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journal of dentistry 42 (2014) 15091527

Available online at www.sciencedirect.com

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journal homepage: www.intl.elsevierhealth.com/journals/jden

Review

Periodontally compromised vs. periodontally


healthy patients and dental implants: A systematic
review and meta-analysis
Bruno Ramos Chrcanovic a,*, Tomas Albrektsson a,b, Ann Wennerberg a
a
b

Department of Prosthodontics, Faculty of Odontology, Malmo University, Malmo, Sweden


Department of Biomaterials, Goteborg University, Goteborg, Sweden

article info

abstract

Article history:

Objectives: To test the null hypothesis of no difference in the implant failure rates, postop-

Received 22 April 2014

erative infection, and marginal bone loss for the insertion of dental implants in periodon-

Received in revised form

tally compromised patients (PCPs) compared to the insertion in periodontally healthy

28 August 2014

patients (PHPs), against the alternative hypothesis of a difference.

Accepted 25 September 2014

Methods: An electronic search without time or language restrictions was undertaken in


March 2014. Eligibility criteria included clinical human studies, either randomized or not.
Results: 2768 studies were identified in the search strategy and 22 studies were included. The

Keywords:

estimates of relative effect were expressed in risk ratio (RR) and mean difference (MD) in

Dental implants

millimetres. All studies were judged to be at high risk of bias, none were randomized. A total

Periodontal disease

of 10,927 dental implants were inserted in PCPs (587 failures; 5.37%), and 5881 implants in

Periodontitis

PHPs (226 failures; 3.84%). The difference between the patients significantly affected the

Implant failure rate

implant failure rates (RR 1.78, 95% CI 1.502.11; P < 0.00001), also observed when only

Postoperative infection

the controlled clinical trials were pooled (RR 1.97, 95% CI 1.382.80; P = 0.0002). There were

Marginal bone loss

significant effects of dental implants inserted in PCPs on the occurrence of postoperative

Meta-analysis

infections (RR 3.24, 95% CI 1.696.21; P = 0.0004) and in marginal bone loss (MD 0.60, 95% CI
0.330.87; P < 0.0001) when compared to PHPs.
Conclusions: The present study suggests that an increased susceptibility for periodontitis
may also translate to an increased susceptibility for implant loss, loss of supporting bone,
and postoperative infection. The results should be interpreted with caution due to the
presence of uncontrolled confounding factors in the included studies, none of them
randomized.
Clinical Significance: There is some evidence that patients treated for periodontitis may
experience more implant loss and complications around implants including higher bone loss
and peri-implantitis than non-periodontitis patients. As the philosophies of treatment may
alter over time, a periodic review of the different concepts is necessary to refine techniques
and eliminate unnecessary procedures. This would form a basis for optimum treatment.
# 2014 Elsevier Ltd. All rights reserved.

* Corresponding author at: Department of Prosthodontics, Faculty of Odontology, Malmo University, Carl Gustafs vag 34, SE-205 06, Malmo,
Sweden. Tel.: +46 725 541 545; fax: +46 40 6658503.
E-mail addresses: bruno.chrcanovic@mah.se, brunochrcanovic@hotmail.com (B.R. Chrcanovic).
http://dx.doi.org/10.1016/j.jdent.2014.09.013
0300-5712/# 2014 Elsevier Ltd. All rights reserved.

1510

1.

journal of dentistry 42 (2014) 15091527

Introduction

In an attempt to decrease implant failure rates, more


attention is being placed on understanding the etiologic
and risk factors that lead to the failure of dental implants.1
The question if patients with a history of periodontitis are
more at risk for peri-implant disease has received increasing
attention in the last years.2 There is some evidence that
patients treated for periodontitis may experience more
implant loss and complications around implants including
higher bone loss and peri-implantitis than non-periodontitis
patients.3 A history of treated periodontitis does not seem to
adversely affect implant survival rates over short times of
follow-up.4 A small number of periodontal maintenance
patients seem to be refractory to treatment and go on to
experience continued and significant tooth loss. These
subjects also have a high level of implant complications
and failure.5 However, the finding that titanium implants are
but foreign bodies have resulted in a general questioning
whether periodontitis and peri-implantitis are at all related
forms of disease.6
Some clinicians assume that periodontally compromised
patients (PCPs) present a potentially higher risk for
implant failure than healthy individuals. The reason
for this assumption is that a similar pathological
bacterial flora forms around diseased teeth and diseased
implants, though with some differences in partially and
completely edentulous patients.7 Implants are rapidly
colonized by indigenous periodontal pathogens in partially
dentate patients harbouring periodontal lesions.7 Moreover,
long-term outcomes demonstrated that implants in nonsmoking PCPs previously treated for periodontitis
were more prone to developing marginal bone loss compared with those in PHPs.8 These results were obtained
despite the fact that all patients were regularly enrolled in
and were compliant with a supporting periodontal therapy
(SPT) programme over 10 years.8 Fardal and Linden5
observed that smoking, stress and a family history of
periodontal disease were identified as factors associated
with a refractory outcome, and these variables remained
significant after multivariate analysis. Another study
showed that marginal bone level at 10 years was significantly associated with smoking, implant location, fullmouth probing attachment levels, and change, over time,
in full-mouth probing pocket depths.9 Having said this,
recent
investigation
demonstrated
significantly
a
different mRNA signatures between periodontitis and
peri-implantitis.10
Therefore, a pertinent question in relation to implant
therapy in patients susceptible to periodontitis is whether
these patients may also show an elevated risk for periimplant tissue destruction. Thus, the aim of this metaanalysis is to compare the survival rate of dental implants,
postoperative infection, and marginal bone loss of dental
implants inserted in PCPs and in periodontally healthy
patients (PHPs). The present study presents a more detailed
analysis of the influence of periodontal disease on the
implant failure rates, previously assessed in a published
systematic review.1

2.

Materials and methods

This study followed the PRISMA Statement guidelines.11 A


review protocol does not exist.

2.1.

Objective

The purpose of the present review was to test the null


hypothesis of no difference in the implant failure rates,
postoperative infection, and marginal bone loss for the
insertion of dental implants in PCPs compared to the insertion
in PHPs, against the alternative hypothesis of a difference.

2.2.

