long-term analysis of osseointegrated implants in non-smoker patients with a previous history of...

Long-term analysis ofosseointegrated implants in non-smoker patients with a previoushistory of periodontitisMeyle J, Gersok G, Boedeker R-H, Gonzales JR. Long-term analysis of osseointegratedimplants in non-smoker patients with a previous history of periodontitis. J ClinPeriodontol 2014; 41: 504–512. doi: 10.1111/jcpe.12237.

AbstractAim: To evaluate long-term clinical and radiographic parameters of osseointe-grated implants in non-smoker patients with a previous history of chronicperiodontitis.Materials and Methods: Fifty-four screw-type implants with a moderately rough-ened surface and internal hexagonal implant–abutment connection were placedaccording to a two-phase protocol and 40 reference teeth were analysed at base-line, and after 5 and 10 years. Pocket probing depth (PPD), clinical attachmentlevel (CAL) and bleeding on probing were analysed 6x/tooth in all teeth, implantsand reference teeth. Radiographic peri-implant bone level was measured on themesial and distal surfaces. The prevalence of peri-implantitis and the survival rateof the implants were assessed at the patient and implant levels. Data were analysedusing descriptive statistics, Mann–Whitney U-test, and Wald Z-test, at a = 5%.Results: In implants, the CAL at 5 years was 0.3 mm higher, and at 10 years1.2 mm higher in comparison to baseline. The corresponding data for the refer-ence teeth were 0 mm and 0.5 mm respectively. Multilevel testing showed statisti-cal difference for PPD between implants and teeth over time. After 10 years, themean mesial bone loss was 0.63 � 0.26 mm, and the mean distal bone loss was0.56 � 0.25. The survival rates were 100% and 92.3% for the implants in themandible and the implants in the maxilla respectively.Conclusions: Screw-type implants with internal hexagon placed in patients with aprevious history of periodontitis attending a regular maintenance programmedemonstrated stable clinical and radiographic results after 5 and 10 years.

Joerg Meyle1, Gero Gersok2,Rolf-Hasso Boedeker3 and

Jos�e Roberto Gonzales1

1Department of Periodontology, Dental

School Justus-Liebig-University of Giessen,

Giessen, Germany; 2Dentist, Private Practice,

Hameln, Germany; 3Institute of Medical

Statistics, Faculty of Medicine Justus-Liebig-

University of Giessen, Giessen, Germany

Key words: bone level; dental implants; long-term; periodontitis; supportive periodontal

treatment; survival rate

Accepted for publication 23 January 2014

Since the early 1980s, the use of tita-nium dental implants has become apredictable treatment for oral reha-bilitation of completely or partiallyedentulous patients (Branemarket al. 1977, Adell et al. 1981). Sincethe early years, the clinical indica-tions for implant therapy haveincreased considerably. To date, den-tists can choose among a variety of

systems and surgical possibilities forimplant treatment. The high, long-term predictability that has beenshown for implant therapy in par-tially edentulous patients is animportant factor in this development(Hermann et al. 1997, Hultin et al.2000, Rutar et al. 2001, Rasmussonet al. 2005, Roos-Jansaker et al.2006, Esposito et al. 2007, Grutter &

Conflict of interest and source offunding statement

The authors declare that they have noconflicts of interest. No external fund-ing, apart from the support of theauthors’ institution, was available forthis study. The authors declare thatthere are no conflicts of interest in thisstudy.

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd504

J Clin Periodontol 2014; 41: 504–512 doi: 10.1111/jcpe.12237

Belser 2009). Systematic reviewshave reported survival rates ofimplants of more than 95% after anobservation period of at least 5 years(Pjetursson et al. 2004, den Hartoget al. 2008, Jemt 2008, Aglietta et al.2009). In addition, one systematicreview reported survival rates of95.5% addressing immediate, earlyand conventional implantapproaches, when single-implant res-torations in the aesthetic zone withadjacent natural teeth were evaluated(den Hartog et al. 2008).

Retrospective evaluations ofscrew-type implants with internalhexagon demonstrated similar sur-vival rates higher than 90% as withother systems, after a period of5 years (Gomez-Roman et al. 2001,Krennmair et al. 2002, Krennmair &Waldenberger 2004, Ricci et al. 2004,Strietzel et al. 2004). The implant sys-tem (Frialit-2; Dentsply, Mannheim,Germany) represents the evolution ofthe Tuebingen tapered ceramicimplant (Albrektsson & Wennerberg2004a). The implant system has asandblasted and etched surface(Albrektsson & Wennerberg 2004a).Its tapered macrodesign offers thepossibility of placing the implants inslight maxillary or mandibular con-cavities and near adjacent teeth withconverging roots. Furthermore, thewide-diameter implants were con-ceived to enable the elaboration ofemergence profiles that were closer tothe natural dentition. The implantsystem proved to be successful in allareas of indication in partially eden-tulous patients after an observationperiod of a maximum of 7 years(Krennmair et al. 2002). However, todate, no study has reported retrospec-tive or prospective data of thisimplant system placed in patientswith a history of periodontitis.

