Effect of Obesity or Metabolic Syndrome and Diabetes on Osseointegration of Dental Implants in a Miniature Swine Model

A Pilot Study

Paulo G. Coelho*, Benjamin Pippenger, Nick Tovar, Sietse Jan Koopmans, Natalie M. Plana, Dana T. Graves, Steve Engebretson, Heleen M.M. van Beusekom, Paula G.F.P. Oliveira, Michel Dard

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

2 Citations (Scopus)

Abstract

Purpose: The increasing prevalence of obesity or metabolic syndrome (O/MS) and type 2 diabetes mellitus (DM) remains a global health concern. Clinically relevant and practical translational models mimicking human characteristics of these conditions are lacking. This study aimed to demonstrate proof of concept of the induction of stable O/MS and type 2 DM in a Göttingen minipig model and validate both of these disease-adjusted Göttingen minipig models as impaired healing models for the testing of dental implants. Materials and Methods: Nine minipigs were split into 3 groups—control (normal diet), obese (cafeteria diet), and diabetic (cafeteria diet plus low-dosage streptozotocin)—followed by placement of dental implants. Inflammatory markers including tumor necrosis factor α, C-reactive protein, and cortisol were recorded for each study group. Removal torque was measured, and histomorphometric analysis (bone-to-implant contact and bone area fraction occupancy) was performed. Results: O/MS pigs showed, on average, a 2-fold increase in plasma C-reactive protein (P <.05) and cortisol (P <.09) concentrations compared with controls; DM pigs showed, on average approximately, a 40-fold increase in plasma tumor necrosis factor α levels (P <.05) and a 2-fold increase in cortisol concentrations (P <.05) compared with controls. The impact of O/MS and DM on implants was determined. The torque to interface failure was highest in the control group (200 N-cm) and significantly lower in the O/MS (90 N-cm) and DM (60 N-cm) groups (P <.01). Bone formation around implants was significantly greater in the control group than in the O/MS and DM groups (P <.02). Conclusions: Both O/MS and DM minipigs express a human-like disease phenotype, and both presented bone-healing impairment around dental implants. Our finding of no significant difference between type 2 DM and O/MS in bone formation around implants provides evidence that further investigation of the impact of O/MS is warranted.
Original languageEnglish
Pages (from-to)1677-1687
JournalJournal of Oral and Maxillofacial Surgery
Volume76
Issue number8
Early online date1 Mar 2018
DOIs
Publication statusPublished - Aug 2018

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Miniature Swine
Osseointegration
Dental Implants
Obesity
Diabetes Mellitus
Type 2 Diabetes Mellitus
Hydrocortisone
Torque
Osteogenesis
Bone and Bones
C-Reactive Protein
Swine
Lymphotoxin-beta
Diabetic Diet
Diet
Control Groups
Streptozocin
Blood Proteins
Tumor Necrosis Factor-alpha
Phenotype

Cite this

Coelho, Paulo G. ; Pippenger, Benjamin ; Tovar, Nick ; Koopmans, Sietse Jan ; Plana, Natalie M. ; Graves, Dana T. ; Engebretson, Steve ; van Beusekom, Heleen M.M. ; Oliveira, Paula G.F.P. ; Dard, Michel. / Effect of Obesity or Metabolic Syndrome and Diabetes on Osseointegration of Dental Implants in a Miniature Swine Model : A Pilot Study. In: Journal of Oral and Maxillofacial Surgery. 2018 ; Vol. 76, No. 8. pp. 1677-1687.
@article{1314c99a6ab04223bc0fec83a83c0254,
title = "Effect of Obesity or Metabolic Syndrome and Diabetes on Osseointegration of Dental Implants in a Miniature Swine Model: A Pilot Study",
abstract = "Purpose: The increasing prevalence of obesity or metabolic syndrome (O/MS) and type 2 diabetes mellitus (DM) remains a global health concern. Clinically relevant and practical translational models mimicking human characteristics of these conditions are lacking. This study aimed to demonstrate proof of concept of the induction of stable O/MS and type 2 DM in a G{\"o}ttingen minipig model and validate both of these disease-adjusted G{\"o}ttingen minipig models as impaired healing models for the testing of dental implants. Materials and Methods: Nine minipigs were split into 3 groups—control (normal diet), obese (cafeteria diet), and diabetic (cafeteria diet plus low-dosage streptozotocin)—followed by placement of dental implants. Inflammatory markers including tumor necrosis factor α, C-reactive protein, and cortisol were recorded for each study group. Removal torque was measured, and histomorphometric analysis (bone-to-implant contact and bone area fraction occupancy) was performed. Results: O/MS pigs showed, on average, a 2-fold increase in plasma C-reactive protein (P <.05) and cortisol (P <.09) concentrations compared with controls; DM pigs showed, on average approximately, a 40-fold increase in plasma tumor necrosis factor α levels (P <.05) and a 2-fold increase in cortisol concentrations (P <.05) compared with controls. The impact of O/MS and DM on implants was determined. The torque to interface failure was highest in the control group (200 N-cm) and significantly lower in the O/MS (90 N-cm) and DM (60 N-cm) groups (P <.01). Bone formation around implants was significantly greater in the control group than in the O/MS and DM groups (P <.02). Conclusions: Both O/MS and DM minipigs express a human-like disease phenotype, and both presented bone-healing impairment around dental implants. Our finding of no significant difference between type 2 DM and O/MS in bone formation around implants provides evidence that further investigation of the impact of O/MS is warranted.",
author = "Coelho, {Paulo G.} and Benjamin Pippenger and Nick Tovar and Koopmans, {Sietse Jan} and Plana, {Natalie M.} and Graves, {Dana T.} and Steve Engebretson and {van Beusekom}, {Heleen M.M.} and Oliveira, {Paula G.F.P.} and Michel Dard",
year = "2018",
month = "8",
doi = "10.1016/j.joms.2018.02.021",
language = "English",
volume = "76",
pages = "1677--1687",
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}