Search strategies

An electronic search without time or language restrictions was


undertaken in March 2014 in the following databases: PubMed,
Web of Science, and the Cochrane Oral Health Group Trials
Register. The following terms were used in the search strategy
on PubMed:
(dental implant [Text Word]) AND periodontal disease [Text
Word]
(dental implant [Text Word]) AND periodontitis [Text Word]
The following terms were used in the search strategy on
Web of Science, in all databases, refined by selecting the term
dentistry oral surgery medicine in the filter research area:
(dental implant [Topic]) AND periodontal disease [Topic]
(dental implant [Topic]) AND periodontitis [Topic]
The following terms were used in the search strategy on the
Cochrane Oral Health Group Trials Register:
(dental implant OR dental implant failure OR dental
implant survival OR dental implant success AND (periodontal disease OR periodontitis))
A manual search of dental implants-related journals,
including British Journal of Oral and Maxillofacial Surgery,
Clinical Implant Dentistry and Related Research, Clinical Oral
Implants Research, European Journal of Oral Implantology,
Implant Dentistry, International Journal of Oral and Maxillofacial Implants, International Journal of Oral and Maxillofacial
Surgery, International Journal of Periodontics and Restorative
Dentistry, International Journal of Prosthodontics, Journal of
Clinical Periodontology, Journal of Dental Research, Journal of
Dentistry, Journal of Oral Implantology, Journal of Craniofacial
Surgery, Journal of Cranio-Maxillofacial Surgery, and Journal
of Maxillofacial and Oral Surgery, Journal of Oral and
Maxillofacial Surgery, Journal of Oral Rehabilitation, Journal
of Periodontology, and Oral Surgery Oral Medicine Oral
Pathology Oral Radiology and Endodontology was also
performed.
The reference list of the identified studies and the
relevant reviews on the subject were also scanned for
possible additional studies. Moreover, online databases
providing information about clinical trials in progress were

journal of dentistry 42 (2014) 15091527

checked (https://clinicaltrials.gov/; www.centerwatch.com/


clinicaltrials; www.clinicalconnection.com).

2.3.

Inclusion and exclusion criteria

Eligibility criteria included clinical human studies, either


randomized or not, comparing implant failure rates in
any group of patients receiving dental implants that are
being inserted in PCPs compared to their insertion in PHPs.
For this review, implant failure represents the complete loss
of the implant. Exclusion criteria were case reports,
technical reports, animal studies, in vitro studies, and
review papers.

2.4.

Study selection

The titles and abstracts of all reports identified through the


electronic searches were read independently by the three
authors. For studies appearing to meet the inclusion criteria,
or for which there were insufficient data in the title and
abstract to make a clear decision, the full report was obtained.
Disagreements were resolved by discussion between the
authors.

2.5.

Quality assessment

Quality assessment of the studies was executed according to


the NewcastleOttawa scale (NOS).12 The NOS calculates the
study quality on the basis of 3 major components: selection,
comparability, and outcome for cohort studies. It assigns a
maximum of 4 stars for selection, a maximum of 2 stars for
comparability, and a maximum of 3 stars for outcome.
According to that quality scale, a maximum of 9 stars/points
can be given to an observational study, and this score
represents the highest quality, where six or more points were
considered high quality.

2.6.

Data extraction and meta-analysis

From the studies included in the final analysis, the following


data was extracted (when available): year of publication, study
design, unicenter or multicenter study, number of patients,
patients age, follow-up, days of antibiotic prophylaxis, mouth
rinse, implant healing period, failed and placed implants,
postoperative infection (reported incidence of peri-implantitis), marginal bone loss, implant surface modification,
periodontal disease definitions, periodontal therapy adopted,
use of grafting procedures, and presence of smokers among
the patients. Contact with authors for possible missing data
was performed.
Implant failure and postoperative infection were the
dichotomous outcome measures evaluated. Weighted mean
differences were used to construct forest plots of marginal
bone loss, a continuous outcome. The statistical unit for the
outcomes was the implant. Whenever outcomes of interest
were not clearly stated, the data were not used for analysis.
The I2 statistic was used to express the percentage of the
total variation across studies due to heterogeneity, with 25%
corresponding to low heterogeneity, 50% to moderate and
75% to high. The inverse variance method was used for

1511

random-effects or fixed-effects model. Where statistically


significant (P < 0.10) heterogeneity is detected, a randomeffects model was used to assess the significance of
treatment effects. Where no statistically significant heterogeneity is found, analysis was performed using a fixedeffects model.13 The estimates of relative effect for
dichotomous outcomes were expressed in risk ratio (RR)
and in mean difference (MD) in millimetres for continuous
outcomes, both with a 95% confidence interval (CI). The
degree of statistical significance was considered P < 0.05.
Only if there were studies with similar comparisons
reporting the same outcome measures was meta-analysis
to be attempted. In the case where no events (or all events)
are observed in both groups the study provides no
information about relative probability of the event and is
automatically omitted from the meta-analysis. In this
(these) case(s), the term not estimable is shown under
the column of RR of the forest plot table. The software used
here automatically checks for problematic zero counts, and
adds a fixed value of 0.5 to all cells of study results tables
where the problems occur.
A funnel plot (plot of effect size vs. standard error) will be
drawn. Asymmetry of the funnel plot may indicate publication
bias and other biases related to sample size, although the
asymmetry may also represent a true relationship between
trial size and effect size.
The data were analyzed using the statistical software
Review Manager (version 5.2.11, The Nordic Cochrane
Centre, The Cochrane Collaboration, Copenhagen, Denmark,
2014).

3.

Results

3.1.

Literature search

The study selection process is summarized in Fig. 1. The


search strategy resulted in 2768 papers. Two combinations of
terms were used for PubMed and Web of Science, which
resulted in a number of 360 duplicates. The three reviewers
independently screened the abstracts for those articles related
to the focus question. The initial screening of titles
and abstracts resulted in 34 full-text papers; 2374 were
excluded for not being related to the topic. The full-text
reports of the remaining 34 articles led to the exclusion of 12
because they did not meet the inclusion criteria (6 did not
inform of the number of implants per group, 2 were not
evaluating implant failures, 2 had earlier follow-up of the
same study, 1 had the same study published in another
journal, 1 compared between patients with different types of
periodontitis and not between PCPs and PHPs). Additional
hand-searching of the reference lists of selected studies did
not yield additional papers. Thus, a total of 22 publications
were included in the review.

3.2.

Description of the studies

Detailed data of the 22 included studies are listed in Tables 1


and 2. Ten CCTs,2,1422 and twelve retrospective analyses5,8,2332 were included in the meta-analysis.

