App Ref 73
App Ref 73
application of a nanocrystalline
hydroxyapatite (Ostimt) or
a bovine-derived xenograft
(Bio-Osst) in combination with a
collagen membrane (Bio-Gidet).
A case series
Schwarz F, Bieling K, Latz T, Nuesry E, Becker J. Healing of intrabony peri-
implantitis defects following application of a nanocristalline hydroxyapatite (Ostimt)
or a bovine-derived xenograft (Bio-Osst) in combination with a collagen membrane
(Bio-Gidet). A case series. J Clin Periodontol 2006; 33: 491–499. doi: 10.1111/
j.1600-051X.2006.00936.x.
Abstract
Objectives: The aim of the present case series was to evaluate the healing of
intrabony peri-implantitis defects following application of a nanocrystalline
hydroxyapatite (NHA) or a bovine-derived xenograft in combination with a collagen
membrane (BDX1BG).
Material and Methods: Twenty-two patients having moderate peri-implantitis
(n 5 22 intrabony defects) were randomly treated with (i) access flap surgery (AFS)
and the application of NHA, or with AFS and the application of BDX1BG. Clinical
parameters were recorded at baseline and after 6 months of non-submerged healing.
Results: Post-operative wound healing revealed that NHA compromized initial
adhesion of the mucoperiosteal flaps in all patients. At 6 months after therapy, NHA
showed a reduction in the mean PD from 7.0 0.6 to 4.9 0.6 mm and a change in
the mean clinical attachment loss (CAL) from 7.5 0.8 to 5.7 1.0 mm. In the
Key words: bone graft; clinical study; collagen
BDX1BC group, the mean PD was reduced from 7.1 0.8 to 4.5 0.7 mm and the
membrane; non-submerged healing; peri-
mean CAL changed from 7.5 1.0 to 5.2 0.8 mm. implantitis
Conclusion: Within the limits of the present case series, it can be concluded that at
6 months after surgery both therapies resulted in clinically important PD reductions Accepted for publication 31 March 2006
and CAL gains.
Nowadays, the term peri-implant dis- and peri-implantitis. While peri-implant implantitis was defined as an inflamma-
ease is collectively used to describe mucositis includes reversible inflamma- tory process that affects all tissues
biological complications in implant den- tory reactions located solely in the around an osseointegrated implant in
tistry including peri-implant mucositis mucosa adjacent to an implant, peri- function, resulting in a loss of the sup-
r 2006 The Authors. Journal compilation r 2006 Blackwell Munksgaard 491
492 Schwarz et al.
porting alveolar bone (Albrektsson & non-resorbable materials such as ex- implantitis defects following treatment
Isidor 1994). The prevalence of peri- panded polytetrafluorethylene (e-PTFE) with access flap surgery (AFS) and the
implantitis is difficult to estimate as the to bioabsorbable membranes composed application of NHA or a bovine-derived
determination of criteria for implant of dura-mater, polylactic acid, polygly- xenograft in combination with a col-
success is not uniform (Albrektsson colic acid and polyurethane (Magnusson lagen membrane.
et al. 1986, Buser et al. 1990, van Steen- et al. 1988, Greenstein & Caton 1993,
berghe 1997). However, considering the Hutmacher et al. 1996, Kohal et al.
clinical and radiological threshold para- 1998). Most recently, many investiga- Materials and Methods
meters assessed at different implant tions have focused on the use of products Study population
designs, it may vary between 10% and derived from type I and type III porcine
29% (Brägger et al. 1996, Buser et al. or bovine collagen (for a review, see Twenty-two partially edentulous patients
1997, Karoussis et al. 2003, 2004). To- Bunyaratavej & Wang 2001). Some ad having moderate peri-implantitis (Mom-
day, there is considerable evidence sup- vantageous properties of collagen over belli & Lang 1994) attending the Depart-
porting the view that microbial coloni- other materials include haemostatic fun- ment of Oral Surgery, Heinrich Heine
zation plays a major role in the aetiology ction, allowing an early wound stabiliza- University, Düsseldorf, Germany, for
of peri-implant infections (Mombelli et tion, chemotactic properties to attract peri-implant bone augmentation proce-
al. 1988, Becker et al. 1990, Alcoforado fibroblasts and, semipermeability, facil- dures were included in this parallel-
et al. 1991). Even though bone resorp- itating nutrient transfer (Postlethwaite et design case series (i.e. 11 patients in
tion in peri-implantitis defects may also al. 1978, Yaffe et al. 1984, Schwarz et al. each group). Each patient was given a
be intensified by occlusal overload (Isi- 2006b). However, a major drawback of detailed description of the procedure and
dor 1996, 1997), it was assumed that the native collagen is the fast biodegradation was required to sign an informed consent
removal of bacterial plaque biofilms by the enzymatic activity of macro- before participation. The study was in
from the implant surface seems to be a phages, polymorphonuclear leucocytes accordance with the Helsinki Declara-
pre-requisite in order to stop disease and periodontopathic bacteria, resulting tion of 1975, as revised in 2000, and all
progression. Accordingly, several con- in a poor membrane resistance to col- participants signed informed consent
ventional treatment approaches includ- lapse, allowing undesirable cell types to forms. The study protocol was approved
ing plastic curettes, sonic/ultrasonic enter the secluded wound area (Tatakis by the ethical committee of the Heinrich
scalers and air-powder flow have been et al. 1999, Sela et al. 2003, Rothamel et Heine University.
