Accepted: 8 June 2017

DOI: 10.1111/idh.12300

ORIGINAL ARTICLE

The association between three attitude-­related indexes of

oral hygiene and secondary implant failures: A retrospective
longitudinal study

S Tecco1 | MG Grusovin2 | S Sciara3 | F Bova4 | G Pantaleo3 | P Capparé1

1
Dental School, Vita-Salute San Raffaele
University and IRCCS San Raffaele, Milan, Italy
2
Dental School, Vita-Salute San Raffaele
University, Milan, Italy
3
UniSR-Social Lab (Research Methods), Faculty
of Psychology, Vita-Salute San Raffaele
University, Milan, Italy
4
Center for Oral Hygiene and Prevention,
Dental School, Vita-Salute San Raffaele
University and IRCCS San Raffaele, Milan, Italy
Correspondence
Paolo Capparé, Dentistry Department, IRCCS
San Raffaele Hospital, Milan, Italy.
Email: paolocappare@gmail.com
Abstract
Objective: This study evaluated the strength of the association between three widely
used clinical indexes considered as distal behavioural indicators of attitude-­related
oral status (an index of oral hygiene, the plaque index [PI] and two periodontal indexes,
that is the presence of bleeding on probing [BOP] and of pockets probing depth [PPD])
and secondary implant failure due to peri-­implantitis in patients rehabilitated with ce-
mented prosthesis.
Materials and Methods: The study included patients who underwent implant-­
prosthetic rehabilitation and had joined the programme of maintenance of the same
hospital. Implant failures, number of months between implant insertion and implant
loading, and patients’ surgical protocol were monitored and recorded. Further, PI, BOP
and PPD—all attitude-­related indicators of oral hygiene and periodontal inflamma-
tion—were recorded and related, in terms of odds ratios (ORs) and corresponding risk
factors, to secondary implant failures.
Results: A total of 1427 patients (2673 implants) were enrolled. The follow-­up ranged
from 1.5 to 9 years (mean 5.3 years±1.3). The cumulative survival rate was 98.01%.
Thirty-­two patients (36 implants, 1.36% of all implants) had implant failure. A statisti-
cally significant association between PI, BOP, PPD and secondary failures due to peri-­
implantitis was observed.
Conclusion: Within the limitations of this study, all three attitude-­related behavioural
indicators—the plaque index (PI), bleeding on probing (BOP) and abnormal probing
pocket depth (PPD)—proved to be significant risk indicators for secondary implant
failure due to peri-­implantitis, both from a clinical and from a socio-­psychological
attitude-­related perspective.

KEYWORDS
dental implant, failure, oral hygiene, retrospective

1 |  INTRODUCTION
Despite the remarkably high survival rate of dental implants, it is im-
portant to understand factors related to implant failures so that pre-
vention of negative events can be implemented both at the clinical
and at the psychosocial level. Whereas at the clinical level, careful
consideration of oral health status may seem fairly obvious to clini-
cians, background psychological aspects and behavioural indexes of
patients’ attitude-­related poor oral hygiene are often neglected, even
when they actually may play a crucial role in determining desirable clin-
ical outcomes. In line with the tenets of experimental social psychol-
ogy—a relatively new life science typically proceeding by hypothesis

