Patient
M. salivarium
V. parvula
S. aureus
P. gingivalis
P. micra
T. forsythia
Fungal organisms
1
7.05E + 01
7.00E + 01
-
...
Patient
M. salivarium
V. parvula
S. aureus
P. gingivalis
P. micra
T. forsythia
Fungal organisms
1
-
2.26E + 03
-
1...
Patient
Severity
M. salivarium
V. parvula
S. aureus
P. gingivalis
P. micra
T. forsythia
Fungal organisms
1
i-m
-
7.96E + 04
...
Species
Gene
Primer/probe
Sequences (5′-3′)
Aspergillus spp. plus
ITS2
aspe-F
CTG TCC GAG CGT CAT TG
Penicillium spp.
pen1-F
...
Species
Gene
Primer/probe
Sequences (5′-3′)
Mycoplasma salivarium
rpoB
msali-F
CCG TCA AAT GAT TTC GAT TGC
msali-R
GAA CTG CTT GAC GTT GCA TGT T
...
Schwarz, F., Becker, K., Rahn, S. et al. Real-time PCR analysis of fungal organisms and bacterial species at peri-implantitis sites. Int J Implant Dent 1, 9 (2015). https://doi.org/10.1186/s40729-015-0010-6
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Received: 16 January 2015
Accepted: 11 March 2015
Published: 21 April 2015
DOI: https://doi.org/10.1186/s40729-015-0010-6
Frank Schwarz, Kathrin Becker, Sebastian Rahn, Andrea Hegewald, Klaus Pfeffer, and Birgit Henrich declare that they have no competing interests.
FS, BH, and KP have made substantial contributions to study conception and design, analysis, and interpretation of data as well as manuscript preparation. KB performed the statistical analysis. AH and SR were involved in data acquisition. All authors rea...
Department of Oral Surgery, Westdeutsche Kieferklinik, Heinrich Heine University, Moorenstraße 5, D-40225, Düsseldorf, Germany
Frank Schwarz & Andrea Hegewald
Department of Orthodontics, Westdeutsche Kieferklinik, Heinrich Heine University, Moorenstraße 5, D-40225, Düsseldorf, Germany
Kathrin Becker
Institute of Medical Microbiology and Hospital Hygiene, Heinrich Heine University, Univer...
We kindly appreciate the skills and commitment of Ms. Dana Belick (Institute of Medical Microbiology and Hospital Hygiene, Heinrich Heine University, Düsseldorf) in the DNA preparation and bacterial analysis and the Jürgen Manchot Foundation for financial support.
Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B. Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res. 2002;13:349–58.
Engel LD, Kenny GE. Mycoplasma salivarium in human gingival sulci. J Periodontal Res. 1970;5:163–71.
Jarvensivu A, Hietanen J, Rautemaa R, Sorsa T, Richardson M. Candida yeasts in chronic periodontitis ti...
McDonald RR, Antonishyn NA, Hansen T, Snook LA, Nagle E, Mulvey MR, et al. Development of a triplex real-time PCR assay for detection of Panton-Valentine leukocidin toxin genes in clinical isolates of methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:6147–9.
Morillo JM, Lau L, Sanz M, Herrera D, Martin C, Silva A. Quantitative real-time polymerase chain reaction based on si...
Lindhe J, Meyle J, Group DoEWoP. Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol. 2008;35:282–5.
Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol. 2011;38 Suppl 11:203–13.
Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35:292–30...
Bleeding on probing
Mycoplasma salivarium
Porphyromonas gingivalis
Parvimonas micra
Probing pocket depth
Staphylococcus aureus
Tannerella forsythia
Veillonella parvula
Within the limitations of the present analysis, it was concluded that Candida spp. and other fungal organisms were frequently identified at peri-implantitis as well as healthy implant sites and co-colonized with P. micra and T. forsythia.
Furthermore, the present analysis failed to identify any significant correlation of either fungal organisms or disease severity with opportunistic bacteria, such as M. salivarium, V. parvula, and S. aureus. At tooth sites, M. salivarium was mainly isolated from the sulcus area and associated with gingivitis lesions [27]. Interestingly, S. aureus has only been identified at one single peri-implanti...