recommended for the debridement of al. 2005). However, the collapse may be The patient population consisted of
contaminated implant surfaces (Fox et prevented by means of implantation of eight men and 14 women (mean age
al. 1990, Rühling et al. 1994, Matarasso bone grafts or bone graft substitutes into 54.4 12.5 years), exhibiting a total of
et al. 1996, Augthun et al. 1998). How- the defect to support the membrane, n 5 22 implants. Patients reporting to
ever, as mechanical methods alone have preserving its original position. Preli- smoke only occasionally were not con-
been proven to be insufficient in the minary experimental studies have shown sidered as smokers (Tonetti et al. 1995).
elimination of plaque biofilms and bac- that nanosized ceramics may represent According to the given definition, there
teria on roughened implant surfaces a promising class of bone graft substi- were no smokers included in the present
(Kreisler et al. 2005, Schwarz et al. tutes due to their improved osseointe- study. All patients had been previously
2006a), the adjunctive use of chemical grative properties (Webster et al. 2000, treated by a single course of non-surgi-
agents (i.e. irrigation with local disin- Chris Arts et al. 2006). Accordingly, cal instrumentation of respective tita-
fectants, local or systemic antibiotic a ready-to-use paste in a syringe, avail- nium implants using plastic curettes
therapy) (Mombelli & Lang 1992, able under the name Ostimt (Heraeus (Straumann, Waldenburg, Switzerland),
Ericsson et al. 1996, Schenk et al. Kulzer, Hanau, Germany) (NHA), con- followed by pocket irrigation with a
1997) and different laser systems (Deppe taining about 65% water and nanoscopic 0.2% chlorhexidine digluconate solution
et al. 2001, Schwarz et al. 2005) has apatite particles (35%) in aqueous dis- (Corsodyls, GlaxoSmithKline Consu-
been recommended in order to enhance persion, has recently been recommended mer Healthcare, Bühl, Germany) (CHX)
healing following treatment. In addition for augmentation procedures in osseous and subgingival application of CHX gel
to these conventional tools, regenerative defects (Moghadam et al. 2004, Thor- 0.2% (Corsodyls Gel, GlaxoSmithKline
treatment procedures have been advo- warth et al. 2005). In particular, experi- Consumer Healthcare, Bühl, Germany).