Int J Dent Hygiene. 2017;1–8. wileyonlinelibrary.com/journal/idh   © 2017 John Wiley & Sons A/S. |  1
Published by John Wiley & Sons Ltd
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2       TECCO et al.
testing1—at the psychological level of functioning, poor oral care and
hygiene may easily stem from wrong habits, beliefs and attitudes to-
wards the dentist and oral hygiene maintenance.2,3 Insufficient oral
hygiene may in turn result into severe conditions of poor oral health,
as part of a process leading from periodontal inflammation to irre-
versible implant failure.4 Negative oral health-­related outcomes such
as teeth decay, deteriorated dental aesthetics, teeth loss and implant
failure are not negligible events, as they all deeply affect patients’ self-­
regard, self-­esteem and, ultimately, patients’ broader social function-
5-7
ing. Good oral health and quality-­of-­life bolstering psychological
conditions, by contrast, have been demonstrated to be systematically
linked—among others—to successful crown therapy,3 reduced den-
tine hypersensitivity,8,9 and, more generally, proper orthodontic treat-
6
ments and interventions.
On a concrete, behavioural plan, some distal behavioural indica-
tors commonly used in clinical practice, such as the plaque index (PI),
presence of bleeding on probing (BOP) and of probing pockets depth
(PPD), play a crucial role because they allow the clinician to directly
monitor what patients do or have actually done in order to maintain
proper oral conditions, rather than limiting the measurements only to
the more abstract “emotional” or “cognitive” components of patients’
attitude-­related behaviours towards oral health.
Implant failures can be divided into early and late failures.10,11
Early failure occurs before implant loading,12 while late failure after
occlusal loading.13,14 Peri-­implantitis is one of the causes of late im-
plant failure and can be defined as the presence of bleeding and/or
suppuration on probing, redness and swelling of the mucosa, deep-
ening of the pockets adjacent to the dental implants and loss of sup-
porting bone.15 Treatment of peri-­implantitis represents a challenge
for clinicians. Thus, it becomes important to understand which factors
can lead to the development of the disease. Plaque accumulation is
a risk factor for infection. The majority of the authors recommend to
routinely assess plaque, marginal bleeding, bleeding on probing and
probing depth during the follow-­up visits of their patients treated
with implant-­prosthetic rehabilitation. This is because inflammatory
processes can ultimately lead to implant failure and, thus, good oral
hygiene is considered as a positive predictor of implant success.16 A
correlation between previous periodontal disease and peri-­implant
status is also supported by the literature.17 The presence of peri-
odontal bacteria around failing implants could suggest a correlation
between periodontitis and peri-­implantitis.18
Inflammatory processes can be diagnosed through presence of
bleeding on probing and of deepened probing depth.19
Dental practitioners play an important role in the diagnosis of gin-
gival, periodontal and peri-­implant diseases. It is not yet known the
level at which peri-­implant indexes can be used to predict the risk of
implant failure, that is to say above which values the clinician should
fear the possibility of implant failure and which is the role that the
periodontal follow-­up performed by the hygienists can have.20
The aim of this work was to assess the strength of association
between three widely used indicators (the index of oral hygiene,
the plaque index [PI], and two periodontal indices, that is presence
of bleeding on probing [BOP] and presence of probing pocket depth
[PD]), considered as distal behavioural indicators of attitude-­related
oral status, and secondary implant failure due to peri-­implantitis in pa-
tients following a dedicated maintenance programme.
2 | MATERIALS AND METHODS
The participants of this retrospective longitudinal study were selected
among those who had undergone implant-­prosthetic rehabilitation
at the Department of Dentistry, IRCCS San Raffaele Hospital, Milan,
Italy. Patient records and data recorded at the department in the digi-
tal database software (Dental Management System DMS, ET Edizioni
Tecnologiche, Milan, Italy) were analysed. The STROBE Statement for
improving the quality of cohort studies was followed.
Conical implants with rough surface (Micro Rough Surface—MRS®)
and internal hexagon connection were used (K implants, WinSix®,
BioSAFin. S.r.l.—Ancona, Italy).
Inclusion criteria were as follows:
• Adult patients (>18 years) with partial edentulous status, submit-
ted at the Department of Dentistry, IRCCS San Raffaele Hospital,
Milan, Italy, for the implant-prosthetic therapy, with the insertion of
at least one fixture;
• Patients referred, at the end of their implant-prosthesis rehabilita-
tion, to the implant maintenance programme at the Centre for Oral
Hygiene and Prevention (COHP) of the same Department, and in-
serted in the programme to follow-up.
• No systemic contraindications to implant-prosthetic therapy;
• Complete medical records present;
• Follow-up of at least 1.5 years.
Exclusion criteria were as follows:
• Patients who had not joined the programme of maintenance and
follow-up at the COHP of the same hospital;
• Patients with incomplete data about implant failures;
• Full-arch rehabilitations;
• Rehabilitations with at least one tilted implant;
• Rehabilitations with implants shorter than 9 mm;
• Screw-retained rehabilitations.
All patients signed a consent form for implant-­prosthetic rehabilita-
tions and implant surgery.
Eligible patients had undergone at the COHP the following
protocol:
• An initial examination (t0) performed about 30 days before the im-
plant/s insertion;
• A second visit performed at the time of prosthetic functionalization
(t1);
• Thereafter, a series of check-ups organized periodically, every
4 months (t2, t3,…, tn,…), during which the PI, BOP and PD were
detected.
