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Yasmin Alsabagh

5th Year, Group 12

THE OUTCOME OF IMPLANTS IN PATIENTS WITH

PREVIOUS PERIODONTAL DISEASE: A SYSTEMATIC

LITERATURE REVIEW

Master’s Thesis

Supervisor

Dr. Povilas Daugela

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2

FINAL MASTER‘S THESIS IS CONDUCTED

AT THE DEPARTMENT OF ORAL AND MAXILLOFACIAL SURGERY

STATEMENT OF THESIS ORIGINALITY

I confirm that the submitted Final Master‘s Thesis: "The Outcome of Implants In Patients with Previous Periodontal Disease. A Systematic Literature Review"

1. Is done by myself.

2. Has not been used at another university in Lithuania or abroad.

3. I did not use any additional sources that are not listed in the Thesis, and I provide a complete list of references.

I confirm by e-mail, and the work will be signed after the end of the quarantine and emergency situation due to the COVID-19 pandemic in the republic of Lithuania.

Yasmin Alsabagh

(date) (author‘s full name) (signature)

CONCLUSION OF FINAL MASTER‘S THESIS ACADEMIC SUPERVISOR

ON THE DEFENSE OF THE THESIS

I confirm by e-mail, and the work will be signed after the end of the quarantine and emergency

situation due to the COVID-19 pandemic in the republic of Lithuania.

Povilas Daugela

(date) (author‘s full name) (signature)

FINAL MASTER‘S THESIS IS APPROVED AT THE DEPARTMENT

I confirm by e-mail, and the work will be signed after the end of the quarantine and emergency situation due to the COVID-19 pandemic in the republic of Lithuania.

Department of Oral and Maxillofacial Surgery

(date of approval) (name of the Department and full name of the Head of the Department) (signature)

Final Master‘s Thesis reviewer

I confirm by e-mail, and the work will be signed after the end of the quarantine and emergency situation due to the COVID-19 pandemic in the republic of Lithuania.

(full name) (signature)

Evaluation of Final Master‘s Thesis Defense Board:

I confirm by e-mail, and the work will be signed after the end of the quarantine and emergency situation due to the COVID-19 pandemic in the republic of Lithuania.

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3 LITHUANIAN UNIVERSITY OF HEALTH SCIENCES

MEDICAL ACADEMY FACULTY OF ODONTOLOGY

DEPARTMENT OF ORAL AND MAXILLOFACIAL SURGERY

THE OUTCOME OF IMPLANTS IN PATIENTS WITH PREVIOUS PERIODONTAL DISEASE: A SYSTEMATIC LITERATURE REVIEW

Master’s Thesis

The thesis was done

By student ……… Supervisor………

(signature) (signature)

………. …..………

(name, surname, year, group) (degree, name, surname)

…………...………20….… ……...…………20…...

(day/month) (day/month)

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4

EVALUATION TABLE OF THE MASTER’S THESIS

OF THE TYPE OF SYSTEMIC REVIEW OF SCIENTIFIC LITERATURE Evaluation: ... Reviewer: ...

(scientific degree, name and surname) Reviewing date: ...

No .

MT parts MT evaluation points

Compliance with MT requirements and evaluation Yes Partially No 1 Summary (0.5 points)

Is summary informative and in compliance with the thesis content and requirements?

0.3 0.1 0

2 Are the keywords in compliance with the

thesis essence? 0.2 0.1 0 3 Introduction , aim and tasks (1 point)

Are the novelty, relevance and significance of the work justified in the introduction of the thesis?

0.4 0.2 0

4 Are the problem, hypothesis, aim and tasks

formed clearly and properly?

0.4 0.2 0

5 Are the aim and tasks interrelated? 0.2 0.1 0

6 Selection criteria of the studies, search methods and strategy (3.4 points)

Is the protocol of systemic review present? 0.6 0.3 0

7 Were the eligibility criteria of articles for

the selected protocol determined (e.g., year, language, publication, condition, etc.)

0.4 0.2 0

8 Are all the information sources (databases

with dates of coverage, contact with study authors to identify additional studies) describes and is the last search day indicated?

0.4 0.1 0

9 Is the electronic search strategy described

in such a way that it could be repeated (year of search, the last search day; keywords and their combinations; number of found and selected articles according to the combinations of keywords)?

