, Barhoum A, Uludag H (2018) A review of nanostructured surfaces and materials for dental implants: surface coating, patterning and functionalization for improved performance. Biomater Sci 6:1312–1338. https://doi.org/10.1039/c8bm00021b

    Article  PubMed  Google Scholar 

  19. Calciolari E, Mardas N, Dereka X, Anagnostopoulos AK, Tsangaris GT, Donos N (2018) Protein expression during early stages of bone regeneration under hydrophobic and hydrophilic titanium domes. A pilot study. J Periodontal Res 53:174–187. https://doi.org/10.1111/jre.12498

    Article  PubMed  Google Scholar 

  20. Abaricia JO, Shah AH, Ruzga MN, Olivares-Navarrete R (2021) Surface characteristics on commercial dental implants differentially activate macrophages in vitro and in vivo. Clin Oral Implants Res. https://doi.org/10.1111/clr.13717

  21. Schlegel KA, Prechtl C, Möst T, Seidl C, Lutz R, von Wilmowsky C (2013) Osseointegration of SLActive implants in diabetic pigs. Clin Oral Implants Res 24:128–134. https://doi.org/10.1111/j.1600-0501.2011.02380.x

    Article  PubMed  Google Scholar 

  22. Sugita Y, Honda Y, Kato I et al (2014) Role of Photofunctionalization in mitigating impaired osseointegration associated with type 2 diabetes in rats. Int J Oral Maxillofac Implants 29:1293–1300. https://doi.org/10.11607/jomi.3480

    Article  PubMed  Google Scholar 

  23. Khandelwal N, Oates TW, Vargas A, Alexander PP, Schoolfield JD, Alex McMahan C (2013) Conventional SLA and chemically modified SLA implants in patients with poorly controlled type 2 diabetes mellitus - a randomized controlled trial. Clin Oral Implants Res 24:13–19. https://doi.org/10.1111/j.1600-0501.2011.02369.x

    Article  PubMed  Google Scholar 

  24. Cabrera-Domínguez JJ, Castellanos-Cosano L, Torres-Lagares D, Pérez-Fierro M, Machuca-Portillo G (2019) Clinical performance of titanium-zirconium implants with a hydrophilic surface in patients with controlled type 2 diabetes mellitus: 2-year results from a prospective case-control clinical study. Clin Oral Investig 24:2477–2486. https://doi.org/10.1007/s00784-019-03110-9

    Article  PubMed  Google Scholar 

  25. Lee RSB, Hamlet SM, Ivanovski S (2017) The influence of titanium surface characteristics on macrophage phenotype polarization during osseous healing in type I diabetic rats: a pilot study. Clin Oral Implants Res 28:e159–e168. https://doi.org/10.1111/clr.12979

    Article  PubMed  Google Scholar 

  26. Sartoretto SC, Alves ATNN, Resende RFB et al (2015) Early osseointegration driven by the surface chemistry and wettability of dental implants. J Appl Oral Sci 23:272–278. https://doi.org/10.1590/1678-775720140483

    Article  Google Scholar 

  27. Lee SB, Retzepi M, Petrie A, Hakimi AR, Schwarz F, Donos N (2013) The effect of diabetes on bone formation following application of the GBR principle with the use of titanium domes. Clin Oral Implants Res 24:28–35. https://doi.org/10.1111/j.1600-0501.2012.02448.x

    Article  PubMed  Google Scholar 

  28. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the arrive guidelines for reporting animal research. PLoS Biol 8:6–11. https://doi.org/10.1371/journal.pbio.1000412

    Article  Google Scholar 

  29. Yan JE, Yuan W, Lou X, Zhu T (2012) Streptozotocin-induced diabetic hyperalgesia in rats is associated with upregulation of toll-like receptor 4 expression. Neurosci Lett 526:54–58. https://doi.org/10.1016/j.neulet.2012.08.012

    Article  PubMed  Google Scholar 

  30. Claudino M, Gennaro G, Cestari TM, Spadella CT, Garlet GP, Assis GF (2012) Spontaneous periodontitis development in diabetic rats involves an unrestricted expression of inflammatory cytokines and tissue destructive factors in the absence of major changes in commensal oral microbiota. Exp Diabetes Res 2012:1–10. https://doi.org/10.1155/2012/356841

    Article  Google Scholar 

  31. Samarghandian S, Borji A, Delkhosh MB, Samini F (2013) Safranal treatment improves hyperglycemia, hyperlipidemia and oxidative stress in streptozotocin-induced diabetic rats. J Pharm Pharm Sci 16:352–362. https://doi.org/10.18433/j3zs3q

    Article  PubMed  Google Scholar 

  32. Bartold PM, Kuliwaba JS, Lee V, Shah S, Marino V, Fazzalari NL (2011) Influence of surface roughness and shape on microdamage of the osseous surface adjacent to titanium dental implants. Clin Oral Implants Res 22:613–618. https://doi.org/10.1111/j.1600-0501.2010.02024.x

    Article  PubMed  Google Scholar 

  33. Marão H, Jimbo R, Neiva R et al (2017) Cortical and trabecular bone healing patterns and quantification for three different dental implant systems. Int J Oral Maxillofac Implants 32:585–592. https://doi.org/10.11607/jomi.4856