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', Journal of Oral and Maxillofacial Surgery, vol. 76, no. 8, pp. 1677-1687. https://doi.org/10.1016/j.joms.2018.02.021

Effect of Obesity or Metabolic Syndrome and Diabetes on Osseointegration of Dental Implants in a Miniature Swine Model : A Pilot Study. / Coelho, Paulo G.; Pippenger, Benjamin; Tovar, Nick; Koopmans, Sietse Jan; Plana, Natalie M.; Graves, Dana T.; Engebretson, Steve; van Beusekom, Heleen M.M.; Oliveira, Paula G.F.P.; Dard, Michel.

In: Journal of Oral and Maxillofacial Surgery, Vol. 76, No. 8, 08.2018, p. 1677-1687.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Effect of Obesity or Metabolic Syndrome and Diabetes on Osseointegration of Dental Implants in a Miniature Swine Model

T2 - A Pilot Study

AU - Coelho, Paulo G.

AU - Pippenger, Benjamin

AU - Tovar, Nick

AU - Koopmans, Sietse Jan

AU - Plana, Natalie M.

AU - Graves, Dana T.

AU - Engebretson, Steve

AU - van Beusekom, Heleen M.M.

AU - Oliveira, Paula G.F.P.

AU - Dard, Michel

PY - 2018/8

Y1 - 2018/8

N2 - Purpose: The increasing prevalence of obesity or metabolic syndrome (O/MS) and type 2 diabetes mellitus (DM) remains a global health concern. Clinically relevant and practical translational models mimicking human characteristics of these conditions are lacking. This study aimed to demonstrate proof of concept of the induction of stable O/MS and type 2 DM in a Göttingen minipig model and validate both of these disease-adjusted Göttingen minipig models as impaired healing models for the testing of dental implants. Materials and Methods: Nine minipigs were split into 3 groups—control (normal diet), obese (cafeteria diet), and diabetic (cafeteria diet plus low-dosage streptozotocin)—followed by placement of dental implants. Inflammatory markers including tumor necrosis factor α, C-reactive protein, and cortisol were recorded for each study group. Removal torque was measured, and histomorphometric analysis (bone-to-implant contact and bone area fraction occupancy) was performed. Results: O/MS pigs showed, on average, a 2-fold increase in plasma C-reactive protein (P <.05) and cortisol (P <.09) concentrations compared with controls; DM pigs showed, on average approximately, a 40-fold increase in plasma tumor necrosis factor α levels (P <.05) and a 2-fold increase in cortisol concentrations (P <.05) compared with controls. The impact of O/MS and DM on implants was determined. The torque to interface failure was highest in the control group (200 N-cm) and significantly lower in the O/MS (90 N-cm) and DM (60 N-cm) groups (P <.01). Bone formation around implants was significantly greater in the control group than in the O/MS and DM groups (P <.02). Conclusions: Both O/MS and DM minipigs express a human-like disease phenotype, and both presented bone-healing impairment around dental implants. Our finding of no significant difference between type 2 DM and O/MS in bone formation around implants provides evidence that further investigation of the impact of O/MS is warranted.

AB - Purpose: The increasing prevalence of obesity or metabolic syndrome (O/MS) and type 2 diabetes mellitus (DM) remains a global health concern. Clinically relevant and practical translational models mimicking human characteristics of these conditions are lacking. This study aimed to demonstrate proof of concept of the induction of stable O/MS and type 2 DM in a Göttingen minipig model and validate both of these disease-adjusted Göttingen minipig models as impaired healing models for the testing of dental implants. Materials and Methods: Nine minipigs were split into 3 groups—control (normal diet), obese (cafeteria diet), and diabetic (cafeteria diet plus low-dosage streptozotocin)—followed by placement of dental implants. Inflammatory markers including tumor necrosis factor α, C-reactive protein, and cortisol were recorded for each study group. Removal torque was measured, and histomorphometric analysis (bone-to-implant contact and bone area fraction occupancy) was performed. Results: O/MS pigs showed, on average, a 2-fold increase in plasma C-reactive protein (P <.05) and cortisol (P <.09) concentrations compared with controls; DM pigs showed, on average approximately, a 40-fold increase in plasma tumor necrosis factor α levels (P <.05) and a 2-fold increase in cortisol concentrations (P <.05) compared with controls. The impact of O/MS and DM on implants was determined. The torque to interface failure was highest in the control group (200 N-cm) and significantly lower in the O/MS (90 N-cm) and DM (60 N-cm) groups (P <.01). Bone formation around implants was significantly greater in the control group than in the O/MS and DM groups (P <.02). Conclusions: Both O/MS and DM minipigs express a human-like disease phenotype, and both presented bone-healing impairment around dental implants. Our finding of no significant difference between type 2 DM and O/MS in bone formation around implants provides evidence that further investigation of the impact of O/MS is warranted.

U2 - 10.1016/j.joms.2018.02.021

DO - 10.1016/j.joms.2018.02.021

M3 - Article

VL - 76

SP - 1677

EP - 1687

JO - Journal of Oral and Maxillofacial Surgery

JF - Journal of Oral and Maxillofacial Surgery

SN - 0278-2391

IS - 8

ER -