Fig. 3. Histological magnifications of specimens exposing a significant areas of lamellar bone in-between and parallel to the surface of older trabeculae (accentuated by green overlay), b osteoclastic activity, and c active bone formation at intrabony marginal regions
Fig. 3. Histological magnifications of specimens exposing a significant areas of lamellar bone in-between and parallel to the ...
Fig. 2. Histological view (buccal aspect) displaying mean BIC (%) and mean bone density (%) at corresponding regions (500 μm zones) from BD to A. Blue lines along the implant perimeter display BIC presence and yellow lines display BIC absence
Fig. 2. Histological view (buccal aspect) displaying mean BIC (%) and mean bone density (%) at corresponding regions (500 μm zones) from BD to A. Blue...
Fig. 1. Histological section illustrating the landmarks to determine the conducted histomorphometrical length measurements: DL, RB, and BIC at buccal RB. The red square frames the intra-thread area (ROI) for OD and ELD analysis
Fig. 1. Histological section illustrating the landmarks to determine the conducted histomorphometrical length measurements: DL, RB, and BIC at buccal RB. The red squar...
SP ID Mean OD (number/mm2)Mean ELD (number/mm2)Osteocyte/empty lacuna ratio12932311.2622211021.3231122450.4541721021.6851621431.12Mean1921651.17SD ±6869.20.4595% CI(132–251)(103–225) Table 3 Mean osteocyte (OD) and empty lacunae density (ELD) at peri-implant residual bone
Specimen IDDL (mm)RB (mm)B.Ar/T.Ar (%)BIC (%)14.83.572.480.025.68.992.375.035.65.388.173.843.87.781.868.753.63.292.571.1Mean4.75.785.574.0SD ±1.02.58.04.095% CI3.1–4.93.3–6.878–9270.6–77.6Table 2 Results from histomorphometric measurements exhibiting DL, RB, bone density (%), residual bone-to-implant contact (%) values
Sample ID
Gender
Age
Location
Prosthesis type
Loading time (years)
lmplant surface
Mean BOP (%)
Supp (+/−)
Mean PD (mm)
MBL (mm)
1
M
69
Maxilla
Single-screwed
5.1
Machined
100
+
6.4
B: 4.0P: 6.0
2
F
60
Mandible
Single-screwed
10.0
Machined
100
−
6.0
B: 4.5L: 5.0
3
F
60
Mandible
Single-screwed
10.0
Machined
100
−
6.2
B: 4.0L: 5...
Galárraga-Vinueza, M., Tangl, S., Bianchini, M. et al. Histological characteristics of advanced peri-implantitis bone defects in humans. Int J Implant Dent 6, 12 (2020). https://doi.org/10.1186/s40729-020-00208-8
Download citation
Received: 08 January 2020
Accepted: 19 February 2020
Published: 25 March 2020
DOI: https://doi.org/10.1186/s40729-020-00208-8
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material...
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The study protocol no. 3437751 was approved by the Human Research Committee at Federal University of Santa Catarina-Brazil, 2016–2021, and all patients signed an informed consent according to the university ethics regulations.
Not applicable
The authors declare that they have no competing of interests.
MG, FS, RG, and MB contributed to the design of the study. ST and KO contributed to study selection and data extraction. MG, RM, FS, RG, MB, ST, and KO contributed to the drafting of the paper and revising it critically. All authors read, revised, and approved the final manuscript.
Correspondence to
Reinhard Gruber.
Department of Oral Surgery and Implantology, Carolinum, Goethe University, Frankfurt, Germany
Maria Elisa Galárraga-Vinueza, Karina Obreja & Frank Schwarz
Post-Graduate Program in Implant Dentistry (PPGO), Federal University of Santa Catarina (UFSC), Florianópolis, SC, Brazil
Maria Elisa Galárraga-Vinueza, Marco Bianchini & Ricardo Magini
Core Facility Hard Tissue and Biomaterial Rese...
The present study was funded by the authors’ own departments.
Kohal R-J, Patzelt SBM, Butz F, Sahlin H. One-piece zirconia oral implants: one-year results from a prospective case series. 2. Three-unit fixed dental prosthesis (FDP) reconstruction. J Clin Periodontol [Internet]. 2013 [cited 2018 Nov 15];40(5):553–562. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23506654.
Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell ... and mor...
Berglundh T, Gislason O, Lekholm U, Sennerby L, Lindhe J. Histopathological observations of human periimplantitis lesions. J Clin Periodontol [Internet]. 2004 [cited 2019 Mar 13];31(5):341–347. Available from: http://doi.wiley.com/10.1111/j.1600-051X.2004.00486.x.
