Achard Julien
Fifth year, group 14
Can overweight/obesity be considered as a risk factor for periodontitis? As systematic review
Master’s Thesis
Supervisor
LITHUANIAN UNIVERSITY OF HEALTH SCIENCES
MEDICAL ACADEMY
FACULTY OF ODONTOLOGY
DEPARTMENT OF PERIODONTOLOGY
Can overweight/obesity be considered as a risk factor for periodontitis? As systematic review
Master’s Thesis
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EVALUATION TABLE OF THE MASTER’S THESIS
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1 Is summary informative and in compliance with the 0.3 0.1 0
Summary thesis content and requirements?
2 (0.5 point) Are keywords in compliance with the thesis 0.2 0.1 0
essence?
3 Introduc- Are the novelty, relevance and significance of the work justified in the introduction of the thesis? 0.4 0.2 0
tion, aim
4 and tasks Are the problem, hypothesis, aim and tasks formed clearly and properly? 0.4 0.2 0
(1 point)
5 Are the aim and tasks interrelated? 0.2 0.1 0
6 Is the protocol of systemic review present? 0.6 0.3 0
Were the eligibility criteria of articles for the
7 selected protocol determined (e.g., year, language, 0.4 0.2 0 publication condition, etc.)
Are all the information sources (databases with
8 dates identify additional studies) described and is the last of coverage, contact with study authors to 0.2 0.1 0 search day indicated?
Is the electronic search strategy described in such a
Selection way that it could be repeated (year of search, the
9 criteria of last search day; keywords and their combinations; 0.4 0.1 0
the studies, number of found and selected articles according to
search the combinations of keywords)?
methods and Is the selection process of studies (screening,
10 (3.4 points)strategy eligibility, included applicable, included in the meta-analysis) in systemic review or, if 0.4 0.2 0
described?
Is the data extraction method from the articles
11 (types of investigations, participants, interventions, 0.4 0.2 0 analysed factors, indexes) described?
Are all the variables (for which data were sought
12 and any assumptions and simplifications made) 0.4 0.2 0
information is to be used in data synthesis,
described?
14 Were the principal summary measures (risk ratio, 0.4 0.2 0
difference in means) stated?
Is the number of studies screened: included upon
15 assessment for eligibility and excluded upon giving 0.6 0.3 0 the reasons in each stage of exclusion presented?
Are the characteristics of studies presented in the
16 Systemiza- included articles, according to which the data were extracted (e.g., study size, follow-up period, type of 0.6 0.3 0
tion and respondents) presented?
analysis of
Are the evaluations of beneficial or harmful
data outcomes for each study presented? (a) simple
17 (2.2 points) summary data for each intervention group; b) effect 0.4 0.2 0
estimates and confidence intervals)
Are the extracted and systemized data from studies
18 presented in the tables according to individual 0.6 0.3 0
tasks?
19 Are the main findings summarized and is their 0.4 0.2 0 relevance indicated?
20 Discussion Are the limitations of the performed systemic 0.4 0.2 0
(1.4 points) review discussed?
21 Does results? author present the interpretation of the 0.4 0.2 0
22 Do the conclusions reflect the topic, aim and tasks 0.2 0.1 0
Conclusions of the Master’s thesis?
23 (0.5 points) Are the conclusions based on the analysed material? 0.2 0.1 0
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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
Practical
Are the practical recommendations suggested and
30 recommen- are they related to the received results? +0.4 +0.2 0
dations
Were additional methods of data analysis and their
31 results used and described (sensitivity analyses, +1 +0.5 0 meta-regression)?
Was meta-analysis applied? Are the selected
32 statistical methods indicated? Are the results of +2 +1 0
each meta-analysis presented?
General requirements, non-compliance with which reduce the number of points
33 Is the thesis volume sufficient (excluding 15-20 pages <15 pages
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(-2 points) (-5 points)
34 Is the thesis volume increased -2 points -1 point
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36 Is the thesis written in correct language, -0.5 point -1 points scientifically, logically and laconically?
37 Are there any grammatical, style or -2 points -1 points
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38 Is text consistent, integral, and are the volumes of its structural parts balanced? -0.2 point -0.5 points
39 Generalrequire- Amount of plagiarism in the thesis. (not evaluated) >20%
ments Is the content (names of sections and sub-
40 sections and enumeration of pages) in compliance with the thesis structure and -0.2 point -0.5 points
aims?
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41 compliance with the text? Are the titles of -0.2 point -0.5 points sections and sub-sections distinguished
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42 Are there explanations of the key terms -0.2 point -0.5 points and abbreviations (if needed)?
