Obesity, Bone Loss, and Periodontitis: History
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Contributor:
Pengfei Zhao
,
Aimin Xu
,
Wai Keung Leung

Obesity and periodontitis are both common health concerns that have given rise to considerable economic and societal burden worldwide. There are established negative relationships between bone metabolism and obesity, obesity and diabetes mellitus (DM), and DM and periodontitis, to name a few, with osteoporosis being considered a long-term complication of obesity. In the oral cavity, bone metabolic disorders primarily display as increased risks for periodontitis and alveolar bone loss. Obesity-driven alveolar bone loss and mandibular osteoporosis have been observed in animal models without inoculation of periodontopathogens. Clinical reports have also indicated a possible association between obesity and periodontitis.

  • alveolar bone loss
  • bone and bones
  • bone remodeling
  • obesity
  • periodontitis

1. Introduction

Obesity is defined as someone with a body mass index of >30 kg/m2 [1] with excessive body fat accumulation leading to exaggerated health risks. According to the World Health Organization, the prevalence of obesity is increasing worldwide. For instance, it tripled from 1975 to 2016, with nearly 13% of adults (11% men and 15% women) being considered as obese [2]. The pathogenesis of multiple diseases, including type 2 diabetes mellitus (T2DM), cardiovascular disease, cancer, and osteoporosis, is associated with obesity. Osteoporosis manifests as impaired bone quality and increased risk of fracture, resulting in a reduction in mobility and quality of life [3]. The majority of clinical studies have suggested a correlation between obesity and reduced bone mass [4][5]. The systemic bone loss caused by obesity is expressed as various severities of osteoporosis and could involve alveolar bone resorption. According to the 2017 periodontal diseases classification, obesity was recognized as a significant metabolic disorder that is associated with loss of periodontal tissues [6], and an increased risk of periodontitis in obese individuals, suggesting a comorbidity effect between obesity and periodontitis. In particular, inflammatory environment and imbalanced bone homeostasis caused by obesity were widely recognized [7]. A series of studies have explored the possible molecular links between obesity and periodontitis, highlighting the concepts of shared inflammatory pathways and immune dysfunction [8][9]. However, these reviews focused on the connections between obesity and periodontal disease from the perspective of bone, rather than obesity and its negative systemic influences. With the increasing trends of obesity worldwide, there is currently insufficient evidence to guide clinicians on how to effectively manage both health problems in obese individuals with periodontitis.