Study

Published

Study design

Patients (n)
(number per group)

Patients age range


(average) (years)

1996

RA (unicenter)

51 (31, G1; 20, G2)

1672 (32.9)

2000

RA (multicenter)

440 (147, G1; 293, G2)

1690 (53)

Polizzi et al. [14]

2000

CCT (multicenter)

143 (NM)

Watson et al. [15]

2000

CCT (unicenter)

26 (7, G1; 19, G2)

Hardt et al. [25]

2002

RA (unicenter)

50 (25, G1; 25, G2)

Karoussis et al. [16]

2003

CCT (unicenter)

Evian et al. [26]

2004

Rosenberg et al. [27]


Mengel and

Healing period/
loading

Failed/placed
implants (n)

Implant
failure
rate (%)

6 months (maxilla)
4 months (mandible)
6 months

5/62 (G1)
2/47 (G2)
39/375 (G1)
29/647 (G2)

8.06 (G1)
4.26 (G2)
10.40 (G1)
4.48 (G2)

14/98 (G1)
3/166 (G2)
0/7 (G1)
0/26 (G2)
8/100 (G1)
3/92 (G2)
2/21 (G1)

14.29 (G1)
1.81 (G2)
0 (G1)
0 (G2)
8 (G1)
3.26 (G2)
9.52 (G1)

3/91 (G2)
16/77 (G1)
6/72 (G2)
86/923 (G1)
37/588 (G2)
2/120 (G1a)

3.30 (G2)
20.78 (G1)
8.33 (G2)
9.32 (G1)
6.29 (G2)
1.67 (G1)

0/30 (G2)
10/122 (G1)
67/1803 (G2)

0 (G2)
8.20 (G1)
3.72 (G2)

1/41 (G1)
0/13 (G2)
17/68 (G1)

2.44 (G1)
0 (G2)
25 (G1)

0/2 (G2)
2/155 (G1b)
0/72 (G2)
16/252 (G1a)
8/261 (G2)
61/1171 (G1)

0 (G2)
1.29 (G1)
0 (G2)
6.35 (G1)
3.07 (G2)
5.21 (G1)

16/455 (G2)
204/5346 (G1c)
15/497 (G2)
4/40 (G1)
2/40 (G2)
5/34 (G1)
9/97 (G2)

3.52 (G2)
3.82 (G1)
3.02 (G2)
10 (G1)
5 (G2)
14.71 (G1)
9.28 (G2)

3/20 (G1)
1/20 (G2)
70/1512 (G1d)
23/747 (G2)
16/185 (G1b)
2/61 (G2)

15 (G1)
5 (G2)
4.63 (G1)
3.08 (G2)
8.65 (G1)
3.28 (G2)

6/198 (G1b)
0/54 (G2)

3.03 (G1)
0 (G2)

Antibiotics/
mouth rinse
(days)

Mean 30.5 months


(range 167)
7 years

10/NM

NM (47, females)
NM (40, males)
2263 (NM)

1, 3, and 5 years

NM

4 years

NM

6 months (maxilla)
34 months (mandible)
delayed

5 years

NM

NM

53 (8, G1; 45, G2)

NM (53.5, G1)
NM (57.3, G2)
NM

10 years

NM

46 months

RA (unicenter)

149 (77, G1; 72, G2)

NM

184030 days

NM

46 months

2004

RA (unicenter)

334 (151, G1; 183, G2)

13 years

710/28 days

59 months

2005

CCT (unicenter)

39 (27, G1a; 12, G2)

NM (61.1, G1)
NM (49.5, G2)
1959 (3234, G1; 31, G2)

3 years

NM

NM

Flores-de-Jacoby [17]
Wagenberg
and Froum [28]

2006

RA (unicenter)

891 (NM)

1494 (57.9)

Mean 71 months
(range 12193)

12/NM

Mengel et al. [18]

2007

CCT (unicenter)

17 (9, G1; 8, G2)

1959 (34, G1; 31, G2)

NM

Fardal and Linden [5]

2008

RA (multicenter)

16 (14, G1; 2, G2)

NM (48)

Every 3 months
over a 3-year period
Mean 13.4 years

Gatti et al. [19]

2008

CCT (multicenter)

62 (33, G1b; 29, G2)

De Boever et al. [20]

2009

CCT (unicenter)

194 (84, G1a; 110, G2)

3585 (56, G1)


1861 (40, G2)
2080 (53.8)

Anner et al. [29]

2010

RA (unicenter)

475 (311, G1; 164, G2)

NM (52)

(range 819)
5 years
Mean 46.8 (G1) and
48.1 months (G2)
Mean 30 months

NM
NM/14

6 months (maxilla)
3 months (mandible)
6 months (maxilla)
3 months (mandible)
(64 immediately loaded)
6 months (maxilla)
3 months (mandible)
NM

0/7

Ranging from immediate


to 11 months
5.9  2.1 months

NM

NM

(range 1114)
5 years

35/14

10 years

NM

Ranging from immediate


to 9 months
46 months

Gianserra et al. [30]

2010

RA (multicenter)

1477 (1281, G1c; 196, G2)

Matarasso et al. [8]

2010

RA (multicenter)

80 (40, G1; 40, G2)

1885 (5054, G1)


1785 (29.9, G2)
NM (46.548.1)

Simonis et al. [31]

2010

RA (unicenter)

55 (NM)

2988 (68.7)

1016 years

710/NM

34 months

Aglietta et al. [32]

2011

RA (multicenter)

40 (20, G1; 20, G2)

NM (51)

10 years

NM

46 months

Levin et al. [21]

2011

CCT (unicenter)

717 (434, G1d; 283, G2)

NM

2012

CCT (unicenter)

101 (73, G1b; 28, G2)

Mean 54 months
(up to 144 months)
10 years

NM

Roccuzzo et al. [2]

NM (54, G1)
NM (46, G2)
NM

NM

36 months

Roccuzzo et al. [22]

2014

CCT (unicenter)

123 (91, G1b; 32, G2)

NM (53, G1)
NM (43, G2)

10 years

NM

612 weeks

journal of dentistry 42 (2014) 15091527

Rosenquist and
Grenthe [23]
Brocard et al. [24]

Follow-up visits
(or range)

1512

Table 1 Detailed data of the included studies.

Study

Published

Study design

P value
(for failure
rate)

Postoperative
infection

P value (for
postoperative
infection)

Marginal
bone loss
(mean  SD) (mm)

Periodontal
therapy

Periodontal
disease
definitions

Implant surface
modification
(brand)

Rosenquist and
Grenthe [23]

1996

RA (unicenter)

NM

4 (G1)
1 (G2)

NM

NM

Turned
(Nobelpharma,
Nobelpharma AB,
Goteborg, Sweden

Extraction indication
had been
periodontitis

NM

Brocard
et al. [24]

2000

RA (multicenter)

NM

NM

NM

NM

TPS (hollow screws,


n = 464; solid
screws, n = 251;
hollow cylinders,
n = 307; ITI,
Straumann,

Prior to implant
placement, some
patients were treated
for periodontal
disease

Prior to implant
placement, the G1
patients were
treated for
periodontal disease.
This involved a

Waldenburg,
Switzerland)

Observations

All implants in
fresh extraction
sockets, use of
membranes in 5
patients
132 smokers, 66
bruxers, 177
sites with GBR

followed in some
cases by periodontal
surgery. All patients
were enrolled in a
periodontal
maintenance
programme with