Is the quality of the thesis typography
43 (quality of printing, visual aids, binding) -0.2 point -0.5 points
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Reviewer’s comments: ___________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________ ______________________________________________________________________________
TABLE OF CONTENT 1. SUMMARY
2. ABBRAVIATIONS 3. INTRODUCTION
4. SELECTION CRITERIA OF THE STUDIES, SEARCH METHODS AND STRATEGY
4.1. Scope of review 4.2. Search terms 4.3. Inclusion criteria 4.4. Exclusion criteria
4.5. Bias and research strategy 4.6. Full text for data extraction 4.7. Data analysis
5. SYSTEMIZATION AND DATA ANALYSIS
5.1. Search result and characteristics of studies 5.1.1. Types of studies included
5.1.2. Country of inclusion
5.1.3. Number of participant, age range and gender 5.1.4. Intervention in this study
5.2. Protocol of the included studies 5.2.1. Periodontal protocol
5.2.1.1. Periodontal protocol 5.2.1.2. Periodontal calibration
5.2.1.3. Periodontal disease classification and classification
5.2.2. Anthropometric protocol
5.2.2.1. Anthropometric indices
5.2.2.2. Definition of obesity and anthropometric classification
5.3. Outcome
5.3.1. Measurement outcome result 5.3.2. Result of the studies
5.4. Influence of covariates
5.5. Quantitative data analysis result 6. DISCUSSION
6.1. Obesity and behavior
6.1.1. Obesity and oral hygiene behavior 6.1.2. Nutrition and its roles
6.1.2.1. Role of nutrition on the periodontium 6.1.2.2. Nutrition and obesity
6.2. Obesity and inflammatory response
6.2.1. Inflammatory response: reminders
6.2.2. Peculiarity of inflammatory response in obese individuals 6.2.3. Effect on periodontium
6.3. The infectiobesity theory
6.4. Obesity as a risk factor for periodontitis 7. CONCLUSIONS 8. PRACTICAL RECOMMENDATION 9. CONFLICT OF INTEREST 10. ACKOWNLEDGEMENT 11. REFERENCES ANNEXES
1. Individual development plan for the master thesis 2. Tittle page 1
3. Tittle page 2
4. Evaluation table of systematic review type of master thesis 5. Descriptive result of the included study for the master thesis
TABLES
1. Search terms
2. Characteristics of the included studies
3. Adipokines increased in obesity, Makki et al, 2014, France
GRAPH
1. Participant and gender
FIGURE
1. Meta-analysis forest plot of the subgroup of the publications included in this work 2. Meta-analysis forest plot of the mean BMI and its standard deviation in experiment and
control group
3. Flow diagram of the search methods
4. Antioxydant affection on the periodontium, Najeeb et al, 2016, Saudia Arabia
5. Prevalence of micronutrient deficiencies in obesity and diabetes. Via et Al, 2016, USA 6. Inflammatory reaction leading to bone loss in periodontitis, Hajishengallis, 2014, USA
8. Hypothesis by which oral bacteria could affect body weight and contribute to obesity, Goodson et al, 2009, USA
1. SUMMARY
Background: Obesity nowadays is a worldwide epidemic associated with a lot of co-morbidity
factor. A lot of previous review investigated the relationship between periodontitis and different chronic diseases such as diabetes mellitus. As obesity is on the rise and is supposed to keep rising up over the years, the project of investigating obesity as a risk factor for periodontitis in the general population came to life.
Methods: For this research, access to online database was made through the LUHS ezyproxy system,
from those different databases, different type of works have been screen for inclusion. After the acknowledgement of the search terms, inclusion and exclusion criteria were defined for this systematic review. Sixteen different studies have been selected for complete analysis.
Result: Sixteen studies were considered as eligible for review and analysis. Of those 14 studies all
showed some kind of relation between the two parameters studied in this systematic review which are overweight/obesity and periodontitis. The obesity indicators that could have been used such as body mass index, the waist hip ratio, the waist circumference and the body fat index, have demonstrated to have a significant association with the measure of periodontitis such as bleeding on probing, clinical attachment loss, gingival index, and community periodontal index.
2. ABREVIATION:
WHO: world health organization BMI: Body mass index
WC: Waist circumference PD: probing depth
BOP: Bleeding on probing CAL: Clinical attachment loss CPI: Community periodontal index GI: gingival index
TNF: tumor necrosis factor
IL: interleukin (followed by a number)
3. INTRODUCTION
Obesity is a medical condition expressed by an excessive amount of body fat and that fat has accumulated to a certain extent that it has negative repercussion on the health of an individual [35]. It can be associated with multiple etiological factors. Obesity can be associated with an excess amount of calories ingested everyday, poor diet and a lack of physical activity which is the case in most of the obese patients. Obesity might be associated with other type of etiological factors such as genetics (the Prader-Willi syndrome - characterize by a decrease in the muscular tonus and a food addiction) but those are rare cases [46]. Obesity can also develop from medical conditions such as an underactive thyroid gland and Cushing’s syndrome that are manifested by an over productions of hormones [46]. Obesity is nowadays a worldwide epidemic crisis. At least 2,8 millions of people die each year from complications of being WHO criteria. This is especially a trend in developed or in developing country due to the fact that processed food and food presenting a lot of fat and carbohydrates are more available and cheap in those countries. Obesity also is demonstrated to be more important in people with high or middle level income compared to the one with medium income level. A lot of complications have been shown to arise from obesity such as diabetes mellitus, cardiac diseases and some kind of cancers. [50] [49]
Periodontitis is one of the most common disease of the oral cavity, it is a silent disease where in most of the case the patient doesn’t realize he is sick until he has a consultation with a dental professional [21]. In case of periodontitis multiple changes occurs in the periodontium of the patient, the main symptoms are an increase in the pocket depth, with a loss of alveolar bone. Clinical attachment loss which refers to the estimated position of the structure that support the tooth as much as measured with a periodontal probe is increased in case of periodontitis [52]. Periodontitis will ultimately result in an important loss of alveolar bone and eventually to the loss of the tooth, if it stays untreated. Periodontitis is very widespread allover the world and is commonly known to be responsible for most of the teeth extractions. Periodontitis is associated with an important number of risk factors, such as age, gender, genetics but also other factors that are acquired such as diabetes mellitus, condition of the oral hygiene and cardiovascular diseases. [26] [21]
Periodontitis and obesity/overweight have been at the center of multiple research over the last decades, this is probably because obesity is increasing worldwide and periodontitis is not a receding disease. Different types of studies have been made to show the relation between the two, such as
review and literature review. Multiple studies suggested an association between these two parameters. It is still a great topic of investigation in the scientific community.
In this systematic review we decided to investigate the relationship between obesity/overweight and periodontitis by reviewing the research made on the two conditions in the past ten years. We stated the hypothesis, that obesity is not related to periodontitis. The ultimate goal was to elucidate if obesity could be considered as a risk factor for periodontitis.