TECCO et al.
The clinical protocol adopted during the sessions of follow-­up is
described in Table 1, which reports the operating sequence used for
healthy implants.
Instead, when the implant site appeared to suffer from mucositis
and/or peri-­implantitis, the operational protocol was modified adopting
the addition of the so-­called cumulative interceptive supportive ther-
apy (C.I.S.T.),21 depending on the severity of the pathology observed.
According to Sanz et al.,15 peri-­
implant mucositis and peri-­
implantitis were defined as:
• Peri-implant mucositis: Presence of redness and swelling in the
peri-implant soft tissue. Bleeding on probing is currently recognized
as the important feature. No appreciable peri-implant bone loss.
• Peri-implantitis: Presence of an inflammatory process around an im-
plant, including both soft-tissue inflammation and progressive loss
of supporting bone beyond biological bone remodelling.
A vertical distance of 2 mm from the expected crestal bone level
following remodelling after implant placement was considered as the
threshold level.22 Moreover, the parameter used to assess soft-­tissue
inflammation in either mucositis or peri-­implantitis was the bleeding on
22
probing (BoP) index.
2.1 | Data collection and preliminary coding
The primary outcome measure was secondary implant failure due to
peri-­implantitis, with “implant failure,” meaning the removal or loss of
an implant for progressive peri-­implantitis after successful loading.
For each patient, the number, the time, the reason of implant failure
and the surgical protocol adopted for the insertion were recorded.
The plaque index (PI O’Leary), the presence of bleeding on probing
(BOP) and of probing pockets depth (PPD) were recorded on teeth,
whereas modified plaque index (mPI) and modified bleeding index
23,24
(mBOP) referred to implants. Each measurement was acquired at
mesial, distal, palatal and vestibular sites.25
Data were considered from the first maintenance visit, at 4 months
from prosthetic functionalization of implants to the end of the follow-­
ups. Mean values were calculated at patient level, for each of the study
variables and across all follow-­up visits. Thus, with respect to the PI
O’Leary and mPI variables, data were coded into “low presence of
plaque” (PI≤25%) vs “presence of plaque” (PI>25%). Analogously, with
respect to the BOP and mBOP variables, data were coded into “low
presence of bleeding on probing” (BOP≤30%) vs “presence of bleeding
on probing” (BOP>30%). Finally, with respect to the PPD variable, data
were coded into “absence of probing depth” (PPD≤4) vs “presence of
at least one site with probing depth” (PPD>4 mm). All analyses were
conducted at patient level.
2.2 | Statistical methods and plan for the analyses
Odds ratios (ORs) were calculated separately for PI (O’Leary)/mPI,
BOP/mBOP and PPD to test their role as attitude-­related risk indica-
tors of secondary implant loss. Confidence intervals at 95% and Z-tests
|
      3
of significance for ORs were also computed, to provide an estimate of
range of expected results, along with a test of statistical significance,
for each of the three potential risk factors. The degree of independ-
ence vs. association in the cross-­tabulations of categorical variables re-
lated to each of the three ORs was established by χ2 tests. The P-­value
for each statistical test of significance was set at .05.
3 | RESULTS
A total of 1751 patients (4637 implants) were rehabilitated from
March 2006 to March 2013.
Thirty-­eight patients (266 implants) were excluded because they
were treated with full-­arch rehabilitation after grafting procedures;
31 patients (296 implants) were excluded because they were treated
with full-­arch rehabilitation without grafting; 137 patients (742 im-
plants) were excluded because they were treated with tilted implants
for full-­arch rehabilitation; 8 patients (21 implants) were excluded be-
cause they were treated with tilted implants for partial rehabilitation.
Subjects excluded because treated with screw-­retained rehabilitations
were all part of these excluded cases. Finally, 1537 subjects (3312
implants) were considered as eligible subjects and treated between
March 2006 and March 2013.
Further, 110 patients from this latter group were excluded, as
they did not adhere to the maintenance programme. Indeed, the
110 patients were excluded because they were not present at least
at one recall visit. So, the minimum adherence was three visits each
12 months (1 visit each 4 months). Thus, the ratio between suggested
and attended visits each year was one. A total of 1427 subjects (2673
implants) were thus included in the study. Patients’ clinical follow-­up
ranged from 1.5 to 9 years (mean 5.3 years±1.3), and the number of
detections/visits per patient ranged from a minimum of four detec-
tions/visits (for patients with follow-­up of 1.5 years) to a maximum of
22 detections/visits (for patients with follow-­up of 9 years). The flow
chart of the study is depicted in Figure 1.
3.1 | Implant failure
Preliminary descriptive analyses showed that a total of 31 patients
(M: 10; F: 21) experienced implant loss. Thirty-­six implants (1.35% of
2673 implants) failed. The cumulative survival rate was 98.01% (36
implants failed). Twenty patients (among 31 patients) experienced
early failure of 24 implants in a range of time of 1-­3 months from im-
plant insertion (in these cases, implant failure was due to primary in-
fection). Eleven patients (12 implants) experienced secondary implant
failure, all because of peri-­implantitis.
In total, 803 implants (30.04%) in 314 patients suffer from mucosi-
tis and 238 implants (8.90%) in 98 patients suffer from peri-­implantitis.
Data about the location, size and type of failed implants for sec-
ondary infections are reported in Table 2. Ten of these 11 subjects
were females. Among these subjects, four patients experienced im-
plant failure before 20 months and four patients more than 3 years
from insertion (Table 2).
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4       TECCO et al.