Polizzi
et al. [14]

2000

CCT (multicenter)

NM

NM

NM

NM

Turned (Branemark,
Nobel Biocare AB,
Goteborg, Sweden)

Periodontitis cited as
a reason for tooth
extraction, history
of periodontitis before

regular professional
plaque control
NM

tooth extraction

Watson
et al. [15]

2000

CCT (unicenter)

NM

NM

NM

NM

Hydroxyapatitiecoated (Calcitek
omniloc, Carlsbad,

Chronic periodontitis:
pockets 4 mm and
radiographic bone

USA)

loss

NM

146 implants in
fresh extraction
sockets,
membranes
used in 64
implants, 8
grafts
Smokers were
included, but the
exact number

journal of dentistry 42 (2014) 15091527

hygienic phase
consisting of
scaling, root
planning, and oral
hygiene
instructions,

was not
informed, no
grafts, only
single-tooth
restorations

1513

1514

Table 1 (Continued )
Study

Hardt
et al. [25]

2002

2003

Study design

RA (unicenter)

CCT (unicenter)

P value
(for failure
rate)

Postoperative
infection

P value (for
postoperative
infection)

NM

NM

NM

NM

NM

NM

et al. [16]

Evian
et al. [26]

2004

RA (unicenter)

NM

NM

NM

Marginal
bone loss
(mean  SD) (mm)
2.2  0.8 (G1)
1.7  0.8 (G2)

Implant surface
modification
(brand)

Periodontal
disease
definitions

Turned (Branemark,
Nobel Biocare AB,
Goteborg, Sweden)

An overall descriptor
of the patients
experience of
periodontal
destruction before the
time of implant
therapy was
generated through
the calculation of an
age-related
periodontal bone loss
score
Patients having lost

Mesial, 1.00  1.38 (G1)

TPS (hollow screws,

0.48  1.10 (G2)


Distal, 0.94  0.73 (G1)
0.50  1.08 (G2)

ITI, Straumann,
Waldenburg,
Switzerland)

their teeth due to


chronic periodontitis

NM

? (Paragon, Zimmer
Dental, Carlsbad,
USA)

Periodontal disease
was diagnosed if
probing depths were
5 mm or greater and
associated with
radiographic signs of
bone loss. Patients
who exhibited 1 or
more teeth with
periodontal disease,
or who originally lost
their teeth as a result
of periodontitis, were
considered to have
periodontal disease

Periodontal
therapy

Observations

NM

Fixed partial
dentures in the
maxillary
posterior
segments, no
grafts

The patients had

28 implants

been treated for


periodontal disease
according to a
comprehensive
treatment strategy
prior to the
installation of

placed in 12
smokers (10 in
G1, 18 in G2) and
in 41 nonsmokers (11 in
G1, 73 in G2)

implants
Periodontal
treatment was
performed prior to
or in conjunction
with implant
placement

Only patients
who received a
single implant

journal of dentistry 42 (2014) 15091527

Karoussis

Published

Rosenberg
et al. [27]

2005

RA (unicenter)

CCT (unicenter)

NM

NM

NM

NM

NM

NM

NM

Turned (Branemark,
Nobel Biocare AB,
Goteborg, Sweden),
TPS and SLA (ITI,
Straumann,
Waldenburg,
Switzerland), TPS

Patients were
classified as
periodontally
compromised if they
had a history of
periodontal disease
that resulted in tooth

Prior to implant
placement, all
necessary
periodontal,
restorative, and
endodontic
treatment was

(IMZ, Biomet, Irvine,


USA) acid-etched
(Osseotite, 3i, Palm
Beach Gardens,
USA),
hydroxyapatite-

loss. Patients were


classified as
periodontally healthy
if tooth loss was not
caused by periodontal
disease and if no loss

completed,
including extraction
of hopeless teeth

coated (Swede-vent,
Screw-vent,
Corevent, Paragon,
Encino, USA)

of attachment (with
the exception of facial
or lingual recession)
or probing depth
greater than 34 mm
was present at the
time of implant

1 year, 0.83  0.71


(G1 GA)
0.68  0.54 (G1 GC)
0.58  0.45 (G2)
3 years, 0.31  0.22

Turned (Mk II
Branemark, Nobel
Biocare AB,
Goteborg, Sweden;
n = 83), acid-etched

(G1 GA)
0.18  0.11 (G1 GC)
0.12  0.08 (G2)

(Osseotite, 3i
Implant
Innovations, Palm
Beach Gardens,
USA; n = 67)

placement
The diagnosis of
generalized chronic
and aggressive
periodontitis was
based on the
American Academy of
Periodontology
criteria

All patients
underwent
periodontal surgery
and were entered
into a 3-month

No smokers

recall system, with


an oral hygiene
control with
motivation and
instruction where
necessary.
Subgingival scaling
with root planing
was performed at
tooth surfaces with
probing depths
>4 mm and
bleeding on probing

Wagenberg
and Froum
[28]

2006

RA (unicenter)

0.02

NM

NM

NM

Turned (Branemark,
Nobel Biocare AB,
Goteborg, Sweden,
n = 1398), acidetched (Osseotite, 3i
Implant
Innovations, Palm
Beach Gardens,
USA; n = 527)

Teeth were lost


because of
periodontal disease

All patients were


treated for their
periodontal disease
prior to or in
conjunction with
their implant
treatment

journal of dentistry 42 (2014) 15091527

Mengel and
Flores-deJacoby [17]

2004

All implants
placed in fresh
extraction
sockets, bone
grafts were
utilized in all
cases in which
there was a
residual space
around the
implant, 13
implants in
sinus-lifts, 323

1515

implants in
smokers

Study

Mengel
et al. [18]

Published

2007

Study design

CCT (unicenter)

P value
(for failure
rate)

Postoperative
infection

P value (for
postoperative
infection)

NM

NM

NM

Periodontal
therapy

Observations

Marginal
bone loss
(mean  SD) (mm)

Implant surface
modification
(brand)

Periodontal
disease
definitions

1 year, 1.02  0.89 (G1)


0.52  0.23 (G2)
3 years, 0.27  0.22 (G1)
0.19  0.23 (G2)

Acid-etched
(Osseotite, BIOMET/
3i, Palm Beach
Gardens, USA)

The diagnosis of
generalized
aggressive
periodontitis was
based on the

All generalized
aggressive
periodontitis
patients underwent
periodontal

Edentulous
patients. G1
patients were
fitted with
removable

American Academy of
Periodontology
criteria

treatment and were


entered into a 3month recall system

implant-tooth
supported
superstructures,
G2 patients
received either
fixed cemented

Fardal and
Linden [5]

Gatti et al. [19]

2008

2008

RA (multicenter)

CCT (multicenter)

NM

NM

5 (G1)
0 (G2)

