Abstracts

Introduction

The prevalence of obesity is increasing worldwide¹1. Sales-Peres SH, Goya S, Sant'Anna RM, Silva HM, Sales-Peres AC, Silva RP, Lauris JR, Bastos JR. Prevalence of overweight and obesity, and associated factors in adolescents, at the central west area of the state Sao Paulo (SP, Brazil). Cien Saude Colet 2010; 15(Supl. 2):3175-3184.. Obesity, defined as a Body Mass Index (BMI) >30 kg/m², and overweight (BMI >25 kg/m²⁾ are becoming a worldwide epidemic estimated to involve 1.7 billion people in developed and developing countries²2. Buchwald H, Williams SE. Bariatric surgery worldwide 2003. Obesity surgery 2004; 14(9):1157-1164., being considered a public health problem³3. Kopelman PG. Obesity as a medical problem. Nature 2000; 404(6778):635-643.. 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 increase⁴4. World Health Organization (WHO). WHO Global Infobase: International Comparisons. 2010 [cited 2011 Apr 14]; Available from: https://apps.who.int/infobase/Index.aspx
Available from: https://apps.who.int/inf... .

This disease is so common among the world population that it is becoming the most important contributors to ill health³3. Kopelman PG. Obesity as a medical problem. Nature 2000; 404(6778):635-643.. 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 factors⁵5. Barreto Villela N, Braghrolli Neto O, Lima Curvello K, Eduarda Paneili B, Seal C, Santos D, Cruz T. Quality of life of obese patients submitted to bariatric surgery. Nutr Hosp 2004; 19(6):367-371.. Obesity causes or exacerbates a large number of health problems, both independently and in association with other diseases (comorbidities)³3. Kopelman PG. Obesity as a medical problem. Nature 2000; 404(6778):635-643.. These diseases may be type 2 diabetes, hypertension, hypoventilation, sleep apnea, venous stasis, tumor, regenerative joint disease, and others⁶6. Bouldin MJ, Ross LA, Sumrall CD, Loustalot FV, Low AK, Land KK. The effect of obesity surgery on obesity comorbidity. Am J Med Sci 2006; 331(4):183-193..

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 mediators⁷7. Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005; 76(Supl. 11):2075-2084.. 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 loss⁸8. Williams RC. Periodontal disease. N Engl J Med 1990; 322(6):373-382.. The link between periodontitis and obesity may have relevant public health implications because both diseases are important risk factor for cardiovascular diseases⁹9. Lopez-Jimenez F, Cortes-Bergoderi M. Update: systemic diseases and the cardiovascular system (i): obesity and the heart. Rev Esp Cardiol 2011; 64(2): 140-149.

10. Saini R, Saini S, Saini SR. Periodontal diseases: a risk factor to cardiovascular disease. Ann Card Anaesth 2010; 13(2):159-161.^-1111. Trevisan M, Dorn J. The relationship between periodontal disease (pd) and cardiovascular disease (cvd). Mediterr J Hematol Infect Dis 2010; 2(3): e2010030..

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 studies¹²12. Dumitrescu AL, Kawamura M. Involvement of psychosocial factors in the association of obesity with periodontitis. J Oral Sci 2010; 52(1):115-124.

13. Han DH, Lim SY, Sun BC, Paek DM, Kim HD. Visceral fat area-defined obesity and periodontitis among Koreans. J Clin Periodontol 2009; 37(2):172-179.

14. Khader YS, Bawadi HA, Haroun TF, Alomari M, Tayyem RF. The association between periodontal disease and obesity among adults in Jordan. J Clin Periodontol 2009; 36(1):18-24.^-1515. Saxlin T, Suominen-Taipale L, Leiviska J, Jula A, Knuuttila M, Ylöstalo P. Role of serum cytokines tumour necrosis factor-alpha and interleukin-6 in the association between body weight and periodontal infection. J Clin Periodontol 2009; 36(2):100-105. and not in others¹⁶16. Gursoy UK, Marakoglu I, Oztop AY. Relationship between neutrophil functions and severity of periodontitis in obese and/or type 2 diabetic chronic periodontitis patients. Quintessence Int 2008; 39(6): 485-489.

