Michael Korsch Silke-Mareike Marten €tsch Andreas Do  Ruy Jauregui Dietmar H. Pieper Ursula Obst

Authors’ affiliations: Michael Korsch, Dental Academy for Continuing Professional Development, Karlsruhe, Germany Clinic of Operative Dentistry, Periodontology and Preventive Dentistry, University Hospital, Saarland University, Homburg, Germany Silke-Mareike Marten, Andreas D€ otsch, Ursula Obst, Institute of Functional Interfaces, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany Ruy J auregui, Dietmar H. Pieper, Microbial Interactions and Processes Research Group, Helmholtz Centre for Infection Research, Braunschweig,Germany Corresponding author: Dr med. dent. Michael Korsch, MA Dental Academy for Continuing Professional Development Lorenzstrasse 7 76135 Karlsruhe Germany Tel.: +49 721 9181 200 Fax: +49 721 9181 222 e-mail: [email protected]

Effect of dental cements on periimplant microbial community: comparison of the microbial communities inhabiting the peri-implant tissue when using different luting cements

Key words: biofilms, dental cements, in vivo investigations, molecular biological analysis Abstract Background: Cementing dental restorations on implants poses the risk of undetected excess cement. Such cement remnants may favor the development of inflammation in the peri-implant tissue. The effect of excess cement on the bacterial community is not yet known. The aim of this study was to analyze the effect of two different dental cements on the composition of the microbial peri-implant community. Methods: In a cohort of 38 patients, samples of the peri-implant tissue were taken with paper points from one implant per patient. In 15 patients, the suprastructure had been cemented with a zinc oxide–eugenol cement (Temp Bond, TB) and in 23 patients with a methacrylate cement (Premier Implant Cement, PIC). The excess cement found as well as suppuration was documented. Subgingival samples of all patients were analyzed for taxonomic composition by means of 16S amplicon sequencing. Results: None of the TB-cemented implants had excess cement or suppuration. In 14 (61%) of the PIC, excess cement was found. Suppuration was detected in 33% of the PIC implants without excess cement and in 100% of the PIC implants with excess cement. The taxonomic analysis of the microbial samples revealed an accumulation of oral pathogens in the PIC patients independent of the presence of excess cement. Significantly fewer oral pathogens occurred in patients with TB compared to patients with PIC. Conclusion: Compared with TB, PIC favors the development of suppuration and the growth of periodontal pathogens.

Date: Accepted 8 February 2015 To cite this article: Korsch M, Marten S-M, D€ otsch A, J auregui R, Pieper DH, Obst U. Effect of dental cements on peri-implant microbial community: comparison of the microbial communities inhabiting the peri-implant tissue when using different luting cements. Clin. Oral Impl. Res. 00, 2015, 1–6 doi: 10.1111/clr.12582

Cementing fixed dental restorations on implants is a routine procedure in dental practice. Yet, an increasing number of reports are dealing with complications caused by undetected excess cement (Pauletto et al. 1999; Callan & Cobb 2009; Shapoff & Lahey 2012). Excess cement retained in the peri-implant sulcus poses a risk to the adjacent tissues and favors biofilm formation (Obst et al. 2012). As a consequence, the peri-implant tissue may become inflamed (Wilson 2009; Linkevicius et al. 2013a). Peri-implant mucositis or periimplantitis may develop if excess cement is retained in the sulcus for prolonged periods (Linkevicius et al. 2013a; Korsch et al. 2014a). Even some cases of loss of implants have been reported (Gapski et al. 2008; Callan & Cobb 2009). Little is known about the incidence of excess cement (Linkevicius et al. 2011, 2013b;

