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Ten-year results of a three-arm prospective

cohort study on implants in periodontally
compromised patients. Part I
ARTICLE in CLINICAL ORAL IMPLANTS RESEARCH MARCH 2010
Impact Factor: 3.89 DOI: 10.1111/j.1600-0501.2009.01886.x Source: PubMed

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Luca Bonino

Universit degli Studi di Torino

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Retrieved on: 09 October 2015

Mario Roccuzzo
Nicola De Angelis
Luca Bonino
Marco Aglietta

Authors affiliations:
Mario Roccuzzo, Nicola De Angelis, Luca Bonino,
Private Practice, Torino, Italy
Mario Roccuzzo, Department of Maxillofacial
Surgery, University of Torino, Torino, Italy
Marco Aglietta, Department of Periodontology,
University of Bern, Bern, Switzerland

Ten-year results of a three-arm

prospective cohort study on implants in
periodontally compromised patients.
Part 1: implant loss and radiographic
bone loss

Key words: bone level, dental implants, implant failure, peri-implantitis, periodontally
compromised patients, periodontitis, supportive periodontal therapy, survival
Abstract
Objectives: The aim of this study was to compare the long-term outcomes of implants
placed in patients treated for periodontitis periodontally compromised patients (PCP) and

Corresponding author:
Marco Aglietta
Department of Periodontology
University of Bern
Freiburgstrasse 7
3010 Bern
Switzerland
Tel.: 41 0 31 632 25 89
Fax: 41 0 31 632 49 15
e-mail: marco.aglietta@fastwebnet.it

in periodontally healthy patients (PHP) in relation to adhesion to supportive periodontal

therapy (SPT).
Material and methods: One hundred and twelve partially edentulous patients were
consecutively enrolled in private specialist practice and divided into three groups according
to their initial periodontal condition: PHP, moderate PCP and severe PCP. Perio and implant
treatment was carried out as needed. Solid screws (S), hollow screws (HS) and hollow
cylinders (HC) were installed to support fixed prostheses, after successful completion of
initial periodontal therapy (full-mouth plaque score o25% and full-mouth bleeding score
o25%). At the end of treatment, patients were asked to follow an individualized SPT
program. At 10 years, clinical measures and radiographic bone changes were recorded by
two calibrated operators, blinded to the initial patient classification.
Results: Eleven patients were lost to follow-up. During the period of observation, 18
implants were removed because of biological complications. The implant survival rate was
96.6%, 92.8% and 90% for all implants and 98%, 94.2% and 90% for S-implants only,
respectively, for PHP, moderate PCP and severe PCP. The mean bone loss was 0.75
( 0.88) mm in PHP, 1.14 ( 1.11) mm in moderate PCP and 0.98 ( 1.22) mm in severe PCP,
without any statistically significant difference. The percentage of sites, with bone loss
 3 mm, was, respectively, 4.7% for PHP, 11.2% for moderate PCP and 15.1% for severe
PCP, with a statistically significant difference between PHP and severe PCP (Po0.05). Lack of
adhesion to SPT was correlated with a higher incidence of bone loss and implant loss.
Conclusion: Patients with a history of periodontitis presented a lower survival rate and a
statistically significantly higher number of sites with peri-implant bone loss. Furtheremore,
PCP, who did not completely adhere to the SPT, were found to present a higher implant
failure rate. This underlines the value of the SPT in enhancing the long-term outcomes of
implant therapy, particularly in subjects affected by periodontitis, in order to control
reinfection and limit biological complications.

Date:
Accepted 6 November 2009
To cite this article:
Roccuzzo M, De Angelis N, Bonino L, Aglietta M.
Ten-year results of a three arms prospective cohort study
on implants in periodontally compromised patients.
Part 1: implant loss and radiographic bone loss.
Clin. Oral Impl. Res. 21, 2010; 490496.
doi: 10.1111/j.1600-0501.2009.01886.x

490

The use of dental implants for replacement

of missing teeth is also a realistic option in
the rehabilitation of periodontally compromised patients (PCP), even though the

literature regarding the long-term prognosis

is scarce (Renvert & Persson 2009). Dentitions damaged by severe periodontal disease often cause problems not only to the