In recent years, authors have eval-uated the long-term success of vari-ous implant systems in patients withperiodontitis, showing differentresults (Mengel et al. 2001, Hardtet al. 2002, Baelum & Ellegaard2004, Karoussis et al. 2004, 2007,Malo et al. 2007, Arisan et al. 2010,Garcia-Bellosta et al. 2010, Gianserraet al. 2010, Simonis et al. 2010, Roc-cuzzo et al. 2012, Swierkot et al.2012). The available evidence for anassociation between periodontitis andperi-implantitis is scarce (Renvert &Persson 2009). While some authors

concluded that a previous history ofperiodontal disease may not have asignificant impact on implant failuresup to 5 years after loading (Baelum& Ellegaard 2004, Garcia-Bellostaet al. 2010, Gianserra et al. 2010),other authors reported that a previ-ous history of periodontitis was asso-ciated with peri-implantitis and mayrepresent an enhanced risk for thisdisease (Hardt et al. 2002, Karoussiset al. 2004, 2007, Carcuac & Jansson2010, Simonis et al. 2010, Koldslandet al. 2011, Swierkot et al. 2012).Moreover, the few studies reportingresults of implant therapy in patientswith periodontitis after 10 and moreyears are not conclusive. A 10-yearretrospective analysis of radiographicbone level changes in implants sup-porting single-unit crowns in peri-odontitis versus periodontally healthypatients showed that implants in peri-odontitis patients yielded lower sur-vival rates and higher mean marginalbone loss rates compared with thoseof implants placed in periodontallyhealthy patients. The results wereindependent of the implant systemused and the healing modalityapplied (Matarasso et al. 2010). Asystematic review of the risk ofimplant failure and marginal boneloss in subjects with a history of peri-odontitis reported that periodontitissubjects were at significantly higherrisk for implant failure and greatermarginal bone loss compared to peri-odontally healthy subjects (Safii et al.2010). These clinical findings areaggravated in smokers (Aglietta et al.2011, Levin et al. 2011). After10 years, implants placed in smokerswith a history of treated periodontitisand enrolled in a supportive therapyprogramme yielded lower survivalrates and higher marginal bone lossrates compared with those ofimplants placed in periodontallyhealthy smokers (Aglietta et al.2011). Despite these reports, resultsof a further systematic review onimplant treatment in periodontitis-susceptible patients demonstratedthat the survival rates of implantswere high in individuals with a his-tory of periodontitis (Schou 2008).Nevertheless, a higher incidence ofperi-implantitis was also found inthese patients.

The majority of studies and sys-tematic reviews addressing the long-term effects of implant therapy in

association with periodontitis havebeen performed in patients withchronic periodontitis. Studies inpatients with a history of aggressiveperiodontitis are scarce (Mengel et al.2007, De Boever et al. 2009). A 10-year prospective analysis of implantsin subjects treated for generalizedaggressive periodontitis demonstratedthat bone and attachment loss aroundimplants in these patients were higherthan in periodontally healthy sub-jects, or patients with chronic peri-odontitis (Mengel et al. 2007, DeBoever et al. 2009).

The aim of this prospective studywas to evaluate the long-term resultsat 5 and 10 years of two-stage screw-type implants with internal hexagonplaced in patients with a previoushistory of periodontitis.

Materials and Methods

Patient selection

Patients with chronic periodontitiswere included in this prospec-tive study at the Department ofPeriodontology, Dental School, Ju-stus-Liebig-University of Giessen,Germany. The diagnosis of chronicperiodontitis was based on the recentinternational classification of peri-odontal diseases and conditions(Flemmig 1999, Tonetti et al., 2005).Twenty patients (nine males and ele-ven females) participated in thestudy. The patients were includedaccording to the following criteria:Age ≥ 18 years, absence of relevantsystemic conditions, 4–6 months ofhealing after tooth extraction andpresence of sufficient residual alveo-lar bone volume for achievingprimary implant stability. Allpatients were partially edentulous,with missing single or multiple teeth.The reported association betweenperiodontitis and implant loss/peri-implantitis may be confounded bysmoking (a risk for both conditions).As smokers are at higher risk fordeveloping peri-implantitis, to avoidbias, smokers were not included inthe study (Roos-Jansaker et al.2006). The study was approved bythe ethics committee of the Univer-sity of Giessen. All patients gavetheir written informed consent. Thestudy was conducted in accordancewith the ethical guidelines of theHelsinki Declaration and with the

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Long-term implant results in periodontitis 505

guidelines of good clinical practice(GCP).