0.2 0.1 0

10 Is the selection process of studies

(screening, eligibility, included in systemic review or, if applicable, included in the meta-analysis) described?

0.4 0.2 0

11 Is the data extraction method from the

articles (types of investigations, participants, interventions, analysed factors, indexes) described?

0.4 0.2 0

12 Are all the variables (for which data were

sought and any assumptions and

simplifications made) listed and defined?

0.4 0.2 0

13 Are the methods, which were used to

evaluate the risk of bias of individual

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5 studies and how this information is to be

used in data synthesis, described?

14 Were the principal summary measures

(risk ratio, difference in means) stated?

0.4 0.2 0 15 Systemiza- tion and analysis of data (2.2 points)

Is the number of studies screened: included upon assessment for eligibility and

excluded upon giving the reasons in each stage of exclusion presented?

0.6 0.3 0

16 Are the characteristics of studies presented

in the included articles, according to which the data were extracted (e.g., study size, follow-up period, type of respondents) presented?

0.6 0.3 0

17 Are the evaluations of beneficial or

harmful outcomes for each study presented? (a) simple summary data for each intervention group; b) effect estimates and confidence intervals)

0.4 0.2 0

18 Are the extracted and systemized data from

studies presented in the tables according to individual tasks?

0.6 0.3 0

19 Discussion (1.4 points)

Are the main findings summarized and is their relevance indicated?

0.4 0.2 0

20 Are the limitations of the performed

systemic review discussed?

0.4 0.2 0

21 Does author present the interpretation of

the results?

0.4 0.2 0

22 Conclusions (0.5 points)

Do the conclusions reflect the topic, aim and tasks of the Master’s thesis?

0.2 0.1 0

23 Are the conclusions based on the analysed

material?

0.2 0.1 0

24 Are the conclusions clear and laconic? 0.1 0.1 0

25 References (1 point)

Is the references list formed according to the requirements?

0.4 0.2 0

26 Are the links of the references to the text

correct?

Are the literature sources cited correctly and precisely?

0.2 0.1 0

27 Is the scientific level of references suitable

for Master’s thesis?

0.2 0.1 0

28 Do the cited sources not older than 10

years old form at least 70% of sources, and the not older than 5 years – at least 40%?

0.2 0.1 0

Additional sections, which may increase the collected number of points

29 Annexes Do the presented annexes help to understand the analysed topic?

+0.2 +0.1 0

30 Practical recommen- dations

Are the practical recommendations suggested and are they related to the received results?

+0.4 +0.2 0

31 Were additional methods of data analysis

and their results used and described

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6 (sensitivity analyses, meta-regression)?

32 Was meta-analysis applied? Are the

selected statistical methods indicated? Are the results of each meta-analysis

presented?

+2 +1 0

General requirements, non-compliance with which reduce the number of points

33 General require- ments

Is the thesis volume sufficient (excluding annexes)? 15-20 pages (-2 points) <15pag es (-5points )

34 Is the thesis volume increased artificially? -0.2

point

-1 point

35 Does the thesis structure satisfy the

requirements of Master’s thesis?

-1 point -2 points

36 Is the thesis written in correctlanguage,

scientifically, logically andlaconically?

-0.5 point

1 points

37 Are there any grammatical, styleor

computer literacy-related mistakes?

-0.2 point

-1 points

38 Is text consistent, integral, and are the

volumes of its structural parts balanced?

-0.2 point

-0.5 points

39 Amount of plagiarism in the thesis. >20% (not evaluated)

40 Is the content (names of sections and sub-

sections and enumeration of pages) in compliance with the thesis structure and aims?

-0.2 point

-0.5 points

41 Are the names of the thesis parts in

compliance with the text? Are the titles of sections and sub-sections distinguished logically and correctly?

-0.2 point

-0.5 points

42 Are there explanations of the key terms

and abbreviations (if needed)?

-0.2 point

-0.5 points

43 Is the quality of the thesis typography

(quality of printing, visual aids, binding) good?

-0.2 point

-0.5 points

*In total (maximum 10 points): *Remark: the amount of collected points may exceed 10 points.

