outcome of surgical treatment of peri-implantitis: results from a 2-year prospective clinical study...

Outcome of surgical treatment ofperi-implantitis: results from a 2-yearprospective clinical study in humans

Giovanni SerinoAlberto Turri

Authors’ affiliations:Giovanni Serino, Alberto Turri, Specialistic Clinic inPeriodontics, Sodra Alvsborgs Hospital, Boras 50182,SwedenAlberto Turri, Specialistic Clinic in Periodontics,Odontologen, Goteborg, SwedenGiovanni Serino, Research and Developments Unit,Boras, Sweden.

Corresponding author:Giovanni SerinoSpecialistic Clinic in PeriodonticsSodra Alvsborgs HospitalBoras 50182SwedenTel.: þ 46 033 616 2802Fax: þ 46 033 616 1235e-mail: [email protected]

Key words: peri-implantitis, peri-implant bone loss, peri-implant surgery, surgery outcome

Abstract

Aim: The aim of the present study was to evaluate the outcome of a surgical procedure based on

pocket elimination and bone re-contouring for the treatment of peri-implantitis.

Material and methods: The 31 subjects involved in this study presented clinical signs of peri-

implantitis at one or more dental implants (i.e. � 6 mm pockets, bleeding on probing and/or

suppuration and radiographic evidence of � 2 mm bone loss). The patients were treated with a

surgical procedure based on pocket elimination and bone re-contouring and plaque control before

and following the surgery. At the time of surgery, the amount of bone loss at implants was recorded.

Results: Two years following treatment, 15 (48%) subjects had no signs of peri-implant disease; 24

patients (77%) had no implants with a probing pocket depth of � 6 mm associated with bleeding

and/or suppuration following probing. A total of 36 implants (42%) out of the 86 with initial diagnosis

of peri-implantitis presented peri-implant disease despite treatment. The proportion of implants that

became healthy following treatment was higher for those with minor initial bone loss (2–4 mm bone

loss as assessed during surgery) compared with the implants with a bone loss of � 5 mm (74% vs.

40%). Among the 18 implants with bone loss of � 7 mm, seven were extracted. Between the 6-month

and the 2-year examination, healthy implants following treatment tended to remain stable, while

deepening of pockets was observed for those implants with residual pockets.

Conclusion: The results of this study indicated that a surgical procedure based on pocket elimination

and bone re-contouring and plaque control before and following surgery was an effective therapy for

treatment of peri-implantitis for the majority of subjects and implants. However, complete disease

resolution at the site level seems to depend on the initial bone loss at implants. Implants with no signs

of peri-implantitis following treatment tended to remain healthy during the 2-year period, while a

tendency for disease progression was observed for the implants that still showed signs of peri-implant

disease following treatment.

Bleeding and/or suppuration following probing

has been proposed as a valuable clinical sign for

the diagnosis of both peri-implant mucositis and

peri-implantitis while the concomitant detection

of marginal peri-implant bone loss in radiographs

will distinguish a peri-implantitis from a muco-

sitis (Zitzmann & Berglundh 2008).

Bacteria play a major role in the aetiology of

peri-implant mucositis and peri-implantitis (Pon-

toriero et al. 1994; Augthun & Conrads 1997;

Mombelli & Lang 1998; Leonhardt et al. 1999;

Quirynen et al. 2002, 2006). Animal experi-

ments have shown that plaque accumulation on

the implant surfaces seems to be critical to the

development of peri-implant diseases (Berglundh

et al. 1992; Ericsson et al. 1992; Lang et al. 1994)

and may be responsible for altering the biocom-

patibility of the implant surfaces. Thus, the

treatment of both mucositis and peri-implantitis

in human is based on plaque removal from the

implant surfaces. With this type of treatment two

questions arise:

(1) Is it possible to re-establish healthy condition

for the tissues of an implant affected by peri-

implant disease? Regarding this question,

plaque removal using a non-surgical debride-

ment/decontamination of the implant sur-

faces seems to be effective in the treatment

of peri-implant mucositis, while limited effect

of this procedure has been reported for the

treatment of peri-implantitis (for review see

Renvert et al. 2008a, 2008b); experimental

studies have shown resolution of peri-implan-

titis following the surgical exposure of the

implants and the mechanical debridement/

decontamination of the implant surfaces (for

review see Claffey et al. 2008).

