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Obesity and periodontitis: systematic review and meta-analysis/Obesidade e periodontite: revisao sistematica e meta-analise.

Introduction

The prevalence of obesity is increasing worldwide (1). Obesity, defined as a Body Mass Index (BMI) [greater than or equal to] 30 kg/[m.sup.2], and overweight (BMI [greater than or equal to] 25 kg/[m.sup.2]) are becoming a worldwide epidemic estimated to involve 1.7 billion people in developed and developing countries (2), being considered a public health problem (3). According the WHO Global Infobase, the prevalence of obesity among american adults in 2010 was 44.2% in men and 48.3% in women, and the global obesity epidemic keeps to increase (4).

This disease is so common among the world population that it is becoming the most important contributors to ill health (3). This is a complex and multi-factorial disease arising from excessive storage of fat, resulting from the interaction of social, behavioral, cultural, psychological, metabolic and genetic factors (5). Obesity causes or exacerbates a large number of health problems, both independently and in association with other diseases (comorbidities) (3). These diseases may be type 2 diabetes, hypertension, hypoventilation, sleep apnea, venous stasis, tumor, regenerative joint disease, and others (6).

Overweight and obesity have been suggested to be associated with periodontitis, because obesity may have some effects on systemic health by affecting the host susceptibility to periodontitis due to inflammatory mediators (7). Periodontitis is a common chronic inflammatory oral disease of the adult population characterized by a gingival inflammatory response against a pathogenic bacterial microflora, resulting in alveolar bone loss and eventually tooth loss (8). The link between periodontitis and obesity may have relevant public health implications because both diseases are important risk factor for cardiovascular diseases (9-11).

However this association is not entirely clear in the literature because there are controversies on finding of the studies. Obesity have been associated with periodontitis in some studies (12-15) and not in others (16-18). For these reasons the present study aimed to review systematically the studies on the association between overweight/obesity and periodontitis.

Materials and Methods

Search Strategy and Study Selection

The methods applied in this review included a literature search strategy, inclusion and exclusion criteria for selecting the studies, selection process and data extraction and quantitative data synthesis.

The Cochrane Library revealed no systematic review on association between obesity and periodontal disease in adults. Subsequently, we searched PubMed (Medline), Embase and LILACS using the following combinations of keywords in English, Spanish and Portuguese: Obesity OR body weight OR Body mass index OR overweight OR abdominal fat OR obese AND periodontal diseases OR gingivitis OR periodontitis OR alveolar bone loss.

Inclusion and exclusion criteria for selecting studies

The inclusion criteria were human studies with subjects up 15 years old, written in English, Spanish and Portuguese, investigating whether or not obesity is a risk factor for periodontitis. Those papers that were published until 2010 were selected.

Excluded were those case reports describing periodontal conditions in obese, ecological studies, experimental animal studies and reviews. In addition, published studies showing repeated results from the same original study were excluded. Studies that had inadequate or unclear scoring systems for the measurement of periodontal disease and nutritional status were excluded. Periodontal measures were classified as adequate when clinical measures were based on periodontal pocket depths (PPD) and/or clinical attachment loss (CAL) measures or based on Community Periodontal Index (CPI) or alveolar bone loss (Alveolar Bone Score - ABS) assessed using radiographs or tooth mobility. Nutritional status was classified as adequate when it was assessed through Body mass index (BMI) or Waist Circumference (WC).

Selection process and data extraction

Two reviewers (P.G.M.G. and C.A.P.C) independently retrieved and evaluated the articles for eligibility. The extraction of information from studies was conducted by the first and a third reviewer (J.A.M.), and the information included number of patients, the range and the mean of age, gender (n), country of the sample, method of periodontal disease evaluation, method of nutritional status evaluation and the main results. Any discrepancies between reviewers were discussed with a fourth reviewer (S.H.C.S.P.) and resolved by consensus. We recorded general study characteristics in Table 1.

Data Synthesis and Analysis

A descriptive analysis was performed using frequencies and means. Studies that did not present the results of periodontal measures and of nutritional status were scored as unclear and were excluded of meta-analysis. Studies with data type dichotomous the statistical method used was Mantel-Haenszel with odds ratio as effect measure. For this analysis it was considered as event the number of subjects with periodontitis, divided into control group (subjects with normal nutritional status) and experimental group (subjects with overweight and obesity). Studies with data type continuous the statistical method used was Inverse Variance with mean difference as effect measure. Mean and standard deviation of BMI were distributed between control group (without periodontal disease) and experimental group (with periodontal disease). Review Manager 5.0 computer program was used.