Reviewer’s comments: ___________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ _________________________________________ ___________________________

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7

TABLE OF CONTENTS

SUMMARY ... 8

INTRODUCTION ... 9

SEARCH METHODS AND STRATEGY ... 12

Protocol ... 12

Focused question ... 12

Types of publications ... 12

Population ... 13

Literature search strategy ... 13

Inclusion criteria ... 13

Exclusion criteria ... 13

Risk of bias assessment ... 14

SYSTEMIZATION AND ANALYSIS OF DATA... 16

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8 THE OUTCOME OF IMPLANTS IN PATIENTS WITH PREVIOUS PERIODONTAL DISEASE:

A SYSTEMATIC LITERATURE REVIEW

SUMMARY

Objective: The aim of this systematic review was to assess the survival rate of dental implants

placed in patients that have a history of treated periodontal disease and to further evaluate whether a history of periodontal disease increases the risk of having complications after implant placement, such as peri-implant diseases.

Materials and Methods: Electronic databases were used to search (PubMed, Cochrane, Science

Direct) and to identify articles concerning dental implant placement in patients with previous periodontal disease. After selection of the studies, 8 studies were included in this systematic review. The search of articles on the electronic databases was restricted to articles in the English language and articles published in the last 10 years (January 2010 to February 2020).

Results: The results of studies reviewed in this thesis showed that is no negative effect on the

survival of dental implants, however they did show a higher risk of peri-implant diseases in patients with a history of periodontal disease compared to patients without a history of periodontal disease.

Conclusion: Regardless of the limitations of the systematic review, there is no substantial evidence

that a history of periodontal disease may be a risk factor for dental implant failure, however a number of studies showed that there is a correlation between a history of periodontal disease and peri-implant disease. Further research and studies are needed to be able to establish whether or not a history of periodontal disease negatively affects the outcome of the placement of dental implants.

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9

INTRODUCTION

Periodontal disease is a multifactoral disease; it is biologically complex in its pathogenesis action and its associated specific bacteria (primary etiologic factor). Bacteria, in the form of plaque and their products, lead to the loss of periodontal support tissues when faced with a susceptible host [1]. Periodontitis is a bacterially induced chronic inflammatory disease affecting the periodontium surrounding and supporting the teeth [5]. Periodontal disease accounts for the majority of tooth extraction in patients older than 40 years [6]. In this review, the main forms of periodontitis used to compare the survival of implants with healthy patients without a history of periodontitis, was chronic periodontitis and aggressive periodontitis, following the classification of Armitage in 1999 (Table 1) [2], with an exception of 2 studies that follow the new classification of periodontal diseases.

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10 World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions confirmed the current classification of periodontal diseases (Table 2) [3]. The different forms of periodontitis from the newest classification can be seen in (Table 3) [4].

Table 2. Classification of periodontal and peri-implant diseases and conditions 2017. [3]

Table 3. Framework for staging and grading of periodontitis. [4]

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11 involve the adjacent teeth. The generalized form of aggressive periodontitis involves most or all of the permanent teeth [8].

The use of dental implants are commonly used in patients with a history periodontal disease as tooth loss often occurs in advanced periodontitis. Therefore, it is necessary to ensure that there will be no negative side effects after the placement of dental implants.

Dental implants are used to restore missing teeth or periodontally compromised teeth. For dental specialists, it is crucial to know what the correlation between long-term implant survival rate and history of periodontitis is and if there are safe, reliable implant designs which can be used in these particular clinical cases [9].

Even after the treatment of periodontal disease, there can be some situations and risk factors, such as extensive bone loss, that can affect implant placement into alveolar bone negatively and can be the causative factor for the development of peri-implant disease.

Peri-implantitis is a site-specific infectious peri-implant disease that causes an inflammatory process in soft tissues, and bone loss around an osseointegrated implant in function. The etiology of the implant infection is conditioned by the status of the tissue surrounding the implant, implant design, degree of roughness, external morphology, and excessive mechanical load [10]. Certain clinical outcomes shall be observed in progression of peri-implantitis: marginal bone loss, clinical attachment level loss, increasing probing depth, bleeding on probing, microbiologically detected periodontal pathogens and implant loss. Peri‐implant mucositis is an inflammatory lesion of the soft tissues surrounding an endosseous implant in the absence of loss of supporting bone or continuing marginal bone loss [11].