F I G U R E   1   Flow chart of the study

TECCO et al.
T A B L E   1   Operating protocol at C.I.O.P. Visits and data
acquisition performed every 4 months from the prosthetic
functionalization of osseointegrated implants
1. Check the patient’s medical history framework;
2. Assessment of exposure to risk factors for the peri-implant disease;
3. Detection of clinical parameters: PI O’Leary, PPD, BOP;
4. Education and patient motivation to correct and regular oral
hygiene at home, and—where necessary—to the use of at-home
hygiene aids adequate to implant-prosthesis;
5. Supragingival scaling;
6. Supragingival air-polishing with powder of glycine in average grain
size;
7. Subgingival polishing with powder of glycine at a very low particle size
All the failed implants were inserted using a delayed loading proto-
col, with no post-­extractive implants; in one patient, the insertion was
made on previously regenerated alveolar bone.
Considering the entire follow-­up period, further descriptive analy-
ses of the PI, BOP and PD indexes conducted on patients with second-
ary implant failure revealed the following pattern of preliminary results:
• An average PI (O’Leary)/mPI [mean values between PI (O’Leary) val-
ues and mPI values] of 28.4%±14.8% (range: 11%-58.5%), with five
patients of 11 showing a mean PI (O’Leary)/mPI index >25%.
      5|
• An average BOP/mBOP [mean values between BOP values and
mBOP values] of 13.4%±12.7% (range: 2%-33%), with three pa-
tients showing a mean BOP/mBOP index>30%.
• An average PD >4 mm of 34%±26.1% (range: 3%-73% of sites),
with five patients showing a mean PD >4 mm during the follow-up
in more than 25% of sites.
Main statistical analyses revealed that, when the relationships
between (i) mean PI (O’Leary)/mPI and secondary implant failure,
(ii) mean BOP/mBOP and secondary failure and (iii) PD>4 mm and
secondary implant failure were evaluated to test the role of these
variables as potential risk factors, the following results emerged
(Table 3):
• A statistically significant association between PI (O’Leary)/mPI and
secondary implant failure (χ2(1)=5.58, P=.018, without Yates’ correc-
tion), corresponding to an OR for PI (O’Leary)/mPI >25% of 3.82.
• A statistically significant association between BOP/mBOP >30%
and secondary failure (χ2(1)=5.23, P=.022, with Yates’ correction),
corresponding to an OR for BOP/mBOP >30% of 5.86.
• A statistically significant association between PPD >4 mm and im-
plant failure (χ2(1)=7.54, P=.006, without Yates’ correction), corre-
sponding to an OR for PD >4 mm of 4.60.