Date:Accepted 5 October 2010

To cite this article:Serino G, Turri A. Outcome of surgical treatment of peri-implantitis: results from a 2-year prospective clinical studyin humans.Clin. Oral Impl. Res. 22, 2011; 1214–1220.doi: 10.1111/j.1600-0501.2010.02098.x

1214 c� 2011 John Wiley & Sons A/S

mailto:[email protected]

(2) Might osseointegration eventually occur on

previously contaminated implant surfaces?

Recent experimental animal studies have

shown that it is possible to obtain re-osseoin-

tegration on a decontaminated implant sur-

face, if the implants are placed in freshly

prepared alveola bone (Kolonidis et al. 2003;

Alhag et al. 2008). However, non-predictable

re-osseointegration from the surrounding

bone on a decontaminated implant surface

has been observed if the implants are left in

their original position. Histological results

demonstrated a connective tissue capsule se-

parating the implant surface from the adjacent

bone in most cases, except at the most apical

extent of the defect (Grunder et al. 1993;

Ericsson et al. 1996; Persson et al. 1996,

1999, 2001, 2004; Schwartz et al. 2006a).

The effect of access surgery combined with

surface debridement/decontamination of the im-

plants affected by peri-implantitis in human has

been investigated in a few studies involving lim-

ited numbers of patients (for review see Claffey et

al. 2008; Esposito et al. 2008). In one study

involving nine patients with a total of 26 implants,

Leonhardt et al. (2003) tested a treatment based on

surgical debridement and the use of hydrogen

peroxide for the decontamination of the implant

surfaces under systemic antibiotic administration.

Based on radiographic evaluation, the authors

reported that 58% of the treated implants did

not show progression of bone loss at the 5-year

follow-up radiographic examination. Romeo et al.

(2005, 2007) tested on 19 patients the efficacy of

resective surgery based on removal of granulation

tissue around the affected implants, polishing of

the implant surfaces using local antibiotics and

correction of the anatomical architecture of the

bone. In addition, modification of the implant

surface topography (implantoplasty) was per-

formed in nine of those patients. A total of 35

implants with peri-implantitis were treated. The

results at the third year examination showed that

the treatment including the implantoplasty

seemed to influence positively the survival of

implants affected by peri-implantitis and reduce

the peri-implant pockets depth, suppuration and

sulcus bleeding. The radiographic examination

showed lower marginal alveolar bone loss around

implants treated with implantoplasty compared

with the control implants. In a recent short-term

clinical study (Maximo et al. 2009), the authors

presented the clinical results of a treatment of peri-

implantitis based on only open flap mechanical

debridement of 20 implants (in a total of 13

patients). Three months following the treatment,

25% of the treated implants presented clinical

signs of peri-implantitis (i.e. PPD � 5 mmþBoP

and/or suppuration at least at one site).

Although the mentioned clinical studies seem

to indicate healthier conditions of the peri-im-

plant mucosa following the treatment of peri-

implantitis, the clinical parameters used to eval-

uate the treatment outcomes vary between stu-

dies. Currently, there is no consensus on which

clinical parameters should distinguish a condi-

tion of health or disease following treatment of

peri-implantitis.

Aim

The aim of the present study was to evaluate the

outcome of the routine surgical procedure pro-

vided in our clinic for the treatment of peri-

implantitis. The surgical procedure was based

on pocket elimination and bone re-contouring.

Material and methods

Patient recruitment

The subjects involved in this study were selected

from consecutive patients referred to the depart-

ment of Periodontology, Sodra Alvsborgs Hospi-

tal, Boras, Sweden, for treatment of peri-

implantitis during 2005–2007. The 2-year fol-

low-up was the end point of the recruitment.