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12

SEARCH METHODS AND STRATEGY

Protocol

This systematic review was made abiding the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) flowchart [12].Approval by the local bioethics committee was granted (No. BEC-OF(U)-119).

The literature that was found was analyzed and screened in order to decide, which studies are relevant to be included in the literature review.

Focused question

The focused question applied in this study was as following: "Does the history of periodontal disease in a patient have a negative influence on the outcome of dental implants placed in the previously affected alveolar bone?"

The question was decided in a manner conforming with the Patient, Intervention, Comparison and Outcome (PICO) format.

Population/Problem/Patient: Patients who have a history of periodontal diseases and plan to have implant placement.

Intervention/Indicator: Implant placement in patients with a history of periodontal disease. Comparison: Implant placement in patients without a history of periodontal disease. Outcome: Implant failure, peri-implantitis, marginal bone loss.

Types of publications

Retrospective studies, prospective cohort studies, longitudinal studies, short-term studies and pilot studies, that were performed on humans and published in the English language, were included in this systematic review.

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13

Population

Studies that were assessed and included were studies that involved human patients whom have had a history of periodontal disease and patients who have no history of periodontal disease/are periodontally healthy.

Literature search strategy

Articles were searched and included in this systematic review which had information concerning the outcome of dental implants in patients with a history of periodontal disease in accordance to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) flowchart guidelines [12]. The search was carried out an electronic search using Cochrane, Medline (PubMed) and ScienceDirect online databases.

The keywords used with their combinations in the search were: dental implants, periodontal disease, peri-implantitis AND outcomes. The studies included in this systematic review were in the English language, studies that were performed on only humans and publications that are dated from January 1st 2010 to February 14th 2020.

Inclusion criteria

1. Controlled and non-controlled, retrospective clinical studies, prospective clinical studies. 2. Studies that were performed on only humans.

3. Publications written in the English language.

4. Studies published from January 1st 2010 to February 14th 2020.

5. Studies that include a minimum of 5 human subjects/patients with treated periodontitis undergoing implant therapy.

6. Studies that have a follow-up period of at least 1 year after the placement of the dental implants.

Exclusion criteria

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14 2. Publications that are not in the English language.

3. Systematic reviews.

4. Studies that have been performed on animals.

5. Studies in which patients still had periodontal disease and it was not healed.

Risk of bias assessment

Cochrane Collaboration’s tool for assessing risk of bias [13] for the evaluation of the risk of bias was assessed.

The degrees of bias were categorized as follows: low risk, if all the criteria were met; moderate risk, when only one criterion was missing; high risk, if two or more criteria were missing; and unclear risk, if too few details were available to make a judgment of certain risk assessment.

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15

Table 4. Risk of bias assessment. Author/Year Was a clear

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16

SYSTEMIZATION AND ANALYSIS OF DATA

Study selection

The search of literature identified a total of 1790 articles when using the keywords, of which 658 were found on Pubmed, 112 articles found on Cochrane and 1070 identified on ScienceDirect. A total of 160 duplicates were then removed. Following this, 1660 articles were further screened and filtered, as shown on the Prisma flowchart (Fig. 1). Abstracts and the titles of articles were screened to check for their eligibility and the irrelevant publications were also excluded. After full text screening of the articles, 31 articles were then removed due to the fact that they did not match the inclusion criteria and the reported data in those articles were not in accordance to the applied PICO design. Furthermore, 15 articles were also factored out after further examination of full text.

After the application of exclusion and inclusion criteria and full text screening of the text and studies, 8 studies were chosen to be included in this systematic review.

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17

Fig.1. Prisma Flowchart.

Excluded duplicated titles and abstracts

(n =130)

Exclusion criteria - publications older than 10

years, not in the English language, systematic reviews, performed on animal subjects. Id en tif icat ion S cr ee n in g E li gib il ity In clu d ed

Records after duplicates removed (n = 1660) Records screened (n = 1660) Records excluded (n = 1630) Full-text articles assessed for eligibility

(n = 31)

Full-text articles excluded, with reasons

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Author/Year

Study Design Number of

participants/subjects

Follow-up

period Mean Age

Patients with

systemic diseases Outcome variables/Results Conclusions

Graetz et al., 2017 [5]

Retrospective study.