T A B L E   2   Raw data on secondary implant failures

Tooth site (Palmer Months from insertion Months from loading

N Gender numeration) and failure to failure Width (mm) Length (mm)

Patient 1 F 3.2 38 33 3.3 13

Patient 2 F 1.6 6 1 5 10
Patient 3 F 1.5 24 24 6.5 9
Patient 4 F 1.5 33 30 3.3 11
Patient 5 F 1.6 47 44 4.5 11
Patient 6 F 1.6 20 12 5.2 9
Patient 7 M 2.7 4 1 5 10
Patient 8 F 4.6 23 20 3.8 9
Patient 9 F 3.6 15 12 4.5 11
Patient 10 F 4.5 72 69 3.8 11
Patient 11 F 4.6-­3.6 59 56 4.5 11

T A B L E   3   Systematic relationships
Chi-­square and Odds
between secondary implant failure and
P-­values ratios 95% CIs Z-­test P
identified risk factors
PI (O’Leary)/ χ2(1)=5.58 3.82 1.16-­12.62 2.20 .028
mPI >25% P=.018
without Yates’ correction
BOP/mBOP χ2(1)=5.23 5.86 1.53-­22.48 2.58 .01
>30% P=.022
with Yates’ correction
PPD >4 mm χ2(1)=7.54 4.60 1.39-­15.22 2.50 .012
P=.006
without Yates’ correction
 |
6       TECCO et al.
4 |  DISCUSSION
This study found a statistically significant association among poor oral
hygiene and related periodontal inflammation status and secondary
implant failure due to peri-­implantitis. More specifically, all three indi-
cators (PI, BOP and PPD), considered through all maintenance visits,
were systematically and reliably associated with secondary implant
failures due to peri-­implantitis. The risk of experiencing secondary
implant loss was 3.8 times higher for patients with PI (O’Leary)/mPI
>25% than for their counterparts. Analogously, the risk of experienc-
ing secondary implant loss was 5.86 times higher for patients with
BOP/mBOP >30% if compared with their counterparts. Finally, the
risk of experiencing secondary implant loss was 4.60 times higher
for patients with PPD >4 mm than for their counterparts. Taken to-
gether, this pattern of results suggests that PI, BOP and PPD should
be carefully monitored as indicators of a concrete risk of experienc-
ing secondary implant loss—a risk that we estimated, even in the case
of the most favourable observed outcome (PI), of at least four times
(OR=3.8) more pronounced for exposed patients than for their non-­
exposed counterparts.
In showing how poor oral hygiene is linked to deteriorated oral sta-
tus and, in turn, to implant failure, our pattern of results also steers
attention to those implicit socio-­
psychological factors (eg wrong
attitude-­related habits and beliefs towards the dentist and/or oral hy-
giene)2,3 which should constitute the target of informed and specific
interventions, aimed at monitoring and preventing their negative ef-
fects. In this respect, a clear limit of this study is that we considered
only three distal attitude-­related indexes (PI, BOP and PPD) of the be-
havioural component of oral hygiene. Further studies could thus benefit
from considering also the role of more traditional “cognitive” and “emo-
tional” components of patients’ thinking and feeling about oral health.
From a methodological point of view, the identification of risk fac-
tors would be even more informative if conducted on the basis of lon-
gitudinal prospective studies. Nevertheless, retrospective studies with
a considerable sample size—such as ours—can suggest clinically useful
risk indicators as well, to closely monitor patients’ oral status during
maintenance. In this respect, in a 15-­year prospective study on 46
edentulous patients poor oral hygiene was associated with bone loss,
26
while only one secondary failure was recorded. Other retrospective
studies tried to identify risk indicators associated with implant compli-
cations, but substantial differences in the protocols used make a direct
17
comparison with our study difficult. Roos-­Jansåker et al. presented
data on 218 patients with 9-­to 14-­year follow-­up and found a sig-
nificant correlation between implant loss and periodontal bone loss
at remaining teeth. At patient level, peri-­implantitis was related to a
4
previous history of periodontitis and smoking, while no correlation
was found with the frequency of visits to the hygienist/dentist and, at
the implant level, with plaque.
Recently, Daubert et al.27 in examining the time of implant failure
in a sample of 96 patients (225 implants) with a follow-­up time of 10.9-­
1.5 years, reported five secondary failures due to peri-­implantitis, all in
patients with history of periodontitis. Data on oral hygiene and main-
tenance visits were not considered.
Implant survival rate in non-­periodontitis and periodontitis pa-
tients has been analysed in several studies. The data indicate that
patients with periodontitis are more prone to peri-­implantitis,4 bone