Zitzmann NU, Berglundh T, Ericsson I, Lindhe J. Spontaneous progression of experimentally induced periimplantitis. J Clin Periodonto...
Schwarz F, Herten M, Sager M, Bieling K, Sculean A, Becker J. Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs. Clin Oral Implants Res [Internet]. 2007 [cited 2019 Mar 18];18(2):161–170. Available from: http://doi.wiley.com/10.1111/j.1600-0501.2006.01320.x.
Serino G, Turri A, Lang NP. Probing at implants with peri-implantitis and its relati...
Schwarz F, Derks J, Monje A, Wang H-L. Peri-implantitis. J Clin Periodontol. 2018;45(June 2016):S246–66.
Berglundh T, Armitage G, Araujo MG, Avila-Ortiz G, Blanco J, Camargo PM, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol [Internet]. 2018 ...
Most apical extension of the residual bone tissue
Bone area
Bone defect
Bone-to-implant contact
Bleeding on probing
Cone beam computed tomography
Confidence interval
Disto-buccal
Defect length
Disto-oral
Empty lacuna density
Implant shoulder
Mesio-buccal
Marginal bone loss
Mesio-oral
Oral
Osteocyte density
Probing depth
Residual bone
Region of interest
Surface area
Standard de...
The data sets used and/or analyzed during the current study are available from the corresponding author or reasonable request.
In conclusion, the findings of this case series based on dental implants that had to be retrieved because of advanced peri-implantitis and the concomitant inflammatory osteolysis suggest that the residual peri-implant bone might accumulate the functional load and is consequently modeled and reinforced to become cortical bone.
When further interpreting the present study, the peri-implant osteocyte lacunae density after 1 to 27 years in function was reported [28]. In line with our findings, empty osteocytic lacunae adjacent to zirconia implants diagnosed with peri-implantitis were described [29]. Based on counting the osteocyte lacunae, we observed that numerous filled but also empty osteocytic lacunae were present withi...
The present study was inspired by the concept that upon advanced loss of cortical peri-implant bone, the remaining peri-implant trabecular bone is subjected to masticatory forces and reinforced as a consequence of functional adaptation [15]. This adaptation depends on vital osteocytes [16]. Therefore, the present human case series aimed at investigate the peri-implant bone in advanced peri-implant...
The clinical and radiographic characteristics of the implant sites are presented in Table 1. In total, 3 implants were located in the maxilla, while two implants were located in the mandible. While all implants showed bleeding on probing, only 2 implants presented with suppuration on gentle probing. Mean probing depth was 6.3 ± 0.4 mm corresponding to a mean marginal bone loss (MBL) of 4.7 ± 1.0...
RB was divided into 500-μm-wide horizontal zones (from BD to A) following the long axis of the implant. For each of these individual zones, BIC and bone density (B.Ar/T.Ar) were determined. Osteocyte and empty osteocytic lacunae were counted along the region of interest (ROI) (i.e., the area encompassing the intra-thread regions along the buccal RB extension) (Fig. 1) using a software program (Im...
Cone beam computed tomographic (CBCT) scans were obtained from each patient for the surgical planning of implant removal. Linear measurements of the defect length (DL) at affected implants were made by drawing a vertical line, following the long axis of the implant, from the implant shoulder (IS) to the bottom of the defect (BD) at buccal and oral aspects in the CBCT data sets (Implant viewer, ver...
The present study included 4 patients, 3 female and 1 male (mean age of 66 ± 5 years), who attended the Implant Dentistry Department at Federal University of Santa Catarina, complaining of pain, discomfort, suppuration, and/or bleeding at implant sites. All patients revealed a history of periodontal disease, were non-smokers (100%), and reported no additional systemic diseases. The patients exhi...
Peri-implantitis was recently defined as a “pathological condition occurring in tissues around dental implants”, which is “characterized by inflammation in the peri-implant connective tissue and a progressive loss of supporting bone” [1,2,3,4].
Human biopsies confirmed the presence of plasma cells, macrophages, and neutrophils [5] and elevated expression of inflammatory cytokines [6, 7] a...
Inflammatory osteolysis is the clinical hallmark of peri-implantitis. The morphology of the remaining peri-implant bone and the level of osseointegration, however, remain unknown. Our aim was to characterize advanced peri-implantitis bone defects in humans.
Four patients (3 female and 1 male) were diagnosed with peri-implantitis. A total of 5 implants with machined surfaces and a mean loading tim...