2. Obesity and Periodontitis: Epidemiological and Clinical Association

The first report to suggest an association between obesity and periodontitis was the 241 Japanese cross-sectional study by Saito et al. [10]. More studies, by other researchers, were later conducted, focusing on obesity as a risk indicator for periodontitis. Al-Zahrani et al. [11] extracted data from the third National Health and Nutrition Examination Survey (NHANES III) and found a significant association between obesity and the prevalence of periodontitis in young adults with an adjusted odds ratio (OR) of 1.37. Since then, many systematic reviews and meta-analyses have been published. Researchers performed a search in the PubMed, EMBASE and Web of Science databases and identified 11 systematic reviews concerning this important association.
In summary, eight reports were a systematic review with meta-analysis [12][13][14][15][16][17][18][19], while three studies only attempted a systematic review [20][21][22]. Relevant characteristics and findings are summarized in Table 1. These studies were published between 2010 and 2022. One 2010 report [12] designed its own scale to evaluate the quality of the studies reported. Nevertheless, 4/1/1/1 studies used the Newcastle-Ottawa Quality Assessment Scale (N-OQAS)/Downs and Black checklist/the Critical Appraisal Checklist/STROBE checklist, while three investigations [14][20][21] reported no evaluation of quality concerning the included studies. One of the three systematic reviews [22] claimed to use N-OQAS, but without any account of the outcomes. Two reports focused on the systematic review and meta-analyses of children, adolescents, or young adults [15][18] (589 or 1983 participants) while another report was a systematic review concerning young adults [22]. A recent report focused on the association between obesity and periodontitis in pregnant women [19]. The assessment of risk of bias in the included papers was performed with the Risk of Bias in Systematic Reviews (ROBIS) tool [23]. Included were three systematic reviews with meta-analysis [12][14][18] that exhibited a high risk of bias due to considerable heterogeneity, a high risk of bias in primary studies included, and/or loss of quality assessment. Another three systematic reviews [20][21][22] were also rated as having a high risk of bias, mainly due to loss of quality assessment and merely descriptive results. There were five reports [13][15][16][17][19] with acceptable merits which included 5–19 primary studies for meta-analyses. The number of subjects ranged from 589–42,430, and various ethnicities were reported including Americans (mixed ethnicity), Europeans (predominantly Caucasians), Chinese (east Asians), and so on. One study focused on children and adolescence [15] while another focused on pregnant women [19] (Table 1).
Table 1. Systematic reviews and meta-analyses evaluating the association between obesity and periodontal disease (in chronological order).
Authors and Year
(Report Nature)		 Aim and Objective Studies Included and Disease Definition No. of Participants (Grand Total and Range in Parenthesis) and Outcome of MA Quality Assessment Subgroup Analysis (I);
Sensitivity Analysis (II); and Publication Bias Assessment (III)		 Summary
Chaffee et al. 2010 [12]
(SR and MA)		 To compile the evidence concerning relationship between obesity and periodontal disease. 70/28 studies included for SR/MA.
Obesity definition: BMI or WHR
Periodontal disease definition—up to 18 different selected clinical criteria with top 3 as: (1) CPI = 4; (2) CPI ≥ 3; (3) ≥1 site with CAL ≥ 3 mm and PPD ≥ 4 mm.		 70,855 (96–13,665) participants; ORs, or MD of CAL between obese and non-obese groups. Using a specific scale design by the authors. 13, 7, and 8 studies were rated with high, medium, or low quality of evidence, respectively. (I) Yes. Based on study characteristics.
(II) Attempted. Exclusion of any single study only slightly altered the outcome. (III) Limited bias detected.		 A positive association between periodontal disease and obesity. Overall OR: 1.35, 95% CI (1.23, 1.47).
Obese patients were prone to show greater mean CAL. Summary MD = 0.58 mm; 95% CI (0.40, 0.74).
Suvan et al. 2011 [13]
(SR and MA)		 To systematically review the evidence investigating the association between obesity and periodontitis. 33/19 studies included for SR/MA.
Obesity definition: BMI, WHR, WC, or body fat%.