c 2010 John Wiley & Sons A/S

Roccuzzo et al  Implants in periodontally compromised patients

patient but also to the dentist, in particular

regarding the choice of therapy, i.e. to save
or to extract (Lundgren et al. 2008).
At the 4th European Workshop on Periodontology, Berglundh et al. (2002) suggested that implant therapy has a
favorable long-term prognosis, even though
data on the incidence of biological and
technical complications may be underestimated and should be interpreted with caution. Karoussis et al. (2003) first provided
evidence that, in patients treated for periodontal disease and provided with hollowscrew dental implants, a higher failure rate
and number of biological complications
may be expected compared with periodontally healthy patients (PHP).
A greater peri-implant bone loss in PCP
compared with PHP has also been reported
in other studies (Mengel et al. 2001, 2007;
Hardt et al. 2002; Mengel & Floresde-Jacoby 2005), and the presence of periimplant lesions has been correlated to a
previous history of periodontitis (RoosJansaker et al. 2006).
The European Association for Osseointegration (EAO) organized a consensus conference in February 2006 in Zurich,
Switzerland, with 34 participants from 13
different countries. For the meeting, a systematic review was presented that indicated
that significantly increased incidence of
peri-implantitis and significantly increased
peri-implant marginal bone loss were revealed in individuals with periodontitisassociated tooth loss. Nevertheless, the
small sample size and the methodological
quality assessment of the only two studies
selected suggested interpreting the results
with great caution (Schou et al. 2006).
More recently, Ong et al. (2008) presented a systematic review, based on the
results of nine studies, that suggested that
there is some evidence that patients treated
for periodontitis may experience more implant loss and complications around implants than non-periodontitis patients.
Evidence was stronger for implant survival
than implant success. Anyhow, methodological issues of the studies included in the
review limited the potential to draw robust
conclusions. In particular, the authors
underlined the importance of reporting
long-term data on well-defined patient populations. Similar conclusions were presented
by other recently published reviews (HeitzMayfield 2008; Renvert & Persson 2009).

c 2010 John Wiley & Sons A/S

Even if the European Academy of Periodontlogy (EAP) described the history of

periodontitis as a risk indicator for periimplantitis (Lindhe & Meyle 2008), longterm studies focusing particularly on the
outcome of implant treatment in adults
with various degrees of periodontitis are still
needed to better understand the nature and
the clinical relevance of this association.
The most recent research on the subject, to
the best of our knowledge, presented a
statistically significant greater loss of attachment around implants in the group with
severe periodontitis compared with the no/
mild periodontitis group, even though the
range of the follow-up was 15 years, with a
mean of 3 years (Aloufi et al. 2009).
The aim of this study was to prospectively assess the 10-year results of implant
therapy in a group of PHP compared with a
group of PCP of both moderate and severe
grade. The results regarding implant loss,
mean peri-implant bone loss and number of
peri-implant sites with bone loss  3 mm
are described in this article.

Material and methods

Study population

All patients attending the principal investigator (M.R.), a specialist in periodontology, for dental implant therapy
between May 15, 1996 and May 15, 1998
were screened for possible inclusion in the
study. The specialist practice receives referrals from general dental practitioners,
specialists in orthodontics, specialists in
maxillo-facial surgery and physicians,
mainly located in the North-west of Italy.
Exclusion criteria were:
(1)
(2)
(3)
(4)
(5)
(6)
(7)
(8)

complete edentulism;
presence of dental implants;
mucosal diseases;
alcohol and drug abuse;
pregnancy;
uncontrolled metabolic disorders;
aggressive periodontitis; and
no interest in participating in the
study.

Patients were informed that their data

would be used for statistical analysis, and
gave their informed consent to the treatment. The study was performed in accordance with the principles stated in the
Declaration of Helsinki.

Pre-treatment clinical examination

Gender, date of birth, smoking habits,

medical history at the time of the initial
visit and treatment planning were obtained. Moreover, subjects were clinically
and radiographically monitored at baseline.
Full-mouth plaque score (FMPS), fullmouth bleeding score (FMBS) and pocket
depth (PD) were measured at four sites per
tooth for all teeth by means of a periodontal
probe (XP23/UNC 15, Hu-Friedy, Chicago, IL, USA), and rounded off to the
nearest millimeter.
At the baseline, patients were classified
into two groups:
PHP: periodontally healthy patients and
PCP:
periodontally
compromised
patients.
Moreover, PCP received a score (S) on
the basis of the number and depth of
periodontal pockets according to the following formula:
S PD527 mm 2PD 8 mm
with PD(57mm) and PD(8mm) being the
number of sites with probing pocket depth
of 5 to 7 mm and of 8 mm or more,
respectively.
These patients were arbitrarily divided
into two groups:
Moderate PCP with S  25.
Severe PCP with S425.
Periodontal therapy

Following selection, all patients received

appropriate initial therapy, consisting, depending on the cases, of motivation, oral
hygiene instruction and scaling and root
planing, with the aim to reduce periodontal
pathogens to a minimal level. Hopeless
teeth were recorded and extracted. Periodontal surgery was performed as needed
after re-evaluation. Guided tissue regeneration was pursued, when feasible. Individual
treatment was thoroughly discussed with
the patients and established according
to their personal needs and desires. No
implant surgery was performed before
the assurance of good motivation and
compliance from each single patient
(FMPSo25%; FMBSo25%).
Implant placement and prosthesis
reconstruction