4. SELECTION CRITERIA OF THE STUDIES. SEARCH METHODS AND
STRATEGY
4.1 Scope of review:
The research was made with computer and internet (electronic research) multiple websites were used for that goal. The website used were: PUBMED, COCHRANE, GOOGLE SCHOLAR, WILEY ONLINE LIBRARY and the JOURNAL OF PERIODONTOLOGY. All those websites were access through the online library of the Lithuanian University of Health Science. The main search engine used was PUBMED with the search terms mentioned below. The limitations of PUBMED is that a lot of publications with no scientific relevance can be published on it and then need to be screened. The search was focused on finding clinical trials about the relations between periodontitis and obesity/overweight. The systematic reviews or meta-analysis were also registered as they could be used as reference work.
4.2 Search terms:
The systematic research was conducted by one person, in the research engine tool mentioned above (2.1 scope of review). At first titles of relevance were selected in order to read the abstract, publications that came as double in different databases were screened and the duplicates were removed. Reviews, and clinical trials were selected for their abstract to be read. After this first screening publications eligible for the study were downloaded in order to have them read in their entirety and the publications were filtered in order to match the inclusion and exclusion criteria (seen below 2.3).
Table 1. Search terms Search terms 1. Periodontitis 2. Periodontal disease 3. Periodontal patient 4. Overweight 5. Obesity 6. Malnutrition 7. Metabolic syndrome 8. Body Mass Index 9. Obese
10. Body weight 11. Waist Hip Ratio 12. Periodontal indicators 13. Adult
14. Tooth loss
15. Alveolar bone loss
16. Periodont* (*used in PubMed for all the terms that start with periodont) 17. Combination of search items such as: 1+5 or 1+7+8…
4.3 Inclusion criteria:
Publications were decided to be included when treating about periodontitis and obesity/overweight. Cohort-studies, randomized controlled trials and cross-sectional studies. All the studies had to be conducted in a period less than 10 years (2007-2017) and must have been published. The publications must have a cohort number (N) equal or superior to 50 patients, with all of the patients being older than 18 years of age with no gender predilections. All the published studies were in vivo studies. In all the selected publications obesity was defined by using the Body Mass Index (BMI), waist circumference ratio, waist to hip ratio, or waist to height ratio.
Periodontitis was defined according the study selected.
4.4 Exclusion criteria:
All the different review type of research were excluded of the research for data extraction and analysis such as literature review, mini-review or previous systematic review; although those publications could be used as reference work or for the introduction of this particular systematic review. All the publications done in vitro or on other species than humans were also excluded from the research.
4.5 Bias and research strategy:
Among other limitations, the risk of bias in this research had not been a major source of attention in few of the collected publications. This in its turn, could or not cause an increase risk of bias that should be taken in consideration for the readers of this paper. This can be explained as well, by the fact that in the publications selected for full data extraction, some present in this systematic review could give an increased number of correlation between periodontitis and obesity/overweight which may or may not be a truth in the clinical work. Despite this, it doesn’t mean that the correlation found between periodontitis and overweight/obesity is untrue especially in the case of randomized clinical trials.
For the research bias, each publication has been screened by the author and reviewed by the supervisor of this work (Dr. Pranckevičienė Alma).
4.6 Full text for data extraction:
30 publications were considered as eligible for full text data extractions. Those publications were then downloaded as PDF from the search engines. Of this 30 publications 8 were excluded for the reason that they didn’t match the inclusion or exclusion criteria. Those publications didn’t used any index recognize by the scientific community. The clinical trials didn’t have enough patient to be included. Other publications were rejected because of anthropometric measurement. For this systematic review the anthropometric measurement must have been based on body mass index, waist hip circumference ratio at least or combination of both.
Publications that were of meta-analysis or systematic review types could be used as reference for this work.
Sixteen publications were included for full data extraction. Sixteen published studies were included in the qualitative analysis and of those sixteen publications, twelve were included for quantitative analysis.
PRISMA 2009 Flow Diagram
Records identified through database searching (n = 605 ) Scr e e n in g In cl u d e d El ig ib ili ty Id e n ti fi ca ti on
Additional records identified through other sources
(n = 0 )
Records after duplicates removed (n = 424 )
Records screened (n = 424 )
Records excluded (n = 394 )
Full-text articles assessed for eligibility
(n = 30 )
Full-text articles excluded, after evaluation of inclusion
and exclusion criteria (n = 8) Studies included in qualitative synthesis (n = 16) Studies included in quantitative synthesis (meta-analysis) (n =12) )
Author Study Design Number of participant, age range, gender
Result: Positive or negative correlation
D. Ekuni, 2008 Cross sectionnal examination N=618
18-24 years old range 296 female; 322 male
Positive
Elangovan, 2014 Cross sectionnal examination N=73
Older than 18 years old N/A
Positive
Eremenko, 2016 Cross sectionnal examination
N= 2089
Older than 18 years old 1107 female; 982 male
Positive
Furutura, 2010 Cross sectionnal examination
N= 2225
18-19 years old range 961 females; 1264 males
Positive
Haffajjee, 2009 Longitudinal study analysis
N= 744
18-86 years old range 345 female; 350 male
Positive
Jentsch, 2017 Cross sectionnal examination N=60
Older than 18 years old Gender: N/A
Positive
Kim, 2011 Cross sectionnal survey
N= 4246
19-103 years old range 1762 female; 1262 male
Positive
Linden, 2007 Longidutinal regression analysis N= 1362 Older than 21 Only male
Positive
Martinez-Herrera, 2016 Cohort studies
N= 212 20-65 years old Gender: N/A
Positive
Meissel, 2015 Longidutinal regression analysis N= 2746
20-79 years old range 1409 females, 1377 males
Positive
Morita, 2009 Cross sectionnal examination
N= 2478
24-60 years old range 450 females; 2018 males
Positive
Nguyen, 2015 Cross sectionnal examination
N= 118 Older than 18 103 females; 15 male
Positive
Pataro, 2010 Cross sectionnal examination
N= 594
18-65 years old range Only female
Positive
Shimazaki, 2010 Observative, comparative study N= 1160
20-77 years old range Gender: N/A
Positive
Shreshta, 2016 Cross sectionnal survey
N= 100
27-58 years old range 53 female, 47 male
Positive
Wilkins, 2017 Observative, comparative study N= 292
26-64 years old range, Only male
Positive
4.7 Data analysis
A descriptive analysis of all the studies included was performed and can be find in the annex 5. A data analysis was made in the form of a meta-analysis. To that end, the computer system Review Manager 5 (Review Manager (RevMan) [Computer program]. Version 5.3. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014.) was used. Two different types of analysis were made. The first one a dichotomous, inverse variance with odds ratio as effect measure. For this, was considered as events the number of subject suffering from periodontitis in obese/overweight or periodontal group. Not all the studies could be included in it, only the studies that reported the data
needed for the analysis (N= 9).