Periodontal disease definition—up to 16 different selected clinical criteria, with top 3 criteria are: (1) CPI ≥ 3; (2) > 4 teeth with minimum one site with CAL ≥ 3 mm and PPD ≥4 mm; (3) ≥ 1 site with CAL ≥3 mm and PD ≥ 4 mm.		 39,777 (96–13,665) participants; pooled estimates of ORs. Newcastle-Ottawa Quality Assessment Scale (N-OQAS) [24]. (I) Yes. Based on BMI categories. (II) Not reported. (III) Not reported. Significant associations between periodontitis and obesity (OR: 1.81, 95% CI (1.42, 2.30]), or overweight (OR: 1.27, 95% CI (1.06, 1.51]), and obese and overweight combined (OR: 2.13, 95% CI (1.40, 3.26]).
Results suggested a positive association of BMI categories, obese and overweight with presence of periodontitis, although the magnitude appeared unclear.
de Moura-Grec et al. 2014 [14]
(SR and MA)		 To systematically review the studies regarding association between overweight/ obesity and periodontitis. 31/22 studies included for SR/MA.
Obesity definition: BMI or WC.
Periodontal disease definition—up to 16 different selected clinical criteria, with top 3 as: (1) PPD ≥ 4 mm; (2) CPI ≥ 3; (3) PPD ≥ 5 mm.		 69,089 (79–13,665) participants; ORs, MD in BMI between periodontitis and periodontally healthy group. Not reported. (I) Not reported.
(II) Not reported. (III) Not reported.		 Obesity and overweight showed an increased odds for periodontitis (OR: 1.3, 95% CI (1.25, 1.35)).
Participants with periodontitis had higher BMI compared to periodontally healthy participants. MD: 2.74 kg/m2 (95% CI (2.70, 2.79]).
Keller et al. 2015 [20]
(SR)		 To longitudinally examine the association between obesity and periodontitis. 13 studies included for SR.
Obesity definition: BMI or WC.
Periodontal disease definition—7 clinical outcomes: PPD, CAL, ABL, PI, GI, CPI, BOP, and FMBS with thresholds not reported.		 44,758 (46–36,910) participants; NA. Not reported. (I) Not reported. (II) Not reported. (III) Not reported. Suggests overweight, obesity, weight gain, and increased waist circumference could be considered as risk factors for development of periodontitis.
Li et al. 2015 [15]
(SR and MA)		 To investigate the association between anthropometric measurements and periodontal diseases in children and adolescents. 16/5 studies included for SR/MA.
Obesity definition: BMI or WC.
Periodontal disease definition—3 clinical criteria: (1) either two sites between adjacent teeth with CAL ≥4 mm, or at least two such sites with PPD ≥ 5 mm; (2) ≥1 sites with CAL ≥ 3 mm and PPD ≥ 3 mm; (3) ≥ 1 bleeding site.		 589(87–164) participants; ORs. Strengthening the Reporting of Observational studies in epidemiology (STROBE) checklist [25]. (I) Yes, based on different periodontal markers. (II) Not reported.
(III) No substantial bias detected.		 Reported positive association between obesity and presence of subgingival calculus (OR: 3.07, 95% CI (1.10, 8.62]), visible Plaque Index (OR: 4.75; 95% CI (2.42, 9.34]), BOP (OR: 5.41; 95% CI (2.75, 10.63]), and risk of PPD > 4 mm (OR: 14.15; 95% CI (5.10, 39.25]) in children and adolescents.
Concluded that obesity is associated with some signs of periodontal disease in children and adolescents.
Nascimento et al. 2015 [16]
(SR and MA)		 To systematically review the effect of weight gain on incidence of periodontitis. Both 5 studies included for SR and MA.
Obesity definition: BMI or WC.
Periodontal disease and progression definition— 3 sets of clinical criteria: (1) PPD ≥ 4 mm; (2) ABL ≥ 40% or PPD or CAL ≥ 5 mm; (3) self-reported periodontal disease.		 42,158 (224–36,910) participants; RRs. N-OQAS (I) Yes, based on obese status.
(II) Attempted. Omission of any single study did not alter the findings. (III) No substantial bias detected.		 Results showed overweight (RR: 1.13, 95% CI (1.06, 1.20]) and those participants who became obese (RR: 1.33, 95% CI (1.21, 1.47]) had a significant higher risk to develop periodontitis.
Nascimento et al. 2016 [17]
(SR and MA)		 To examine the bidirectional association of tooth loss and obesity. 25/16 studies included for SR/MA.
Obesity definition: BMI.
Periodontal disease and progression manifestation: number of teeth lost.		 42,430 (186–16,416) participants; ORs. The Critical Appraisal Checklist (Joanna Briggs Institute [26]). (I) Yes, based on tooth loss or edentulism. (II) Attempted. Omission of any single study did not alter the findings. (III) Presence of a small-study effect when any tooth loss was considered as an exposure. Results indicated obese individuals had higher odds of having any tooth loss (OR: 1.49, 95% CI (1.20, 1.86)) or being edentulous (OR: 1.25, 95% CI (1.10, 1.42]), respectively.