Inclusion criteria

To be included in this study, the patients had

clinical signs of peri-implantitis at one or more

dental implants (i.e. PPD � 6 mm, bleeding on

probing and/or suppuration) and radiographic

evidence of bone loss (� 2 mm at mesial or distal

site of the implants). The implants should have

been in function for more than 1 year. Both

edentulous and partial edentulous patients were

included.

Exclusion criteria

Any medical condition, which contraindicated

dental surgery, precluded the enrolment to the

study. Two subjects were not included, one

because of chemotherapy and the other because

of bisphosphonates.

Patient sample

The inclusion criteria resulted in the selection of

31 subjects of which 19 were female and 12 male.

Eight were smokers who all smoked more than

10 cigarettes/day.

Following the clinical and radiographic exam-

ination, all patients were informed about the

diagnosis and treatment plan. They were also

informed that their data would be used for statis-

tical analyses and gave their informed consent to

the treatment.

The study was performed in accordance with

the principle stated in the Declaration of Hel-

sinki.

Clinical examination

The following clinical variables were recorded:

Plaque Index (PI) as percentage of sites with

the presence of plaque as determined at four

surfaces (mesial, distal, buccal, lingual) per

tooth/implant after staining with disclosing solu-

tion.

Access/Ability for oral hygiene at implant site:

At the time of the clinical examination, an

assessment of the restoration was made to deter-

mine if access for OH had been provided (yes/no).

When there was access, the quality of the pa-

tient’s current home care was assessed by run-

ning the probe across the marginal surface of the

implant and recording either the absence or the

presence of plaque based on the modified PI

(Mombelli et al. 1987) in the following way: no

plaque¼score 0; plaque present¼score 1, 2, 3.

Positive or negative value (yes/no) was recorded

for each implant.

Modified Sulcus Bleeding Index (mBI): pre-

sence or absence of bleeding was recorded by

running the probe along the soft tissue margin

of the implants. Bleeding was recorded if any site

of the implants was positive to the test (score 1,

2, 3 Mombelli et al. 1987).

Bleeding/Suppuration on Probing (BoP/Sup)

presence or absence of bleeding/suppuration up

to 15 seconds after probing was assessed.

Probing Pocket Depth (PPD) was measured in

millimeters with a manual Hu-Friedy PCP15

periodontal probe (Hu-Friedy Inc., Leimen, Ger-

many) to the closest millimetre at the mesial,

buccal, distal and lingual surfaces of all implants.

Bone Loss at implants: during the surgery,

following the elevation of the flaps and the

removal of the granulation tissue, the bone loss

was measured around each implant to the nearest

mm with the periodontal probe. Depending on

the implant system, the bone loss was measured

either from fixture–abutment junction (Brane-

marks [Nobel Biocare, Gothenburg, Sweden],

Astra Techs [Molndal, Sweden]) or the shoulder

of the implants (ITIs [Straumann Institute AG,

Waldenburg, Switzerland]) to the level where the

bone was seen to be in intimate contact with the

implant. The highest value at any site around

each affected implant was recorded.

Radiographic examination

Radiographic bone loss was evaluated from peri-

apical radiographs and measured from the fixture–

abutment junction/shoulder of the implants,

respectively, to the bone level mesial and distal

to the implants. For the purpose of this study, the

Serino & Turri �Outcome of surgical treatment of peri-implantitis

c� 2011 John Wiley & Sons A/S 1215 | Clin. Oral Impl. Res. 22, 2011 / 1214–1220

radiographic threshold value to discriminate bone

loss at implants was � 2 mm.

Implant grouping

According to the clinical and radiographic data at

the baseline examination, the implants were

divided into one of the following groups:

Healthy¼PPDo4 mm without BoP and/or

Sup and no radiographic bone loss;

Mucositis¼PPD � 4 mm at least at one site,

associated with Bop and/or Sup without radio-

graphic bone loss;

Peri-implantitis¼PPD � 6 mm at least at

one site, associated with BoP and/or Sup and

concomitant radiographic images of bone loss

of � 2 mm.

