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Bone quality analysis of jaw bones in individuals with type 2 diabetes mellitus—post mortem anatomical and microstructural evaluation

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Abstract

Objectives

With the higher risk of dental implant failure with type 2 diabetes mellitus (T2DM), there is a need to characterize the jaw bones in those individuals. The aim of this post mortem study was to compare jaw bone quality of individuals with T2DM to healthy controls.

Material and methods

Bone cores from the edentulous lower first molar region and the region of mandibular angle were collected from male individuals with T2DM (n = 10, 70.6 ± 4.5 years) and healthy controls (n = 11, 71.5 ± 3.8 years) during autopsy. Within the T2DM, a subgroup treated with oral antidiabetics (OAD) and one on insulin were identified. Bone quality assessment encompassed evaluation of bone microstructure, matrix composition, and cellular activity, using microcomputed tomography (micro-CT), quantitative backscattered electron imaging (qBEI), Raman spectroscopy, and bone histomorphometry.

Results

In the mandibular angle, T2DM showed 51% lower porosity of the lingual cortex (p = 0.004) and 21% higher trabecular thickness (p = 0.008) compared to control. More highly mineralized bone packets were found in the buccal cortex of the mandibular angle in insulin-treated compared to OAD-treated T2DM group (p = 0.034). In the molar region, we found higher heterogeneity of trabecular calcium content in T2DM insulin compared to controls (p = 0.015) and T2DM OAD (p = 0.019). T2DM was associated with lower osteocyte lacunar size in the trabecular bone of the molar region (vs. control p = 0.03).

Conclusions

Alterations in microstructure, mineralization, and osteocyte morphology were determined in jaw bone of individuals with T2DM compared to controls.

Clinical relevance

Future studies will have to verify if the mild changes determined in this study will translate to potential contraindications for dental implant placements.

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Acknowledgments

Authors thank medical technicians who assisted during sample collection: Branislav Milivojevic, Bojan Kacarevic, and Milos Knezevic (Institute for Pathology, University of Belgrade, Serbia).

Funding

This work was supported by institutional partnership grant of Alexander von Humboldt Foundation, South-East-Europe Cooperation of the University Medical Center Hamburg-Eppendorf under direction of Prof. H.J. Seitz, German Research Foundation (DFG, BU 2562/3-1), German Academic Exchange Service (DAAD), Ministry of Education and Science of the Republic of Serbia (III 45005), and Science Fund of the Republic of Serbia (PROMIS, #6064549, DiaBoNet). This project has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no. 860898.

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Authors and Affiliations

  1. Laboratory for Anthropology and Skeletal Biology, Institute for Anatomy, School of Medicine, University of Belgrade, Dr Subotica starijeg 4, Belgrade, 11000, Serbia

    Teodora Rodic, Petar Milovanovic & Marija Djuric

  2. Institute for Osteology and Biomechanics, University Medical Center Hamburg- Eppendorf, Lottestrasse 55, 22529, Hamburg, Germany

    Eva Maria Wölfel, Petar Milovanovic, Imke A. K. Fiedler, Katharina Jähn, Michael Amling & Björn Busse

  3. Institute for Forensic Medicine, School of Medicine, University of Belgrade, Deligradska 31/A, Belgrade, 11000, Serbia

    Danica Cvetkovic, Slobodan Nikolic & Vladimir Zivkovic

  4. Institute for Pathology, School of Medicine, University of Belgrade, Dr Subotica starijeg 1, Belgrade, 11000, Serbia

    Jelena Sopta

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  1. Teodora Rodic
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  6. Katharina Jähn
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  7. Michael Amling
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  8. Jelena Sopta
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  12. Marija Djuric
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Contributions

Conceptualization: Marija Djuric; methodology: Marija Djuric, Björn Busse, and Petar Milovanovic; formal analysis and investigation: Teodora Rodic, Eva Maria Wölfel, Petar Milovanovic, Imke A.K. Fiedler, Katharina Jähn-Rickert, and Danica Cvetkovic; writing—original draft preparation: Teodora Rodic; writing—review and editing: Teodora Rodic, Petar Milovanovic, Marija Djuric, Eva Maria Wölfel, Imke A.K. Fiedler, Katharina Jähn-Rickert, Björn Busse; supervision: Marija Djuric, Björn Busse, Katharina Jähn, Michael Amling, Jelena Sopta, Slobodan Nikolic, and Vladimir Zivkovic; All authors read and approved the final manuscript.

Corresponding author

Correspondence to Marija Djuric.

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The authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Ethics Committee of the Faculty of Medicine, University of Belgrade, Serbia, and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from the families of all individual participants included in the study. The aspect of confidentiality was respected.

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Appendix

Appendix

Table 1 Comparison of the 3D microstructural parameters in the cortical bone between control group and T2DM groups
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Table 2 Comparison of the 3D microstructural parameters in the trabecular bone between control and T2DM groups
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Table 3 Values of the qBEI parameters in control and T2DM groups
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Table 4 Values of the osteonal morphology parameters of the trabecular bone in the molar region in control and T2DM groups
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Table 5 Values of the osteonal morphology and osteocyte lacunar parameters of the cortical bone in control and T2DM groups
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Table 6 Values of tissue composition and maturity parameters of cortical bone and trabecular bone in control and T2DM groups
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Table 7 Values of bone cellular parameters of the trabecular bone in control and T2DM groups
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Table 8 Values of cortical bone thickness in control and T2DM groups
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Rodic, T., Wölfel, E.M., Milovanovic, P. et al. Bone quality analysis of jaw bones in individuals with type 2 diabetes mellitus—post mortem anatomical and microstructural evaluation. Clin Oral Invest 25, 4377–4400 (2021). https://doi.org/10.1007/s00784-020-03751-1

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