Periodontal treatment

All patients underwent systematicperiodontal therapy. The periodontaltreatment consisted of a hygienicphase, achieving full-mouth plaqueand bleeding scores ≤30% beforeimplant placement. After supragingi-val professional tooth cleaning, sub-gingival debridement in the form ofscaling and root planing was per-formed in all teeth with probingpocket depth ≥4 mm and bleeding onprobing (BOP). The therapy was per-formed with manual and mechanicalinstruments by an experienced dentalhygienist. If necessary, reconstructiveor resective periodontal surgerieswere performed by two experiencedspecialists for Periodontology (J.G.,J.M.). Thereafter, all patients activelytook part in a regular supportiveperiodontal treatment programme.During the first year, they were eval-uated at intervals of 3–4 months;subsequently, patients were recalledat intervals of 6 months.

Implant placement

The patients were consecutively pro-vided with implants (Frialit-2; Dents-ply, Mannheim, Germany). This typeof implant has a rough surface witha grit-blasted and thermal etchedFriadent� plus microstructure, withthe exception of the most cervicalportion, where a smooth collar waspresent (Albrektsson & Wennerberg2004b). The implants were placedfollowing the classic two-stage proto-col by two experienced specialists inperiodontology and implantology(J.M., J.G.). Implants were usuallyinserted using a pre-fabricated stentwith the implant guides and posi-tioned with the coronal border of therough surface at the level of the alve-olar bone crest and left to heal underthe mucoperiosteal flap.

After 4–6 months of osseointe-gration, the prosthetic restorationswere built on the implants by thesame two specialists who performedthe surgeries. The abutments usedwere matching in all cases withoutexception. The prosthetic treatmentof choice was cemented singlecrowns. This time point was consid-ered to be the baseline for the fur-

ther analyses. All patients receivedoral hygiene instructions to maintainappropriate oral hygiene around theimplants and remaining teeth. Intotal, 54 implants were placed andanalysed at baseline, and at the 5- and10-year follow-up examinations.

Clinical evaluation

Clinical and radiographic evalua-tions were performed at the stage ofloading (baseline) and at least everyyear. Specifically after 5 and 10years, a complete documentation ofperiodontal and peri-implant condi-tions was recorded, using the follow-ing parameters: pocket probingdepth (PPD), clinical attachmentlevel (CAL) and BOP (6x/tooth),using a PCP UNC 15 periodontalprobe. Oral hygiene indices includedthe O’Leary simplified plaque indexand the papillary bleeding index (4x/tooth) (O’Leary et al. 1972, Saxer &Muhlemann 1975). The clinicalparameters were assessed for allteeth, and specifically for the refer-ence teeth. These teeth were matchedto the implants according to theirposition, as there were the teethlocated on the contra-lateral side ofthe implants. These teeth were analy-sed as a reference to the implants,since data from long-term (10 years)controlled studies comparing teethand implants in well-maintainedpatients demonstrated that changesin soft tissues occurred in a similarmanner around implants and aroundteeth (Klinge et al. 2006).

The clinical parameters PPD,CAL and BOP of the implants weremeasured analogously to that of thenatural teeth. In implants, CAL wasthe distance from the crown marginto the deepest point reached by thepocket probing depth. These mea-surements were performed withoutlocal anaesthesia, thus, they werenot bone sounding measurements.

Radiographic examination

Patients were screened by panoramicX-rays taken after implant surgery,and at every 24 months thereafter.At the time of crown insertion (base-line), and at the 5- and 10-year fol-low-up examinations, periapicalradiographs were obtained using theparallel long-cone technique. Thesewere used to calculate the marginal

bone level changes of the implants.The previously calibrated radio-graphic examinations were performedseparately by two different investiga-tors (G.G. and J.G.). The location ofthe marginal bone level in relation tothe implant shoulder was assessed atthe mesial and the distal sites of theimplants using a magnifying loupe2X (120 mm diameter; GFS,Warstein, Germany) and an x-rayviewer Planilux 61 9 61 cm (Plani-lux� GmbH, Warstein, Germany)(Gomez-Roman et al. 1997). Twodistances were measured: (a) the dis-tance from the implant shoulder tothe deepest contact of the marginalbone with the implant surface (boneto implant level) and (b) the distancefrom the implant shoulder to thehighest point of the crestal marginalbone in the inter-dental space (crestalperi-implant level).