TPS dental implants (Institut Straumann

AG, Waldenburg, Switzerland) were placed,

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Clin. Oral Impl. Res. 21, 2010 / 490496

Roccuzzo et al  Implants in periodontally compromised patients

under local anesthesia, by the same operator

(M.R.), according to the manufacturers instructions. Full-body screws, hollow screws
and hollow cylinders were used, 8, 10 and
12 mm long and 3.3, 4.1 and 4.8 mm in
diameter. All implants were placed using a
standardized surgical procedure (Buser et al.
2000). The implants were placed with the
border of the rough surface approximating the
alveolar bone crest leaving the machined neck
portion in the transmucosal area. Implants
that required bone augmentation and/or sinus
lift elevation were not included in the study.
If necessary, an excision of soft tissue
was performed in order to allow a close
adaptation of the wound margins to the
implant shoulder without submerging it.
The number, position and type of implants
in each patient were determined after a
thorough diagnosis of the anticipated needs
for the planned prosthesis and the presence
of anatomic limitations.
Appropriate healing screws were placed on
top of the implants and the flaps were
sutured, in a non-submerged fashion. Abutment connection was carried out at 35 Ncm
36 months postsurgery, by the same operator. Abutments for cemented restoration
were selected according to the intermaxillary
space. All patients were provided with implant-supported fixed restorations. All restorations were fabricated in order to
facilitate both the oral hygiene procedures
and probing along their circumference.
Baseline measurements

After crown/bridge cementation, a baseline

intraoral radiograph was obtained by using
the parallel long-cone technique and a film
holder (Updegrave 1981). The distance between the implant shoulder and the most
coronal visible bone-to-implant contact
(DIB) measured both at the mesial and at
the distal aspect of each implant was registered. Baseline probing measurements were
also recorded around the implants.
Follow-up

Patients were recalled at various intervals,

depending on the initial diagnosis and the
results of the therapy, for supporting periodontal therapy (SPT). For this purpose, the
following parameters were considered:
 percentage of surfaces with plaque;
 percentage of bleeding on probing
(BOP);

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Clin. Oral Impl. Res. 21, 2010 / 490496





residual pockets  5 mm;

number of teeth lost; and
smoking habits.

Patients were placed on an individually

tailored maintenance care program, including continuous evaluation of the occurrence and the risk of disease progression.
Motivation, reinstruction, instrumentation
and treatment of re-infected sites were
performed as needed. Implant-related biological complications were treated with
mechanical debridment, antiseptic therapy, antibiotic therapy and surgical therapy
(mucogingival or regenerative therapy), depending on the circumstances. If a patient
expressed the desire not to attend follow-up
examinations, he/she was classified as a
drop-out.
Final clinical examination

After 10 years, two calibrated examiners,

blinded to the initial classification of the
patients, collected the following parameters: FMPS, FMBS, number of probing
sites around teeth  5 mm and o8 mm,
number of probing sites around teeth
 8 mm, smoking habits and number of
lost teeth. Complete adhesion to the SPT
(yes or no) was assessed for each patient.
Moreover, for each test implant, probing
depth was measured at four sites (mesial,
buccal, distal and lingual) by means of a
periodontal probe (XP23/UNC 15, HuFriedy) and rounded off to the nearest
millimeter. At the same time and sites,
the presence of dental plaque and of BOP
was recorded (Lang et al. 2000). The distance between the implant shoulder and
the most coronal visible bone-to-implant
contact (DIB) measured in millimeter both
at the mesial and at the distal aspect of each
implant was collected using standardized
periapical intraoral films. Radiographs
were digitalized and measurements were
taken by means of a software (Roccuzzo
et al. 2001; Bornstein et al. 2005). The
10-year DIB values were compared with
the baseline values (abutment connection)

and the radiographic bone-level changes

(radiographic bone loss BL) were calculated. The number of lost implants was
registered. Sites that showed, during the
SPT, radiographic bone loss  3 mm,
either successfully treated by regenerative
approaches or adjacent to implant later
removed, were recorded.

Statistical analysis
For the statistical analysis, heterogeneity
between groups for age, gender, smoking
status, compliance and number of implants
per patients was verified with the Pearson
w2-test. A P-value o0.05 was accepted to
indicate a statistically significant difference.
To evaluate the implant survival rates in
the three groups of patients, the Kaplan
Meier analysis with log-rank pooled per
strata was adopted both for all the implants
and for the solid screws only. The absence
of biases due to multiple implant positioning per patient was assessed comparing the
months of implant survival in patients who
lost at least one implant with a KolmogorovSmirnov test.
Non-parametric analysis of variance
(ANOVA) (KruskalWallis rank ANOVA)
and the MannWhitney U-test were used
to compare the mean bone loss in the three
groups.
The relation between adhesion or not to
SPT and the number of patients displaying
bone loss  3 mm or implant loss was
analyzed with the Fisher exact test.
All statistical analyses were performed
with SPSS 13.0 (SPSS Inc., Chicago, IL,
USA) software.