29 patients in the test group and 29 in the

control group. 69 implants in total. 5 years. F=49.7 ± 11.2 years M=56.0 ± 10.8 years Yes

No significant difference of implant survival (p = 0.562). There is a significant difference between MBL (p < 0.05) and PPD (p < 0.05) between the test group and the control group.

There is no impact of a history of periodontal disease on dental implant survival, but there is a

risk of increased MBL and PPD.

Correia et al., 2017 [1]

Retrospective

cohort study. 202 participants and

689 implants. 3.03 years. 50 years No

No significant difference of implant survival. (p = 0.24)

There is a similar outcome between the test group and the control group.

There is no correlation between dental implant success and a history of periodontal disease.

Altay et al., 2018[7] Retrospective study. 13 participants and 55 implants. 35 months. 55 years

Yes Implant survival rate = 100% However, 11/13 participants had PID.

There is a higher risk of PID in patients with a history of periodontal disease. Oral hygiene

influences the outcome of dental implants.

Akram et al., 2019 [14]

Prospective study.

7 patients, 48 implants in the test group. 7 patients, 11 implants in

the control group.

1, 2, 3 years. 36-47 years Yes

BOP and CAL show a significant difference between test group and control group (p = 0.01). Implant success rate of test group is 81.25%, and

of control group is 100%.

A history of periodontal disease decreases chances of dental implant success.

Pałka et al., 2019 [9]

Retrospective review.

77 patients in the test group and 10 in the control group. 1019 implants in total.

22.2 months. 54 years Yes

No significant difference.

Implant survival after 1 year = 99.3% in both test and control groups.

There is no impact on dental implant survival as there is a 99% success rate of dental implants after the first year in patients with or without a

history of periodontal disease.

Gianserra et al., 2010 [19]

Retrospective cohort study.

1727 participants and

2813 implants. 5 years. n/a Yes

No statistical difference in implant survival between the 3 test groups (p > 0.05).

There is no impact of a history of periodontal disease on dental implant failures up to 5 years.

Yan et al., 2020 [18] Longitudinal study. 24 patients in test group, 5 in control group. 60 implants. 3 years n/a No

There is a significant difference (p < 0.05), as detection of periodontal micro-organisms in the

control group was 0%.

Patients with a history of periodontal disease have a higher risk of PID.

Meyle et al., 2014 [15]

Prospective

study. 20 participants. 5, 10 years. 48.7 years No

No significant difference in implant survival rate or PPD/CAL (p < 0.05)

Implant success rate = 91.1% over 5 years.

Dental implants, peri-implant variables and radiographic bone level are stable in patients with

a history of periodontal disease.

Table 5. Summary of the included studies. PPD = periodontal probing depth; PID = peri-implant disease; CAL = clinical attachment loss; MBL = marginal bone loss;

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RESULTS

In 2017, Graetz et al. completed a study on the effect of periodontitis history on implant success [5]. The study compared 29 patients who were diagnosed with chronic periodontitis and had dental implants placed after active periodontal treatment, against 29 periodontally healthy patients. The control group underwent complete radiographic documentation and periodontal records at baseline T1 (implant insertion) and at the final documented visit (T2). In order to evaluate the results, periodontal pocket depth, radiological marginal bone loss, implant loss, tooth loss, medical history, periodontal treatment of each tooth, smoking status and medical history were all evaluated. The findings of this study demonstrated the survival rate of the implants placed in the patients with previous chronic periodontitis in the test group was 97.1% over 5 years, and 92.5% over 10 years. The implant survival rate in the control group was 97.4% over 5 years and 91.4% over 10 years. There was no significant difference in implant survival between the test group and control group (p = 0.562). In regard to the mean measurement of periodontal probing depth around the dental implant, for the test group was 3.4 ± 1.0 mm at T1, and 4.2 ± 1.6 mm at T2. For the control group the mean measurement was 1.0 ± 1.2 mm at T1 and was 2.9 ± 0.8 mm at T2. At T1 as well as at T2, between the 2 groups, the periodontal probing depths shared an increase (p <0.05) [5]. The radiological measured marginal bone loss in the test group at T1 was 6.8 ± 13.7% and at T2 the marginal bone loss was 15.7 ± 17%. For the control group, the marginal bone loss at T1 was 1.4 ± 9.2% and was 4.8 ± 13.2% at T2. The differences between groups and time points were statistically significant (p <0.05), as an increase of almost 10% is seen in the measured marginal bone loss in the test group, whereas only a slight increase of around 3% in the control group was measured. The conclusion of this study was that although there may not be a large statistical difference in terms of dental implant survival rates between patients with a history of periodontitis and patients without a history of periodontitis, patients with a history of periodontitis showed a higher percentage of marginal bone loss and periodontal probing depth, which could pose a significant prognostic factor for implant survival [5].