Definition and prevalence of peri-

implantitis

For assessing peri-implantitis, thedefinition used in this study was mod-ified from previously reported defini-tions (Lindhe et al., 2008, Koldslandet al. 2011, Lang et al., 2011). Thedefinition used was as follows: loss ofradiographic bone (at the mesial, orthe distal, or both peri-implant sites)after 5 or 10 years compared to base-line, combined with BOP/suppuration(at least at one peri-implant site). Theprevalence of peri-implantitis after 5and 10 years was analysed on theimplant and subject levels. Thus, thepercentages of implants and subjectspresenting with loss of radiographicbone combined with BOP/suppura-tion were calculated.

Data analysis

The statistical analysis included adescriptive analysis of the data, con-sisting of mean values and standarddeviations (SD). Three time pointswere evaluated: baseline was the timewhen the implants were loaded withthe supra-structure, and from thatpoint, the evaluations after 5 years,and after 10 years followed. The vari-ables taken into consideration for thestatistical analysis were as follows:pocket probing depth (PPD), clinicalattachment level (CAL) and BOP (6x/sites) of the implants, and of the refer-ence teeth. In addition, to demon-


506 Meyle et al.

strate the periodontal status of thepatients, the clinical parameters PPDand CAL were assessed in all teeth,and divided into three measurementcategories: (a) 1–3 mm, (b) 4–5 mmand (c) >5 mm.

The primary outcome variable wasthe change in CAL at implants andreference teeth between baseline and5 years, and baseline and 10 years.The null hypothesis was: there are nochanges in CAL between these timepoints. As the primary outcome vari-able is the change in CAL, theimplant (and not the patient) wastaken as the statistical unit, despitethe fact that multiple implants werepresent per patient. To correct forwithin-patient dependency, multilevelmodelling was used to determine theeffect over time on the clinical param-eters CAL, PPD and BOP (Wald Ztest). Since follow-up was conductedat irregularly time intervals, time wasincluded in the model. The differencesin the clinical parameters between thetwo time points, baseline and 5 yearsand baseline and 10 years, were eval-uated using the Mann–WhitneyU-test. In addition, the analysis of thedifference in CAL after 10 yearsbetween implants and reference teethwas performed using the unpairedt-test. A p-value of <0.05 was consid-ered to indicate a statistically signifi-cant difference.

The cumulative survival rate (CSR)was calculated using the Kaplan–Meier analysis which is a good indica-tor of the cumulative survival rate.

All statistical analyses were per-formed using IBM SPSS Statistics 20 soft-ware (IBMCorp. 2011, NY, USA).

Results

Clinical measurements

The population consisted of ninemales and eleven females. The meanage of the patients at baseline was48.7 � 8.9 years. 43.9% of theimplants were placed in the posteriormandible, 33.6% in the posteriormaxilla, 14.6% in the anterior max-illa and 7.8% in the anterior mandi-ble. The distribution of the diameterof the implants was 51.8%(4.5 mm), 33.6% (3.8 mm) and14.5% (5.5 mm). The distribution ofthe length of the implants was54.5% (13 mm), 40.2% (15 mm),2.7% (11 mm) and 2.6% (10 mm).

Table 1 shows the mean values andSD of the number of teeth per sub-ject, and the clinical parametersPPD, CAL and BOP of all teeth atthe three examination times: (a)baseline, (b) examination after5 years and (c) examination after10 years. The mean number of teethdecreased from 17.1 to 15 after10 years. Mean PPD and CAL of allteeth demonstrated a slight increaseafter 5 years (0.1 mm and 0.2 mmrespectively). After 10 years, bothmean PPD and CAL increased incomparison to the baseline values(0.3 mm and 0.4 mm respectively).Similarly, the mean percentages ofBOP slightly increased after 5 years(1.7%), and after 10 years (3.1%), incomparison with the baseline meanvalue.

The clinical parameters PPD andCAL of all teeth were also subdi-vided into three measurement cate-gories to analyse the periodontalstatus of the patients: 1–3 mm, 4–5 mm and >5 mm. The percentageof sites with PPD 1–3 mm decreased,and the percentage of sites with PPD

4–5 mm and those >5 mm increasedafter 10 years. Similar changes wereobserved for the parameter CAL.