Results
One hundred and twelve patients were
enrolled in the study. Eleven patients (18
implants) were lost at the 10-year followup (Table 1). The demographic and clinical

Table 1. Patients lost to 10-year follow-up

Total

Number of patients

Number of implants

Reason for drop-out

4
2
3
2
11

6
4
5
3
18

Death
Severe health problems
Moved
Refused to accept a visit


c 2010 John Wiley & Sons A/S

Roccuzzo et al  Implants in periodontally compromised patients

Table 2. Demographic and clinical parameters at the time of patient selection

PHP
Moderate PCP
Severe PCP

Number of
patients

Mean age

Mean number of
missing teeth

mFMPS

mFMBS

32
42
38

45  13
49  15.3
44  8.6

8  4.7
9.6  5.9n
6.4  3.2n

37  15.3%w
45  12.7%w
58.7  18.1%w

29.2  13.4%z
36.7  12%z
53  19.6%z

Statistically significant difference between moderate PCP and severe PCP (Po0.05).
wStatistically significant difference among all the groups (Po0.05).
zStatistically significant difference between PHP and severe PCP and between moderate PCP and severe PCP (Po0.0001).
PHP, periodontally healthy patients; PCP, periodontally compromised patients; mFMPS, mean full-mouth plaque score; mFMBS, mean full-mouth bleeding
score.

Table 3. Demographic and clinical parameters at the 10-year follow-up

PHP
Moderate PCP
Severe PCP

Patients

mFMPS

mFMBS

Mean number
of lost teeth

Patients
within SPT

Patients out
of SPT

28
37
36

23.2  10%
24.1  12.4%
25.2  9.8%

19.1  11.3%n
21  8.2%n
26.6  12.9%n

0.9  1.2
1.3  1.6
1.5  1.7

24
26
29

4
11
7

n
Statistically significant difference between PHP and severe PCP and between moderate PCP and severe PCP (Po0.05).
SPT, Supportive Periodontal Therapy; PHP, periodontally healthy patients; PCP, periodontally compromised patients; mFMPS, mean full mouth plaque score;
mFMBS, mean full mouth bleeding score.

Table 4. Survival rate for all implants and for solid screws only, in the three groups

PHP
Moderate PCP
Severe PCP

Number of
patients

Number of
implants placed

Number of
implants lost

SR all
implants (%)

SR solid
screws (%)

28
37
36

61
95
90

2
7
9

96.6
92.8
90

98
94.2
90

SR: survival rate; PHP, periodontally healthy patients; PCP, periodontally compromised patients.

Survival rate %

100

95

90
PHP
Moderate PCP
Severe PCP

85

40

60

80

100

120

Months
Fig. 1. The KaplanMeier estimate of the survival rate of solid-screw implants as a function of time since
insertion in PHP, moderate PCP and severe PCP.

parameters at the time of patient selection

are listed in Table 2. No inter-group differences for age, gender, implant type, smoking and number of implants placed per
patient were found. Both the FMPS and
the FMBS were significantly different at
the time of recruitment.
The final analysis was performed on
101 subjects: 28 PHP, 37 moderate PCP

c 2010 John Wiley & Sons A/S

and 36 severe PCP (Table 3). No intergroup differences for age, gender, implant
type, smoking, number of teeth lost
during the follow-up and acceptance of
SPT were found. FMPS was also similar
in the three groups, whereas FMBS
was still different between PHP and severe
PCP and between moderate PCP and
severe PCP.

Twenty-two patients did not participate

in the SPT: 4, 11 and 7 in the PHP,
moderate PCP and severe PCP group,
respectively.
Table 4 reports on implant loss and implant survival. Two out of 61 (3.4%) implants were lost in PHP, seven out of 95
(7.2%) in moderate PCP and nine out of 90
(10%) in severe PCP. No implant was lost
as a consequence of early failure or implant
facture. The survival rate was 96.6%,
92.8% and 90% for all implants and
98%, 94.2% and 90% for the solid-screw
implants, respectively, for PHP, moderate
PCP and severe PCP (Fig. 1).
The mean bone loss was equal to 0.75
( 0.88) mm in PHP, 1.14 ( 1.11)
mm in moderate PCP and 0.98
( 1.22) mm in severe PCP (Table 5). No
statistically significant differences were
found among the groups. Regarding bone
loss  3 mm, 4.7%, 11.2% and 15.1% of
sites in PHP, moderate PCP and severe
PCP, respectively, were involved at least
once during the follow-up (Table 5). Nonparametric ANOVA did not reveal any
statistically significant difference between
the three groups, whereas with the Mann
Whitney U-test, a difference was found between groups PHP and severe PCP (Po0.05).
Non-ideal SPT was found to be correlated with greater implant loss in both
moderate and severe PCP groups
(Po0.05) (Table 6).