Results

As shown in Figure 1, from a total of 822 identified records by the three search strategies, 103 were manually selected on the basis of their titles and abstracts, with interobserver agreement. A further 72 were excluded, leaving 31 papers for the meta-analysis (Figure 1). All studies were cross-sectional.

The risk of periodontal disease was associated with obesity in 17 studies, it had a tendency for this in 8 studies, and 6 studies had not associated.

The studies that showed the number of participants with events (periodontal disease) and total number of participants in experimental (obese) and control groups (normal weight) were included in dichotomous meta-analysis (n = 22; Figure 2). Compared with normal weight, overweight and obesity conferred increased odds of periodontal disease, with an odds ratio (OR) of 1.30 [95% CI, 1.25-1.35].

Studies with data of the BMI mean, standard deviation and number of participants in experimental (with periodontal disease) and control groups (periodontally healthy) were included in continuous meta-analysis (n = 13; Figure 3). Meta-analysis showed a significant difference of 2.74 kg/[m.sup.2] [95% CI, 2.70 - 2.79] on BMI mean. Compared with the control group (without disease), the experimental group presenting greater BMI.

Discussion

This systematic review was performed to contribute to higher cientific evidence about the association between periodontitis and obesity, and a statistical method (meta-analysis) was incorporated to strengthen the findings.

The weight of the studies toke into account mainly the sample size in meta-analysis. Studies with a larger sample, therefore relevant weights, showed an odds ratio of 1.15 or more of disease occurs among obese, or that individuals with periodontitis presented a difference of 2.70 to 3.96 Kg/[m.sup.2] over in BMI compared to periodontally healthy individuals. It points to an association between obesity and periodontitis. The odds of periodontitis in overweight/obesity group was significant statistically. Of the 31 studies, more than 50% (n = 17) observed association between overweight or obesity with periodontitis and the other half considered this association equivocal (n = 6) or unclear (n = 8), because found that body weight weakly predicts the development of periodontal infection, so the evidence for an association between obesity and periodontitis may be insufficient. However, the meta-analysis also showed that mean BMI was lower in the periodontally healthy group. Of the 13 studies that presented data for this analysis, only 4 did not showed great differences in mean BMI between the groups. Therefore, the association between obesity and periodontitis became true again.

Some recent cross-sectional studies have suggested an association between body weight and periodontal disease in young subjects (23,26,44), however no association was detected in the study of Lundin et al. (29). Regarding to older subjects, no association was observed in this age group in numerous studies (17,20,27,28,39), suggesting that other systemic factors, not the obesity, related to age may contribute to periodontitis, factors that possibly have not been present in elderly Japanese women because in the studies of Saito (35) and Saito et al. (34) reported an association of BMI with periodontal disease.

These conflicting findings occurred probably due the methodological heterogeneity among the studies. In the meta-analysis it was high (I2 = 98%). Although we have been chosen studies with similar methodologies in obesity and periodontal evaluations, they differ in some aspects, such as sample size, confounder variables control, age range and preliminary calibration, characterizing low homogeneity among them. Some factors determine the quality of the studies, such as sampling calculation, calibration of examiners and adjustment for potential confounders (45).

It may be noted that only 2 studies performed the sample calculation (22,26) and other 5 studies obtained their sample from a National Survey, which usually is performed the sample calculations, moreover, because it is nationwide study, the sample size is large which makes the data more reliable and relevant. If we analyze just these 7 studies, considering them of better quality, we can confirm that this association is true be cause five studies observed association between obesity and periodontitis and only 2 observed a trend of association (21,46).

The calibration of examiners is important to standardize the periodontal assessment and to obtain reliable results. Despite this, clinical calibration was not performed in 13 papers. Of the 18 studies that performed the calibration, 10 presented the results with kappa value. The degree of agreement ranged from moderate to very good (47). Only 2 found no link between obesity and periodontitis, wich evaluated only older population (39) and another study the kappa value was 0.52 (17).

The most of the studies adjusted the confounding variables by multivariate statistical analysis, especially regarding to gender, age and smoking status. Few studies reported the influence of sociodemograph factors or physical activity and few bothered to consider the presence of diabetes in the exclusion criteria and the diabetes often coexists with obesity and periodontal infection (48), but the most excluded the individual that had not received systemic treatment with antibiotics.

Confounding control is of increasing importance as periodontal research addresses the associations between periodontal disease and systemic diseases. This is especially pertinent when dealing with smoking that is a major risk factor for both periodontal disease and systemic diseases (49). The association between high body weight and periodontitis could be due to common lifestyle characteristics that make subjects more prone to both obesity and periodontitis (46), for example, an unhealthy dietary patterns with insufficient micronutrients and excess sugar and fat content could thus pose a risk both diseases (19). As well as obesity can be a indirect predictor of periodontitis because insulin resistance (7) and low social class (43) appeared to mediate this relationship.