Treatment

Pre-surgical phase

Any prosthesis, which had been assessed as

having poor access for OH at baseline, was

removed and the form was corrected. This was

facilitated by them all being screw-retained. Each

patient was then given OH and supra/sub-gingi-

val scaling by dental hygienists to treat gingivitis

and mucositis. Any patients with remaining

natural dentition exhibiting periodontal disease

were given conventional periodontal treatment.

However, the severity of periodontitis in these

subjects was limited (for details see Serino &

Strom 2009).

Once all these stages were completed (1–3

months according to individual patient needs)

and the standard of OH was considered appro-

priate (PlIo20% around natural dentition and

modified PI score of 0 around the implants), the

surgical treatment was planned.

Surgical phase

One day before the surgery, all patients received

systemic antibiotic prophylactic therapy (Dalacins,

[Pfizer Sollentuna, Sweden], tabl. 300mg � 3/day

for 1 week). To facilitate good surgical access

around the implants, the prostheses were removed

(for all but two of the subjects). Only sites showing

peri-implantitis were surgically treated.

The incision was made using a Bard–Parker

blade (No. 15) under local anaesthesia (2% xylo-

caine/adrenaline). The positions of the incisions

were dependent on the pocket depth as well as the

width and thickness of the peri-implant mucosa.

Flaps were designed to optimize the removal of the

pocket epithelium and the inflammatory granulo-

matous capsule from the internal aspects of the

mucoperiosteal flap and from the peri-implant

defect. Vertical releasing incisions extending into

the alveolar mucosa were placed at the mesial and

distal boundaries of the horizontal incisions. Mu-

coperiosteal full-thickness flaps were raised buc-

cally and palatally/lingually. The granulation

tissue was removed using hand curettes. Correc-

tion of the anatomical architecture of the bone,

aiming to eliminate angular bony defect, was

performed using a rotating round bur under saline

irrigation. The implant surfaces were scaled and

polished using an ultrasonic instrument (EMS

Piezon Master 400þPerio Slim Tips, EMSs

,

Nyon, Switzerland) and rotating rubber cup under

chlorhexidine irrigation. In our hands, these in-

struments gave the possibility to remove plaque

and calculus more efficiently compared with ti-

tatnium or carbon-fibre curettes. The flaps were

trimmed and apically repositioned, and the pros-

theses were re-fitted.

Following surgery, the patients rinsed twice a

day for 1 min with chlorhexidine 0.12% for a

period of 2 weeks. The sutures were removed 10

days after the surgery. One week following suture

removal, the patients received new oral hygiene

instructions appropriate to the new contour of the

peri-implant mucosa. The patients were recalled

at 3, 6, 12, 18 and 24 month for re-evaluation and

maintenance care. At each recall, the prostheses

were removed in order to have proper access for

implant examination. The maintenance care was

based on motivation and oral hygiene instruction

according to the patient’s need, supragingival

plaque control and subgingival scaling at im-

plants presenting residual pockets. The subgingi-

val scaling was performed using an ultrasound

instrument (EMS Piezon Master 400þPerio

Slim/Perio Implant Tips, EMSs

, Nyon, Switzer-

land). At the 3-month recall, any implants show-

ing deep pockets, pus formation and causing

discomfort to the patient were extracted.

Drop Out

Two of the 31 patients could not be examined at

the 2-year control, (one moved, one ill). The 1-

year data of these two patients were included in

the analyses.

Data analyses

Mean values (� SD) for subjects were used for

descriptive statistic. The non-paired t-test was

applied for the difference between smoker and

non-smokers. Fisher’s exact probability test was

applied at the subject level to assess difference in

probability of healing related to the two catego-

rical variables (implants with bone loss 2–4 vs.

� 5 mm). A P-value of o0.05 was considered to

be statistically significant.

Results

At the baseline examination, 31 patients (19

female) having one or more implants with signs

of peri-implantitis were examined; five (16%) of

those were edentulous and eight were smokers

(who all smoked 410 cigarette/day) (Table 1).