The present study aimed at analyzing and correlating fungal organisms with several periodontopathogenic and opportunistic bacterial species at peri-implantitis sites using real-time PCR. These outcomes were compared with those noted at healthy implant sites as well as teeth with a history of periodontitis.
Basically, the present analysis has pointed to a high prevalence of fungal organisms in sub...
The Kendall-Tau-b coefficients failed to reveal any significant correlations between the presence of fungal organisms and the proportions of M. salivarium (0.25), V. parvula (0.34), P. gingivalis (0.60), P. micra (0.32), T. forsythia (0.12), and S. aureus (0.66) (P > 0.05, respectively).
According to the given definition, the present analysis was based on a total of n = 13 initial to moderate and n = 6 advanced peri-implantitis lesions (n = 19 patients), 10 healthy implant sites (n = 10 patients), as well as 10 teeth with a history of periodontitis (n = 10 out of 19 patients suffering from peri-implantitis).
The analysis of fungal organisms as well as of M. sa...
The statistical analysis was performed using a commercially available software program (SPSS Statistics 22.0, IBM Corp., Ehningen, Germany). Kendall-Tau-b correlation coefficients were calculated to evaluate the dependence between fungal organisms, bacterial species as well as disease severity (i.e., initial to moderate and advanced sites). Results were considered statistically significant at P
In the peri-implantitis group, one additional subgingival plaque sample was obtained from partially edentulous patients with a history of periodontitis (n = 10) and obtained at a tooth exhibiting the highest PD but no signs of acute periodontal disease (i.e., BOP/no suppuration). None of these teeth were located adjacent to the sampled implant sites. The control samples were also prepared for ...
A total of 29 partially or fully edentulous patients were consecutively recruited from the Department of Oral Surgery, Heinrich Heine University, Düsseldorf, Germany, between April 2013 and July 2014. Nineteen patients (7 men and 13 women; mean age 58.8 ± 12.6 years) suffered from initial to moderate or advanced peri-implantitis, while ten patients (6 men and 4 women; mean age 55.2 ± 1...
There is considerable evidence supporting the view that peri-implant diseases are infectious in nature and mainly linked to an uncontrolled accumulation of bacterial plaque biofilms [1]. Basically, diseased implant sites are dominated by gram-negative anaerobic bacteria and therefore feature microbiological characteristics similar to those noted for chronic periodontal infections [2]. Even though ...
The potential role of fungal organisms and their co-aggregation with either periodontopathogens or opportunistic pathogens at peri-implantitis sites is unknown. The aim of the present study was to qualitatively/quantitatively analyze and correlate fungal organisms and bacterial species at peri-implantitis sites.
In a total of 29 patients, submucosal/subgingival plaque samples were collected at pe...
Fig. 1. Flow diagram
Fig. 1. Flow diagram
Outcome variable
Crude modela
β (95% CI)
p value
Adjusted modelb
β (95% CI)
p-value
% Sites BoP
...
Control
Test
T0 (n = 22)
T3 (n = 20)
T0 (n = 31)
T3 (n = 30)
...
N = 47a
Total anaerobic bacterial load
Log-transformed mean (SD)
T0
T3
Difference
β (95% CI)b
p value
Control
...
N = 40a
Total anaerobic bacterial load
Log-transformed mean (SD)
Tpre
Tpost
Difference
β (95% CI)b
p value
...
Characteristics
Control
Test
Number of patients
14
14
...
Hentenaar, D.F.M., De Waal, Y.C.M., Strooker, H. et al. Implant decontamination with phosphoric acid during surgical peri-implantitis treatment: a RCT.
Int J Implant Dent 3, 33 (2017). https://doi.org/10.1186/s40729-017-0091-5
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Received: 28 March 2017
Accepted: 22 June 2017
Published: 17 July 2017
DOI: https://doi.org/10.1186/s40729-017-0091-5
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were...
Diederik F. M. Hentenaar, Yvonne C. M. de Waal, Hans Strooker, Henny J. A. Meijer, Arie-Jan van Winkelhoff, and Gerry M. Raghoe declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Correspondence to
Gerry M. Raghoebar.