All these studies about the link between obesity and periodontitis were cross-sectional or case-control, so prospective studies are needed because it is still unclear how obesity may have an adverse effect on the periodontium. One of the possible mechanisms that explains an association between obesity and periodontitis may include hepatic disorders (50) the fact of the adipose tissue secrete proinflammatory cytokines which may be the molecules linking the pathogenesis of these diseases (7). The association between BMI and tumor necrosis factor- a (TNF- [alpha]) in gingival crevicular fluid (29) suggests that TNF-[alpha] in this fluid is derived from adipose tissue in obese subjects (51). In addition, an increase in serum level of interleukin 6 and resistin, both secreted by adipocytes, has been proposed to be associated with periodontitis (15,35). Furthermore, Haffajee and Socransky (25) observed an overgrowth of Tannerella forsythia in the subgingival biofilms of periodontally healthy obese individuals, that might put them at risk for initiation of periodontitis. It suggests a possible relationship between obesity and periodontitis.

The results of the present systematic review provide evidence that there is an association between overweight/obesity and periodontal infection, nonetheless the strength of the association may be underestimated due the heterogenecity of the studies. Thus, all health professionals, including the dental team, can provide to education, prevention and treatment for obese patients about the risk of periodontal diseases.

Conclusion

There is a link between obesity and periodontitis, however the risk factors that aggravate these diseases should be clarified to elucidate the direction of this association. Nevertheless, oral health care measures should be implemented to obese patients. Working with paired samples and avoid confounding factors may contribute to the homogeneity of the studies. These suggestions can improve the scientific evidence that might address these concerns.

Collaborations

PG Moura-Grec was involved in the original conception of the research, carrying out the study (data search, paper selection, extraction of information and meta-analysis) and writing of the manuscript. JA Marsicano contributed at the extraction of information from studies. CAP Carvalho contributed at the evaluation of the articles for eligibility and reviewed the manuscript. SHC Sales-Peres was involved in the original conception of the research, contributed at the extraction information from studies, and reviewed the final version of the manuscript.

DOI: 10.1590/1413-81232014196.13482013

Acknowledgements

The authors thank the librarian of the Bauru School of Dentistry, Cybelle de Assumpcao Fontes, for guiding on the literature search strategy.

References

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Artigo apresentado em 05/08/2013

Aprovado em 18/11/2013

Versao final apresentada em 26/11/2013

Patricia Garcia de Moura-Grec [1]

Juliane Avansini Marsicano [1]

Cristiane Alves Paz de Carvalho [1]

Silvia Helena de Carvalho Sales-Peres [1]

[1] Department of Pediatric Dentistry, Orthodontics and Public Health, Bauru School of Dentistry, University of Sao Paulo (USP). Alameda Octavio Pinheiro Brisola 9-75, Vila Universitaria. 17.012-101 Bauru SP Brazil. shcperes@usp.br

Table 1. Characteristics of the included studies (n = 31).

Reference (Author, year)          Subjects (n)   Age range    Mean
                                                               age
                                                             (years)

Al-Zahrani et al., 2003 (19)           13.665    [greater        NR
                                                  than or
                                                 equal to]
                                                       18
Borges et al., 2007 (20)                  318    [greater      57.0
                                                  than or
                                                 equal to]
                                                       30
D'Aiuto et al., 20 0 8 (21)            13.677        > 17        NR
Dalla Vecchia et al., 2005 (22)           706       30-65        NR
Dumitrescu; Kawamura, 2010 (12)            79       19-69        NR
Ekuni et al., 2008 (23)                   618       18-24      21.4
Furuta et al., 2010 (24)                2.225       18-19      18.6
Genco et al., 2005 (7)                 12.367          NR      43.5

Haffajee; Socransky, 2009 (25)            695       18-86      46.8
Han et al., 2009 (13)                   1.046       15-84      40.8
Khader et al., 2009 (14)                  340       18-70        NR

Kongstad et al., 2009 (17)              1.504       20-95      52.8
Kumar et al., 2009 (26)                   513       18-54      32.6
Kushiyama et al.,2009 (18)              1.070       40-70        NR
Li et al., 2009 (27)                      208       37-78      61.1
Linden et al., 2007 (28)                1.362       60-70      64.2
Lundin et al., 2004 (29)                   32       13-24      17.8
Machado et al., 2005 (30)                  60        > 20      43.9
Morita et al., 20 09 (31)               2.478       24-60      43.3
Pitiphat et al., 2008 (32)                121       20-67      40.5
Saito et al., 2001 (33)                   643          NR      45.6
Saito et al., 2005 (34)                   584       40-79      56.6