There was no statistical difference between the

mean number of implants with peri-implantitis

between smokers and non-smokers (2.8� 1.5SD

vs. 3.0 � 1.5SD, P¼0.7). The majority of the

subjects (22) had up to three implants affected by

peri-implantitis, while nine had four, five or six

(Fig. 1). A total number of 168 implants were

examined, 54 (32%) had a diagnosis of mucositis

and 86 (52%) of per-implantitis; 73 (44%) im-

plants were in function for more than 10 years, 51

(30%) between 5 and 10 years, and 44 (26%) o5

years. The majority of the implants (87%) were

machined surfaced implants. Marginal bleeding

was present at 89 (53%) implants and 105 (62%)

were assessed as having no access/ability for oral

hygiene (Table 1). Figure 2 shows the location as

well as the number of implants with different

degrees of bone loss; 58 implants with diagnosis

of peri-implantitis were located in the maxilla and

28 in the mandible. The highest number of

implants with advanced bone loss ( � 7 mm)

was found in the incisor area of the maxilla. No

implants were present in the molar area of the

maxilla and only four implants were located in the

molar areas of the mandible. Six subjects had all

the implants with peri-implantitis presenting a

bone loss of 2–4 mm, 11 subjects had all the

implants with a bone loss of 5–6 mm, two subjects

with � 7 mm bone loss, while 12 subjects had

all their implants presenting the three different

degrees of ‘‘bone loss’’.

At the follow-up examinations, the number of

implants presenting marginal bleeding and no-

Table 1. Baseline data of the 31 patients and the168 implants

Number of patients 31Age (years, mean � SD) 63.2 (8.7)Female 19Number (%) edentulous 5(17%)Number (%) partially edentulous 26(83%)Number (%) smokers 8 (26%)Function time and number of implantso 5 years 44 (26%)5–10 years 51 (30%)410 years 73 (44%)Tot. 168Type and number of implantsBranemark

s

122ITI

s

40Astra

s

6Surfaces and number of implantsMachined surfaced implants 146Plasma sprayed implants 22Number (%) of implants with no accessTo oral hygiene 105 (62%)Number (%) of implants with 89 (53%)Marginal bleeding (MBI)Number (%) of healthy implants 28 (16%)Number (%) of mucositis 54 (32%)Number (%) of peri-implantitis 86 (52%)Total 168


1216 | Clin. Oral Impl. Res. 22, 2011 / 1214–1220 c� 2011 John Wiley & Sons A/S

access/ability for oral hygiene decreased notably

as a consequence of the improved access and

patient’s ability to brush around the neck of the

implants (Fig. 3). Figure 1 shows that 2 years

following treatment, 15 (48%) subjects had no

signs of peri-implant disease, i.e. no implants

presenting pocket associated with bleeding/sup-

puration; 24 patients (77%) had no implants with

PPD � 6 mmþBop/SuP. Four patients had one

implant with PPD � 6 mmþBoP/Sup, eight

patients had one implant with peri-implant dis-

ease. Only one patient had three implants with

� 6 mm PPDþBop/Sup and two patients had

six implants with PPD of 4–5 mm PPDþBop/

Sup. No statistical difference was found in the

mean number of implants with peri-implantitis

at the 2-year examination between smokers and

non-smokers (1.9 � 1.8 SD vs. 1.5 � 0.8 SD,

P¼0.7). Figure 4 shows that the number of

healthy implants following treatment remained

stable up to 2 years while the number of implants

presenting a PPD � 6 mm associated with

bleeding/suppuration increased between the 6-

month and 2-year examination.

Following the 3-month examination seven

implants were extracted because of persisting

deep pockets, pus formation and patients discom-

fort; all these implants had a bone loss of

47 mm. At the 2-year review, 14 implants

presented PPD � 6 mm associated with bleed-

ing/suppuration and 15 implants had PPD 4–

5 mmþBop/Sup. Including the seven implants

that were extracted, a total of 36 implants (42%)

out of the 86 with an initial diagnosis of peri-

implantitis exhibited peri-implant disease despite

treatment. Table 2 shows the outcome of treat-

ment related to the initial severity of bone loss as

measured following flap elevation during surgery;