For the second one a dichotomous analysis, with inverse variance and mean differences as effect measure. In this analysis the mean and its standard deviation of the BMI in periodontitis and control groups were compared. Only few studies had the data available for this analysis (N=5).
5. SYSTEMIZATION AND ANALYSIS OF DATA
5.1 Search result and characteristics of studies:A total of 16 publications were selected to be fully included in this study, those article have had their data extracted in order to realize those work; Those publications matched the inclusion criteria, and once read were assumed to be of an enough quality to be included (descriptive result are shown in annex 5).
5.1.1 Types of studies included:
Of all the publications that were selected for full data extraction. From those included, eight were designed as cross sectional examination. A cross sectional examination is a type of observational study that will analyze from a representative population at specific point in time [6]. Three of the published studies are observational, comparative studies, were a group of population is compare to another one with different intervention in both group.
Four of the publications are observative, comparative studies which can also be named as logistic regression analysis. This is a type of analyzes where the researcher looks for inferences from a sample to a population, and the independent variable should not be under the control of the researcher [36].
5.1.2 Country of inclusion
The included publications were conducted in the following countries:
- Japan: D. Ekuni ,2008; Shimazaki, 2010, Frutura, 2010 Morita, 2009 [9] [41] [55] [56] - United State of America: Wilkins, 2017; Haffajjee, 2009, Elangovan, 2014 [51] [15] [10] - South Korea: Kim, 2011 [22]
- United Kingdom: Linden, 2007 [23] - Vietnam: Nguyen, 2015 [31]
- Spain: Martinez-Herrera, 2016 [27]
- Germany: Meisel, 2015; Eremenko, 2016; Jentsch, 2017, [28] [11] [18] - Nepal: Shrestha, 2016, [53]
- Brazil: Pataro, 2009 [57]
5.1.3. Number of participants, age range and gender:
As the inclusion criteria stated it, the publications that could be included in this systematic review were only the one presenting a number of patient superior or equal to 50 (n). The maximum participant in a study present were 4,246 [22]. The lower number of included participant were 60 [18]. The mean number of participant in the included study for this systematic review is 681.
Two of the included studies for data extraction [51] [23], were made only with male participants, and one with only females [57]. In all the other studies males and females were included.
In all the study with available information on the gender of the participant it should be noted that the mean number of female participant was 522 and the mean number of male participant was 350.
All of the studies, included patients older than 18 years of age as mentioned in the inclusion criteria (4.3). Some studies didn’t include participants younger than 29 years [51]. It should be noted that in some studies although the age range is wide, the participant were mainly older.
5.1.4. Intervention in the study:
The studies included; mainly analyzed the correlation between periodontitis and obesity without any interventions.
In neither of the studies treatment was performed or any kind of medication were provided to the patients.
Although it should be noted that one of the studies recorded the physical fitness of the patients by the handgrip strength.
5.2 Protocol of the included studies: 5.2.1 Periodontal Protocol
5.2.1.1 Periodontal protocol:
Five of the included studies used the community periodontal index (CPITN) defined in the “oral health and survey” of 1997 to evaluate the periodontal state of the subjects participating in the study [9] [22] [41] [53] [56]. Using this index, a score was assigned for the participant. A score of 3 or more showed periodontitis.
All the other studies used multiple indices in order to examine the patient. The indexes
0 2000 4000 6000 8000 10000 12000 14000 16000 18000 20000
Graph 1. Participant and Gender
and plaque index were as well used. In most of the studies, clinical attachment loss was defined as the distance from the cemento-enamel junction to the bottom of the pocket. In case of gingival recession, then the clinical attachment loss was express as a negative value. [51] [15] [10] [23] [28] [57] [55]
5.2.1.2 Periodontal calibration:
All of the included publications, recruited one or multiple experienced dentist in order to record the data used in this study. Some published study recruited periodontists only. As for the examination of the periodontal status: eight studies the periodontal probe used wasn’t mentioned. Four of the included studies used a lightweight CPI probe that is recommended by the WHO. Three of the studies used a PCP 11 periodontal probe (Ho Friedy, Chicago, IL, USA), one of the study used a PCP UNCLK periodontal probe (Ho Friedy, Chicago, IL, USA) and finally one of the studies used a Williams probe.