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Roccuzzo et al  Implants in periodontally compromised patients

Table 5. Mean bone loss and percentage of sites showing bone loss of 3 mm or more during the 10-year period

PHP
Moderate PCP
Severe PCP

mBL (mm)

Sites with BL  3 mm
(all implants)

Sites with BL  3 mm
(solid screws)

0.75 ( 0.88)
1.14 ( 1.11)
0.98 ( 1.22)

4.7%n
11.2%
15.1%n

4%n
11.1%
15.1%n

Statistically significant difference between PHP and severe PCP in the percentage of sites with BL  3mm for both all implants and solid screws (P 0.05).
BL, bone loss; PHP, periodontally healthy patients; PCP, periodontally compromised patients.

Table 6. Incidence of bone loss  3 mm and implants loss in relation to adhesion to Supportive Periodontal Therapy (SPT) in the three
groups

PHP
Moderate PCPn
Severe PCPnn

Adhesion
to SPT

Total number
of patients

Patients with no
bone loss  3 mm

Patients with
bone loss  3 mm

Patients with
no implant loss

Patients with
implant loss

No
Yes
No
Yes
No
Yes

4
24
11
26
7
29

4
22
4
23
3
22

0
2
7
3
4
7

4
22
6
25
3
26

0
2
5
1
4
3

Statistically significant difference in the number of patients with sites with bone loss  3 mm (P 0.003) and for implant loss (P 0.005) between subjects
adhering and not adhering to SPT.
nn
Statistically significant difference in the number of patients with implant loss (P 0.016) between subjects adhering and not adhering to SPT.
PHP, periodontally healthy patients; PCP, periodontally compromised patients.

Minor prosthetic complications, namely

partial fracture of ceramic cuspids, were
registered but not statistically analyzed.

Discussion
Recent systematic reviews have consistently pointed out the necessity of studies
reporting on long-term data of wellcharacterized subjects and a study sample
with an appropriate size (Heitz-Mayfield
2008; Ong et al. 2008; Schou 2008;
Renvert & Persson 2009).
The aim of this study is to present the
long-term implant outcomes in over 100
patients, most of whom had a previous
history of periodontitis, recruited from a
private clinic. The benefit, in accordance
with the Consensus Report of 6th European Workshop on Periodontology
(Lindhe & Meyle 2008), is that subjects
recruited from private or public dental
clinics, rather than university clinics, provide information on the effectiveness
rather than the efficacy of implant
therapy.
One of the greatest difficulties is the
definition of the various degrees of periodontal disease, because the international
definition of chronic periodontitis (Lindhe
et al. 1999) has only limited value for

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Clin. Oral Impl. Res. 21, 2010 / 490496

establishing the case definition for study

purposes (Page & Eke 2007; Preshaw
2009). Nevertheless, an attempt was
made during this research to differentiate
not only between periodontally healthy
and compromised subjects but also between various degrees of periodontal involvement, based on the number and the
depth of the periodontal pockets at the
initial visit.
Periodontal therapy was effective in promoting plaque control in all the groups of
patients. At the time of the first visit,
patients presented high values of FMPS
and FMBS, with a significant difference
among the three groups. All patients
revealed an improvement in the plaque
control, with a statistically significant difference between baseline and 10-year
values, even though plaque and BOP were
registered before the final session of motivation, reinstruction and instrumentation.
In spite of the lack of differences among the
three groups at the 10-year evaluation in
FMPS, BOP was statistically more frequent
among patients with severe periodontitis.
This confirms that patients classified as
severe PCP developed a higher inflammatory response than PHP even though the
mFMPS was similar in the two groups, as
already reported previously (Van der Velden
et al. 1985), and thus confirming the