Fig. 3. Histological magnifications of specimens exposing a significant areas of lamellar bone in-between and parallel to the surface of older trabeculae (accentuated by green overlay), b osteoclastic activity, and c active bone formation at intrabony marginal regions
Fig. 3. Histological magnifications of specimens exposing a significant areas of lamellar bone in-between and parallel to the ...
Fig. 2. Histological view (buccal aspect) displaying mean BIC (%) and mean bone density (%) at corresponding regions (500 μm zones) from BD to A. Blue lines along the implant perimeter display BIC presence and yellow lines display BIC absence
Fig. 2. Histological view (buccal aspect) displaying mean BIC (%) and mean bone density (%) at corresponding regions (500 μm zones) from BD to A. Blue...
Fig. 1. Histological section illustrating the landmarks to determine the conducted histomorphometrical length measurements: DL, RB, and BIC at buccal RB. The red square frames the intra-thread area (ROI) for OD and ELD analysis
Fig. 1. Histological section illustrating the landmarks to determine the conducted histomorphometrical length measurements: DL, RB, and BIC at buccal RB. The red squar...
SP ID Mean OD (number/mm2)Mean ELD (number/mm2)Osteocyte/empty lacuna ratio12932311.2622211021.3231122450.4541721021.6851621431.12Mean1921651.17SD ±6869.20.4595% CI(132–251)(103–225) Table 3 Mean osteocyte (OD) and empty lacunae density (ELD) at peri-implant residual bone
Specimen IDDL (mm)RB (mm)B.Ar/T.Ar (%)BIC (%)14.83.572.480.025.68.992.375.035.65.388.173.843.87.781.868.753.63.292.571.1Mean4.75.785.574.0SD ±1.02.58.04.095% CI3.1–4.93.3–6.878–9270.6–77.6Table 2 Results from histomorphometric measurements exhibiting DL, RB, bone density (%), residual bone-to-implant contact (%) values
Sample ID
Gender
Age
Location
Prosthesis type
Loading time (years)
lmplant surface
Mean BOP (%)
Supp (+/−)
Mean PD (mm)
MBL (mm)
1
M
69
Maxilla
Single-screwed
5.1
Machined
100
+
6.4
B: 4.0P: 6.0
2
F
60
Mandible
Single-screwed
10.0
Machined
100
−
6.0
B: 4.5L: 5.0
3
F
60
Mandible
Single-screwed
10.0
Machined
100
−
6.2
B: 4.0L: 5...
Galárraga-Vinueza, M., Tangl, S., Bianchini, M. et al. Histological characteristics of advanced peri-implantitis bone defects in humans. Int J Implant Dent 6, 12 (2020). https://doi.org/10.1186/s40729-020-00208-8
Download citation
Received: 08 January 2020
Accepted: 19 February 2020
Published: 25 March 2020
DOI: https://doi.org/10.1186/s40729-020-00208-8
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material...
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The study protocol no. 3437751 was approved by the Human Research Committee at Federal University of Santa Catarina-Brazil, 2016–2021, and all patients signed an informed consent according to the university ethics regulations.
Not applicable
The authors declare that they have no competing of interests.
MG, FS, RG, and MB contributed to the design of the study. ST and KO contributed to study selection and data extraction. MG, RM, FS, RG, MB, ST, and KO contributed to the drafting of the paper and revising it critically. All authors read, revised, and approved the final manuscript.
Correspondence to Reinhard Gruber.
Department of Oral Surgery and Implantology, Carolinum, Goethe University, Frankfurt, Germany
Maria Elisa Galárraga-Vinueza, Karina Obreja & Frank Schwarz
Post-Graduate Program in Implant Dentistry (PPGO), Federal University of Santa Catarina (UFSC), Florianópolis, SC, Brazil
Maria Elisa Galárraga-Vinueza, Marco Bianchini & Ricardo Magini
Core Facility Hard Tissue and Biomaterial Rese...
The present study was funded by the authors’ own departments.
Kohal R-J, Patzelt SBM, Butz F, Sahlin H. One-piece zirconia oral implants: one-year results from a prospective case series. 2. Three-unit fixed dental prosthesis (FDP) reconstruction. J Clin Periodontol [Internet]. 2013 [cited 2018 Nov 15];40(5):553–562. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23506654.
Dallas SL, Prideaux M, Bonewald LF. The osteocyte: an endocrine cell ... and mor...
Berglundh T, Gislason O, Lekholm U, Sennerby L, Lindhe J. Histopathological observations of human periimplantitis lesions. J Clin Periodontol [Internet]. 2004 [cited 2019 Mar 13];31(5):341–347. Available from: http://doi.wiley.com/10.1111/j.1600-051X.2004.00486.x.