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Korsch et al. 2014a). Besides the position of the abutment margin (Linkevicius et al. 2011), the implant diameter also seems to influence the frequency of undetected excess cement (Vindasiute et al. 2013; Korsch et al. 2015). Although many techniques supposedly reducing the risk of excess cement (Dumbrigue et al. 2002; Wadhwani & Pineyro 2009; Yuzbasioglu 2014) have been described, this type of complication has not yet been eliminated. In vitro studies observed a correlation between the type of cement and biofilm formation (Korsch et al. 2014b). Clinical investigations also indicate that different types of cement influence the peri-implant tissue differently (Korsch & Walther 2014). Methacrylate-based cements seem to be more disposed toward favoring biofilm formation (Busscher et al. 2010) than cements on a zinc

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Korsch et al  Effect of dental cements on peri-implant microbial community

oxide–eugenol basis which are assumed to have an antibacterial effect (Boeckh et al. 2002). Whether and to what extent the type of cement has an influence on peri-implant biofilm formation is unknown. The aim of this study was to compare the microbial peri-implant communities developing after using different dental cements. In addition, the effect of undetected excess cement on the peri-implant bacterial community was investigated.

Material and methods To facilitate the suprastructure revision in routine therapy, a methacrylate-based temporary cement was used in the period from April 2009 to February 2010 for luting fixed dental restorations on implants. A subset of patients treated with this luting cement (Premier Implant Cement [PIC]; Premierâ Dental Products Company, Plymouth Meeting, PA, USA) developed peri-implant inflammation several months later, which was related to the cement used. In view of this complication, a temporary cement based on zinc oxide eugenol (Temp Bond [TB]; Kerr Sybron Dental Specialities, Glendora, CA, USA) was used from March 2010 on. PIC and TB used in this study were not radiopaque at the time they were applied. To analyze the effect of cementation on the peri-implant community, patients with cemented fixed implant-supported restorations were followed up. In connection with a revision of the suprastructure, microbial samples of the peri-implant tissue were taken. Moreover, the effect of undetected excess cement on the biofilm was evaluated.

methacrylate-based cement (PIC) or a cement on zinc oxide eugenol (TB) basis between January and May 2010 were followed up in the period from September to December 2013. PIC population

This cohort included 23 patients (15 men, 8 women) at the age of 19–77 years at the time of cementation (average age 58.7 years). The retention time of the suprastructure (i.e., time between cementation and revision) was 4.1 years. TB population

This cohort included 15 patients (7 men, 8 women) at the age of 33–72 years at the time of cementation (average age 60.8 years). The average retention time (i.e., time between cementation and revision) of the suprastructure was 3.7 years. Clinical procedure of revision, documentation of clinical findings, and sampling

Fig. 2. Suppuration (blue arrow) from the peri-implant tissue.

the abutments, the excess cement around each implant was documented (Fig. 3). Finally, the peri-implant tissue was rinsed with chlorhexidine 0.12%, and the suprastructure was recemented with TB cement.

Patients were interrogated about their case history, nicotine abuse, diabetes, regular use of mouth rinses (at least once per week), and antibiotics in the past 12 months and whether periodontitis had been diagnosed. Before the revision of the suprastructure, a pool sample was taken with sterile paper points from the peri-implant sulcus around each implant (Fig. 1). Any existing signs of inflammation (pocket suppuration) were documented (Fig. 2). At revision, the suprastructure was removed with dental forceps or a hook. In all cases, the restorations could be removed without being damaged. After revision of the suprastructure including

All patients were informed in advance about the clinical procedure to be performed. In addition, the patients were informed about obtaining cement samples and paper point samples for a future microbial analysis in connection with the study. All patients gave their informed consent in writing. The institutional review board of the Medical Council of the Saarland examined and confirmed the project. For the microbial analysis of the periimplant tissue, the bacterial DNA from the paper point samples of a total of 38 patients was obtained and analyzed for taxonomic composition by sequencing the V1–V2 variable regions of the 16S rRNA gene.

Fig. 1. Taking a sample with paper point from the periimplant tissue.

Fig. 3. Excess cement from the peri-implant tissue: the part from inside the crown (blue arrow) clearly differs from the part from outside the crown (green arrow: inhomogeneous surface with change in color).