validity of the classification criteria

adopted in the present study.
Two types of implants were used, i.e.
solid screws and hollow screws/cylinders.
These latter types have not been in use
since several years. For this reason, the
failure rate was reported separately for all
implants and for solid screws. For solidscrew implants, the failure rate tended to
be higher in relation to the severity of the
initial periodontal involvement (PHPo
moderate PCPosevere PCP), even though
no statistically significant difference could
be demonstrated.
The results of this study compare well
with a 7-year life analysis (Romeo et al.
2002) and a 10-year life analysis (Ferrigno
et al. 2002) previously published with a
similar implant system. The actual 5-year
survival and success rates were 96.8% and
93.6%, respectively, for the former study
and 97.7% and 95%, respectively, for the
latter.
The mean bone loss at 10 years was
around 1 mm, with no differences among
the groups. It should be noted, however,
that more implants were removed in moderate PCP and in severe PCP, reducing the
overall number of sites with complications
that were measured at the end of the study.
Because of the lack of an international nonequivoque definition of perimplantitis,

c 2010 John Wiley & Sons A/S

Roccuzzo et al  Implants in periodontally compromised patients

the number of sites with a bone loss of

3 mm or more was, instead, collected on
the mesial and distal aspect of each implant. This cut-off was chosen to exclude
implants that could present a physiologic
remodelling according to Albrektsson et al.
(1986).
The advantage of using this parameter is
the possibility to account for all the implants that had advanced peri-implant bone
loss, including the lost ones.
The percentage of sites with a
BL 3 mm varied among the three groups.
Similar to implant loss, the number of
sites with BL 3 mm was greater in PCP
as compared with PHP, and a correlation with the initial classification of the
patients was observable: it was limited for
PHP, more pronounced for moderate PCP
and even higher for severe PCP. From a
statistical point of view, a significant difference was found between PHP and severe
PCP.
One of the most remarkable results of
the present study was the correlation between implant loss and lack of full adhesion to SPT, during the follow-up in the
PCP. Patients in both PCP groups, who did
not completely adhere to SPT, demonstrated a higher incidence of implant loss.
In the moderate PCP group, 5 patients not
attending SPT lost implants out of 11,
whereas the figure was 1 out of 26
for patients who received a regular SPT.
In a similar manner, for severe PCP, 4
patients out of 7 not attending SPT
lost implants vs. only 3 out of 29 for the
ones who did adhere. These differences
were statistically significant, confirming
the clinical impression that the lack of
adhesion to SPT increases the risk for
biological complications and implant failures. Nevertheless, an individualized and
correctly performed SPT can maintain high
expectations of implant survival even in
PCP.

In the present study, implant surgery

was performed only after completion of
initial periodontal therapy for the infection
control and each patient presented
FMPSo25% and FMBSo25%. Although
periodontal therapy has been suggested to
precede implant therapy in partially dentate patients, a standard definition of successful treated periodontitis has not been
formulated as yet. Ong et al. (2008) proposed to define treated periodontitis as
patients who, before implant placement,
are in a supportive periodontal program
with all sites showing probing depth of
 5 mm without BOP. This is, indeed, a
definition that sets up high standards of
infection control, but it is probably not
always easily applicable for a patientoriented good clinical practice. In fact,
teeth with both residual pockets and furcation involvement can still be present after
effective active therapy and can be maintained for a long follow-up (Hirschfeld &
Wasserman 1978), even though a higher
risk for tooth loss has been demonstrated
(Carnevale et al. 2007; Matuliene et al.
2008). During this research, even
though every attempt was made to insert
implants only after the control of the infection, under many circumstances, due to
strategic reasons, and for the overall benefit
of the patient, implant surgery was performed in conjunction with periodontal
surgery for residual pocket elimination,
particularly if the sites were in adjacent
areas.
SPT, as suggested by other authors (Lang
& Tonetti 2003), was then planned on the
basis of several factors related to the results
of the therapy as well to the patient.
All implants used in the present study
presented a TPS surface, which was
a common surface over a decade ago.
Later on, new surfaces were introduced
to reduce the healing period between surgery and prosthesis. Among the others, a

sandblasted and acid-etched (SLA) surface

was recently confirmed to yield an excellent survival rate even in the case of early
loading (Roccuzzo et al. 2008). While the
TPS surface has Sa values of approximately
3.1 mm, SLA has Sa values of approximately
2 mm (Buser et al. 1999). This feature
should be particularly important in PCP,
because micro-roughness is an important
factor influencing the amount of plaque
accumulation and the consequent risk of
peri-implantitis. (Berglundh et al. 2007;
Albouy et al. 2008). For this reason, the
authors have stopped use of TPS implants
in favor of SLA implants in 1999. Hollow
screws and hollow cylinders have not been
used for many years, now, as they presented a higher incidence of complications,
as it is also evident in this study.
Moreover, the confirmation that plaque
control is of paramount importance has
led the authors to further tighten the inclusion criteria regarding the control of
the infection before implant placement in
PCP. A new investigation is currently in
progress, under these new circumstances,
to assess the long-term clinical and radiographic results around solid screw SLA
implants, placed in patients with excellent
compliance, and to compare the results
with the ones obtained in the present
research.
In conclusion, patients with a history of
periodontitis should be informed that they
are at a higher risk for peri-implant disease.
Moreover, patients have to be strongly
motivated to strictly adhere to SPT as it
has proven to be a key factor in enhancing
the long-term outcomes of implant therapy
by controlling re-infection.