Table 2 shows the mean values �SD of the clinical parameters of theimplants at baseline, at the 5-yearand at the 10-year examinations. Incomparison to the baseline PPD andCAL mean values, both parametersshowed higher mean values at the 5-year examination (0.3 mm, p < 0.05,Mann–Whitney U-test). After10 years, the mean PPD and themean CAL were 0.7 mm and 1.2 mmhigher, respectively, in comparisonwith the baseline values (p < 0.05,Mann–Whitney U-test). The meanpercentage of BOP was 5% lower at5 years compared to baseline. After10 years, the mean percentage ofBOP was 6% higher in comparisonwith the baseline value. With regardto BOP, there were no differencesbetween the two time points.

Table 3 shows the mean values �SD of the clinical parameters of thereference teeth at the three timepoints. Whereas the mean PPD andCAL values at the 5 years examina-

Table 1. Mean values � standard deviation (SD) of the clinical parameters in the completedentition of the patients at baseline, at the 5-year and at the 10-year follow-up examina-tions. PPD and CAL were divided into three categories, 1–3 mm, 4–5 mm and >5 mm(n = 20)

Time Baseline 5 years 10 years

ParametersNumber of teeth 17.1 � 7.2 16.9 � 7.2 15 � 7.2PPD (mm) 2 � 0.7 2.1 � 0.6 2.3 � 0.9CAL (mm) 2.3 � 0.9 2.5 � 1 2.7 � 1.2BOP (%) 11.2 � 10 12.9 � 11.8 16 � 9.6PPD 1–3 mm (%) 92.3 � 14.7 85.8 � 27.1 88 � 20.5PPD 4–5 mm (%) 7.3 � 14.7 12.5 � 25.5 10.2 � 17.3PPD > 5 mm (%) 0.4 � 2.7 1.7 � 6.3 1.9 � 5.4CAL 1–3 mm (%) 77.4 � 31.6 74.2 � 34.4 75.9 � 28.7CAL 4–5 mm (%) 18.4 � 25.3 19.2 � 26.3 16.7 � 18.1CAL > 5 mm (%) 4.3 � 12.5 6.7 � 17.6 7.4 � 16.4

BOP, bleeding on probing; CAL, clinical attachment level; PPD, pocket probing depth.

Table 2. Mean values � standard deviation (SD) of the clinical parameters in implants atbaseline, at the 5-year and at the 10-year follow-up examinations (n = 54)


ParametersPPD (mm) 2.6 � 0.8 2.9 � 0.8* 3.3 � 1.0†

CAL (mm) 2.7 � 0.9 3.0 � 0.8* 3.9 � 2.4†

BOP (%) 21 � 25 16 � 16 27 � 17

*Statistically significant at the level of p < 0.05 with the Mann–Whitney-U-test for thedifferences in mean clinical parameters between baseline and 5 years.†Statistically significant at the level of p < 0.05 with the Mann–Whitney-U-test for thedifferences in mean clinical parameters between baseline and 10 years.BOP, bleeding on probing; CAL, clinical attachment level; PPD, pocket probing depth.



tion were similar to that of baselinevalues (p > 0.05, Mann–Whitney U-test), after 10 years, the values ofboth parameters were 0.5 mm higherthan those at baseline (p < 0.05,Mann–Whitney U-test). Similar tothe implants, the mean percentage ofBOP was 5% lower at 5 years and2% higher at 10 years compared tothe percentage at baseline. However,no differences were calculated forthis parameter between the two timepoints.

In this study, we further evaluatedthe differences in the CAL measure-ments at baseline and at 5 years, andat baseline and at 10 years. Theresults are shown in box plots. Thehorizontal line inside the box marksthe median value. The box is wherethe main data reside, covering 50%of the data around the median. Thelower line of the box marks the 1stquartile, the upper line the 3rd quar-tile. The whiskers, the vertical linesextending from the box, mark thesmallest and highest value, except theoutliers. If the distance of a valuefrom the box is more than 1.5 timesthe length of the box it is identifiedas an outlier, represented by an “o”or an “*”. Figure 1 demonstrates theCAL change in the implants. Ahigher change in the CAL was deter-mined from baseline to 10 years,compared to the change from base-line to 5 years (p < 0.05, t-test). Con-versely, in the reference teeth nodifferences were determined in thechange in the CAL from baseline to10 years in comparison with thechange in the CAL from baseline to5 years (Fig. 2).

The results from the multilevelanalysis regarding the clinicalparameters CAL, PPD and BOPover time are shown in Table 4. Theparameter PPD showed significantdifferences between implants and ref-erence teeth over time. No significantdifferences were observed over timebetween implants and reference teethin CAL and BOP.