    Article  PubMed  Google Scholar 

  34. Von Wilmowsky C, Stockmann P, Harsch I et al (2011) Diabetes mellitus negatively affects peri-implant bone formation in the diabetic domestic pig. J Clin Periodontol 38:771–779. https://doi.org/10.1111/j.1600-051X.2011.01746.x

    Article  Google Scholar 

  35. Serrão C, Bastos M, Cruz D et al (2017) Role of metformin in reversing the negative impact of hyperglycemia on bone healing around implants inserted in type 2 diabetic rats. Int J Oral Maxillofac Implants 32:547–554. https://doi.org/10.11607/jomi.5754

    Article  PubMed  Google Scholar 

  36. Coelho PG, Pippenger B, Tovar N, Koopmans SJ, Plana NM, Graves DT, Engebretson S, van Beusekom HMM, Oliveira PGFP, Dard M (2018) Effect of obesity or metabolic syndrome and diabetes on osseointegration of dental implants in a miniature swine model: a pilot study. J Oral Maxillofac Surg 76:1677–1687. https://doi.org/10.1016/j.joms.2018.02.021

    Article  PubMed  PubMed Central  Google Scholar 

  37. Calciolari E, Hamlet S, Ivanovski S, Donos N (2018) Pro-osteogenic properties of hydrophilic and hydrophobic titanium surfaces: crosstalk between signalling pathways in in vivo models. J Periodontal Res 53:598–609. https://doi.org/10.1111/jre.12550

    Article  PubMed  Google Scholar 

  38. McCracken M, Lemons JE, Rahemtulla F et al Bone response to titanium alloy implants placed in diabetic rats. Int J Oral Maxillofac Implants 15:345–354

  39. Fujisaka S (2021) The role of adipose tissue M1/M2 macrophages in type 2 diabetes mellitus. Diabetol Int 12:74–79. https://doi.org/10.1007/s13340-020-00482-2

    Article  PubMed  Google Scholar 

  40. Dai X, Heng BC, Bai Y, You F, Sun X, Li Y, Tang Z, Xu M, Zhang X, Deng X (2021) Restoration of electrical microenvironment enhances bone regeneration under diabetic conditions by modulating macrophage polarization. Bioact Mater 6:2029–2038. https://doi.org/10.1016/j.bioactmat.2020.12.020

    Article  PubMed  Google Scholar 

  41. Xiang G, Liu K, Wang T, Hu X, Wang J, Gao Z, Lei W, Feng Y, Tao TH (2021) In situ regulation of macrophage polarization to enhance osseointegration under diabetic conditions using injectable silk/sitagliptin gel scaffolds. Adv Sci 8:2002328. https://doi.org/10.1002/advs.202002328

    Article  Google Scholar 

  42. Burgess M, Wicks K, Gardasevic M, Mace KA (2019) Cx3CR1 Expression identifies distinct macrophage populations that contribute differentially to inflammation and repair. ImmunoHorizons 3:262–273. https://doi.org/10.4049/immunohorizons.1900038

    Article  PubMed  Google Scholar 

  43. Oliveira PGFP, Coelho PG, Bergamo ETP et al (2020) Histological and nanomechanical properties of a new nanometric hydroxiapatite implant surface. An in vivo study in diabetic rats. Materials (Basel) 13:5693. https://doi.org/10.3390/ma13245693

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Neodent’s Research Support Program for supplying the dental implants used in the study.

Funding

This research was financed in part by the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES)—Finance code 001.

Author information

Authors and Affiliations

  1. Department of Restorative Dentistry, School of Dentistry, Federal University of Pelotas, Gonçalves Chaves Street 457, Pelotas, RS, 96015-560, Brazil

    Alessandra Julie Schuster & Fernanda Faot

  2. Analytic Laboratory of Restorative Materials - LaBiom-R, School of Dentistry, Federal Fluminense University, Niteroi, RJ, Brazil

    João Luiz Bittencourt de Abreu

  3. Department of Clinical Semiology, School of Dentistry, Federal University of Pelotas, Pelotas, RS, Brazil

    Natalia Marcumini Pola

  4. Department of Biomaterials, New York University College of Dentistry, New York, NY, USA

    Lukasz Witek & Paulo G. Coelho

  5. Department of Biomedical Engineering, New York University Tandon School of Engineering, New York, NY, USA

    Lukasz Witek

  6. Hansjörg Wyss Department of Plastic Surgery, New York University School of Medicine, New York, NY, USA

    Paulo G. Coelho

  7. Department of Mechanical and Aerospace Engineering, New York University Tandon School of Engineering, New York, NY, USA

    Paulo G. Coelho

Authors
  1. Alessandra Julie Schuster
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. João Luiz Bittencourt de Abreu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Marcumini Pola
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lukasz Witek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo G. Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernanda Faot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernanda Faot.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

For this type of study, formal consent is not required.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schuster, A.J., de Abreu, J.L.B., Pola, N.M. et al. Histomorphometric analysis of implant osseointegration using hydrophilic implants in diabetic rats. Clin Oral Invest 25, 5867–5878 (2021). https://doi.org/10.1007/s00784-021-03892-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-021-03892-x

Keywords

Search

Navigation