Department of Oral and Maxillofacial Surgery, University of Groningen, University Medical Center Groningen, PO Box 30.001, 9700 RB, Groningen, The Netherlands
Diederik F. M. Hentenaar, Henny J. A. Meijer & Gerry M. Raghoebar
Center for Dentistry and Oral Hygiene, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands
Yvonne C. M. De Waal, Hans Strooker, He...
Van Winkelhoff AJ, van Steenbergen TJ, Kippuw N, De Graaff J. Further characterization of Bacteroides endodontalis, an asaccharolytic black-pigmented Bacteroides species from the oral cavity. J Clin Microbiol. 1985;22:75–9.
Zambon JJ. Periodontal diseases: microbial factors. Ann Periodontol. 1996;1:879–925.
Héritier M. Effects of phosphoric acid on root dentin surface. A scanning and transm...
Htet M, Madi M, Zakaria O, Miyahara T, Xin W, Lin Z, Aoki K, Kasugai S. Decontamination of anodized implant surface with different modalities for peri-implantitis treatment: lasers and mechanical debridement with citric acid. J Periodontol. 2016;87:953–61.
Mouhyi J, Sennerby L, Van Reck J. The soft tissue response to contaminated and cleaned titanium surfaces using CO2 laser, citric acid and hy...
Esposito M, Grusovin MG, Worthington HV. Treatment of peri-implantitis: what interventions are effective? A Cochrane systematic review. Eur J Oral Implantol. 2012;5:21–41.
Louropoulou A, Slot DE, Van der Weijden F. The effects of mechanical instruments on contaminated titanium dental implant surfaces: a systematic review. Clin Oral Implants Res. 2014;25:1149–60.
Ramanauskaite A, Daugela P, F...
Lang NP, Berglundh T, Working Group 4 of Seventh European Workshop on Periodontology. Periimplant diseases: where are we now?—Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38(Suppl):11,178–181.
Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol. 2015;42:158–71.
Derks J, Schaller D, Hå...
Gerry Raghoebar
Diederik Hentenaar
Yvonne de Waal
Implant surface decontamination is considered a highly susceptible step in the treatment of peri-implantitis. The application of 35% phosphoric acid after mechanical debridement is superior to mechanical debridement combined with sterile saline rinsing for decontamination of the implant surface during surgical peri-implantitis treatment. However, phosphoric acid as implant surface decontaminant do...
Recent studies that zoom in on titanium surface physico-chemistry reveal interesting results [38, 39]. Kotsakis et al. [38] hypothesized that chemical residues alter the titanium surface physicochemistry and subsequently compromise cellular response to these decontaminated surfaces. However, they report on effective restoring of biocompatibility when sterile saline, citric acid, and EDTA/sodium hy...
Phosphoric acid gel as agent for implant surface decontamination has only been investigated in two other clinical studies [26, 27]. Strooker et al. [26] used phosphoric acid 35% for peri-implant supportive therapy and found greater reductions in bacterial load, but no significant clinical differences compared to conventional mechanical supportive therapy. They concluded that local application of 3...
This randomized controlled trial aimed to determine the effect of 35% phosphoric etching gel on decontamination of the implant surface during resective surgical treatment of peri-implantitis. Both decontamination procedures (mechanical debridement with curettes and gauzes combined with phosphoric acid 35% and mechanical debridement combined with sterile saline) resulted in a significant immediate ...
The progress of patients throughout the different phases of the study is illustrated in Fig. 1. Table 1 depicts the baseline demographic patient and implant characteristics. The included patients had a total of 128 implants of which 53 implants showed signs of peri-implantitis. Different implant brands and types with different implant surfaces were present, including Straumann (Straumann AG, Bas...
Angular bony defects were eliminated, and bone was recontoured using a rotating round bur under saline irrigation. Mucosal flaps were apically positioned and firmly sutured (Vicryl Plus® 3-0; Ethicon Inc., Somerville, NJ, USA), and suprastructures were re-positioned. For both control and test group, surgery was followed by 2 weeks of mouth rinsing with 0.12% CHX + 0.05% CPC without alcohol t...
Implant mobility;
Implants at which no position could be identified where proper probing measurements could be performed;
Previous surgical treatment of the peri-implantitis lesions.