Radiographic bone levels of implants

The mean bone to implant measure-ments on the mesial side were:3.55 � 1.69 mm at baseline, 3.71 �1.59 mm at 5 years and 4.18 � 1.95mm at 10 years. On the distal side,the corresponding values were:

3.66 � 1.63 mm at baseline, 3.89 �1.97 mm at 5 years and 4.22 � 2.15mm at 10 years. The mean crestalperi-implant bone measurements onthe mesial side were: 2.45 � 1.36 mmat baseline, 2.46 � 1.37 mm at 5years and 2.63 � 1.30 mm at 10years. On the distal side, the corre-sponding values were: 2.51 � 1.15mm at baseline, 2.52 � 1.44 mm at5 years and 2.89 � 1.40 mm at10 years. Thus, the mean loss of boneto implant level after 5 years was0.16 � 0.10 mm on the mesial sideand 0.23 � 0.34 mm on the distalside. The mean loss of bone toimplant level after 10 years was0.63 � 0.26 mm on the mesial sideand 0.56 � 0.25 mm on the distal

Table 3. Mean values � standard deviation(SD) of the clinical parameters in the refer-ence teeth at baseline, at the 5-year and atthe 10-year follow-up examinations (n = 40)


ParametersPPD(mm)

2.1 � 0.6 2.2 � 0.7 2.6 � 0.8†

CAL(mm)

2.4 � 0.8 2.4 � 0.8 2.9 � 1.2†

BOP(%)

18 � 20 13 � 17 20 � 18

†Statistically significant at the level ofp < 0.05 with the Mann–Whitney-U-test forthe differences in mean clinical parametersbetween baseline and 10 years.BOP, bleeding on probing; CAL, clinicalattachment level; PPD, pocket probingdepth.

Fig. 1. Changes in CAL in the implants, between baseline and 5 years (left), andbetween baseline and 10 years (right) (see text). *p < 0.05, Mann–Whitney U-test.

Fig. 2. Changes in CAL in the reference teeth, between baseline and 5 years (left), andbetween baseline and 10 years (right).


508 Meyle et al.

side. The mean loss of crestal peri-implant bone level after 5 years was0.01 � 0.01 mm on the mesial sideand 0.01 � 0.29 mm on the distalside. The mean loss of crestal peri-implant bone level after 10 years was0.18 � 0.06 mm on the mesial sideand 0.38 � 0.25 mm on the distalside.

This means that there was aradiographic mean bone loss of<1 mm in all implants after 5 and10 years.

Prevalence of peri-implantitis

Based on the definition used in thisstudy, radiographic characteristics ofperi-implantitis were observed after 5and 10 years. Although the radio-graphic mean bone loss was <1 mmin all implants, there was bleedingupon probing in sites showing boneloss. In this case, the prevalence ofperi-implantitis on the implant levelwas 8.9% after 5 years and 23.8%after 10 years. On the patient level itwas 18.2% after 5 years and 30%

after 10 years. This is in accordancewith recently published data on otherimplant systems (Mir-Mari et al.2012, Renvert et al. 2012). However,in this study, we detected horizontalor angular bone loss at the mesial,the distal, or both sites. No circum-ferential peri-implant loss of bonewas determined. It is important tonote that in this study the patientsunderwent a periodontal supportivetreatment at regular intervals.

Survival and success rates of implants

After 10 years, two implants placedin the maxilla were lost yielding asurvival rate of 92.3%. The survivalrate in the mandible was 100%. Noearly failures were observed (Fig. 3).One further implant in the maxillawas lost after the observational per-iod of the study. The data of the lostimplants were evaluated after 5 yearsbut not after 10 years.

Implant success was calculatedconsidering the occurrence of peri-implantitis found within the cohort

of implants investigated in thisstudy. Thus, 91.1% and 76.2% ofimplants were successful after 5 and10 years respectively.

Discussion

This prospective 10-year studyanalysed clinical parameters andperi-implant bone level changes ofscrew-type implants with internalhexagon placed in patients with ahistory of chronic periodontitis. Ourclinical and radiographic results arein accordance with studies reportingeffective long-term results of implanttreatment in patients with periodon-titis if an adequate infection controland an individualized maintenanceprogramme are provided (Garcia-Bellosta et al. 2010, Al Zahrani2008, Klokkevold & Han 2007, Junget al. 2008, Evian et al. 2004, Fardal& Grytten 2013). Due to its macro-structure, this implant system iswell suited for implantation in thefresh alveolus (Schulte et al. 1992).However, in the patients analysedhere, it was used only for lateimplantations after finishing peri-odontal treatment and completelyhealed alveolar ridge.