Inclusion and exclusion criteria

The cohort included patients with cemented fixed implant-supported restorations placed more than 3.5 years ago with a temporary cement either on a methacrylate or on a zinc oxide–eugenol basis. Inclusion required a complete documentation drawn up at the time of incorporating the dental restoration including the cement used. Patients with subsequent suprastructure decementation were excluded. The patients were informed in advance about the project, and those participating in the study agreed to a follow-up examination and a future microbial analysis. Study population

A total of 38 patients who had been restored prosthetically and had received temporary

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© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Korsch et al  Effect of dental cements on peri-implant microbial community

Microbial methods DNA extraction

Paper points were placed in sterile 1.5-ml tubes, covered with nuclease-free water (Ambion, Thermo Fisher, Paisley, UK), and vortexed for 10 s. For debonding of biofilm microbes, the samples were treated for 2:30 h on a thermomixer (Eppendorf, Hamburg, Germany) at 22°C and 1400 rpm, followed by 10-s vortexing, 5-min sonication at 43 kHz, and again vortexed for 10 s. The supernatants of the paper points were collected and centrifuged for 10 min at 17,000 9 g (Biofuge Pico, Heraeus, Hanau, Germany). All supernatants were discarded, and the pellets stored for 24 h at 80°C. DNA was extracted using commercial extraction protocols for genomic DNA (QIAamp Mini Kit; Qiagen, Hilden, Germany). The collected pellets of the supernatant were treated with 180 ll lysozyme solution (20 mg/ ml; Sigma-Aldrich, Taufkirchen, Germany; 20 mM Tris-HCl, pH 8.0, 2 mM EDTA, 1.2% Triton) under shaking at 37°C for 2:15 h, followed by proteinase K digestion (20 ll proteinase K and 200 ll buffer AL) for 1:15 h under shaking at 56°C. DNA was extracted using commercial extraction protocols for genomic DNA (QIAamp Mini Kit; Qiagen). Finally, the DNA was eluted with 100 ll PCR-clean water, and the concentration was quantified using the NanoDrop equipment (PEQLAB, Erlangen, Germany). Amplicon library preparation

Amplicons of the V1–V2 region of the bacterial 16S rRNA gene were prepared as published elsewhere (Camarinha-Silva et al. 2013). Briefly, the genomic sequence of the 16S rRNA gene was amplified with primers that were derived from the previously described primers 27F and 338R (Lane 1991; Etchebehere & Tiedje 2005) and contained sequences compatible with Illumina sequencing platforms and a 6-nt bar code sequence. The resulting DNA was used as template for a second PCR, using primers designed to introduce full-length Illumina (San Diego, CA, USA) adapter sequences including Illumina 6-nt index sequences to enable highlevel multiplexing. Libraries were pooled and subjected to 250 nt paired-end sequencing on an Illumina MiSeq machine (Illumina). Both forward and reverse read sets were quality trimmed as previously described (CamarinhaSilva et al. 2013) and nucleotides from the 30 end removed if the average quality in a sliding window dropped below a quality score of 15. After quality processing, forward and reverse reads were trimmed to exactly

140 nt, matched to give 280 nt for downstream analysis, collapsed into unique copies, and clustered using the mothur precluster program (Schloss et al. 2009) allowing two mismatches. Taxonomic analysis of pathogen groups

The sequence dataset was filtered to consider only those phylotypes that (1) were present in at least one sample at a relative abundance >1% of the total sequences of that sample, (2) were present in at least 2% of samples at a relative abundance >0.1% for a given sample, or (3) were present in at least 5% of samples at any abundance level. A total number of 1003 different phylotypes passed the filter and were taxonomically characterized to the genus level using the “classifier” tool of the Ribosomal Database Project (Wang et al. 2007) with a confidence threshold of 80%. A species name was assigned to a phylotype when only 16S rRNA gene fragments of previously described isolates of that species showed ≤2 mismatches with the respective representative sequence read. For phylotypes that belonged to the genera Treponema, Tannerella, or Porphyromonas, the species description was curated by manual inspection of the 20 best database hits to unambiguously classify the three species belonging to the “red complex” (Socransky & Haffajee 2005), Treponema denticola, Tannerella forsythia, and Porphyromonas gingivalis. Statistical methods