Saito, 2008 (35)                           76       55-59      55.0

Saxlin et al. 2010 (36)                   214       30-59      44.3
Saxlin et al., 2008 (37)                1.297       30-49        NR
Shimazaki et al., 2007 (38)               584       40-79      55.7
Torrungruang et al., 2005 (39)          2.005       50-73      60.0
Wang et al., 2009 (40)                 12.123       35-44      39.5
Wood et al., 2003 (41)                  8.842    [greater        NR
                                                  than or
                                                 equal to]
                                                       18
Wood; Johnson, 2008 (42)                1.098        > 18        NR

Borges-Yanez et al., 2006 (43)            365        > 60      73.0

Reference (Author, year)          Percent     Country
                                  female
                                    (%)

Al-Zahrani et al., 2003 (19)        52.7        USA

Borges et al., 2007 (20)            55.0      Brazil

D'Aiuto et al., 20 0 8 (21)           NR        USA
Dalla Vecchia et al., 2005 (22)     53.4      Brazil
Dumitrescu; Kawamura, 2010 (12)     60.8      Norway
Ekuni et al., 2008 (23)             52.1       Japan
Furuta et al., 2010 (24)            43.2       Japan
Genco et al., 2005 (7)              53.1        USA

Haffajee; Socransky, 2009 (25)      49.6        USA
Han et al., 2009 (13)               54.5    South Korea
Khader et al., 2009 (14)            50.6      Jordan

Kongstad et al., 2009 (17)          53.9      Denmark
Kumar et al., 2009 (26)               NR       India
Kushiyama et al.,2009 (18)          73.7       Japan
Li et al., 2009 (27)                54.8       China
Linden et al., 2007 (28)             0.0        UK
Lundin et al., 2004 (29)            65.6      Sweden
Machado et al., 2005 (30)           43.3      Brazil
Morita et al., 20 09 (31)           18.2       Japan
Pitiphat et al., 2008 (32)          73.6     Thailand
Saito et al., 2001 (33)             79.6       Japan
Saito et al., 2005 (34)            100.0       Japan

Saito, 2008 (35)                   100.0       Japan

Saxlin et al. 2010 (36)             58.4      Finland
Saxlin et al., 2008 (37)            60.8      Finland
Shimazaki et al., 2007 (38)        100.0       Japan
Torrungruang et al., 2005 (39)      25.6     Thailand
Wang et al., 2009 (40)              64.3      Taiwan
Wood et al., 2003 (41)              51.3        USA

Wood; Johnson, 2008 (42)              NR        USA

Borges-Yanez et al., 2006 (43)        NR      Mexico

Reference (Author, year)                 Method of periodontal
                                        evaluation and criteria

Al-Zahrani et al., 2003 (19)      PPD [greater than or equal to] 4 mm
                                   and CAL [greater than or equal to]
                                                  3 mm

Borges et al., 2007 (20)                   CPI scores 3 and 4

D'Aiuto et al., 20 0 8 (21)       PPD [greater than or equal to] 4 mm
Dalla Vecchia et al., 2005 (22)   CAL [greater than or equal to] 5 mm
Dumitrescu; Kawamura, 2010 (12)                PPD > 6mm
Ekuni et al., 2008 (23)                    CPIscores 3 and 4
Furuta et al., 2010 (24)          PPD [greater than or equal to] 4 mm
Genco et al., 2005 (7)               CAL [greater than or equal to]
                                                 1.5 mm
Haffajee; Socransky, 2009 (25)    PPD [greater than or equal to] 4 mm
Han et al., 2009 (13)                      CPI scores 3 and 4
Khader et al., 2009 (14)          PPD [greater than or equal to] 4 mm
                                  and CAL [greater than or equal to] 3
                                                   mm

Kongstad et al., 2009 (17)        CAL [greater than or equal to] 3 mm
Kumar et al., 2009 (26)                    CPI scores 3 and 4
Kushiyama et al.,2009 (18)                    CPI score 4
Li et al., 2009 (27)              CAL [greater than or equal to] 3 mm
Linden et al., 2007 (28)          PPD [greater than or equal to] 5 mm
Lundin et al., 2004 (29)          PPD [greater than or equal to] 4 mm
Machado et al., 2005 (30)         PPD [greater than or equal to] 5 mm
Morita et al., 20 09 (31)                  CPI scores 3 and 4
Pitiphat et al., 2008 (32)        PPD [greater than or equal to] 5 mm
Saito et al., 2001 (33)           PPD [greater than or equal to] 4 mm
Saito et al., 2005 (34)              PPD [greater than or equal to]
                                           1.9 mm (quintile)