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20 treated with intravenous or oral biphosphonates; patients with uncontrolled diabetes; patients with serious coagulation problems; patients who are dependent on alcohol or psychotropic substances; patients with poor oral hygiene and low motivation; patients with dental implants placed out of clinic or by a different clinician; and patients with tooth implant-supported prosthesis [1]. Included in this study were 202 patients, of which 53% were those with a history of chronic periodontitis and 47% were those without a history of chronic periodontitis. Out of the 689 implants placed, only 42 were lost, therefore there was a survival rate of 93.9% overall. The dental implant survival rate of the control group was 95.8%, whereas the dental implant survival rate of the test group was 93.1%, showing no significant statistical difference (p = 0.24). The test group was also divided as a function of periodontitis severity, and there was no significant differences observed in the dental implant survival rate (p = 0.08), as seen in Table 5. Overall, there is a relatively similar outcome in survival rates of dental implants between the two groups, thus allowing us to conclude from this study that there is no correlation between a history of periodontal history and dental implant success.

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21 In 2019, Akram et al. conducted a study focusing more on the clinical and radiographic peri-implant outcomes of short dental implants placed in posterior jaws of patients with treated generalized aggressive periodontitis [14]. In this 3-year follow-up study, the test group consisted of 7 participants whom had been diagnosed with generalized aggressive periodontitis, but over 5 years had received periodontal treatment. The control group was made up of 7 participants who were periodontally healthy. Peri-implant and periodontal parameters, bleeding on probing, probing depth, clinical attachment level, plaque index and gingival recession were all recorded. Marginal bone loss was also recorded in this study in both groups. The results of this study showed that the clinical attachment loss and bleeding on probing around the dental implants in the test group were notably higher in comparison to the values of clinical attachment loss and bleeding on probing in the control group throughout the follow-up (p = 0.01). Furthermore, probing depth was slightly greater in the test group after the first year of dental implantation but was not considered significant statistically (p = 0.053). The clinical attachment level around the teeth of the patients in the test group was significantly greater during the follow-up period than around the teeth of periodontal healthy subjects in the control group (p = 0.02) [14]. The overall implant success rate in this study measured to be 81.25% 3 years after dental implantation in patients with a history of generalized aggressive periodontitis. In periodontally healthy patients, the implant success rate was 100%. These results show that there is a higher chance of dental implant success in patients without a history of generalized aggressive periodontitis.

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22 period. The final conclusion was made that dental implants placed in patients with a history of chronic periodontitis showed stable survival rates, radiographic bone levels and stable peri-implant variables after 5 and 10 years.

In a retrospective review carried out by Pałka et al. in 2019, immediately loaded bicortical screw implants placed in fresh extraction sockets and healed bone, used to retain full-arch and segment cemented prostheses in the rehabilitation of mandible and maxilla in patients with and without a history of periodontal disease was investigated [9]. In this study, patients who were undergoing radiotherapy or chemotherapy in the head-and-neck area, were pregnant or breastfeeding, had general health conditions that could cause complications, participants who had uncontrolled diabetes and patients who had psychiatric problems were excluded. In total, a number of 87 patients were included to participate in this study, of which 77 had been previously treated for periodontitis and 10 patients who had not. The majority of patients had undergone a follow-up period at 12 months and then at 24 months after the implant had been placed. For this study, certain criteria were followed according to Misch et al. [17] which included the following: absence of severe bone loss, absence of persistent subjective complaints (pain, foreign body sensation, and/or dysesthesia) or exudates on function, absence of mobility, and absence of continuous radiolucency around the implant. Overall the results of implant survival at 12 months were 99.3% for both groups 98.6% at 24 months and 97.0% at 35 months. To conclude, bicortical smooth surface implant concept with immediate loading protocol provided predictable outcomes and survival rate of 99% in patients with and without a history of periodontitis [9].