currently used dental implants: a review and

proposed criteria of success. The International
Journal of Oral & Maxillofacial Implants 1:
1125.
Aloufi, F., Bissada, N., Picara, A., Faddoul, F. &
Al-Zahrani, M.S. (2009) Clinical assessment
of peri-implant tissues in patients with
varying severity of chronic periodontitis. Clinical

Implant Dentistry & Related Research 11:

3740.
Berglundh, T., Gotfredsen, K., Zitzmann, N.U.,
Lang, N.P. & Lindhe, J. (2007) Spontaneous
progression of ligature induced peri-implantitis
at implants with different surface roughness:
an experimental study in dogs. Clinical Oral
Implants Research 18: 655661.

Acknowledgement: The authors wish

to thank Dr Andrea Blasi for his
precious help with the statistical
analysis.

References
Albouy, J.P., Abrahamsson, I., Persson, L.G. &
Berglundh, T. (2008) Spontaneous progression of
peri-implantitis at different types of implants. An
experimental study in dogs. I: clinical and radiographic observations. Clinical Oral Implants
Research 19: 9971002.
Albrektsson, T., Zarb, G., Worthington, P. & Eriksson, A.R. (1986) The long-term efficacy of


c 2010 John Wiley & Sons A/S

495 |

Clin. Oral Impl. Res. 21, 2010 / 490496

Roccuzzo et al  Implants in periodontally compromised patients

Berglundh, T., Persson, L. & Klinge, B. (2002) A

systematic review of the incidence of biological
and technical complications in implant dentistry
reported in prospective longitudinal studies of at
least 5 years. Journal of Clinical Periodontology
29 (Suppl. 3): 197212.
Bornstein, M.M., Schmid, B., Belser, U.C., Lussi,
A. & Buser, D. (2005) Early loading of nonsubmerged titanium implants with a sandblasted
and acid-etched (SLA) surface: 5-year results of a
prospective study in partially edentulous patients.
Clinical Oral Implants Research 16: 631638.
Buser, D., Nydegger, T., Oxland, T., Cochran, D.L.,
Schenk, R.K., Hirt, H.P., Snetivy, D. & Nolte,
L.P. (1999) Interface shear strength of titanium
implants with a sandblasted and acid-etched surface: a biomechanical study in the maxilla of
miniature pigs. Journal of Biomedical Materials
Research 45: 7583.
Buser, D., von Arx, T., ten Bruggenkate, C. &
Weingart, D. (2000) Basic surgical principles
with ITI implants. Clinical Oral Implants
Research 11 (Suppl. 1): 5968.
Carnevale, G., Cairo, F. & Tonetti, M.S. (2007)
Long-term effects of supportive therapy in periodontal patients treated with fibre retention osseous resective surgery. I: recurrence of pockets,
bleeding on probing and tooth loss. Journal of
Clinical Periodontology 34: 334341.
Ferrigno, N., Laureti, M., Fanali, S. & Grippaudo,
G. (2002) A long-term follow-up study of nonsubmerged ITI implants in the treatment of totally
edentulous jaws. Part I: ten-year life table analysis
of a prospective multicenter study with 1286
implants. Clinical Oral Implants Research 13:
260273.
Hardt, C.R.E., Grondahl, K., Lekholm, U. & Wennstrom, J.L. (2002) Outcome of implant therapy in
relation to experienced loss of periodontal bone
support. A retrospective 5-year study. Clinical
Oral Implants Research 13: 488494.
Heitz-Mayfield, L.J. (2008) Peri-implant diseases:
diagnosis and risk indicators. Journal of Clinical
Periodontology 35 (Suppl. 8): 292304.
Hirschfeld, L. & Wasserman, B. (1978) A long-term
survey of tooth loss in 600 treated periodontal
patients. Journal if Periodontology 49: 225237.
Karoussis, I.K., Salvi, G.E., Heitz-Mayfield, L.J.,
Bragger, U., Hammerle, C.H. & Lang, N.P.
(2003) Long-term implant prognosis in patients
with and without a history of chronic periodontitis: a 10-year prospective cohort study of