Five of the publications used exclusively the CPITN to examine the patient. Nine of the included studies used different indexes to record the periodontal status. All of the indexes were the same for all of them, some publications used more indexes (cf. Table
3 for complete description) the indexes mainly used by the studies was the PD, CAL,
BOP. Every time those indexes were used they were recorded on the six classic point of the tooth: mesio-buccal, mesial, mesio-lingual, disto-buccal, distal, disto-lingual. One of the publication used the half mouth method were probing depth and clinical attachment level are recording on one side of the mouth left or right [11].
5.2.1.3 Periodontal disease definition and classification:
The publications that used the CPITN to record the periodontal status defined periodontitis when the CPITN score was 3 or more. As for the studies that used all of the indexes mentioned above. Three of them described periodontitis as a result of the clinical attachment loss and the probing depth increased, those studies stated that 5% of the present tooth must have a probing depth > 4mm and/or a clinical attachment loss of 4 mm or more. One of the studies (Wilkins et al, 2017, USA) described periodontitis according the alveolar bone loss. Periodontitis in this study was set when 7 or more of the examine teeth had an alveolar bone loss superior or equal to 20%.
The other publications didn’t describe how periodontitis was defined or didn’t mentioned how they classified the patient as suffering for periodontitis in most of the cases these studies were aimed to defined periodontal status in general.
Six of the included publications made two group of patient they divided them into healthy or gingivitis and periodontitis group. The other published study made different classification. One of them divided the patients not according the periodontal status but according obesity. So the patients were divided into an obese and a non-obese groups (Martinez-Herrera et al, 2016). The other study decided to work only with patients suffering from periodontitis, in this case the patients were divided into a low-threshold periodontitis group (defined as two teeth had at least 6 mm of attachment loss and one pocket of 5 mm of more) and a high-threshold periodontitis (define as if >15% of all teeth had an attachment loss superior to 6 mm and one with deep pocket superior two 6 mm) (Linden, 2007).
Finally, only one of the publication decided to divide the patient into different groups: healthy, moderate periodontitis, and severe periodontitis. (Wilkins, 2017)
5.2.2 Anthropometric protocol:
5.2.2.1 Anthropometric indices:
The relevant index in order to obtain anthropometric measurement is the Body mass index. This index is used in all the publication present in this systematic review. This index was defined by the WHO and the way of calculating is very precise [49]. The BMI can be calculated by dividing the weight of an individual in kilograms and his height in centimeter in the power of two [49]. The majority of the included publications in this systematic review used also other indices in order to have a good overview of the anthropometric characteristic of an individual. The main one that almost every publication use, was the waist circumference ratio which is measurement of the midpoint between the lower margin of the last rib and the top of the iliac crest. The hip circumference should be measured around the widest portion of the buttocks. [48]
to 25 is considered as overweight and when the BMI reaches 30 or more an individual is considered as obese [49] [50]. Under those BMI numbers the patient is considered as normal weight or underweight. All the publications present in this systematic review used the classification of the WHO to define obesity and overweight or at least used the number of a BMI superior or equal to 25 to categorize the patient to an overweight or obese group. Waist circumference and waist hip ratio were also used in the studies, but they weren’t used to state the obesity or the overweight of a subject, those data were use to confirm the overweight or obesity. Also, those data when recorded sometimes showed that someone with the same BMI but different waist hip ratio could have different result on the periodontal status.
5.3 Outcome:
5.3.1: Measurement outcome result:
The outcome result of the periodontal status is mentioned above (3.2.1.3), as a reminder we can say that most of the publications classified the patients into periodontitis and non periodontitis group. Sometimes the group were as well classified according the severity of periodontitis. Other factors have been recorded by some studies that weren’t periodontal neither anthropometric. Those factors were often and in most of the cases inflammatory markers, due to the fact that those markers play a major role in the periodontitis development and it is now known that obesity has an impact on them. Four of the publications (Wilkins,
2017; Elangovan, 2014; Martinez-Herrera, 2016 and Jentsch, 2017) recorded the
inflammatory markers. In both publications those factors are the Interleukins (IL-1, 2, 3, 4 …and their variations). Elangovan, 2014 as well has two variates recorded, other types of inflammatory factors such as the cytokines, TNF and more. He also recorded the gingival crevicular fluid level and the peri-implant sulcular fluid. It should be also noted that
Martinez-Herrera, 2016 recorded the insulin resistance factor and the cholesterol, in order to place the
participant into lean and obese groups. In the study made by Jentsch, 2017 the focus was mainly, on Ghrelin and its relation to cytokines in obese patient compare to non obese. So in total 25% of the studies included in this systematic reviewed, produced result about the inflammatory markers, and their relation to obesity and periodontitis.
Two of the publications included the fitness or strength of the participant in their study in order to see if obesity was correlated to periodontitis or if physical condition was a part of it as well. One of this publications, recorded the VO2max (Shimazaki, 2010) and the other one
was more focused on the strength, and in that purpose they recorded the handgrip strength of the participant included in the study. 12,5% of the studies presented in this analysis included fitness or strength to the relation between obesity and periodontitis.
Finally, 62,5% of the studies, recorded only the relation between periodontitis and obesity, without any other variables involved.
5.3.2. Result of the publications:
All of the present publications, showed a sort of association between the obesity, overweight and the prevalence of periodontitis. Although some studies demonstrated that there was a correlation between obesity and bad oral hygiene which could then lead to periodontitis. (Kim
et al, 2011)
It is also interesting to note that sometimes the body mass index wasn’t the best indicators. In the study by Meisel, 2015 was showed that women although having a healthier periodontium had an increase in their inflammatory markers compared to the men with an equival waist hip ratio.