The data were analyzed with IBM SPSS Statistics 21 (IBM SPSS Statistics; IBM, Armonk, NY, USA). The difference in excess cement between PIC and TB was analyzed using the chi-squared test for statistical independence. The differences in the relative abundance of pathogen groups were analyzed using the Mann–Whitney U-test, a nonparametrical test of the null hypothesis that the mean ranks of two populations are equal. The resulting P-values were corrected for multiple testing using the Benjamini–Hochberg method. A principal component analysis (PCA) of the relative abundances was performed using a singular value decomposition algorithm with centering of the data. The Mann–Whitney U-tests and the PCA were performed using the rank sum and pca functions of the Matlab Statistics toolbox R2013a (Mathworks Inc., Natick, MA, USA).

Results The two patient populations having received PIC or TB were homogeneous terms of gen-

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

der distribution, average age, and oral retention times of the suprastructures, as no significant differences of these factors were found. Fourteen (61%) of the 23 PIC patients had excess cement. In the patients with TB, excess cement was not fob served around any of the implants during revision treatment. The difference was significant (v2 = 14.457; P < 0.001). At 17 (74%) of the PIC-cemented implants, pocket suppuration was documented, whereas none of the TB-cemented implants had any signs of inflammation or suppuration. This difference was also significant (v2 = 29.937; P < 0.001). In the presence of excess cement (PIC), all implants were affected by suppuration. In the absence of excess cement (PIC), three (33%) of the implants were suppurating. Six patients (40%) treated with TB, and 11 patients (48%) of the PIC group (PIC without excess cement four patients [44%]; PIC with excess cement seven patients [50%]) were affected by periodontal disease. There was no significant correlation between suppuration and the periodontal status of the patient. Results of the microbial evaluation

Samples were taken from 23 implants of the PIC population and from 15 implants of the TB population and analyzed for microbial community composition by sequencing the V1–V2 variable 16S rRNA gene regions. The number of phylotypes detected (altogether 1003 phylotypes belonging to 460 different species and 110 different genera) corresponded roughly to the diversity of the human oral microbiome described in the literature (Dewhirst et al. 2010). The relative abundances of each of the 110 genera showed large variations across all patients. However, a PCA of the genus abundance across all 38 patients revealed differences in the overall taxonomic composition between microbial communities inhabiting TB or PIC cement, respectively (Fig. 4). PCA is a method of multivariate data analysis that attempts to reduce the complexity of a dataset by combining correlated variables (i.e., in our case the genus abundances). The first two principal components that are depicted in Fig. 5 account for 53.3% of the total variance present in all samples. Although a variation between different patients remains obvious, the samples of patients with TB (green dots in Fig. 4) exhibited a community composition that differs from the samples of patients with PIC with and without excess cement (orange and red dots in Fig. 4). Patients with TB show high abundances of commensal oral bacteria

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0.4 Fusobacterium

Principal component 2 (15.4%)

0.3 Prevotella

0.2 Streptococcus 0.1

Actinomyces 0

Tannerella Treponema

–0.1 –0.2 –0.3

Legend TB PIC-ex PIC+ex class average

–0.4 –0.4

–0.2

Porphyromonas 0

0.2

0.4

Principal component 1 (37.4%) Fig. 4. Principal component analysis of the genus abundances. Each dot represents the genus composition of an individual patient’s sample. Different colors indicate the different groups of samples: TB – TempBond cement, PICex – PremierImplant cement without excess cement, PIC+ex – PremierImplant cement with excess cement. The average of each of the three groups is shown as a star in the corresponding color. Arrows indicate the load of the seven most abundant genera, that is, the weight or influence of the genera on the first two principal components. For each principal component, the percentage of total variance explained by this principal component is given in brackets.