Saito, 2008 (35)                   PPD 3 teeth [greater than or equal
                                  to] 4 mm or 1 tooth [greater than or
                                             equal to] 6 mm

Saxlin et al. 2010 (36)           PPD [greater than or equal to] 4 mm
Saxlin et al., 2008 (37)          PPD [greater than or equal to] 4 mm
Shimazaki et al., 2007 (38)       PPD [greater than or equal to] 2 mm
Torrungruang et al., 2005 (39)    CAL [greater than or equal to] 4 mm
Wang et al., 2009 (40)                     CPI scores 3 and 4
Wood et al., 2003 (41)            PPD [greater than or equal to] 3 mm

Wood; Johnson, 2008 (42)          PSR scores 3 and 4 (pocket [greater
                                       than or equal to] 3.5 mm)

Borges-Yanez et al., 2006 (43)    PPD [greater than or equal to] 6 mm

Reference (Author, year)           Method of nutritional evaluation
                                    and criteria to define obesity

Al-Zahrani et al., 2003 (19)        BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Borges et al., 2007 (20)                       BMI mean

D'Aiuto et al., 20 0 8 (21)           WC > 102cm (male) or > 88cm
                                               (female)

Dalla Vecchia et al., 2005 (22)     BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Dumitrescu; Kawamura, 2010 (12)     BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Ekuni et al., 2008 (23)             BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Furuta et al., 2010 (24)            BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Genco et al., 2005 (7)              BMI [greater than or equal to]
                                            27Kg/[m.sup.2]

Haffajee; Socransky, 2009 (25)      BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Han et al., 2009 (13)               BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Khader et al., 2009 (14)            BMI [greater than or equal to]
                                  30Kg/[m.sup.2] and WC > 102cm (men)
                                               or > 88cm
                                                (women)

Kongstad et al., 2009 (17)          BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Kumar et al., 2009 (26)             BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Kushiyama et al.,2009 (18)          BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Li et al., 2009 (27)                BMI [greater than or equal to]
                                        25Kg/[m.sup.2] and WC >
                                     90cm (men) or > 80cm (women)

Linden et al., 2007 (28)            BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Lundin et al., 2004 (29)                       BMI mean

Machado et al., 2005 (30)           BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Morita et al., 20 09 (31)           BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Pitiphat et al., 2008 (32)                     BMI mean

Saito et al., 2001 (33)             BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Saito et al., 2005 (34)                        BMI mean

Saito, 2008 (35)                    BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Saxlin et al. 2010 (36)             BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Saxlin et al., 2008 (37)            BMI [greater than or equal to]
                                      28.6Kg/[m.sup.2] (quintile)

Shimazaki et al., 2007 (38)       WC [greater than or equal to] 88cm
                                                (women)

Torrungruang et al., 2005 (39)      BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Wang et al., 2009 (40)              BMI [greater than or equal to]
                                            25Kg/[m.sup.2]

Wood et al., 2003 (41)                         BMI mean

Wood; Johnson, 2008 (42)            BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Borges-Yanez et al., 2006 (43)      BMI [greater than or equal to]
                                            30Kg/[m.sup.2]

Reference (Author, year)           Sampling
                                  calculation

Al-Zahrani et al., 2003 (19)           #

Borges et al., 2007 (20)              No

D'Aiuto et al., 20 0 8 (21)            #

Dalla Vecchia et al., 2005 (22)       Yes

Dumitrescu; Kawamura, 2010 (12)       No

Ekuni et al., 2008 (23)               No

Furuta et al., 2010 (24)              No

Genco et al., 2005 (7)                No

Haffajee; Socransky, 2009 (25)        No

Han et al., 2009 (13)                 No

Khader et al., 2009 (14)              No

Kongstad et al., 2009 (17)            No

Kumar et al., 2009 (26)               Yes

Kushiyama et al.,2009 (18)            No

Li et al., 2009 (27)                  No

Linden et al., 2007 (28)              No

Lundin et al., 2004 (29)              No

Machado et al., 2005 (30)             No

Morita et al., 20 09 (31)             No

Pitiphat et al., 2008 (32)            No

Saito et al., 2001 (33)               No

Saito et al., 2005 (34)               No

Saito, 2008 (35)                      No

Saxlin et al. 2010 (36)                #

Saxlin et al., 2008 (37)               #

Shimazaki et al., 2007 (38)           No

Torrungruang et al., 2005 (39)        No

Wang et al., 2009 (40)                No

Wood et al., 2003 (41)                 #

Wood; Johnson, 2008 (42)              No

Borges-Yanez et al., 2006 (43)        No

Reference (Author, year)          Were the examiners calibrated
                                   for periodontal assessment?
                                          (Kappa values)