4 (G1)
0 (G2)

NM

NM

NM

2.57  1.06 (G1 GA)


2.72  0.44 (G1 GC)
1.24  1.09 (G2)

NM

The term refractory


periodontal disease
has been applied to
such individuals who
are characterized by
continued

Patients received
initial periodontal
therapy, followed by
at least 8 years of
maintenance
treatment in the

Even though the


number of
smokers was
informed for the
whole sample of
the study, only

degeneration of the
periodontium despite
ongoing sanative,
surgical and/or
pharmacological
therapy

specialist practice

the patients who


received
implants were
considered here,
and the number
of smokers
among these

Several (Nobel
Biocare,
Gothenburg,
Sweden; Zimmer

The periodontal
conditions were
assessed using a
modification of the

At the first visit, the


periodontal
conditions were
assessed using a

Dental, Carlsbad,
USA; Mathys,
Bettlach,
Switzerland;
Straumann,
Waldenburg,
Switzerland;

Periodontal Screening
and Recording index

modification of the
Periodontal
Screening and
Recording index,
and subsequently
periodontal therapy

Dentsply Friadent,
Mannheim,
Germany)

patients was not


informed
39 implants in
grafts, 14
smokers (8 in G1,
6 in G2)

journal of dentistry 42 (2014) 15091527

implantsupported
dentures in the
maxilla or
single-tooth
implants. No
smokers.

1516

Table 1 (Continued )

De Boever
et al. [20]

Anner et al.

2009

2010

CCT (unicenter)

RA (unicenter)

NM

0.1498

NM

NM

NM

NM

Mesial, 0.28  0.7


(G1 + G2)
Distal, 0.24  0.6
(G1 + G2)

NM

TPS and SLA (ITI,


Straumann,
Waldenburg,
Switzerland; n = 259,
TPS; n = 254, SLA)

NM

Periodontally
susceptible patients
with tooth loss due to
periodontal disease
and patients with
periodontal disease

Before implant
placement, all
patients received, if
necessary,
periodontal nonsurgical and/or

11.4% of the
patients were
smokers (13
smokers in G1, 9
in G2), 10.3%
former smokers,
134 ridge
augmentations
(75, G1; 59, G2)

NM

surgical therapy.
Periodontally
susceptible patients
were enrolled in a
strict maintenance
programme
246 patients (51.7%)
participated of a
structured
supportive
periodontal
programme
Periodontal therapy

smokers

[29]

2010

RA (multicenter)

NM

NM

NM

NM

Several (3i Biomet,

Periodontal
conditions were
assessed using a
modification of the
Periodontal Screening
and Recording (PSR)
index
The classification of

(non-surgical and
surgical) was
administered as
required

in G1, 63 in G2)

Turned, 2.78  0.48 (G1)

Astra Tech, Camlog,


Friadent-Dentsply,
Nobel Biocare,
Straumann, Sweden
& Martina, Zimmer
Dental)
Turned (Branemark,

The patients

No smokers,

Nobel Biocare AB,


Goteborg, Sweden;
n = 40), TPS (ITI,
Straumann,
Waldenburg,
Switzerland; n = 40)

the patients in the


two groups was
carried out on the
basis of the diagnosis
reported in the
patients chart.

received
individualized
periodontal
treatment before
implant surgery. On
the basis of the

only dental
implants in a
single-unit gap

et al. [30]

Matarasso

2010

RA (multicenter)

NM

NM

NM

et al. [8]

1.95  0.42 (G2)


TPS, 2.32  0.41 (G1)
1.43  0.38 (G2)

549 smokers (486

results achieved
after the
periodontal
treatment, the
patients were
placed on an

Simonis
et al. [31]

2010

RA (unicenter)

0.327

13 (G1)
10 (G2)

0.006

Mesial, 2.2  3.4 (G1 + G2)


Distal, 2.3  3.4 (G1 + G2)

TPS (ITI,
Straumann,
Waldenburg,
Switzerland; solid
screw, n = 116;
hollow screw,
n = 15)

NM

individually tailored
maintenance care
programme
All patients were
instructed on how
to maintain
appropriate oral

journal of dentistry 42 (2014) 15091527

Gianserra

49 diabetics, 63

9 smokers, only
implantsupported fixed
restorations

hygiene around the


implants and
remaining teeth.

1517

1518

Table 1 (Continued )
Study

Aglietta
et al. [32]

Roccuzzo
et al. [2]

2011

2011

2012

Study design

RA (multicenter)

CCT (unicenter)

CCT (unicenter)

P value
(for failure
rate)

Postoperative
infection

P value (for
postoperative
infection)

NM

NM

NM

NM

NM

NM

NM

NM

NM

Marginal
bone loss
(mean  SD) (mm)
Turned, 3.47  1.09 (G1)
2.65  0.31 (G2)
TPS, 3.77  1.43 (G1)
2.51  0.31 (G2)

NM

0.98  1.22 (G1 severe)


1.14  1.11 (G1 moderate)
0.75  0.88 (G2)

Implant surface
modification
(brand)
Turned (Branemark,
Nobel Biocare AB,
Goteborg, Sweden;
n = 20), TPS (ITI,
Straumann,
Waldenburg,
Switzerland; n = 20)
NM

TPS (ITI,
Straumann,
Waldenburg,
Switzerland)

Periodontal
disease
definitions

Periodontal
therapy

Observations

Patients treated for


generalized chronic
periodontitis

Patients were
treated for
periodontitis

All patients were


smokers, only
dental implants
in a single-unit
gap

Patients were divided


into different
periodontal groups
according to their

All periodontally
involved patients
had undergone
cause-related as

81 diabetics, 103
smokers (71 in
G1, 32 in G2)

periodontal diagnosis
that was based on a
classification of
periodontal diseases

well as correctivephase periodontal


interventions (if
indicated) before
dental implant
placement

PCP received a score


(S) on the basis of the
number and depth of
periodontal pockets
according to the
following formula:
S = Number of

All patients received


appropriate initial
therapy, consisting,
depending on the
cases, in motivation,
oral hygiene
instruction and

pockets (57 mm) + 2


Number of pockets
(8 mm)

scaling and root


planing, with the aim
to reduce to a
minimal level
periodontal
pathogens. Hopeless
teeth were extracted.
Periodontal surgery
was performed as
needed. Guided
tissue regeneration
was pursued, when
feasible

18 smokers (15
in G1, 3 in G2)

journal of dentistry 42 (2014) 15091527

Levin
et al. [21]

Published

Roccuzzo
et al. [22]

2014

CCT (unicenter)

NM

NM

NM

NM

Sandblasted and
acid-etched (SLA,
Straumann,
Waldenburg,
Switzerland)

PCP received a score


(S) on the basis of the
number and depth of
periodontal pockets
according to the
following formula:

All patients received


appropriate initial
therapy, consisting,
depending on the
cases, in
motivation, oral

S = Number of
pockets (57 mm) + 2
Number of pockets
(8 mm)

hygiene instruction
and scaling and root
planing, with the
aim to reduce to a
minimal level
periodontal
pathogens.