To demonstrate periodontal con-ditions, we assessed clinical parame-ters in the complete dentition atbaseline (the time point where theimplants were loaded and providedwith the prosthetic restorations), andat the 5- and 10-year examinations.Compared with baseline, the meanvalues of PPD, CAL and BOP wereslightly higher after 5 years, andagain after 10 years. This was alsoin accordance with the percentage ofsites with PPD and CAL > 5 mmthat was also higher after 5 yearsand after 10 years. Conversely, thepercentage of sites with PPD andCAL 1–3 mm was similar to baselineafter 5 years, showing higher levelsat 10 years. This indicates a stableclinical situation in the patientsbetween baseline and 5 years, how-ever, with slight increments in thepercentages of deeper periodontalpockets (PPD > 5 mm) and higherloss of attachment (CAL > 5 mm)after 10 years. This result is inaccordance with studies analysingimplants on a long-term basis thatwere placed in patients with previousperiodontitis (Matarasso et al. 2010,Simonis et al. 2010, Roccuzzo et al.

Table 4. Average differences in CAL, PPD and BOP between implants and reference teethat baseline, at the 5-year and at the 10-year follow-up examinations

Baseline p

Parameters b (95% CI)PPD (mm) 2.48 (0.03 to 0.23) <0.013*CAL (mm) 0.27 (�0.11 to 0.15) = 0.78BOP (%) 0.66 (�0.09 to 0.12) = 0.51

*Statistically significant at the level of p < 0.05 with the Wald Z-test. The regression coeffi-cients (b) indicate the differences in the clinical parameters between reference teeth andimplants over the measurement periods (5 and 10 years) from baseline.BOP, bleeding on probing; CAL, clinical attachment level; PPD, pocket probing depth.

Fig. 3. Kaplan–Meier cumulative survival rate (CSR) of the implants in the maxillaand mandible placed in patients with a history of periodontitis.



2012, Fardal & Grytten 2013). Forexample, in this study, there was anincrease in BOP after 5 and 10 years,although the patients were wellsupported. An increase in bleeding isan indicator of the long-term oralhygiene practices and its relevancefor maintaining healthy periodontaland peri-implant tissues (Mombelli& Lang 1998, Ferreira et al. 2006).

The main outcome variable of thestudy was the change in CAL ofimplants from baseline to 5, andfrom baseline to 10 years. We com-pared these data with the data ofcontra-lateral teeth, to analyse CALin implants in comparison with CALin natural teeth used as reference inthe same patients. Our results showan increase in the mean CAL inimplants from baseline to 10 years,and from baseline to 5 years, beingsignificantly higher between baselineand 10 years. The analysis in the ref-erence teeth did not show differencesbetween baseline and 5 years. Ourdata are in accordance with theresults of the periodontal parametersanalysed by Ricci et al. (2004) in thesame type of implants after 5 years,although different evaluation formswere used. The authors reported thatin 71.4% of the implants probingdepth did not exceed 3 mm, in24.1% PPD was between 3 and5 mm and in 4.5% PPD was greaterthan 5 mm (Ricci et al. 2004). Wefound similar data. In implants, themean probing depth was 2.6 mm atbaseline, 2.9 mm after 5 years and3.3 mm after 10 years, in accordancewith the 95.5% of sites with lessthan 5 mm reported by the study ofRicci et al. (2004).In this study, wealso found lower PPD and CALvalues in the reference teeth than inimplants. Other studies assessingclinical parameters of peri-implanttissues in patients with varying sever-ity of chronic periodontitis reporteda greater loss of attachment(p < 0.05) around implants in thegroup with severe periodontitis com-pared to the no/mild periodontitisgroup (Ferreira et al. 2006, Aloufiet al. 2009).

In addition, the clinical data wereanalysed using multilevel modelling,to correct for the difference in num-ber of implants per patient and thedependency of the observationswithin each patient over time. Theclinical parameter PPD showed

differences between implants andreference teeth over time. The param-eters CAL and BOP demonstrated nodifferences between implants andreference teeth over time.