such as that are human patients

Streptococcus (mostly S. sanguinis) found abundantly in the healthy oral microbiome. In contrast, with PIC showed an increased

abundance of pathogenic bacteria. The three genera containing the red complex species, Tannerella, Treponema, and Porphyromonas, which are commonly associated with peri-implantitis, made the strongest contribution to the community compositions of the PIC samples. Other abundant bacterial genera included Prevotella and Actinomyces. The occurrence of members of the genus Fusobacterium was correlated neither with the presence of the commensal Streptococci nor with the pathogenic red complex bacteria. Most of the sequences indicating the presence of Fusobacterium were assigned to the species Fusobacterium nucleatum, including the subspecies F. nucleatum ssp. nucleatum, which belongs to the Socransky orange complex comprising bacteria with a mild effect on periodontitis. This subspecies was the only phylotype of F. nucleatum that was correlated with the red complex bacteria (data not shown). As the occurrence of red complex bacteria was found to be correlated with the cement type, we analyzed the abundance of the three red complex species P. gingivalis, T. forsythia, and T. denticola in greater detail. Comparing the three patient groups, the abundance of the red complex bacteria was clearly increased in patients with PIC, both in the presence and in the absence of excess cement (Fig. 5a). An individual examination

Red complex

(a)

of the three species revealed a trend of increased abundance of T. forsythia and T. denticola in the presence of excess cement compared to patients with PIC without excess cement (Fig. 5b). The abundance of red complex bacteria in patients with PIC generally showed a large variation, and even some of the TB patients carried substantial amounts of the pathogens despite the lack of symptoms of an infection (Fig. 5c). Bacteria that are constituting the orange complex according to Socransky and Haffajee (Socransky & Haffajee 2005) were found in the samples with different abundance. The most frequent species was F. nucleatum that was represented by a variety of phylotypes and was found at an average abundance of 13% across all samples. Other orange complex bacteria were also found, such as Campylobacter gracilis, Eubacterium nodatum, and Streptococcus constellatus, although less frequently. Comparing the orange complex species across different cement types, no significant differences could be observed.

Discussion Invisible excess cement retained in the oral cavity is a big risk of cementation. The present study could demonstrate a difference in the effect of a methacrylate cement and a zinc oxide eugenol cement on the frequency

(c)

0.5

TB

0.4 0.3 0.2

PIC–ex

0.1

PIC+ex

0

p=0.023 p=0.001

TB

PIC–ex PIC+ex

(b) Porphyromonas gingivalis 0.4

Tannerella forsythia

Treponema denticola

0.10

0.10

0.3

0.08

0.08

0.2

0.06

0.06

0.04

0.04

0.02

0.02

0.1

0

0

0 p=0.002

TB

PIC–ex PIC+ex

TB

p=0.008

PIC–ex PIC+ex

TB

PIC–ex PIC+ex

Fig. 5. Abundance of the red complex pathogenic species. (a) Boxplots showing the summarized relative abundance of the three species classified as “red complex” by Socransky and Haffajee (Socransky & Haffajee 2005) in each of the three groups of samples: TB – TempBond cement, PICex – PremierImplant cement without excess cement, PIC+ex – PremierImplant cement with excess cement. Brackets and P-values indicate a statistically significant difference between two sample groups (P < 0.05), calculated using the Mann–Whitney U test. P-values were adjusted using the Benjamini-Hochberg correction for multiple testing. (b) Boxplots showing the relative abundances of each of the three red complex species individually. (c) Relative abundance of red complex bacteria in individual samples. Each pie represents an individual sample within the three groups with red indicating the fraction of sequences assigned to one of the three red complex species. Pies with a black margin indicate the presence of suppuration.