cated for the restoration of the implant- mental animal studies have pointed to an The criteria needed for inclusion were as
supporting tissues (Ericsson et al. 1996, indisturbed ossoeous-integration and com- follows: (1) the presence of at least one
Persson et al. 1996, Hürzeler et al. 1997, plete resorption of the material within screw-type implant exhibiting an intrab-
Nociti et al. 2001b, Schou et al. 2003a–c, 12 weeks (Thorwarth et al. 2005, Chris ony defect with a probing depth (PD) of
2004). Most of these studies used the Arts et al. 2006). Owing to its specific 46 mm and an intrabony component of
concept of guided bone regeneration physicochemical properties, NHA is 43 mm as detected on radiographs, (2)
(GBR), which involves the placement intended to be used without the addi- no implant mobility, (3) single tooth and
of a barrier membrane to protect the tional application of a barrier mem- bridgework restaurations without over-
blood clot and create a secluded space brane. So far, however, there are no hangings or margins, (4) no evidence of
around the bone defect, enabling bone data from controlled clinical studies occlusal overload, (5) the presence of
regeneration without competition from evaluating the healing of peri-implanti- keratinized peri-implant mucosa, (6) no
other tissues (Dahlin et al. 1988). In tis lesions following treatment with signs of acute periodontitis, (7) a good
recent years, a variety of different mem- NHA. Therefore, the aim of this case level of oral hygiene [plaque index
brane materials have been successfully series was to evaluate and compare the (PI) o1 (Löe 1967)] and (8) no systemic
used for GBR procedures, ranging from healing of moderate intrabony peri- diseases that could influence the out-
r 2006 The Authors. Journal compilation r 2006 Blackwell Munksgaard
Regenerative therapy of peri-implantitis 493
Table 1. Distribution and mean age (years SD) of different implant systems in both groups 1. supra-alveolar component – s(a) of
the defect, measured as maximum
Group BRA CAM ITI KSI MTX TSV ZL Age
linear mesial or distal distance from
Test (n 5 11) 1 1 2 1 4 1 1 3.6 1.9 the borderline between the bony and
Control (n 5 11) 1 1 2 1 3 2 1 4.0 0.9 transmucosal part (BTB) of the
implant to the alveolar bone crest,
BRA Brånemark Systems, Nobel Biocare, Göteborg, Sweden.
2. circumferential component – s(c) of
CAM Camlog Screw Lines, Camlog, Wimsheim, Germany.
ITI ITI (SLA, TPS)s, Straumann, Waldenburg, Switzerland.
the defect, measured as the linear
KSI KSI Bauer Schraubes, KSI Bauer Schraube GmbH, Bad Nauheim, Germany. distance from the vestibular – s(c-v),
MTX Spline Twist (MTX)s, Zimmer Dental, Freiburg, Germany. mesial – s(c-m), distal – s(c-d) and
TSV Tapered Screw Vents, Zimmer Dental, Freiburg, Germany. oral – s(c-o) bone wall of the defect
ZL ZL-Duraplant (Ticer)s, ZL Microdent, Breckerfeld, Germany. to the implant surface and
3. intrabony component of the defect,
measured as the linear distance from
the alveolar bone crest to the bottom
Table 2. Position of implants in both groups of the defect (v, m, d, o).
Group Upper jaw Lower jaw
Intra-examiner reproducibility
s(a)
anterior posterior anterior posterior
Five patients, each showing two implants
Test 2 4 0 5 with PDsX4 mm on at least one aspect,
(n 5 11) were used to calibrate the examiner. The
Control 1 5 0 5
examiner evaluated the patients on two
(n 5 11)
separate occasions, 48 h apart. Calibra-
tion was accepted if measurements at
baseline and at 48 h were within a milli-
metre at 490% of the time.
a
come of the therapy (i.e. diabetes, osteo-
porosis). s(c − v)
Randomization procedure
Hollow cylinder implants were i(v)
excluded from the study. The distribu- The defects were randomly assigned
tion, mean age and position of different before surgery to the following test
implant systems in both groups are pre- s(c − m) s(c − d)
and control groups according to a com-
sented in Tables 1 and 2. puter-generated protocol (RandLists,
i(m)
i(d)
Results
Surgical defect examination revealed
that all implants in the test and control
groups exhibited a semi-/or circumfer-
ential bone loss without dehiscence or
fenestration of the adjacent vestibular
and oral alveolar bone. However, in all
cases, semi-/or circumferential bone
loss was also associated with a horizon-
tal loss of the supporting alveolar bone.
The configuration of the defects is sum-
marized in Table 3.
Fig. 2. (a) Semi-circumferential intrabony defect. (b) Situation following application of The post-operative healing was con-
nanocrystalline hydroxyapatite. (c) Situation following application of bovine-derived xeno- sidered as generally uneventful. Minor
graft in the circumferential bone defect. BG was trimmed and adapted over the oral and (d)
complications were related to usual
the vestibular aspect of the defect.
post-operative swelling and occurred
within the first days after surgery in
both groups. Neither allergic reactions
Table 3. Baseline defect characteristics in mm (mean SD) nor suppuration or abscesses were
observed in any of the patients. How-
Treatment s(a) s(c) i semi-circular circular
ever, NHA seemed to compromise initi-
Test (n 5 11) 1.8 0.9 2.5 0.5 4.4 0.5 2 9 al adhesion of the mucoperiosteal flaps
Control (n 5 11) 1.5 0.5 2.4 0.7 4.3 0.6 3 8 in all patients. This was particularly
observed within the first 10 days after
surgery. In contrast, the mucoperiosteal
flap seemed to be well attached over
Straumann AG, Basel, Switzerland). Following grafting, a bioresorbable col- BDX1BG.