At the microbiological level two published studies demonstrated that the patients with an elevated BMI compared to the normed, had an increase amount of pathogenic bacteria related to periodontitis present in their oral cavity. This can be explained by the modifications of the immune response and inflammatory reactions in overweight/obese people. Haffajee, 2009 demonstrate the increase in T. Forsythia, whereas Jentschl, 2017 demonstrate an increase in
Porphyromonas gingivalis and Treponema Denticola. [15] [18]
Two of the publications recruited in this systematic review managed to show a statistical correlation between the BMI and the risk of periodontitis. Both of them, stated that by an increase of Kg/m2 the risk of periodontitis is thus elevated. According to the study by
Martinez-Herrera et al, 2016, the risk of periodontitis is increase by 1,11 per kg/m2. In the
one by Shrestha S et al, 2016, it is stated that the risk of periodontitis is increase by 39% for each Kg/m2. [27] [53]
Four publications, that assessed the inflammatory markers IL-1 was shown to have an impact on periodontitis in 75% of them. Although one of the study showed that only
pro-(Elangovan, 2014 and Jentsch, 2017). Jentsch, 2017 also showed association between the level of ghrelin and a body mass index for obese patient. [51] [10] [18]
5.4 Influence of covariates:
In all of the publications, except one (D. Ekuni et al. 2008), the covariates have been assessed. In most of the cases the covariates account for the socioeconomic status, the smoking, and the oral health behavior. Those are important to be assessed because they play a role in the periodontitis and the result can be bias in function of the importance of the covariates in the number of participants.
5.5 Quantitative data analysis result:
Events: define here as the number of subjects suffering from periodontitis in the overweight/obesity and control/normal group
Total: total number of subjects in the two different group
Figure 1. Meta-analysis forest plot of the subgroup of the publications included in this work. The blue box shows the odds ratio and the line the standard deviation of this one. The diamond box shows the overall odds ratio.
According the forest plot presented in figure 1. all the publications included in it had a statistical significance except the study made by Jentsch, 2017. The diamond that indicated the mean odds ratio of the included publications shows us that overall the statistical significance. This significance is present for the publications included here
Experimental: periodontitis patient Control: Healthy patient
Mean and SD of the BMI
Total: total of patient in each group experimental or control.
Figure 2. Meta-analysis forest plot of the mean BMI and its standard deviation in experiment and control group. The green box shows the mean difference and the line the standard deviation of this one. The diamond box shows the overall odds ratio
According to the forest plot presented in figure 1. All studies included in it had a statistical significance. The diamond that indicated the mean odds ratio of the included publications shows us, that overall the statistical significance is present, for the publications included here
6. DISCUSSION:
6.1. Obesity and behavior:6.1.1 Obesity and oral hygiene behavior: [32] [22]
As known already oral hygiene behavior plays a big role in the development of periodontal disease. So the goal of our review was to determine if people suffering from obesity have different oral hygiene habit than people considered as non obese.
Multiple publications have demonstrated that the oral hygiene in obese patients was different and more worrying than in patient being of normal weight. A study published in 2016, in Finland (Nihitla, 2016), demonstrated that 22,2% of the overweight individuals were brushing their teeth once a day. In this published study it was also estimated that 18,4% obese patients had their last dental visit more than 2 years ago, however only 13,2% patients with normal weight had their last dental visit more than 2 years ago. Another finding of the publication was that 21,3% obese patients were visiting their dentist for emergency treatment, however only 13,2% patients with normal weight had dental emergency requirement
.
Also in the study review in the annex 5 by Kim, 2011, showed that the correct and consistent use of dental floss decrease the risk of periodontal disease. However, in case of obesity even the use of dental floss doesn’t decrease the risk of periodontitis.6.1.2 Nutrition and its roles: [12]
6.1.2.1 Role of Nutrition on the periodontium: [30] [16] [30]
The alimentary composition of macro and micronutrients has an impact on the periodontium. This data is acquired by the scientific community since a certain number of year. Unfortunately, obese individuals have different alimentary composition than people considered as normal. The publication by, Najeeb, 2016 made an update on the role of nutrition in the periodontal health. In their review it is explained how vitamins B, D and E can help in the post surgical healing of the periodontium. They also explain that deficiency in vitamins C and K can accelerate gingival bleeding.
As well, they develop the fact that antioxidant may help reducing the gravity of periodontal diseases due to the fact that after a trauma the periodontium is under a state
of oxidative stress but if the balance of antioxidant is not good disease can develop faster.
Figure 1. Antioxydant affection on the periodontium, Najeeb, 2016 [30]
It was explained that magnesium helps in bone formation as well as calcium and that iron and zinc can play the role of antioxidant.
6.1.2.1 Nutrition and obesity: [47]
Via, 2012, published a review about the micronutrient deficiencies in obese people.
This has been widely known for a certain time, especially due to the fact that nowadays obese people can find processed food poor in micronutrient essential for health. They stated that obese people lack in vitamin D, (between 80-90% of obese individual are lacking vitamin D). They also showed that obese people lack of Vitamins C, A, E, Zinc and vitamin B.
Figure 2. Prevalence of micronutrient deficiencies in obesity and diabetes. Vial, 2016 [47]
From this data it can be concluded, that nutrients are essential for development, progression and healing of periodontal disease, and that most of obese/overweight individual are lacking those important nutrient. According to this data, obese/overweight people need more time to heal from periodontal disease.
6.2 Obesity and inflammatory response: [2] [3] [14] [24] [25] [29] [45] 6.2.1 Inflammatory response: reminders
Immunity is the response or the resistance of the organism to an infectious disease such as periodontitis. The immune system is divided into innate and acquired. The acquired immune system can be humoral or cell mediated. The first response to periodontitis by the organism is from the humoral immune system. [40]. Different proteins, cells and pro-inflammatory mediators are secreted by the periodontium:
Cytokines: are soluble proteins. It’s a type of signaling molecules that are excreted from t cells. They include a wide range of different component such as IL_1, IL_12, IL_8, tumor necrosis factors and others. They contribute to the inflammatory reactions. [7]
IL-1 and 8: IL_1 inhibits the expression of pro-collagen. It helps in retaining various inflammatory cells, and they increase the osteoclastic activity by stimulating the osteoclasts. IL-8 is affecting a wide range of responses. They have an influence on the migration and activity of the
phagocytes. When the IL-8 are exposed to the fibroblast it leads to inflammatory changes. [17] [40]
Defensins: small proteins that bind to the cell membrane and form defect on the bacterial membrane to help for phagocytic activity. [40].