loss around implants and eventually implant failure.28,29 Patients with
chronic periodontitis had four times more chance of developing peri-­
implant disease than patients with healthy periodontal tissues.30 A re-
cent study states that within the same subjects, putative periodontal
pathogens are common to both periodontal and peri-­implant sites irre-
spective of health status, while the prevalence and levels of P. gingivalis
and F. nucleatum are significantly associated with periodontitis, but not
with peri-­implantitis.31
All the patients included in the study were treated using similar re-
habilitation protocols, followed an accurate maintenance programme.
The low failure rate suggests that implant therapy can be successfully
used in patients who undergo proper therapy and regular periodontal
maintenance.32
Patients with different follow-­up periods were included in the
study. All patients included followed the proposed maintenance
programme, and the periodicity of their visits remained more or less
constant in all patients during their entire follow-­up. This seems to
confirm the validity of a maintenance programme organized based on
the mechanism of the phone recalls.
Only cemented rehabilitations were used to examine a more ho-
mogenous sample, because the presence of cement can be one fac-
tor in the development of peri-­implantitis.4,33 All the patients had
cemented restoration and were treated in the same way with careful
removal of all remaining cement.
With the aim of obtaining indications that could be easily applied in
clinical practice, we chose to correlate presence of secondary failures to
dichotomized indexes. Thus, with respect to PI O’Leary/mPI, the cut-­off
level was set at 25%, because this is the most common cut-­off value
used in periodontal studies to discriminate between patients with ac-
ceptable vs. bad oral hygiene.23 Analogously, a cut-­off value of 30% was
used for BOP/mBOP in accordance with Joss et al.34 who considered
as clinical indicators of disease progression or periodontal stability, re-
spectively, mean BOP and mBOP values >30% or ≤30%. Finally, a cut-­
off level of PPD >4 mm was established because, in clinical practice, it
has been widely used to individuate subjects with periodontitis.35
5 | CONCLUSIONS
Within the limitations discussed above, all three attitude-­
related
behavioural indicators of oral hygiene and periodontal status moni-
tored in this study—the plaque index (PI), the presence of bleeding
on probing (BOP), and abnormal probing pocket depth (PPD)—proved
to be significant risk indicators for secondary implant failure due to
peri-­
implantitis. All three monitored variables revealed significant
increases in the risk of experiencing secondary implant failure due
to peri-­implantitis—a risk that we estimated, even in the case of the
most favourable observed outcome (PI), of at least (circa) four times
(OR=3.8) more pronounced for exposed patients than for their non-­
exposed counterparts. This pattern of results has clear and distinct
TECCO et al.
relevance for preventing implant failure, both from a clinical and from
an attitude-­related socio-­psychological perspective.
6 | CLINICAL RELEVANCE
6.1 | Scientific rationale
In the current literature, it is not yet known how peri-­implant attitude-­
related indexes can be used to predict the risk of implant failure; that
is, above which values the clinician should fear the possibility of im-
plant failure, and which is the role that the periodontal maintenance
performed by the hygienists can have.
6.2 | Principal findings
Attitude-­related behavioural indicators of oral hygiene—the plaque
index (PI), and the periodontal indices bleeding on probing [BOP] and
abnormal probing pocket depth (PPD)—proved to be significant risk
indicators for secondary implant failure due to peri-­implantitis.
6.3 | Practical implications
A correct maintenance protocol can preserve good oral hygiene in implant
patients and can lower the risk of secondary implant failure, both from a
clinical and from a socio-­psychological attitude-­related perspective.
ACKNOWLE DG E MEN TS
Authors disclosed any commercial or other relationships that could
constitute a conflict of interest.
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How to cite this article: Tecco S, Grusovin MG, Sciara S,
Bova F, Pantaleo G, Capparé P. The association between three
attitude-­related indexes of oral hygiene and secondary implant
failures: A retrospective longitudinal study. Int J Dent Hygiene.
2017;00:1–8. https://doi.org/10.1111/idh.12300