Following cleaning, the exposed implant lagen membrane of porcine origin The mean PI and BOP for each of the
and bony surfaces were rinsed with (BioGides, Geistlich) (BG) was trim- groups at baseline and after 6 months
sterile physiologic saline. med and adapted over the entire defect are summarized in Table 4. In both
At the test sites, bleeding into the so as to cover 2–3 mm of the surround- groups, the mean PI values remained
defects was reduced to a minimum and ing alveolar bone and to ensure stability low throughout the study period. In both
they were subsequently filled with of the graft material. Neither sutures nor groups, the mean BOP scores improved
NHA, starting from the bottom of the pins were used for membrane fixation or compared with baseline. The mean PD,
defect. Care was taken to obtain a direct stabilization (Fig. 2). GR and CAL in both groups at baseline
contact between NHA and the adjacent Finally, the mucoperiosteal flaps and after 6 months are summarized in
alveolar bone, without interposition of a were repositioned coronally and fixed Table 4. In particular, at 6 months after
blood clot. Defects were slightly over- with vertical or horizontal mattress therapy, the test group showed a reduc-
filled, as NHA has a creamy consistence sutures in such a way as to ensure a tion in the mean PD from 7.0 0.6 to
and tends to leak from the defect. non-submerged healing procedure. 4.9 0.6 mm and a change in the mean
At the control sites, the defects were CAL from 7.5 0.8 to 5.7 1.0 mm.
filled with a bovine-derived xenograft Post-operative care
In the control group, the mean PD was
(BioOsss spongiosa granules, particle reduced from 7.1 0.8 to 4.5 0.7 mm
size 0.25–1 mm, Geistlich, Wolhusen, Post-operative care consisted of rinsing and the mean CAL changed from
Switzerland) (BDX). The graft material with a 0.2% chlorhexidine digluconate 7.5 1.0 to 5.2 0.8 mm.
was moistened in sterile saline for solution (Corsodyls, GlaxoSmithKline The frequency distribution of CAL
5 min. before placement into the defect. Consumer Healthcare, Bühl, Germany) gains in both treatment groups is shown
r 2006 The Authors. Journal compilation r 2006 Blackwell Munksgaard
Regenerative therapy of peri-implantitis 495
Table 4. Clinical parameters (mean SD) at baseline and after 6 months (n 5 11 patients in NHA, which in turn might result in a
each group) poor resistance to collapse of the muco-
Baseline 6 Months Difference periosteal flap into the intrabony defect,
allowing undesirable cell types to enter
Plaque index the secluded wound area. This collapse
Test 0.7 0.5 0.6 0.5 0.1 0.5 may be prevented by means of implan-
Control 0.8 0.4 0.7 0.5 0.1 0.3 tation of additional bone grafts or bone
graft substitutes into the defect to sup-
Bleeding on probing (%)
port NHA, preserving its original posi-
Test 82 30 52
Control 78 28 50 tion. Further experimental studies are
Probing depth (mm) needed in order to clarify these issues.