Al-Zahrani et al., 2003 (19)                    No

Borges et al., 2007 (20)                        No

D'Aiuto et al., 20 0 8 (21)                   Yes *

Dalla Vecchia et al., 2005 (22)          k = 0.85 to 0.92

Dumitrescu; Kawamura, 2010 (12)                 No

Ekuni et al., 2008 (23)                         No

Furuta et al., 2010 (24)                      Yes *

Genco et al., 2005 (7)                          No

Haffajee; Socransky, 2009 (25)                  No

Han et al., 2009 (13)             k = 0.84 to 0.97 (intra); k =
                                           0.62 (inter)

Khader et al., 2009 (14)                        No

Kongstad et al., 2009 (17)                   k = 0.52

Kumar et al., 2009 (26)                      k = 0.84

Kushiyama et al.,2009 (18)                      No

Li et al., 2009 (27)                            No

Linden et al., 2007 (28)                      Yes *

Lundin et al., 2004 (29)                        No

Machado et al., 2005 (30)                       No

Morita et al., 20 09 (31)                       No

Pitiphat et al., 2008 (32)                    Yes *

Saito et al., 2001 (33)                  k = 0.58 to 0.75

Saito et al., 2005 (34)                         No

Saito, 2008 (35)                              Yes *

Saxlin et al. 2010 (36)                      k = 0.83

Saxlin et al., 2008 (37)                     k = 0.82

Shimazaki et al., 2007 (38)                  k = 0.80

Torrungruang et al., 2005 (39)           k = 0.72 to 0.90

Wang et al., 2009 (40)            k = 0.55 to 0.61 (intra); k =
                                       0.42 to 0.44 (inter)

Wood et al., 2003 (41)                        Yes *

Wood; Johnson, 2008 (42)                      Yes *

Borges-Yanez et al., 2006 (43)                Yes *

Reference (Author, year)             Main variables controlled

Al-Zahrani et al., 2003 (19)      Age, gender, ethnicity, smoking
                                    habits, diabetes, schooling,
                                         last dental visit

Borges et al., 2007 (20)             Ethnicity, schooling, PCR

D'Aiuto et al., 20 0 8 (21)         Age, gender, smoking habits,
                                        schooling, ethnicity

Dalla Vecchia et al., 2005 (22)               Diabetes

Dumitrescu; Kawamura, 2010 (12)                 None

Ekuni et al., 2008 (23)                       Unclear

Furuta et al., 2010 (24)                        None

Genco et al., 2005 (7)             Diabetes, age, gender, smoking
                                   habits, ethnicity, schooling,
                                            cholesterol

Haffajee; Socransky, 2009 (25)    Antibiotic therapy, age, gender,
                                           smoking habits

Han et al., 2009 (13)               Gender, smoking habits, age,
                                  sociodemograph factors, physical
                                              activity

Khader et al., 2009 (14)           Pregnancy, antibiotic therapy,
                                     osteoporosis, cancer, age,
                                   dental plaque, number of teeth

Kongstad et al., 2009 (17)          Age, gender, smoking habits,
                                    diabetes, physical activity

Kumar et al., 2009 (26)                         Age

Kushiyama et al.,2009 (18)          Age, gender, smoking habits

Li et al., 2009 (27)              Antibiotic therapy, age, gender,
                                           smoking habits

Linden et al., 2007 (28)            gender, smoking habits, age,
                                        diabetes, schooling

Lundin et al., 2004 (29)                   smoking habits

Machado et al., 2005 (30)                   age, gender

Morita et al., 20 09 (31)           age, gender, smoking habits

Pitiphat et al., 2008 (32)        medication, pregnancy, sistemic
                                   diseases, periodontal therapy

Saito et al., 2001 (33)              age, gender, social class,
                                   diabetes, smoking habits, oral
                                               hygien

Saito et al., 2005 (34)             age, dental plaque, smoking
                                               habits

Saito, 2008 (35)                               gender

Saxlin et al. 2010 (36)            age, gender, schooling, dental
                                      plaque, number of teeth

Saxlin et al., 2008 (37)              diabetes, smoking habits

Shimazaki et al., 2007 (38)             age, smoking habits

Torrungruang et al., 2005 (39)      age, dental plaque, smoking
                                          habits, diabetes