In 2020, Yan et al. conducted a longitudinal on periodontal micro-organisms of short locking-taper implants and adjacent teeth in patients with history of periodontitis [18]. In this study, the focus is primarily on if having a history of aggressive or chronic periodontitis has an impact on the micro-organisms in the periodontal tissue after a dental implant is placed. From a group of 24 participants, 5 were periodontally healthy or had gingivitis, 5 participants had a history of aggressive periodontitis, and a further 14 had a history of chronic periodontitis. Participants that had systemic diseases, a history of smoking or were pregnant were excluded from this study. In order to conduct this study, samples of subgingival plaque were obtained from the participants at 5 different points in time over the course of the dental implant treatment; before implant placement (T1); before second stage operation (T2); 1 month after restoration (T3); 1 year after loading (T4) and 2 years after loading (T5) [18]. The periodontal micro-organisms studied were T. forsythia, P. gingivalis, T.

denticola, F. nucleatum, P. intermedia and A. actinomycetemcomitans. Out of the 24 patients, 3

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23

forsythia and P. intermedia around dental implants was statistically higher than that of natural teeth

(p < 0.05), almost two folds in implants compared to that of natural teeth. When comparing the test group and control group, the detection rate of all the tested periodonto-pathogens was 0% in the control group, thus no patients were diagnosed with peri-implant disease. This is significant as it shows a correlation that patients with no history of chronic or aggressive periodontitis may have far less of a risk of peri-implant disease. It was concluded that patients who have a history of chronic periodontitis or aggressive periodontitis do in fact have an increased risk for peri-implantitis and peri-implant mucosititis.

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24

DISCUSSION

The aim of this systematic review was to assess the outcome of dental implants placed in patients that have a history of periodontal disease and whether or not there is a difference with dental implants placed in patientswith no history of periodontal disease. In order to evaluate and investigate these outcomes, the following measures in a number of studies reviewed in this systematic review were recorded, such as implant survival rate, marginal bone loss, probing depth, clinical attachment level, bleeding on probing, plaque index, the presence of peri-implant diseases and the presence of periodontal pathogens.

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25 was not clarified whether or not patients also had systemic diseases or were smokers, which could have played a role in dental implant failure.

Moreover, oral hygiene habits of patients must be taken into consideration, as seen in the study by Altay et al. in 2017 [7]. It was found that the patients that followed oral hygiene habits of toothbrushing twice a day were subsequentially the patients whose implants did not fail. This highlights a limitation in this systematic review, due to the fact that not all studies included the knowledge and information of patient’s regular oral hygiene which can be a known contributor to implant survival and the outcome of peri-implant diseases [7].

A further limitation of these studies is that it is difficult to be able to predict and monitor other factors that may lead to implant failure in patients with or without a history of periodontal disease. According to Correia et al. [1], all confounding factors may have affected the long-term outcomes and not just the presence or not of periodontal disease. The impact of these variables on the implant survival rate, post-operative 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 [1]. Moreover, all of the included studies observed a high risk of bias according to the criteria, as seen in Table 4. This limitation may have affected the results of studies.

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26 included in this study to be able to adequately compare the results and make a clear distinction between periodontally healthy patients and those with a history of chronic periodontitis. A further limitation is that only 20 participants were included in the study, which is relatively low in juxtaposition to the number of participants in the study by Casado et al. [21], which included 215 participants, 129 in the control group and 89 in the test group. In both studies, patients with systemic diseases were excluded.

It is appropriate to put forward for consideration that in order to fully understand and make a valid conclusion in regard to implant survival and peri-implant diseases, more in depth research and further studies are required on how the history of periodontal disease prior to the placement of dental implants can negatively influence the outcome of dental implant success. In order to accomplish this, it is imperative to investigate other localized factors that may affect dental implant survival in patients.

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27

CONCLUSIONS

Amid the noted limitations of the present systematic review, there was not a sufficient amount of evidence proving there to be a difference between dental implant survival rates in patients with or without a history of periodontal disease during a medium and short time follow-up period. Notwithstanding, there may be a higher risk of dental implant complications such as peri-implant diseases in patients with a previous history of periodontal disease compared to those without a history of periodontal disease.