Test 7.0 0.6 4.9 0.6 2.1 0.5 When interpreting the present results, it
Control 7.1 0.8 4.5 0.7 2.6 0.4 has to be noted that the mean CAL gain
Gingival recession (mm) as observed 6 months post-operatively
Test 0.5 0.5 0.8 0.5 0.3 0.2 was 1.8 0.6 mm in the NHA group
Control 0.4 0.3 0.7 0.6 0.3 0.2 and 2.3 0.6 mm in the BDX1BG
Clinical attachment level (mm)
group. In this context, it needs to be
Test 7.5 0.8 5.7 1.0 1.8 0.6
Control 7.5 1.0 5.2 0.8 2.3 0.6 pointed out that these are the first data
evaluating the use of both bone grafting
materials for non-submerged healing of
intrabony peri-implantitis defects in
Table 5. Frequency distribution of CAL gain gains of CAL at 6 months after surgery. humans. Therefore, a comparison with
in the test and control groups (n 5 11 patients Even though the clinical results may other studies is not possible. However,
in each group) also be supported by a decreased radio- the clinical improvements noted in both
CAL gain Test Control translucency within the intrabony com- groups seemed to be within the range of
(mm) ponent of respective peri-implant bone other regenerative treatment procedures
No % No % defects in both groups, it must be reported in previous studies (Hämmerle
pointed out that the radiographs were et al. 1995, Mattout et al. 1995, Behneke
1 1 9.1
not standardized. Furthermore, it should et al. 2000, Haas et al. 2000, Khoury &
2 9 81.8 4 36.4
3 2 18.2 6 54.5 be emphasized that the study does not Buchmann 2001). In particular, Haas et
have the statistical power to rule out the al. (2000) used autogenous bone (AB)
CAL, clinical attachment loss. possibility of a difference between the graft particles covered with an e-PTFE
two groups. Further studies, with a membrane around 24 IMZ implants
much higher number of patients and after implant surface decontamination
in Table 5. In particular, in the test defects, would be needed to detect an using photosensitization by Toluidine
group, 18.2% of the sites (n 5 2 defects) eventual difference between the treat- blue and soft laser irradiation. After
gained at least 3 mm of CAL. In con- ments (Gunsolley et al. 1998). From a 9.5 months of submerged healing, radio-
trast, a CAL gain of 3 mm was measured clinical point of view, however, it must graphic evaluation demonstrated a mean
in six defects (54.5%) in the control be pointed out that NHA seemed to bone gain of 2 mm, merely correspond-
group (Table 5). compromise initial adhesion of the ing to 36% of the previous defect height.
In both groups, radiological observa- mucoperiosteal flaps in all patients. In Similar results were also reported by
tion revealed a decreased translucency contrast, the mucoperiosteal flaps were Khoury & Buchmann (2001). After
within the intrabony component of the well attached over BDX1BG. This 6 months of non-submerged healing,
respective peri-implant bone defects. In observation might be due to the specific the mean PD reduction was 1.5 mm for
particular, after 6 months of healing, physicochemical properties noted for AB grafts alone, 1.3 mm for AB1BG
both NHA and BDX1BG seemed to BG. Indeed, native collagen has been and 1.5 mm for AB1e-PTFE. Bone gain
be organized by a dense and compact reported to promote early wound stabi- varied between 1.9 and 2.8 mm after an
hard tissue-like structure exhibiting a lization by its chemotactic properties to observation period of 3 years. In this
quality similar to that of the adjacent attract fibroblasts (Postlethwaite et al. study, the implant surface was cleaned
parent alveolar bone (Fig. 3). However, 1978). This is also in agreement with the with chlorhexidine, citric acid and
one implant of the test group revealed results of recent experimental studies in hydrogen peroxide. Even though several
no or merely a slight decrease in radi- rats, which have shown that BG exhib- treatment approaches have indeed
olucency at the mesial aspect of the ited the highest tissue integration among demonstrated beneficial clinical and
defect (Fig. 4). all barrier membranes investigated radiological effects, the amount of docu-
(Rothamel et al. 2005, Schwarz et al. mented bone regeneration and re-
2006b). In contrast, it is impossible to osseointegration, as observed histologi-
estimate to what extent the specific cally in animals, varied considerably
Discussion physicochemical properties of NHA (Ericsson et al. 1996, Persson et al.
The results of the present case series might have compromised fibroblast 1996, Hürzeler et al. 1997, Nociti et al.
have indicated that treatment of intrab- attachment and subsequently the adhe- 2001b, Schou et al. 2003a–c, 2004). In
ony peri-implantitis defects with both sion of the mucoperiosteal flap. Another most of these studies, the re-establish-
NHA and BDX1BG resulted in clini- problem encountered during the surgical ment of osseointegration has even been
cally important reductions in PD and procedure was the low consistency of questioned (Schou et al. 2004). In parti-
r 2006 The Authors. Journal compilation r 2006 Blackwell Munksgaard
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Clinical Relevance (BDX1BG) might improve healing surgery. However, NHA seemed to
of intrabony peri-implantitis defects. compromise initial adhesion of the
Scientific rationale for the study: Principal findings: The present mucoperiosteal flaps in all patients.
The clinical application of a nano- results have indicated that both treat- Practical implications: Both treat-
crystalline hydroxyapatite (NHA) or ment procedures resulted in clini- ment procedures might improve
a bovine-derived xenograft in com- cally important reductions in PD healing of intrabony peri-implantitis
bination with a collagen membrane and gains of CAL at 6 months after defects at 6 months after surgery.