at the sixth month examination, 34 out of the 46

implants (74%) with an initial bone loss of 2–

4 mm were healthy, compared with 50% of the

implants with initial bone loss of 5–6 mm. The

healing following treatment was evaluated for

each subject separately for the implants with 2–

4 mm bone loss and for those with 5–6 mm bone

loss. The results revealed that 10 out of 14

subjects presenting implant with initial bone

loss of 2–4 mm, had all their implant healthy

following treatment (71% predict positive value

for healing); eight out of 17 subjects presenting

implants with initial bone loss of 5–6 mm, had all

those implants healthy following treatment (32%

predict positive value for healing). The difference

in probability was statistically significant (Two-

tail Fisher Exact Probability Test, P¼0.02). Of

the 18 implants with bone loss of � 7 mm,

seven were extracted. Between the 6-month and

the 2-year examinations, the number of implants

with PPD of � 6 mm associated with BoP/SuP

increased in all three ‘‘bone loss’’ groups while

the number of healthy implants remained stable.

Discussion

The results of the present study indicate that a

surgical approach based on pocket elimination

and bone re-contouring associated with a proper

standard of self-performed plaque control, was an

effective means to treat peri-implantitis for the

0

5

10

15

20

25

30

0 1 2 3 4 5 6 . 0 1 2 3 4 5 6

Peri-impl

≥6mm PPD

4- 5mm and/or ≥6mm PPD

Number of implants

Baseline 2 years

Nu

mb

er o

f su

bje

cts

Fig. 1. Data showing the number of subjects with respect to the number of implants affected by peri-implantitis (Baseline) and

post-treatment peri-implantitis condition at the 2-year examination. At the 2-year examination, 24 subjects did not present

implants with � 6 mm PPD associated with BoP/SuP and 15 subjects did not have implants affected by peri-implant

disease.

≥7 mm5 - 6 mm2 - 4 mm

Incisor Canine Premolar Molar

Maxilla

Mandible

0

10

20

10

30

Nu

mb

er o

f im

pla

nts

Fig. 2. Baseline data: number and location of implants with different degrees of bone loss. The highest number of implants

with bone loss of � 7 mm was found in the incisor area of the maxilla.

0

20

40

60

80

100

120

Baseline 3 months 6 months 2 years

No Oral Hygiene

MBI

Nu

mb

er o

f Im

pla

nts

Fig. 3. The number of implants with no accessibility/ability for oral hygiene and marginal bleeding (MBI) was reduced

following the baseline examination.



majority of subjects and implants. Resolution of

the disease was a frequent finding for those

implants with minor initial bone loss (2–4 mm)

while persistence of peri-implant disease tended

to be more frequent for those implants with an

initial advanced bone loss (� 5 mm).

The overall improvements of the clinical para-

meters following the treatment of peri-implanti-

tis observed in the present investigation are in

agreement with the results of those studies based

on surgical treatment of peri-implantitis (Leon-

hardt et al. 2003; Romeo et al. 2005, 2007;

Maximo et al. 2009). However, the parameters

used to evaluate the treatment outcome vary

among these studies. Leonhardt et al. (2003)

and Romeo et al. (2007) used radiographic bone

level change at implants to assess stability or

progression of disease following treatment, while

changes in clinical parameters compared with the

baseline data have been used in the studies by

Romeo et al. 2005 and Maximo et al. 2009.

Although radiographic examination is a valid

method for the assessment of bone level change

over time (Albrektsson & Sennerby 1991), clin-

ical changes would require some years before

they could be detected on radiographs. Further-

more, the radiographic assessment of marginal

bone loss is limited to the mesial and distal aspect

of the implants. It should be kept in mind that

when using changes in certain clinical or micro-

biological parameters for the treatment evalua-

tion, an improvement in the parameters could be

anticipated following a peri-implant treatment

based on supra and sub-gingival debridement/

decontamination, although complete and suc-

cessful resolution of the peri-implant disease

may not have been obtained (Mombelli et al.