Wang et al., 2009 (40)                severe systemic disease

Wood et al., 2003 (41)            age, gender, ethnicity, smoking
                                    habits, diabetes, schooling,
                                         last dental visit

Wood; Johnson, 2008 (42)                   smoking habits

Borges-Yanez et al., 2006 (43)      age, gender, sociodemograph
                                    factors, schooling, smoking
                                               habits

Reference (Author, year)          Significant association:
                                  obesity and periodontitis

Al-Zahrani et al., 2003 (19)                 Yes

Borges et al., 2007 (20)                  Tendency

D'Aiuto et al., 20 0 8 (21)               Tendency

Dalla Vecchia et al., 2005 (22)              Yes

Dumitrescu; Kawamura, 2010 (12)              Yes

Ekuni et al., 2008 (23)                      Yes

Furuta et al., 2010 (24)                  Tendency

Genco et al., 2005 (7)                       Yes

Haffajee; Socransky, 2009 (25)               Yes

Han et al., 2009 (13)                        Yes

Khader et al., 2009 (14)                     Yes

Kongstad et al., 2009 (17)                   No

Kumar et al., 2009 (26)                      Yes

Kushiyama et al.,2009 (18)                   No

Li et al., 2009 (27)                      Tendency

Linden et al., 2007 (28)                  Tendency

Lundin et al., 2004 (29)                     No

Machado et al., 2005 (30)                    No

Morita et al., 20 09 (31)                    Yes

Pitiphat et al., 2008 (32)                   Yes

Saito et al., 2001 (33)                      Yes

Saito et al., 2005 (34)                      Yes

Saito, 2008 (35)                             Yes

Saxlin et al. 2010 (36)                   Tendency

Saxlin et al., 2008 (37)                     Yes

Shimazaki et al., 2007 (38)                  Yes

Torrungruang et al., 2005 (39)               No

Wang et al., 2009 (40)                    Tendency

Wood et al., 2003 (41)                       Yes

Wood; Johnson, 2008 (42)                  Tendency

Borges-Yanez et al., 2006 (43)               No


NR = Not Reported; ABS = Alveolar Bone Score; PPD = Periodontal Pocket
Depths; CAL = Clinical Attachment Loss; CPI = Community Periodontal
Index; PSR = Periodontal Screening and recording; BMI = Body Mass
Index ; WC = Waist Circumference; # Sample of a National Health
Examination Survey; * Clinical calibration was performed, but the
results were not reported.

Figure 2. Subgroup analysis of studies included in meta-analysis. The
study results contributing to the meta-analysis were divided into
groups (normal weight and overweight-obesity) and fixed-effects ORs
were calculated accordingly.

                          Overweight and   Control (normal)
                             Obesity

Study or Subgroup        Events   Total    Events   Total

Al-Zahraniet al., 2003   1.279    8.050      638    5.590
Borges et al., 2007         53      158       50      160
D'Aiutoet al., 2008        663    2.779    1.256    10.898
Dalla-Vecchia              195      446      105      260
  et al., 2005
Dumitrescu;                  9       37        8       42
  Kawamura, 2010
Furutaet al., 2010          24      196       80    2.029
Gencoet al., 2005        1.433    5.326    1.711    7.041
Haffajee; Socransky,        42      427      189      268
2009
Hanet al., 2009            129      578       69      468
Khaderet al., 2009          88      219       17      121
Kongstadet al., 2009       438      671      187      833
Kushyamaet al., 2009        61      189      255      881
Li et al., 2009            140      152       52       56
Lindenet al., 2007          77    1.026      277      336
Morita et al., 2009        223      629      418    1.849
Saito et al., 2001         118      179      250      464
Saito et al., 2005          45      146       69      437
Saxlinet al., 2008         606      648      630      648
Saxlinet al., 2010          96      129       60       85
Shimazakiet al., 2007       43      181       57      403
Torrungruanget al.,         85      831      789    1.147
  2005
Wang et al., 2009        1.262    3.948    2.194    8.128
Total (95% CI)                    26.945            42.144
Total events             7.607             9.361

                                                      Odds Ratio M-H,
Study or Subgroup        Weight   Odds Ratio M-H,     Fixed, 95% CI
                                  Fixed, 95% CI