21 smokers (16
in G1, 5 in G2)

was pursued, when


feasible
NM not mentioned; CCT controlled clinical trial; RCT randomized controlled trial; RA retrospective analysis; G1 group periodontitis; G2 group non- periodontitis; NP not performed; TPS titanium plasma-sprayed; GBR
guided bone regeneration; GA aggressive periodontitis group; GC chronic periodontitis group.
a
Here the implants and the patients with chronic adult periodontitis and generalized aggressive periodontitis were put together in G1.
b

Here the implants and the patients with severe chronic periodontitis and moderate chronic periodontitis were put together in G1.
Here the number of patients and implants were considered for the patients followed for 5 years. The implants and the patients with severe periodontitis (569 patients, 2938 implants, 130 failures) and moderate periodontitis (712
patients, 2408 implants, 74 failures) at the 5-year follow-up were put together in G1. The numbers at baseline were different (1727 patients; 1469, G1, 258, G2), (severe periodontitis: 630 patients, 3260 implants, 130 failures; moderate
periodontitis: 839 patients, 2813 implants, 74 failures).
d
Here the implants and the patients with severe chronic periodontitis and moderate chronic periodontitis were put together in G1.
c

journal of dentistry 42 (2014) 15091527

Hopeless teeth were


extracted.
Periodontal surgery
was performed as
needed. Guided
tissue regeneration

1519

1520

journal of dentistry 42 (2014) 15091527

Fig. 1 Study screening process.

Three studies17,18,23 had a follow-up up to 3 years, one15 of 4


years, whereas 18 studies2,5,8,14,16,1922,2432 had a maximum
follow-up of at least 5 years. From the studies with available
data of patients age, four23,24,28,30 included non-adults
patients. Three studies2,16,26 did not inform of the patients
age. Only four studies5,19,23,31 provided information about
postoperative infection, with 37 occurrences in a total of 184
patients receiving 537 implants. Some patients in thirteen
studies2,5,15,16,1922,24,2831 were smokers, whereas in one
study32 all patients were smokers, and three studies8,17,18
excluded smokers. One study14 inserted part of the implants in
fresh extraction sockets, whereas in the other two23,28 all
implants were inserted in fresh extraction sockets. Three
studies8,26,32 included only patients who received a single
implant. Patients were submitted to grafting procedures at the
implant site in 5 studies.14,19,20,24,28 One study18 included only
edentulous patients, and one25 inserted implants in the
maxillary posterior segments only. Any kind of periodontal
treatment previous to the implants insertion or a SPT was not
mentioned to be performed in four studies.14,15,23,25
Seven studies2,17,1922,30 included a comparison between
periodontitis of different severities. From the 22 studies
comparing PHPs and PCPs, a total of 10,927 dental implants
were inserted in PCPs, with 587 failures (5.37%), and 5881
implants were inserted in PHPs, with 226 failures (3.84%).
There were no implant failures in one study.15 From the 7
studies2,17,1922,30 comparing periodontitis of different severities, a total of 4460 dental implants were inserted in
patients with a more aggressive type of periodontitis, with

210 failures (4.71%), and 3308 implants were inserted in


patients with a less aggressive type of periodontitis, with 106
failures (3.20%). The inherent problem in a meta-analysis
such as in the present paper is that although some authors
see a difference between periodontitis and aggressive or
chronic periodontitis, others have not split the material in
this manner. Therefore, comparisons are difficult and we
will treat periodontitis as one entity in the remaining part of
the paper.
The most commonly used implants were the titanium
plasma-sprayed from Straumann (Straumann, Waldenburg,
Switzerland), in nine studies,2,8,16,19,20,24,27,31,32 and the Branemark (Nobel Biocare AB, Goteborg, Sweden), in eight studies.8,14,17,19,25,27,28,32 The latter was not exclusively used in six
studies.8,17,19,27,28,32 Three studies5,21,29 did not inform what
kind of implants were used. Three studies28,29,31 informed
whether there was a statistically significant difference or not
between the implant failure rates between the PCPs and PHPs,
and only one28 found a statistical significance favouring PHPs.
Six studies20,23,27,28,30,31 provided information about the use of
prophylactic antibiotics. In one of them,20 it was informed that
antibiotics were not prescribed to any patient. Four studies19,20,27,30 provided information about the use of chlorhexidine mouth rinse by the patients.

3.3.

Quality assessment

All studies except one23 were high quality. The scores are
summarized in Table 2.

Table 2 Quality assessment of the studies by the Newcastle-Ottawa scale.


Study

Published

Selection
Representativeness
of the exposed
cohort

Selection of
external
control

Comparability

Ascertainment
of exposure

Outcome of
interest not
present at
start

Comparability of
cohorts

Rosenquist and
Grenthe [23]
Brocard et al. [24]
Polizzi et al. [14]
Watson et al. [15]
Hardt et al. [25]
Karoussis et al. [16]
Evian et al. [26]
Rosenberg et al. [27]
Mengel and
Flores-de-Jacoby [17]
Wagenberg and
Froum [28]
Mengel et al. [18]
Fardal and Linden [5]
Gatti et al. [19]
De Boever et al. [20]
Anner et al. [29]
Gianserra et al. [30]
Matarasso et al. [8]
Simonis et al. [31]
Aglietta et al. [32]
Levin et al. [21]
Roccuzzo et al. [2]
Roccuzzo et al. [22]

Assessment
of outcome

Follow-up
long
enougha

Total
(9/9)
Adequacy of
follow-up

Additional
factor

1996

5/9

2000
2000
2000
2002
2003
2004
2004
2005

$
0
$
0
$
0
$
$

$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$

$
$
0
0
0
$
$
0

$
$
$
$
$
$
$
$

$
$
0
$
$
$
$
0

0
0
$
$
0
0
0
0

8/9
7/9
7/9
7/9
7/9
7/9
8/9
6/9

2006

7/9

2007
2008
2008
2009
2010
2010
2010
2010
2011
2011
2012
2014

0
$
$
0
$
$
$
$
$
$
0
0

$
$
$
$
$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$
$
$
$
$

$
$
$
$
$
$
$
$
$
$
$
$

0
0
0
$
$
0
$
0
$
$
0
0

$
$
$
$
$
$
$
$
$
$
$
$

0
$
$
0
0
$
$
$
$
0
$
$

$
0
$
0
0
$
$
0
$
0
$
0

6/9
7/9
8/9
6/9
7/9
8/9
9/9
7/9
9/9
7/9
7/9
6/9

journal of dentistry 42 (2014) 15091527

Main
factor

Outcome

a
Five years was chosen to be enough for the outcome implant failure to occur. This time point was chosen due to the fact that Roccuzzo et al.2 showed that the difference between PHP and PCP is
negligible during the first 5 years, but becomes more pronounced later on, being in accordance with the findings of Karoussis et al.,16 who first demonstrated that a 5-year follow-up is usually not
sufficient to evaluate the differences in the clinical outcomes of the various groups of patients.