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Korsch et al  Effect of dental cements on peri-implant microbial community

of excess cement. Whereas excess cement was not found in any of the patients with zinc oxide eugenol cement, the prevalence of excess cement was 61% in the patients with methacrylate cement. As it is unlikely that after cementation with zinc oxide eugenol cement, no cement remnants will be left in the peri-implant tissue, it can be proposed that such excess cement had dissolve over time in contact with liquid (Yanikoglu & Yesil Duymus 2007). Undetected excess cement has an effect on the peri-implant tissue. The prevalence of peri-implant inflammation is described to be between 81% and 85% when excess cement is present (Wilson 2009; Linkevicius et al. 2013a). After the suprastructures had been in the oral cavity for more than 3.5 years, none of the patients with TB cement was affected by suppuration. However, all patients with PIC and excess cement demonstrated suppuration. 33% of the patients with PIC without excess cement were also affected. Whereas zinc oxide eugenol cement is supposed to have an antibacterial effect (Boeckh et al. 2002), materials with methacrylate appear to favor biofilm formation (Busscher et al. 2010). Bone loss around implants associated with peri-implantitis is one of the most frequent biological complications in dental implantology (Linkevicius et al. 2013a). It is a proven fact that bacteria are the etiological key to the development of peri-implantitis (Heitz-Mayfield & Lang 2010). Following the published data (Bik et al. 2010; Dewhirst et al. 2010), the human oral microbiome is extremely diverse and contains large numbers of different taxa which could be underlined by our investigations using amplicon sequences of the bacterial 16S rRNA gene. Following the investigations of Kumar et al. (2005, 2006), Socran-

sky & Haffajee (2005), Shibli et al. (2008), and Riep et al. (2009), a shift was observed in the PIC patients group toward a higher abundance of the red complex (Socransky & Haffajee 2005) in subgingival paper point sampling. Periodontal pathogens belonging to the red complex (Socransky & Haffajee 2005) were more abundant within the microbial populations from the peri-implantitis patients, whereas members of the orange complex were more or less evenly distributed in all patients. These data agree with the data published by Kumar et al. (2006) and Riep et al. (2009). Differences of the taxonomic diversity between the microbiome under periodontal and healthy conditions following Dabdoub et al. (2013) could not be confirmed because the number of taxa was similar in the diseased and the healthy group. Significant correlations of the oral microbiome composition in relation to smoking, disinfection measures, or antibiosis could not be observed either, possibly because of the heterogeneity with respect to these factors in a relatively small patient cohort. Temp Bond seems to be an ideal cement to avoid excess cement and the risk of cementinduced peri-implant inflammation. But in the manufacturers’ product descriptions, it is designated as a temporary cement. Many studies that compare the retentiveness of temporary vs. permanent cements are in vitro studies (Nejatidanesh et al. 2012; Garg et al. 2013). Regarding retentiveness, they do not prove any clinical relevance to the frequency of reconstruction loosening. The use of a temporary zinc oxide eugenol cement does not necessarily lead to an increase in denture loosening based on comparisons between cement-retained dental prostheses and screwretained dental prostheses (Nissan et al.

2011). With respect to cement-induced periimplantitis, TB may be an alternative to permanent cements.

Outlook In a study comparing the microbiome of 38 patients (15 with PIC with excess cement, 8 patients with PIC without excess cement, and 15 patients with TB), differences in the abundance of pathogens of the Socransky red complex (Socransky & Haffajee 2005) could be observed. The differences are consistent with the results of previous in vitro experiments (Korsch et al. 2014b), but were not found to be statistically significant except for T. forsythia. The statistical insignificance may be explained by the large variation combined with a relatively small patient cohort. Thus, a larger patient cohort would further improve the robustness of the findings that are presented here and might allow to assess further contributing factors (e.g., antibiosis). However, it can be stated that PIC cement is more prone to bacterial colonization and subsequent peri-implantitis, especially after the formation of excess cement. The studies undertaken up to now are currently continued including more diagnostic aspects.

Acknowledgements: We thank Winfried Walther and Tamara Jonitz for support during sample and data collection. Conflict of interest The authors declare that there are no conflicts of interest.

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Effect of dental cements on peri-implant microbial community: comparison of the microbial communities inhabiting the peri-implant tissue when using different luting cements.

Cementing dental restorations on implants poses the risk of undetected excess cement. Such cement remnants may favor the development of inflammation i...
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