496 |

Clin. Oral Impl. Res. 21, 2010 / 490496

the ITI Dental Implant system. Clinical Oral

Implants Research 14: 329339.
Lang, N.P. & Tonetti, M.S. (2003) Periodontal risk
assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health & Preventive
Dentistry 1: 716.
Lang, N.P., Wilson, T.G. & Corbet, E.F. (2000)
Biological complications with dental implants:
their prevention, diagnosis and treatment. Clinical Oral Implants Research 11 (Suppl. 1):
146155.
Lindhe, J. & Meyle, J. (2008) Peri-implant diseases:
consensus report of the sixth European Workshop on periodontology. Journal of Clinical
Periodontology 35 (Suppl. 8): 282285.
Lindhe, J., Ranney, R., Lamster, I., Charles, A.,
Chung, C.-P., Flemmig, T., Kinane, D., Listgarten, M., Loe, H., Schoor, R., Seymour, G. &
Somerman, M. (1999) Consensus report: chronic
periodontitis. Annals of Periodontology 1: 3838.
Lundgren, D., Rylander, H. & Laurell, L. (2008) To
save or to extract, that is the question. Natural
teeth or dental implants in periodontitis-susceptible patients: clinical decision-making and
treatment strategies exemplified with patient
case presentations. Periodontology 2000 47:
2750.
Matuliene, G., Pjetursson, B.E., Salvi, G.E., Schmidlin, K., Bragger, U., Zwahlen, M. & Lang, N.P.
(2008) Influence of residual pockets on progression of periodontitis and tooth loss: results after
11 years of maintenance. Journal of Clinical
Periodontology 35: 685695.
Mengel, R., Behle, M. & Flores-de-Jacoby, L. (2007)
Osseointegrated implants in subjects treated for
generalized aggressive periodontitis: 10-year results of a prospective, long-term cohort study.
Journal of Periodontology 78: 22292237.
Mengel, R. & Flores-de-Jacoby, L. (2005) Implants
in patients treated for generalized aggressive and
chronic periodontitis: a 3-year prospective longitudinal study. Journal of Periodontology 76:
534543.
Mengel, R., Schroder, T. & Flores-de-Jacoby, L.
(2001) Osseointegrated implants in patients treated for generalized chronic periodontitis and generalized aggressive periodontitis: 3- and 5-year
results of a prospective long-term study. Journal
of Periodontology 72: 977989.
Ong, C.T.T., Ivanovski, S., Needleman, I.G., Retzepi, M., Moles, D.R., Tonetti, M.S. & Donos,
N. (2008) Systematic review of implant outcomes

in treated periodontitis subjects. Journal of Clinical Periodontology 35: 438462.

Page, R.C. & Eke, P.I. (2007) Case definitions
for use in population-based surveillance of
periodontitis. Journal of Periodontology 78:
13871399.
Preshaw, P.M. (2009) Definition of periodontal
disease in research. Journal of Periodontology
36: 12.
Renvert, S. & Persson, G.R. (2009) Periodontitis as
a potential risk factor for peri-implantitis.
Journal of Clinical Periodontology 36 (Suppl.
10): 914.
Roccuzzo, M., Aglietta, M., Bunino, M. & Bonino,
L. (2008) Early loading of sandblasted and acidetched implants: a randomized-controlled doubleblind split-mouth study. Five-year results.
Clinical Oral Implants Research 19: 148152.
Roccuzzo, M., Bunino, M., Prioglio, F. & Bianchi,
S.D. (2001) Early loading of sandblasted and acidetched (SLA) implants: a prospective split-mouth
comparative study. One-year results. Clinical
Oral Implants Research 12: 572578.
Romeo, E., Chiapasco, M., Ghisolfi, M. & Vogel, G.
(2002) Long-term clinical effectiveness of oral
implants in the treatment of partial edentulism.
Seven-year life table analysis of a prospective
study with ITI dental implants system used for
single-tooth restorations. Clinical Oral Implants
Research 13: 133143.
Roos-Jansaker, A.M., Renvert, H., Lindahl, C. &
Renvert, S. (2006) Nine- to fourteen-year followup of implant treatment. Part III: factors associated with peri-implant lesions. Journal of
Clinical Periodontology 33: 296301.
Schou, S. (2008) Implant treatment in periodontitissusceptible patients: a systematic review. Journal
of Oral Rehabilitation 35 (Suppl. 1): 922.
Schou, S., Holmstrup, P., Worhington, H.V. &
Esposito, M. (2006) Outcome of implant therapy
in patients with previous tooth loss due to periodontitis. Clinical Oral Implants Research 17
(Suppl. 2): 104123.
Updegrave, W.J. (1981) Right angle dental radiography described, simplified, and standardized
(part I). Compendium of Continuing Education
in Dentistry 2: 379384.
Van der Velden, U., Abbas, F. & Hart, A.A. (1985)
Experimental gingivitis in relation to susceptibility to periodontal disease. (I) Clinical observations. Journal of Clinical Periodontology 12:
6168.


c 2010 John Wiley & Sons A/S