Resistins: found in adipose tissue and is implicated in glucose metabolism as well as in pro-inflammatory reaction it increases the production of cytokines such as IL_1, IL_6, TNF and others. [39]
Complement system: proteins that are part of the hematopoietic cells and are at the number of 30 and act as a chain reaction once activated. They enhance the ability of antibodies and phagocytic cell to perform their work. [5]
TNF : one of the cytokines that makes the acute reaction of the inflammation. They regulate the immune cells such as the T and B cells. [40]
Numerous known cells act as well such as neutrophils, leukocytes, macrophages
Figure 3. Inflammatory reaction leading to bone loss in periodontitis, Hajishengallis, 2014, [16]
6.2.2 Peculiarity of inflammatory response in obese individuals
Adipose tissue is the main energy reserve of the human body. It stores the energy as fat. Two different types of lipocytes are differentiated: the white adipose tissue and the brown adipose tissue. The brown adipose tissue is present to make the adipose tissue together [1] [38]. The white adipose
increases. White adipose tissue is responsible for the process named as lipolysis which is the breakdown of lipids to be used by the organism in order to produce energy [1] [38].
In a review publish in France by Makki, 2013 they evaluated that obesity is related to inflammation and insulin resistance. They demonstrated that adipose tissue promotes an inflammatory response in obesity. In 1990 it was demonstrated that adipose tissue had a secretory and endocrine role and subsequently could synthesize and secrete pro-inflammatory cytokines such as tumor necrosis factor (alpha) and the hormone leptine which is responsible for regulating the appetite. Those evidences demonstrated that the adipose tissue had a major role in glucose metabolism and immunity reactions. The adipose tissue of an obese individual mainly secrete pro-inflammatory cytokines such as TNF and IL-6 which have been shown to play a role in the development and progression of periodontitis. [24]
In this table produced by Makki, 2013 it is shown that almost all the cytokines, responsible for the pro-inflammatory reactions increases in obese individual and the insulin resistance factors also. All those cytokines can play a role in periodontitis development.
For example, as it is explained above that IL-1, 6 and 8 as well as TNF are increased in obese individuals and sometimes this increase could be proportional to the BMI of the patient. [24]
The publication by Weisberg, 2003 showed that the number of macrophages present in the adipose tissue of obese individuals were highly increased compared to normal weight individuals. Macrophages are one of the main sources of pro-inflammatory cytokines secreted by the adipose tissue especially TNF and IL-6, as mention above, they play a major role in the periodontitis development. [53]
Additionally, the rise in IL-8 within obese individuals result in the presence of neutrophils within adipose tissue, as the former has a chemotactic effect. The neutrophils as well play a role in the early stages of inflammatory response. [53] [24]
6.2.3 Effect on periodontium:
In a review published, by Graves, 2003 it was shown that, the contribution of the different cytokines or pro-inflammatory factor in the periodontal destruction and thus their role in the development of periodontitis. The review focused mainly on the role of IL-1 and tumor necrosis factor and their implication in periodontal diseases. They showed that IL-1 as well as TNF were stimulated by molecular adhesion and chemokine expression and the production of inflammatory mediators which lead to inflammation. They also enhanced the osteoclastic activity resulting in bone loss. In addition, they induced the expression of the metalloproteinase, which created a connective tissue breakdown. Finally, the apoptosis of the matrix producing cells was increased because of those proteins. [14]
Figure 4. Mechanism by which IL-1 and TNF contribute to periodontal tissue lost, Graves et al, 2003, USA [14]
That information’s are linked with the 4.2.2 paragraphs of this systematic review.
In the review it was explained that TNF and IL-1 were produced and secreted by certain cells such as macrophages [14]. As it is seen above (figure 4) macrophages are highly increased in case of obesity or overweight. Those data could explain a part of the result found in the different publications used in the systematic review that shows an increase of periodontitis in obese patient. The fact that the cytokines are increased in those individuals would increase and accelerate the destruction of the periodontium.
In the same manner as mention above, many studies in this systematic review, demonstrated a correlation of the inflammatory markers (cytokines) and the body weighy. The study by Jentsch,
2017, which recorded the level of Ghrelin which is associated with the expression of cytokines in
healthy and periodontal patients. It was demonstrated that the level of ghrelin was lower in healthy patients but was higher in patients suffering from overweight/obesity and periodontitis [18]. This could be due to the increase of pro-inflammatory mediators in patient with an increased BMI.
So all those inflammatory markers play an important role in the development of periodontitis. In obese patient those markers are increased so the inflammatory process and thus the destruction process of the periodontium is increased as well in patients suffering from periodontitis and obesity.
6.3 The infectiobesity theories: [13]
Infectiobesity is related to the condition of obesity arising from infection. It was first mentioned in the publication, dealing with the micro flora of the intestine and other organs in order to compare it from obese and non obese individuals.
In 2009, Goodson, published a clinical research showed the difference in microbiota between obese and normal weight individuals for this he recruited 232 women as control group and 313 women with a BMI between 27 and 32 in order to collect some saliva samples and then estimate the difference in the bacterial composition. All of the recruited persons were healthy and didn’t have periodontitis. The publication, demonstrated that the number of bacteria, was increased in people suffering from obesity compared to those being considered as normal weight. The main bacterial difference was for the bacteria named as S. Noxia.