A demand on long-term controlled clinical trials, with comparable criteria and further consideration on influential factors such as systemic diseases, oral hygiene habits and smoking is needed to evaluate the long-term implant survival rates in patients with previous history of periodontal disease.

PRACTICAL RECOMMENDATIONS

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28

REFERENCES

1. Correia F, Gouveia S, Felino A, Costa A and Almeida R. Survival Rate of Dental Implants in Patients with History of Periodontal Disease: A Retrospective Cohort Study. The International Journal of Oral & Maxillofacial Implants.2017;32(4):927-934.

2. Armitage G. Development of a Classification System for Periodontal Diseases and Conditions. Annals of Periodontology. 1999;4(1):1-6.

3. Caton J, Armitage G, Berglundh T, Chapple I, Jepsen S, Kornman K et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. Journal of Periodontology. 2018; 89:S1-S8.

4. Tonetti M, Greenwell H, Kornman K. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. Journal of Periodontology. 2018;89:S159-S172.

5. 5.Graetz C, El-Sayed K, Geiken A, Plaumann A, Sälzer S, Behrens E et al. Effect of periodontitis history on implant success: a long-term evaluation during supportive periodontal therapy in a university setting. Clinical Oral Investigations. 2017;22(1):235-244.

6. Chava V, Nuvvula S, Nuvvula S. Primary culprit for tooth loss!!. Journal of Indian Society of Periodontology. 2015;0(0):0.

7. Altay M, Tozoğlu S, Yıldırımyan N, Özarslan M. Is History of Periodontitis a Risk Factor for Peri-implant Disease? A Pilot Study. The International Journal of Oral & Maxillofacial Implants. 2018;33(1):152-160.

8. Joshipura V, Yadalam U, Brahmavar B. Aggressive periodontitis: A review. Journal of the International Clinical Dental Research Organization. 2015;7(1):11.

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29 10. Prathapachandran J, Suresh N. Management of peri-implantitis. Dental Research Journal.

2012;9(5):516.

11. Heitz-Mayfield L, Salvi G. Peri-implant mucositis. Journal of Periodontology. 2018;89:S257-S266.

12. Moher D, Liberati A, Tetzlaff J, Altman D. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. International Journal of Surgery. 2010;8(5):336-341.

13. Higgins JP, Altman DG, Gotzsche PC, Jüni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JA. The Cochrane Collaboration's tool for assessing risk of bias in randomized trials. BMJ 2011; 343:d5928.

14. Akram Z, Vohra F, Sheikh S, Albaijan R, Bukhari I, Hussain M. Clinical and radiographic peri‐implant outcomes of short dental implants placed in posterior jaws of patients with treated generalized aggressive periodontitis: A 3‐year follow‐up study. Clinical Implant Dentistry and Related Research. 2019;.

15. Meyle J, Gersok G, Boedeker R, Gonzales J. Long-term analysis of osseointegrated implants in non-smoker patients with a previous history of periodontitis. Journal of Clinical Periodontology. 2014;41(5):504-512.

16. Lang N, Berglundh T. Periimplant diseases: where are we now? - Consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology. 2011;38:178-181

17. Misch C, Perel M, Wang H, Sammartino G, Galindo-Moreno P, Trisi P et al. Implant Success, Survival, and Failure: The International Congress of Oral Implantologists (ICOI) Pisa Consensus Conference. Implant Dentistry. 2008;17(1):5-15.

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30 19. Gianserra R, Cavalcanti R, Oreglia F, Manfredonia MF, Esposito M. Outcome of dental

implants in patients with and without a history of periodontitis: a 5-year pragmatic multicentre retrospective cohort study of 1727 patients. European Journal of Oral Implantology. 2010 ;3(4):307-314.

20. Swierkot K, Lottholz P, Flores-de-Jacoby L, Mengel R. Mucositis, Peri-Implantitis, Implant Success, and Survival of Implants in Patients With Treated Generalized Aggressive

Periodontitis: 3- to 16-Year Results of a Prospective Long-Term Cohort Study. Journal of Periodontology. 2012;83(10):1213-1225.

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