The study protocol was based on the study protocols of two previous studies evaluating the decontaminating effect of chlorhexidine during surgical peri-implantitis treatment [10, 32] and is briefly described below....
The present study is a double-blind randomized controlled trial evaluating the effect of 35% phosphoric etching gel (test group) compared to the effect of saline (control group) for implant surface decontamination combined with mechanical debridement during surgical peri-implantitis treatment. Patients were randomly assigned to the test or control group using a one-to-one allocation ratio. The stu...
Thus far, the use of phosphoric acid etching gel as decontaminating agent has not been evaluated in a randomized controlled trial. The aim of the present randomized controlled trial is to evaluate the short-term microbiological and clinical effectiveness of 35% phosphoric etching gel as a decontaminating agent of the implant surface during resective surgical treatment of peri-implantitis.
Triggered host defense responses initiate inflammation of the peri-implant soft tissue (peri-implant mucositis), which can lead to loss of peri-implant supporting bone (peri-implantitis), and eventually, result in implant failure [1]. An increasing prevalence of peri-implantitis has been described in recent literature [2], with current incidence ranging from 1 to 47%. A non-linear, accelerating pa...
Peri-implantitis is known as an infectious disease that affects the peri-implant soft and hard tissue. Today, scientific literature provides very little evidence for an effective intervention protocol for treatment of peri-implantitis. The aim of the present randomized controlled trial is to evaluate the microbiological and clinical effectiveness of phosphoric acid as a decontaminating agent of th...
Figure 1. Flow diagram
Figure 1. Flow diagram
Table 5 Average differences in BoP, SoP, and PPD between the control and test group at 3-month follow-up
Outcome variable
Crude modelaβ (95% CI)
p value
Adjusted modelbβ (95% CI)
p-value
% Sites BoP% Sites SoPMean PPD
16.2 (−7.9 to 40.3)0.0 (−10.9 to 10.9)0.6 (−0.6 to 1.8)
0.7431.0000.205
7.9 (−16.4 to 32.3)0.7 (−10.1 to 11.4)0.2 (−1.0 to 1.3)
0.8210.882...
Table 4 Descriptive statistics of clinical parameters
Control
Test
T0 (n = 22)
T3 (n = 20)
T0 (n = 31)
T3 (n = 30)
Plaque
% of sites (SD)% of implants (n)
4.5 (12.5)13.6 (3)
10.0 (18.8)25.0 (5)
4.0 (9.3)16.1 (5)
2.5 (7.6)9.7 (3)
BoP
% of sites (SD)% of implants (n)
86.4 (18.5)100 (22)
28.8 (35.6)50 (10)
66.1 (29.3)96.8 (30)
39.2 (31.3...
Table 3 Log-transformed mean bacterial anaerobic counts (SD) for the control and test group before (T0) and 3 months after (T3) the surgical treatment (paperpoint samples)
N = 47a
Total anaerobic bacterial loadLog-transformed mean (SD)
T0
T3
Difference
β (95% CI)b
p value
Control
6.69 (1.32)
6.31 (1.30)
0.38 (1.36)
−0.26 (−0.84–0.33)
0.377
...
Table 2 Log-transformed mean bacterial anaerobic counts (SD) of culture-positive implants for the control and test group before (Tpre) and after (Tpost) debridement and decontamination of the implant surface (intra-operative microbrush samples)
N = 40a
Total anaerobic bacterial loadLog-transformed mean (SD)
Tpre
Tpost
Difference
β (95% CI)b
p value
Control
5.57 ...
Table 1 Characteristics of included patients/implants
Characteristics
Control
Test
Number of patients
14
14
Age (years; mean [SD])
57.0 (13.7)
60.9 (7.2)
Gender; M (male), F (female)
M5, F9
M7, F7
Smoking; n subjects (%)
1 (7%)
3 (21%)
History of periodontitis; n subjects (%)
4 (29%)
5 (36%)
Dental status; n subjects (%)
- Partially edentul...
References
Lang NP, Berglundh T, Working Group 4 of Seventh European Workshop on Periodontology. Periimplant diseases: where are we now?—Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38(Suppl):11,178–181.
Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol. 2015;42:158–71.
Derks ...
The residual biofilm area was significantly greater after treatment with phosphoric acid compared to air abrasive treatment with powder or even control treatment without powder. Apparently, only water and air might be effective in reducing the biofilm. Nonetheless, when the titanium surface was viewed under a scanning electron microscopy (SEM), no visible titanium surface change was seen aft...
A gel as application mode has the great advantage of being precisely applicable with minimal touching of the surrounding bone or connective tissue. A disadvantage of a gel might be the limited flow in deeper areas of the rough implant surface. To overcome this problem, it was decided to continuously rub the etching gel onto the implant surface with a small brush during the decontamination pe...
Discussion
This randomized controlled trial aimed to determine the effect of 35% phosphoric etching gel on decontamination of the implant surface during resective surgical treatment of peri-implantitis. Both decontamination procedures (mechanical debridement with curettes and gauzes combined with phosphoric acid 35% and mechanical debridement combined with sterile saline) resulted in a sign...
Clinical outcomes
Descriptive statistics of the clinical outcomes at baseline and follow-up are depicted in Table 4. At 3-month follow-up, 75% of the implants (66.7% of the patients) in the control group and 63.3% of the implants (53.8% of the patients) in the test group showed no clinical signs of inflammation (PPD ≤4 mm without bleeding and/or suppuration on probing) (Table 4). The results...
Results
The progress of patients throughout the different phases of the study is illustrated in Fig. 1. Table 1 depicts the baseline demographic patient and implant characteristics. The included patients had a total of 128 implants of which 53 implants showed signs of peri-implantitis. Different implant brands and types with different implant surfaces were present, including Straumann (Strauman...
Assuming a two-sided two sample t test with a significance level (α) of 0.05 and a power (β) of 80% required a sample size of 34 implants. A 20% compensation for dropouts was taken into account (34/0.8 = 42.5 implants). Based on a previous study [10], it was expected that not all baseline microbiological samples would yield a detectable number of cultivable bacteria ([10], 19 out of 79 =...
Peri-implant pocket depth was measured at four sites per implant (mesial, buccal, distal, and lingual) using a pressure sensitive probe (KerrHawe Click Probe®, Bioggo, Switzerland) (probe force of 0.25 N). Bleeding and suppuration were scored up to 30s after pocket probing. Microbiological peri-implant sulcus samples were collected from each implant with peri-implantitis using four sterile paper...
Angular bony defects were eliminated, and bone was recontoured using a rotating round bur under saline irrigation. Mucosal flaps were apically positioned and firmly sutured (Vicryl Plus® 3-0; Ethicon Inc., Somerville, NJ, USA), and suprastructures were re-positioned. For both control and test group, surgery was followed by 2 weeks of mouth rinsing with 0.12% CHX + 0.05% CPC without alcohol t...
Interventions
The study protocol was based on the study protocols of two previous studies evaluating the decontaminating effect of chlorhexidine during surgical peri-implantitis treatment [10, 32] and is briefly described below.
Within 1 month before surgical treatment, all patients received extensive oral hygiene instructions and mechanical non-surgical debridement of implants and remaining de...
Methods
Trial design
The present study is a double-blind randomized controlled trial evaluating the effect of 35% phosphoric etching gel (test group) compared to the effect of saline (control group) for implant surface decontamination combined with mechanical debridement during surgical peri-implantitis treatment. Patients were randomly assigned to the test or control group using a one-to-one al...
Background
Triggered host defense responses initiate inflammation of the peri-implant soft tissue (peri-implant mucositis), which can lead to loss of peri-implant supporting bone (peri-implantitis), and eventually, result in implant failure [1]. An increasing prevalence of peri-implantitis has been described in recent literature [2], with current incidence ranging from 1 to 47%. A non-linear, acc...
Implant decontamination with phosphoric acid during surgical peri-implantitis treatment: a RCT
Abstract
Background
Peri-implantitis is known as an infectious disease that affects the peri-implant soft and hard tissue. Today, scientific literature provides very little evidence for an effective intervention protocol for treatment of peri-implantitis. The aim of the present randomized controlled t...