17. Kongstad J, Hvidtfeldt UA, Gronbaek M, Stoltze K, Holmstrup P. The relationship between body mass index and periodontitis in the Copenhagen City Heart Study. J Periodontol 2009; 80(8):1246-1253.^-1818. Kushiyama M, Shimazaki Y, Yamashita Y. Relationship between metabolic syndrome and periodontal disease in Japanese adults. J Periodontol 2009; 80(10):1610-1615.. 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/m² [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/m² 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 subjects²³23. Ekuni D, Yamamoto T, Koyama R, Tsuneishi M, Naito K, Tobe K. Relationship between body mass index and periodontitis in young Japanese adults. J Periodontal Res 2008; 43(4):417-421.^,2626. Kumar S, Dagli RJ, Dhanni C, Duraiswamy P. Relationship of body mass index with periodontal health status of green marble mine laborers in Kesariyaji, India. Braz Oral Res 2009; 23(4):365-369.^,4444. Sarlati F, Akhondi N, Ettehad T, Neyestani T, Kamali Z. Relationship between obesity and periodontal status in a sample of young Iranian adults. Int Dent J 2008; 58(1):36-40., however no association was detected in the study of Lundin et al.²⁹29. Lundin M, Yucel-Lindberg T, Dahllof G, Marcus C, Modéer T. Correlation between TNFalpha in gingival crevicular fluid and body mass index in obese subjects. Acta Odontol Scand 2004; 62(5):273-277.. Regarding to older subjects, no association was observed in this age group in numerous studies¹⁷17. Kongstad J, Hvidtfeldt UA, Gronbaek M, Stoltze K, Holmstrup P. The relationship between body mass index and periodontitis in the Copenhagen City Heart Study. J Periodontol 2009; 80(8):1246-1253.^,2020. Borges PK, Gimeno SG, Tomita NE, Ferreira SR. Prevalence and characteristics associated with metabolic syndrome in Japanese-Brazilians with and without periodontal disease. Cad Saude Publica 2007; 23(3):657-668.^,2727. Li P, He L, Sha YQ, Luan QX. Relationship of metabolic syndrome to chronic periodontitis. J Periodontol 2009; 80(4):541-549.^,2828. Linden GJ, McClean K, Young I, Evans A, Kee F. Persistently raised C-reactive protein levels are associated with advanced periodontal disease. J Clin Periodontol 2008; 35(9):741-747.^,3939. Torrungruang K, Tamsailom S, Rojanasomsith K, Sutdhibhisal S, Nisapakultorn K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Unkurapinun N, Sritara P. Risk indicators of periodontal disease in older Thai adults. J Periodontol 2005; 76(4):558-565., 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 Saito³⁵35. Saito T. Obesity may be associated with periodontitis in elderly men. J Evid Based Dent Pract 2008; 8(2):97-98. and Saito et al.³⁴34. Saito T, Shimazaki Y, Kiyohara Y, Kato I, Kubo M, Iida M, Yamashita Y. Relationship between obesity, glucose tolerance, and periodontal disease in Japanese women: the Hisayama study. J Periodontal Res 2005; 40(4):346-353. 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 confounders⁴⁵45. Chávarry NG, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent 2009; 7(2):107-127..

It may be noted that only 2 studies performed the sample calculation²²22. Dalla Vecchia CF, Susin C, Rosing CK, Oppermann RV, Albandar JM. Overweight and obesity as risk indicators for periodontitis in adults. J Periodontol 2005; 76(10):1721-1728.^,2626. Kumar S, Dagli RJ, Dhanni C, Duraiswamy P. Relationship of body mass index with periodontal health status of green marble mine laborers in Kesariyaji, India. Braz Oral Res 2009; 23(4):365-369. 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 because five studies observed association between obesity and periodontitis and only 2 observed a trend of association²¹21. D'Aiuto F, Sabbah W, Netuveli G, Donos N, Hingorani AD, Deanfield J, Tsakos G. Association of the metabolic syndrome with severe periodontitis in a large U. S. population-based survey. J Clin Endocrinol Metab 2008; 93(10):3989-3994.^,4646. Iacopino AM. Relationship between obesity and periodontal disease: increasing evidence. J Can Dent Assoc 2009; 75(2):92-93..