1521

1522

journal of dentistry 42 (2014) 15091527

Fig. 2 Forest plot for the event implant failure in the comparison between periodontally compromised vs. periodontally
healthy patients.

3.4.

Meta-analysis

In this study, a fixed-effects model was used to evaluate the


implant failure in the comparison between PCPs vs. PHPs,
since statistically significant heterogeneity was not found
(P = 0.87; I2 = 0%). The insertion of dental implants in PCPs or
PHPs statistically affected the implant failure rates
(P < 0.00001; Fig. 2), in favour of PHPs. A RR of 1.78 (95% CI
1.502.11) implies that failures when implants are inserted in
PCPs are 1.78 times likely to happen than failures when
implants are inserted in PHPs.
Since the effect size could differ depending on the research
methodology of the studies, a sensitivity analysis was
performed. When only the CCTs were pooled, a RR of 1.97
resulted (95% CI 1.382.80; heterogeneity: P = 0.53; I2 = 0%;
Fig. 3), also statistically affecting the implant failure rates
(P = 0.0002). Given the variability of the included studies
(varying lengths of follow-up, patient ages, number of
implants, classification of severity of periodontitis etc.), the

analysis was also performed with a random-effects model.


When all studies were evaluated or when only the CCTs were
pooled, the significance of the treatment effect was the same
as when the fixed-effects model was used, with the exact same
values for the RR and the 95% CI.
Only four studies5,19,23,31 provided information about
postoperative infection. A fixed-effects model was used, due
to lack of statistically significant heterogeneity (P = 0.54;
I2 = 0%). The insertion of dental implants in PCPs or PHPs
statistically affected the incidence of postoperative infections
(P = 0.0004; Fig. 4), in favour of PHPs. A RR of 3.24 (95% CI 1.69
6.21) was observed. When the analysis was performed with a
random-effects model, the values for RR and 95% CI remained
the same, as well as the significance of the treatment effect.
Five studies8,16,18,25,32 provided information about the
marginal bone loss with standard deviation, necessary for
the calculation of comparisons in continuous outcomes,
comparing PCPs and PHPs (212 implants in PCPs and 269
implants in PHPs; Fig. 5). A random-effects model was used to

Fig. 3 Forest plot for the event implant failure in the comparison between periodontally compromised vs. periodontally
healthy patients, when only the CCTs were pooled.

journal of dentistry 42 (2014) 15091527

1523

Fig. 4 Forest plot for the event postoperative infection in the comparison between periodontally compromised vs.
periodontally healthy patients.

Fig. 5 Forest plot for the event marginal bone loss comparing PCPs and PHPs. 1y 1 year; 3y 3 years; turned turned
implants; TPS titanium plasma-sprayed implants.

evaluate the marginal bone loss, since statistically significant


heterogeneity was found (P < 0.00001; I2 = 88%). There was
statistically significant difference (MD 0.60, 95% CI 0.330.87;
P < 0.0001) between the groups concerning the marginal bone
loss, favouring PHPs.

3.5.

Publication bias

The funnel plot showed asymmetry when the studies


reporting the outcome implant failure in the comparison
between PCPs vs. PHPs are analyzed, indicating possible
presence of publication bias. Seven studies2,8,14,16,23,25,32
collaborated with the asymmetry (Fig. 6), and showed a wide
CI range for RR. The study of Polizzi et al.14 was the only one
outside the triangular 95% confidence region, showing a very

Fig. 6 Funnel plot for the studies reporting the outcome


event implant failure.

high value of RR together with a wide CI range (7.90, CI 95%,


2.3326.82), showing heterogeneity in comparison with the
other studies. When only the CCTs were pooled (Fig. 7), a
possible presence of publication bias is still indicated.

4.

Discussion

Narrowing the inclusion criteria of studies increases homogeneity but also excludes the results of more trials and thus risks
the exclusion of significant data.33 The issue is important
because meta-analyses are frequently conducted on a limited
number of RCTs. In meta-analyses such as these, adding more
information from observational studies may aid in clinical
reasoning and establish a more solid foundation for causal
inferences.33 However, potential biases are likely to be greater
for non-randomized studies compared with RCTs, so results
should always be interpreted with caution when they are
included in reviews and meta-analyses.34 The search strategy
adopted here did not find any randomized study on the
subject. Thus, the results must be interpreted carefully.
The statistical heterogeneity stands for the variability in
the intervention effects being evaluated in the different
studies, and is a consequence of clinical or methodological
diversity, or both, among the studies. The low level of
heterogeneity observed when the outcomes implant failure
and postoperative infection were analyzed is surprising,
given the variability of the included studies (varying lengths of
follow-up, patient ages, number of implants, classification of
severity of periodontitis etc.). For this reason, a randomeffects model was also used to incorporate heterogeneity
among studies, resulting in the same significance of the
treatment effects. However, it is important to stress that care

1524

journal of dentistry 42 (2014) 15091527

Fig. 7 Funnel plot for the studies reporting the outcome


event implant failure, when only the CCTs were pooled.

must be taken in the interpretation of the chi-squared test,


since it has low power in the (common) situation of a metaanalysis when studies have small sample size or are few in
number. This means that while a statistically significant result
may indicate a problem with heterogeneity, a non-significant
result must not be taken as evidence of no heterogeneity.34
Some argue that, since clinical and methodological diversity
always occur in a meta-analysis, statistical heterogeneity is
inevitable.35 Thus, the test for heterogeneity is irrelevant to
the choice of analysis; heterogeneity will always exist whether
or not we happen to be able to detect it using a statistical test.35
The present meta-analysis showed that, regardless of how
the studies were pooled, either when the retrospective studies
and the CCTs were considered together, or when only the
CCTs were considered, there was a statistically significant
difference between PCPs and PHPs for the outcome implant
failure, in favour of PHPs. In patients in whom teeth were lost
for periodontal reasons, the disease may have decreased the
available bone following tooth extraction or resulted in the
necessity to place the implant with a more exposed surface to
achieve ideal prosthetic position. Both of these situations may
have resulted in a greater implant failure rate.28
Here it is important to mention the possible high influence
of smoking habits on the implants failure rates. Smokers were
included in 14 studies here reviewed, and the smoking habit is
considered a confounding factor in the present meta-analysis.
Tobacco smoking is considered the principal environmental
risk factor affecting the pathogenesis of periodontitis but it is
also responsible for a great number of other types of disease.
Karoussis et al.16 showed in their study that there was a
tendency for a poorer survival rate of implants in smokers vs.
nonsmokers in patients with a history of periodontitis,
indicating that the smoking patient susceptible to periodontitis yields a documented higher risk for implant loss than the
non-smoking periodontitis patient or the patient not susceptible to periodontitis at all. Aglietta et al.32 showed that tobacco
smokers with a history of treated periodontitis displayed
lower implant survival rates and higher marginal bone loss
rates compared with smokers PHPs, independent of other
factors such as implant type, healing modality and operator,
and despite the fact that smokers PCPs were treated for their