According to the Kaplan–Meiermethod, the CSR was calculated tobe 96.3%. The high CSR in ourstudy is in accordance with the datareported by other authors on sur-vival rates of same type of implantsafter 5 years (Krennmair et al. 2002,Krennmair & Waldenberger 2004,Ricci et al. 2004, Strietzel et al.2004). In contrast, the CSR in ourstudy was higher than the CSRreported in a retrospective studyanalysing the same type of implantsafter 5 years, with 91.08% for themaxilla and 89.1% for the mandible(Perry & Lenchewski 2004).Krennmair & Waldenberger (2004)retrospectively evaluated wide-diam-eter (5.5 mm) implants used for dif-ferent forms of prostheticrestorations, placed in patients with-out a history of periodontal disease.The authors reported a CSR of97.3% in the maxilla and 100% inthe mandible, with two maxillaryimplants lost. The results of ourstudy are similar, and both studiesdemonstrated only few implantlosses in the maxilla after a pro-longed period of time. This is inaccordance with the majority of clin-ical studies of screw-type implantsafter 5 and 10 years. (Lekholm et al.1999, Lambrecht et al. 2003, Striet-zel et al. 2004, Blanes et al. 2007).However, it is important to note thatthe CSR of our analysis after 5 and10 years in patients with a previoushistory of periodontitis is similar tothe CSR data of the study ofKrennmair & Waldenberger (2004)in non-periodontitis patients.

Peri-implant vertical bone loss isconsidered an important radio-graphic parameter for analysingtreatment outcomes and long-termsuccess (Lindhe & Meyle 2008, Meyle2012). In this study, the evaluationof vertical bone loss was performedon intra-oral films using the paralleltechnique. In the study of Ricci et al.(2004), the radiographic resultsshowed that 71.4% had less than3 mm of crestal bone loss, with amean mesial bone loss of 2.18 �1.6 mm and a mean distal bone lossof 2.16 � 1.5 mm after 5 years. Ourstudy showed small changes after 5

and 10 years, which is not in accor-dance with the results that the major-ity of studies of patients withprevious history of chronic or aggres-sive periodontitis have reported(Schou et al. 2006, Mengel et al.2007, Schou 2008, Matarasso et al.2010). However, our data are inaccordance with the data reported ina clinical and radiographic prospec-tive study of implant treatment out-come in periodontally susceptibleand non-susceptible patients (De Bo-ever et al. 2009). After an average of5 years, the authors reported anaverage marginal bone loss for allimplants of 0.12 � 0.71 mm on themesial side and 0.11 � 0.68 mm onthe distal side. Specifically, in thegroup with aggressive periodontitis,the bone loss per year was 0.17 mm.The main difference between this andour study is that in the study of DeBoever et al. (2009) patients weretreated with non-submerged Strau-mann implants. This is less than thereported bone loss by Mengel et al.(2007), with an average of 2.07 mmin the first year and a total of1.3 mm in the subsequent 9 years(Mengel et al. 2007). Our data con-firm the lower bone loss levels foundin the prospective study of DeBoever et al. (2009).

The percentage of peri-implantitisobserved in this study is in accor-dance with recently published dataon other implant systems (Mir-Mariet al. 2012, Renvert et al. 2012). Asit is known that the absence ofmaintenance treatment is associatedwith a higher incidence of peri-im-plantitis, it is important to note thatin this study the patients underwentperiodontal supportive treatment atregular intervals (Costa et al. 2012).

Conclusions

The results of this study demonstratethat patients previously treated forchronic periodontitis and thereafterwith screw-type implants with inter-nal hexagon showed stable peri-implant variables and survival rates,and stable radiographic bone levelsafter 5 and 10 years, if patients wereengaged in a regular periodontalmaintenance programme. Neverthe-less, there was a higher loss of CALaround the implants than around thenatural reference teeth, although notclinically relevant.


510 Meyle et al.

Acknowledgements

The authors thank the colleagues ofthe Department of Periodontology,Justus-Liebig-University of Giessen,who contributed to this study, espe-cially Mrs. V. Petsch, R. Wilhelmand P. Pellizzi. They also thank Dr.R.H. Boedeker (Institute of MedicalStatistics, University of Giessen) forhis valuable statistical assistance.

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Address:Dr. Joerg MeyleDepartment of PeriodontologyJustus-Liebig-University of GiessenGermanySchlangenzahl 1435392 GiessenGermanyE-mail: [email protected]

Clinical Relevance

Scientific rationale for the study:the use of osseointegrated implantsin patients with a history of peri-odontitis is continuously increas-ing, although there is still a lack oflong-term data for this type ofpatient.

Principal findings: there is a stableperi-implant and periodontal situa-tion after 5 and 10 years under thepremise that patients with previousperiodontitis receive regular, sup-portive periodontal treatment.Practical implications: all patientswith a history of periodontitis under-

going implant therapy must beincluded and treated in a long-termperiodontal supportive treatmentprogramme.


512 Meyle et al.

long-term analysis of osseointegrated implants in non-smoker patients with a previous history of...

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