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 good⁴⁷47. Kingman A. A procedure for evaluating the reliability of a gingivitis index. J Clin Periodontol 1986; 13(5):385-391.. Only 2 found no link between obesity and periodontitis, wich evaluated only older population³⁹39. Torrungruang K, Tamsailom S, Rojanasomsith K, Sutdhibhisal S, Nisapakultorn K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Unkurapinun N, Sritara P. Risk indicators of periodontal disease in older Thai adults. J Periodontol 2005; 76(4):558-565. and another study the kappa value was 0.52¹⁷17. Kongstad J, Hvidtfeldt UA, Gronbaek M, Stoltze K, Holmstrup P. The relationship between body mass index and periodontitis in the Copenhagen City Heart Study. J Periodontol 2009; 80(8):1246-1253..

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 infection⁴⁸48. Nishimura F, Iwamoto Y, Mineshiba J, Shimizu A, Soga Y, Murayama Y. Periodontal disease and diabetes mellitus: the role of tumor necrosis factor-alpha in a 2-way relationship. J Periodontol 2003; 74(1):97-102., 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 diseases⁴⁹49. Hyman J. The importance of assessing confounding and effect modification in research involving periodontal disease and systemic diseases. J Clin Periodontol 2006; 33(2):102-103.. The association between high body weight and periodontitis could be due to common lifestyle characteristics that make subjects more prone to both obesity and periodontitis⁴⁶46. Iacopino AM. Relationship between obesity and periodontal disease: increasing evidence. J Can Dent Assoc 2009; 75(2):92-93., for example, an unhealthy dietary patterns with insufficient micronutrients and excess sugar and fat content could thus pose a risk both diseases¹⁹19. Al-Zahrani MS, Bissada NF, Borawskit EA. Obesity and periodontal disease in young, middle-aged, and older adults. J Periodontol 2003; 74(5):610-615.. As well as obesity can be a indirect predictor of periodontitis because insulin resistance⁷7. Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005; 76(Supl. 11):2075-2084. and low social class⁴³43. Borges-Yáñez SA, Irigoyen-Camacho ME, Maupome G. Risk factors and prevalence of periodontitis in community-dwelling elders in Mexico. J Clin Periodontol 2006; 33(3):184-194. 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 disorders⁵⁰50. Makiura N, Ojima M, Kou Y, Furuta N, Okahashi N, Shizukuishi S, Amano A. Relationship of Porphyromonas gingivalis with glycemic level in patients with type 2 diabetes following periodontal treatment. Oral Microbiol Immunol 2008; 23(4):348-351. the fact of the adipose tissue secrete proinflammatory cytokines which may be the molecules linking the pathogenesis of these diseases⁷7. Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005; 76(Supl. 11):2075-2084.. The association between BMI and tumor necrosis factor- α (TNF- α ) in gingival crevicular fluid²⁹29. Lundin M, Yucel-Lindberg T, Dahllof G, Marcus C, Modéer T. Correlation between TNFalpha in gingival crevicular fluid and body mass index in obese subjects. Acta Odontol Scand 2004; 62(5):273-277. suggests that TNF-α in this fluid is derived from adipose tissue in obese subjects⁵¹51. Saito T, Shimazaki Y. Metabolic disorders related to obesity and periodontal disease. Periodontol 2000 2007; 43(1):254-266.. In addition, an increase in serum level of interleukin 6 and resistin, both secreted by adipocytes, has been proposed to be associated with periodontitis¹⁵15. Saxlin T, Suominen-Taipale L, Leiviska J, Jula A, Knuuttila M, Ylöstalo P. Role of serum cytokines tumour necrosis factor-alpha and interleukin-6 in the association between body weight and periodontal infection. J Clin Periodontol 2009; 36(2):100-105.^,3535. Saito T. Obesity may be associated with periodontitis in elderly men. J Evid Based Dent Pract 2008; 8(2):97-98.. Furthermore, Haffajee and Socransky²⁵25. Haffajee AD, Socransky SS. Relation of body mass index, periodontitis and Tannerella forsythia. J Clin Periodontol 2009; 36(2):89-99. 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.

Acknowledgements

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

References

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