2001; Karring et al. 2005; Salvi et al. 2007;

Renvert et al. 2007, 2009). In the consensus

report of the sixth European workshop of perio-

dontology, Lindhe & Meyle (2008) concluded

that ‘‘effectiveness rather than efficacy should

be reported in the evaluation of peri-implant

therapy’’. However, currently there is no con-

sensus on which clinical parameters should the

effectiveness of peri-implant treatment be based

(Esposito et al. 2008). In our study, we chose

elimination of clinical signs of peri-implantitis as

goal of therapy and as well as treatment evalua-

tion. Consequently, we considered healthy fol-

lowing treatment for those implants without

pockets and no BoP/Sup (Fig. 5a), while persis-

tence of peri-implant disease was considered for

those implants exhibiting residual PPD of 4–

5 mm (Fig. 5b) and � 6 mm (Fig. 5c) associated

with BoP/sup. The rationale is that following

treatment, a healthy implant should be without

the clinical signs associated with the initial

diagnosis of peri-implantitis and the presence of

pocket depth with bleeding/suppuration is re-

garded as peri-implantitis (Zitzmann & Ber-

glundh 2008). The differentiation between

healthy, mucositis and peri-implantitis based on

bone loss/no bone loss around implants (Zitz-

mann & Berglundh 2008), it may not be applic-

able following the treatment of peri-implantitis,

because both the healthy and disease conditions

are now associated with bone loss around im-

plants.

Following surgery, although a residual pocket

of 4–5 mm might be regarded as shallow, it must

be kept in mind that the peri-implant tissues

have been apically repositioned and may lie at or

below the head of the implant, on a rough and

threaded surface, as opposed to at the abutment

level in the pre-treatment situation. In our study,

during the 2-year follow-up, some of the im-

plants with PPD 4–5 mm showed deepening of

the pockets despite maintenance consisting of

both supra and sub-mucosal mechanical debride-

ment. Salvi et al. (2007) and Renvert et al.

(2008a, 2008b) showed an improved and sus-

tained (1-year follow-up) clinical condition in

the treatment of ‘‘incipient peri-implantitis’’

using local antibiotics in adjunct to the mechan-

ical debridement. Whether this treatment mod-

ality can be applied in a post-surgical residual

pocket needs further investigation.

In the present study, if the goal of therapy was

the elimination of the pockets � 6 mm asso-

ciated with bleeding/suppuration around im-

plants, 77% of the subjects and 75% of the

implants were successfully treated. If the thresh-

old had been lowered to no pockets � 4 mm,

the treatment would be only effective in 48% of

the subjects and 58% of the implants. Table 2

shows that the success rate (healthy implants)

was much higher if the implants had an initial

minor bone loss. Maximo et al. (2009) reported

resolution of disease in 75% of the implants with

peri-implantitis using no PPD � 5 mm with

bleeding and/or suppuration as threshold value.

However, this result was obtained at the 3-

month evaluation following treatment of 13

patients and the severity of initial bone loss

around the implants was not reported. In our

study, efforts were carried out to ensure the

establishment of adequate plaque control before

and after the surgical procedure. The periodontal

treatment in the partially edentulous subjects, if

necessary, was also completed before the peri-

implant surgery. Furthermore, the prostheses on

the implants were modified to allow access for

proper oral hygiene, if needed. The improved

plaque control around the implants is reflected

by the reduced number of implants showing

marginal bleeding (from n¼89 to 14). These

results were obtained following treatment and

were maintained over the 2-year follow-up. The

importance of plaque control on the onset of

mucositis has been shown in a clinical experi-

0

20

40

60

80

100

120

2 years

Nu

mb

er o

f Im

pla

nts

Baseline 3 months 6 months

Fig. 4. Number of implants with peri-implantitis at baseline and number of implants with or without probing pocket depth

and BoP/Sup following treatment is noticeable. An increased number of healthy implants at 6-month following treatment is

evident and this number remained stable up to the 2-year examination. The number of implants with � 6 mm PPD was

higher at 2-year compared with the 6-month examination. Seven implants were extracted (Extr.) following the third-month

examination.