Goodson by his study developed 3 different hypotheses:
The first one: is that the oral micro flora could increase the metabolic efficiency as suggested by other infectiobesity publication by this a little excess in calories consumption could with no change in diet result in weight gain. An increase by 100 cal/day would add around 4,5kg. The second one: stated that oral bacteria could increase weight gain by increasing appetite. The third one: redirect energy metabolism by increasing insulin resistance by elevating the
level of TNF and/or reducing the level of adiponectin.
Those theories are summarized in a figure and it demonstrate a real vicious circle for people suffering from obesity.
Figure 3. Hypothesis by which oral bacteria could affect body weight and contribute to obesity, Goodson et al, 2009, USA [13]
6.4 Obesity as a risk factor for periodontitis:
As shown in the descriptive result of the publication reviewed in this systematic review, people suffering from obesity are more prone to periodontitis as well. This is possibly due to the multifactorial effect of the obesity. In fact, obesity, adds multiple factors, that also play a role in the periodontal diseases, such as the inflammatory mediators, bone modulation, nutrients, and the oral micro flora.
In this systematic review also it should be noted that in a lot of publications the population of obese people used in the test group were often less than the control group. Also, a lot of the publications had not enough obese people available or not enough obese participants were present and it was then decided to join the groups of overweight and obese people. For example, in the study made by D.
Ekuni, 2008, obese people were available but demonstrated that overweight people were more prone
to periodontitis. So the weight could definitely have an impact on the periodontal health.
Obesity, as well known already, is one of the main risk factors for the development of diabetes which as shown before has an influence on periodontitis as well.
Unfortunately, all the different co-factors used in this thesis has an importance that needs to be taken into account. Especially the amount and duration of smoking, that is important in periodontal disease.
parts for the control of the periodontal disease. As stated before obese people tend to have an oral hygiene compare to a population stated as normal.
The strength of this research work lies on the fact that, the main focus point was the association between obesity and periodontitis and their correlation in the general population. No other factor has been taken into account and the publications reviewed in the systematic reviews have scientific relevance by the number of patients and the methods used.
However, some limitations are present as well, due to the fact that the age was not a concern. Any patient aged more than 18 could be incorporated according the inclusion criteria (4.3). Although, in the descriptive result, it can be seen that, most of the people were mainly of older age, in case of a future research, age group could be included in the inclusion criteria. As well the gender of the participants for the included studies wasn’t a concern for this particular systematic review but it could have been taken into account and could be for future research due to the fact that males are more prone to obesity, as well as periodontal diseases. Two of the studies included only males, which could have an impact on the result found.
Another limitation is the fact that impacts of obesity has been taken into account. Such as the different co-morbidities factors as cardiac disease, or metabolic diseases. As well none of the study mentioned the reasons why the patient were suffering from obesity (eg. food induced, hormone imbalance, genetic diseases…). This can be due to the fact, that in most of the cases, obesity is linked to a poor caloric balance. Only few studies, showed a negative correlation between the two variable studied here. This might be due to the fact that the researcher didn’t publish negative relation.
7. CONCLUSIONS
Obesity is an epidemic that reached the whole world and is spreading even more. This “genotype-environmental” disease will be on the rise in the next few years.
To conclude this systematic review, and after qualitative and quantitative analysis of the recent publications included it can be stated, that a certain relationship exists between obesity and periodontitis. The hypothesis stated in the introduction of this work is contradicted. Obesity is already classified as risk factor for a number of inflammatory diseases such as arthrosis, diabetes mellitus and multiple cardiac problems, it could also be the case for periodontitis. However, a certain number of publications need to keep investigate the relation between the two. We can say that for adult subject that are suffering from overweight or obesity are more prone to an over inflammatory state and then more prone to the development of periodontal disease.
The relation between obesity and periodontitis can be explain by different mean, that are linked to the obesity, especially at the level of the inflammatory reaction regarding obese people. As seen above obese people tend to have an increase amount of inflammatory markers which thus will lead to a faster infection by the bacteria of periodontitis and to its development. Alongside obese people lack different nutrient and have poor oral hygiene, the healing post treatment for obese might be longer as well as that the development of the disease could be faster. Finally, the infectiobesity theory could explain why obese people that are suffering from periodontitis tend to have a harder time to loose weight.
8. PRACTICAL RECOMMENDATIONS
After writing this systematic review, we can say that dentist nowadays should assess the weight and height of their patients and keep tract of them. So in the case of an increase in the body mass index the dentist could try to prevent the periodontal disease with the means such as oral hygiene education, and an increase number of dental visits.
Future research needs to keep investigating the link between overweight/obesity and periodontitis, as well as periodontal disease. The link between the periodontal inflammation and obesity should be thoughtfully researched around the world in order to have a better understanding of it. As well the studies could focus on particular age group and on the difference between male and female reaction to periodontal disease in case of overweight and obesity.
As peri-implantitis is a disease that is increasing around the world and that more and more implants are placed every year, the reaction of the periodontium to implant placement in an obese subjects could be a source of future research as well.
9. CONFLICT OF INTEREST
The author of this study report no conflict of interest.
10. FUNDINGS
No funding was received for this work.
11. ACKOWNLEDGEMENT
I would like to thank:
The member of the jury for reviewing this systematic review;
Dr. Alma Pranckevičienė, as supervisor for this work;
My parents for there support throughout the year and the motivation they provided;
My sister and brother, Romane, Selma, Adam, for always being by my side;
Simon Radmand as a brother during the hard times;
Hassan Younes, Artin Hosseinion, in the hard work that this systematic review will have gave us;
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