periodontal conditions before implant placement and were


regularly enrolled in a SPT.
When marginal bone loss was analyzed, there was a
statistically significant difference between PCPs and PHP,
favouring PHPs. Hardt et al.25 observed that the amount of
longitudinal peri-implant bone loss is related to pretreatment
experience of loss of periodontal bone support. The exact
relationship between periodontitis and peri-implantitis
remains unknown; we really do not know whether these
two types of disease are similar in origin at all since a
demonstrated positive correlation between PCP and implant
failure in itself does not prove such a connection. In some
studies PCPs demonstrated higher implant failure rates but
this difference did not reach statistical significance. Obviously,
treatment of periodontal infections before implant placement
would seem important to avoid placing an implant in an
infected bed. It is important to stress here that heterogeneity
was identified among the group of studies reporting marginal
bone loss. Thus, conclusions should be interpreted with
caution and the analysis can at best lead to the generation of
hypotheses.
The fact that some of these studies reviewed here have a
short follow-up is a confounding factor, even though it is hard
to define what would be considered a short follow-up period to
evaluate implant failures in PCPs. A longer follow-up period
can lead to an increase in the failure rate, especially if it is
extended beyond functional loading, because other prosthetic
factors can influence implant failure from that point onward.
This might have led to an underestimation of actual failures in
some studies. Analysis of the data disclosed different patterns
regarding the distribution of the implant losses over time in
the two categories of patients. Rosenberg et al.27 hypothesized
that one possible explanation for the difference between the
two groups in this pattern of failure is the influence of the host,
which plays an important role in the variable inflammatory
process and may be significant in patients with a history of
periodontal disease. Another possible explanation could be
related to local factors. A reduced quantity of hard tissue in the
PCP group may be related to periodontal loss prior to tooth
extraction.27
Another confounding factor is the fact that the studies used
different definitions for the presence of periodontal disease,
depending on the threshold chosen for the definition of
periodontitis, or which conjunct of characteristics may be
considered a periodontal disease, i.e., the diagnostic criteria
are less clear. Thus, a clear classification system needs to be
implemented with clinical evaluation related to a more
specific pathology. Moreover, the outcome measures were
not related to the type of periodontitis in every study. When it
was reported, there was a statistically significant difference
concerning the implant failure rates, favouring the less
aggressive type of periodontitis in comparison with the more
aggressive.
Numerous implants in some studies26 were placed at the
same time as periodontal surgical procedures were being
carried out. The influence of this co-therapy on implant
contamination during the procedure has not been investigated. At the immediate and early implant placement it can be
speculated that periodontitis-affected tissues might have had
a negative local influence due to the presence of infrabony

journal of dentistry 42 (2014) 15091527

defects; this could increase the gap between bone and


implant36 or jeopardize achievement of primary stability.37
It is unknown whether textured implant surfaces may be
more vulnerable to infection than machined implant surfaces
in patients with past or present periodontal disease.26 Some
studies presented higher failure rates in PCPs when using TPS
implants. The moderate micro-roughness of most modern
implants did not seem coupled to more than 12% of periimplantitis when followed up for 10 years or more as indicated
in a recent review of ten different long term clinical reports of
Tioblast, SLA and TiUnite implants.38 Titanium with different
surface modifications shows a wide range of chemical,
physical properties, and surface topographies or morphologies, depending on how they are prepared and handled,3941
and it is not clear whether, in general, one surface modification is better than another.42
Another possible limitation of some studies is that
implants were not tested for stability during some of the late
follow-up visits since many of the prostheses could not be
removed because they were permanently cemented. This
might have led to an underestimation of actual failures.43
Differences in prosthetic suprastructures including completely or partially edentulous patients in the same study are
variables that must also be taken into account. The small
number of patients in some studies5,15,17,18,32 also counts as a
limitation. Moreover, groups were not completely comparable
at baseline in some cases.5,16,17,29,30 The potentially most
relevant differences were in terms of age and number of
implants/prosthesis. The differences in age and number of
implants could have plausible explanations, such as different
patterns of tooth loss among groups.19 Patients with a
previous history of periodontitis are likely to have lost more
teeth because of periodontal disease, and therefore require
more implants, whereas the healthy group usually includes
patients who had lost teeth through trauma or were affected
by tooth agenesia, and therefore they were likely to be younger
and require fewer implants.19
The results of the present study have to be interpreted with
caution because of its limitations. First of all, all confounding
factors may have affected the long-term outcomes and not
just the presence or not of periodontal disease, and the impact
of these variables on the implant survival rate, postoperative
infection and marginal bone loss is difficult to estimate if these
factors are not identified separately between the two different
procedures in order to perform a meta-regression analysis.
The lack of control of the confounding factors limited the
potential to draw robust conclusions. Second, due to the
retrospective design of some studies the classification of the
patients with respect to their experience of periodontal
disease could be based only on preoperative radiographic
data describing the amount of bone support at remaining
teeth, since clinical data regarding the periodontal conditions
at time for implant therapy or at subsequent follow-ups are
not retrievable.4446 Third, there are no RCTs in the analysis,
and potential biases are likely to be greater for non-randomized studies compared with RCTs.
The authors suggest that more research is needed on the
history of bone tissue loss prior to implant placement in
patients classified as periodontally compromised to evaluate the local factors affecting implant failure in these patients.

1525

Due to the multifaceted aspects of any infectious disease such


as periodontitis, any correlations between this disease and
peri-implantitis need not necessarily indicate that bone loss
around teeth and implants is dependent on the same type of
disease.

5.

Conclusion

The results of the present systematic review should be


interpreted with caution due to the presence of uncontrolled
confounding factors in the included studies, none of them
randomized. Within the limitations of the existing investigations, the present study suggests that an increased susceptibility for periodontitis may also translate to an increased
susceptibility for implant loss, loss of supporting bone, and
postoperative infection.

Acknowledgements
This work was supported by CNPq, Conselho Nacional de
Desenvolvimento Cientfico e Tecnologico Brazil. We would
like to thank Dr. Ricardo Trindade.

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