Table 2. The outcome of treatment related to thebone loss at implant affected by peri-implantitis

Bone loss

2–4 mm 5–6 mm � 7 mm

Treatment outcome3 monthsHealthy 38 17 64–5 mm (Bop/Sup) 8 3 4� 6 mm (Bop/Sup) 0 2 1

Extraction 76 monthsHealthy 34 11 44–5 mm (Bop/Sup) 12 8 4� 6 mm (Bop/Sup) 0 3 3

Extraction2 yearsHealthy 34 12 44–5 mm (Bop/Sup) 7 4 4� 6 mm (Bop/Sup) 5 6 3

Extraction

At the 6 month examination, 34 out of 46 (76%) im-

plants with initial bone loss of 2–4 mm were healthy

compared with 11 out of 22 (50%) with initial bone

loss of 5–6mm. Among the 18 implants with bone loss

of �7 mm, 7 (39%) were extracted at the 3 months

examination.



mental study by Pontoriero et al. 1994. Peri-

implantitis and peri-implant radiographic bone

loss have been associated with inadequate plaque

control around implants (Lindquist et al. 1997;

Serino & Strom 2009). It is interesting to note

that 74% of the patients with peri-implantitis

were non-smokers and no difference was noted in

the number of healthy implants following treat-

ment between smokers and non-smokers. Persis-

tence of disease was a frequent finding for those

implants with an initial advanced bone loss (bone

loss � 7 mm). In most of these cases, the ad-

vanced bone loss was associated with the pre-

sence of deep angular bony defect and the

presence of bony dehiscence at the buccal aspect

similar to the ‘‘Class Id defects’’ described by

Schwartz et al 2007. The presence of buccal bone

dehiscence associated with ligature-induced peri-

implantitis has been reported for those implants

placed close to the buccal bone (Parlar et al.

2009). Furthermore, in a retrospective study,

Alsaadi et al. (2008) analysed 1514 implants in

412 patients to evaluate the impact of local and

systemic factors on the incidence of late oral

implant loss. They found a trend of more loss at

wide-diameter implants that were mostly in-

stalled in site with poor bone quality and quan-

tity. The treatment of implants with advanced

bone loss and deep V shaped defects was in our

study difficult because pocket elimination and

bone re-contouring could not be completed and

the access for mechanical debridement/deconta-

mination was limited. For this type of defect, a

regenerative/defect fill procedure and the use of

antibacterial aids could be beneficial. However,

studies on the efficacy of such treatments in the

cases of peri-implantitis associated with an ad-

vanced bone loss are still at best limited (Claffey

et al. 2008; Renvert et al. 2008a, 2008b).

The number of implants with peri-implant

disease was slightly higher at the sixth-month

compared with the third-month examination.

One possible explanation could be that the sys-

temic antibiotic given before the surgical proce-

dure delayed the proliferation of the sub-mucosal

bacteria left following treatment, but this anti-

microbial effect during the first 3-month period

was not longer sustained at the sixth-month

examination. The sites, which were healthy at

6 months, tended to remain stable over the 2-year

period. From these findings, it could be suggested

that an evaluation at 3 months may be too early

to predictably gauge the success of treatment, but

the corresponding figures at 6 months should be

more accurate.

Conclusion

The results of this study indicated that a surgical

procedure based on pocket elimination and bone

re-contouring before and following surgery was

an effective therapy for treatment of peri-implan-

titis for the majority of subjects and implants.

However, complete disease resolution at site

level seems to depend on the initial bone loss

around the implants. Implants that became

healthy following treatment remained healthy

during the 2-year period, while a tendency for

disease progression was observed for the implants

that still showed signs of peri-implant disease

following treatment.

Acknowledgements: The authors are

grateful to Dr. Patrick Holmes, Seven Fields

Dental Health Centre, Swindon, England, for

his help with the revision of the English text of

the manuscript. Conflict of interest and

source of funding statement: The authors

declare no conflict of interests. No external

funding, apart from the support of the authors’

institution.

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used in reporting randomized trials.

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outcome of surgical treatment of peri-implantitis: results from a 2-year prospective clinical study...

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