Al-Zahraniet al., 2003   14.1%    1.47 [1.32, 1.62]
Borges et al., 2007       0.7%    1.11 [0.69, 1.78]
D'Aiutoet al., 2008       8,7%    2.41 [2.17, 2.67]
Dalla-Vecchia             1.7%    1.15 [0.84, 1.56]
  et al., 2005
Dumitrescu;               0.1%    1.37 [0.47, 4.01]
  Kawamura, 2010
Furutaet al., 2010        0.3%    3.40 [2.10, 5.51]
Gencoet al., 2005          24%    1.15 [1.06,1.24]
Haffajee; Socransky,      4.7%    0.05 [0.03, 0.07]
2009
Hanet al., 2009           1.3%    1.66 [1.20, 2.29]
Khaderet al., 2009        0.3%    4.11 [2.30, 7.34]
Kongstadet al., 2009      1.3%    6.49 [5.17, 8.15]
Kushyamaet al., 2009      1.4%    1.17 [0.83, 1.64]
Li et al., 2009           0.1%    0.90 [0.28, 2.91]
Lindenet al., 2007        8.6%    0.02 [0.01, 0.02]
Morita et al., 2009       3.1%    1.88 [1.55, 2.29]
Saito et al., 2001        1.1%    1.66 [1.16, 2.37]
Saito et al., 2005        0.5%    2.38 [1.54, 3.67]
Saxlinet al., 2008        0.9%    0.41 [0.23, 0.72]
Saxlinet al., 2010        0.4%    1.21 [0.66, 2.23]
Shimazakiet al., 2007     0.6%    1.89 [1.22, 2.94]
Torrungruanget al.,       4.4%    1.07 [0.88, 1.30]
  2005
Wang et al., 2009        21.8%    1.27 [1.25, 1.38]
Total (95% CI)            100%    1.30 [1.25, 1.35]
Total events

Heterogeneity: [Chi.sup.2] = 1211.01, df = 21 (P < 0.00001); [I.sup.2] =
  98%
Test for overall effect: Z = 13.25 (P < 0.00001)

Figure 3. Meta-analysis forest plot. Sizes of the boxes are
proportional to the weight assigned to each result in calculating of
the presence or absence of periodontitis.

                       Periodontal Disease    Control (normal)

Study or Subgroup      Mean    SD     Total   Mean    SD     Total

Borges et al., 2007    25.5    3.9     103    24.5    3.8      215
Ekuniet al., 2009      20.9    2.6      49    21.8    2.4      569
Kumaret al., 2009      24.33   3.4      81    20.84   2.83     432
Li et al., 2009        26.4    2.9     192    22.2    2.4       16
Lundinet al., 2004     38.5    5.2      15    38.9    9.5       17
Machado et al., 2005     25    3.3      30    24.4    2.6       30
Morita et al., 2009      24    3.1     641    22.9    3.1    1.837
Pitiphatet al., 2008   23.7    3.3      83    21.6    2.4       38
Saito et al., 2005     24.1    2.9     114    22.9    3.5      469
Saito et al., 2008     23.3    2.6      34    21.9    3.2       42
Wood et al., 2003      29.8    0.9    1.431   27.1    0.2    7.411
Wood; Johnson, 2008    29.23   1.04    227    25.27   0.6      871
Yanezet al., 2006      25.7    4.9     185    25.6    4.84     180
Total                                 3.185                  12.127

Study or Subgroup      Weight   Mean Difference       Main Difference
                                IV, Fixed, 95% CI     IV, Fixed,
                                                      95% CI

Borges et al., 2007     0.2%    1.00 [0.09, 1.91]
Ekuniet al., 2009       0.3%    -90 [-1.65, -0.15]
Kumaret al., 2009       0.3%    3.39 [2.60, 4.18]
Li et al., 2009         0.1%    4.20 [2.95, 5.45]
Lundinet al., 2004      0.0%    -0.40 [-5.63, 4.83]
Machado et al., 2005    0.1%    0.60 [-0.90, 2.10]
Morita et al., 2009     2.4%    1.10 [0.82, 1.38]
Pitiphatet al., 2008    0.2%    2.10 [1.06, 3.14]
Saito et al., 2005      0.5%    1.20 [0.58, 1.82]
Saito et al., 2008      0.1%    1.40 [0.10, 2.70]
Wood et al., 2003      86.0%    2.70 [2.65, 2.75]
Wood; Johnson, 2008     9.5%    0.10 [-090, 1.10]
Yanezet al., 2006       0.2%    0.10 [-0.90, 1.10]
Total                   100%    2.75 [2.71, 2.80]

Heterogeneity: [Chi.sup.2] = 599.64, df = 12 (P < 0.00001), I2 = 98%

Test for overall effect Z = 124.12 (P < 0.00001)
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Title Annotation:articulo en ingles
Author:de Moura-Grec, Patricia Garcia; Marsicano, Juliane Avansini; de Carvalho, Cristiane Alves Paz; de Ca
Publication:Ciencia & Saude Coletiva
Date:Jun 1, 2014
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