Zitzmann NU, Berglundh T, Ericsson I, Lindhe J. Spontaneous progression of experimentally induced periimplantitis. J Clin Periodonto...
Schwarz F, Herten M, Sager M, Bieling K, Sculean A, Becker J. Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs. Clin Oral Implants Res [Internet]. 2007 [cited 2019 Mar 18];18(2):161–170. Available from: http://doi.wiley.com/10.1111/j.1600-0501.2006.01320.x.
Serino G, Turri A, Lang NP. Probing at implants with peri-implantitis and its relati...
Schwarz F, Derks J, Monje A, Wang H-L. Peri-implantitis. J Clin Periodontol. 2018;45(June 2016):S246–66.
Berglundh T, Armitage G, Araujo MG, Avila-Ortiz G, Blanco J, Camargo PM, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol [Internet]. 2018 ...
Most apical extension of the residual bone tissue
Bone area
Bone defect
Bone-to-implant contact
Bleeding on probing
Cone beam computed tomography
Confidence interval
Disto-buccal
Defect length
Disto-oral
Empty lacuna density
Implant shoulder
Mesio-buccal
Marginal bone loss
Mesio-oral
Oral
Osteocyte density
Probing depth
Residual bone
Region of interest
Surface area
Standard de...
The data sets used and/or analyzed during the current study are available from the corresponding author or reasonable request.
In conclusion, the findings of this case series based on dental implants that had to be retrieved because of advanced peri-implantitis and the concomitant inflammatory osteolysis suggest that the residual peri-implant bone might accumulate the functional load and is consequently modeled and reinforced to become cortical bone.
When further interpreting the present study, the peri-implant osteocyte lacunae density after 1 to 27 years in function was reported [28]. In line with our findings, empty osteocytic lacunae adjacent to zirconia implants diagnosed with peri-implantitis were described [29]. Based on counting the osteocyte lacunae, we observed that numerous filled but also empty osteocytic lacunae were present withi...
The present study was inspired by the concept that upon advanced loss of cortical peri-implant bone, the remaining peri-implant trabecular bone is subjected to masticatory forces and reinforced as a consequence of functional adaptation [15]. This adaptation depends on vital osteocytes [16]. Therefore, the present human case series aimed at investigate the peri-implant bone in advanced peri-implant...
The clinical and radiographic characteristics of the implant sites are presented in Table 1. In total, 3 implants were located in the maxilla, while two implants were located in the mandible. While all implants showed bleeding on probing, only 2 implants presented with suppuration on gentle probing. Mean probing depth was 6.3 ± 0.4 mm corresponding to a mean marginal bone loss (MBL) of 4.7 ± 1.0...
RB was divided into 500-μm-wide horizontal zones (from BD to A) following the long axis of the implant. For each of these individual zones, BIC and bone density (B.Ar/T.Ar) were determined. Osteocyte and empty osteocytic lacunae were counted along the region of interest (ROI) (i.e., the area encompassing the intra-thread regions along the buccal RB extension) (Fig. 1) using a software program (Im...
Cone beam computed tomographic (CBCT) scans were obtained from each patient for the surgical planning of implant removal. Linear measurements of the defect length (DL) at affected implants were made by drawing a vertical line, following the long axis of the implant, from the implant shoulder (IS) to the bottom of the defect (BD) at buccal and oral aspects in the CBCT data sets (Implant viewer, ver...
The present study included 4 patients, 3 female and 1 male (mean age of 66 ± 5 years), who attended the Implant Dentistry Department at Federal University of Santa Catarina, complaining of pain, discomfort, suppuration, and/or bleeding at implant sites. All patients revealed a history of periodontal disease, were non-smokers (100%), and reported no additional systemic diseases. The patients exhi...
Peri-implantitis was recently defined as a “pathological condition occurring in tissues around dental implants”, which is “characterized by inflammation in the peri-implant connective tissue and a progressive loss of supporting bone” [1,2,3,4].
Human biopsies confirmed the presence of plasma cells, macrophages, and neutrophils [5] and elevated expression of inflammatory cytokines [6, 7] a...
Inflammatory osteolysis is the clinical hallmark of peri-implantitis. The morphology of the remaining peri-implant bone and the level of osseointegration, however, remain unknown. Our aim was to characterize advanced peri-implantitis bone defects in humans.
Four patients (3 female and 1 male) were diagnosed with peri-implantitis. A total of 5 implants with machined surfaces and a mean loading tim...