Individual with any tooth loss had higher odds (OR: 1.41, 95% CI [1.11, 1.79]) for obesity; similar for edentulous participants (OR: 1.60, 95% CI: (1.29, 2.00)).

Suggested bidirectional association between tooth loss and obesity.
Martens et al. 2017 [18]
(SR and MA)		 To investigate the association between overweight/ obesity and periodontal disease in children and/or adolescents. 12/7 studies included for SR/MA.
Obesity definition: BMI, WHR, WC, or body fat%, and skinfold thickness.
Periodontal disease definition: ≥ 1 site with CAL≥ 3 mm and PPD ≥ 3 mm.		 1983 (87–1204) participants; ORs. Downs and Black checklist [27]. (I) Not reported.
(II) Attempted. Omission of any single study did not alter the findings. (III) No evidence of publication bias detected.		 Significant association between periodontal disease and obesity in children (OR: 1.46, 95% CI (1.20, 1.77]).
Martinez-Herrera et al. 2017 [21]
(SR)		 To systematically review the association between obesity and periodontal disease. 28 studies included for SR.
Obesity definition: BMI, WC, WHR, or body fat%.
Periodontal disease definition—7 clinical outcomes: PPD, CAL, PI, BOP, ABL, CPI and GI with thresholds not reported.		 102,221 (91–36,910) participants; NA. Not reported. (I) Not reported.
(II) Not reported.
(III) Not reported.		 All studies except two articles described an association between obesity and periodontal disease.
Khan et al. 2018 [22]
(SR)		 To investigate if overweight or obese is risk factor for periodontitis in adolescents and young adults. 25 studies included for SR.
Obesity definition: BMI, WC, WHR, or body fat%.
Periodontal disease definition—up to 17 different selected clinical criteria, with top 2 as: (1) CPI ≥ 3; (2) ≥ 1 sites with PPD ≥ 4 mm.		 51,597 (55–17,660) participants; NA. N-OQAS (I) Not reported. (II) Not reported. (III) Not reported. Suggested evidence available indicating obesity was associated with periodontitis in adolescents and young adults.
Foratori-Junior et al.
2022 [19]
(SR and MA)		 To generate pooled evidence for the association between excess weight and periodontitis during pregnancy. Both 11 studies included for SR and MA.
Obesity definition: BMI.
Periodontal disease definition—up to 8 different selected clinical criteria, with top 3 as: (1) ≥ 2 interproximal CAL ≥ 4 mm on different teeth; (2) ≥ 2 interproximal sites with CAL ≥ 3 mm or PPD ≥ 4 mm (on different teeth), or one site with PPD ≥ 5 mm; (3) interproximal CAL ≥ 2 on nonadjacent teeth or buccal or oral CAL ≥ 3 mm with PPD > 3 mm detectable on ≥ 2 teeth.		 2152 (50–682) participants;
RRs.		 N-OQAS (I) Not reported. (II) Not reported. (III) No evidence of publication bias detected. Positive association between overweight/obesity and periodontitis during pregnancy (RR: 2.21, 95% CI (1.53, 3.17]).
ABL: alveolar bone loss; BMI: body mass index; BOP: bleeding on probing; CAL: clinical attachment level; CI: confidence interval; CPI: Community Periodontal Index; FMBS: full-mouth bleeding score; GI: Gingival Index; MA: meta-analyses; MD: mean difference; NA: not applicable; N-OQAS: Newcastle-Ottawa Quality Assessment Scale; OR: odds ratio; PI: Plaque Index; PPD: probing pocket depth; RR: relative risk; SR: systematic reviews; WC: waist circumference; WHR: waist/hip ratio.
Collectively, there is evidence to support the conclusion that there is a higher prevalence in some form or another of periodontal disease experience, e.g., clinical attachment level (CAL), bleeding on probing (BOP), or subgingival calculus in young individuals, or its surrogate, i.e., tooth loss, or edentulism in overweight or obese individuals. Overweight or obese pregnant women were more prone to experience periodontitis [19]. Notably, two meta-analyses conducting a subgroup analysis based on BMI values suggested an increasing risk of periodontitis with increased BMI values, inferring a dose-response relationship [13][16]. However, it is essential to be aware that BMI values and thresholds originating from epidemiological reports are often not directly applicable in individual clinical situations. Furthermore, the differences between general obesity and abdominal obesity may contribute to the uncertainty of dose-response relationship. One study compared the effect of abdominal obesity and general obesity on periodontal parameters, and found that the former was related to attachment loss and bleeding on probing, but not the latter [28].
The clinical characteristics of periodontium in obese individuals was also denoted in these reviews. Chaffee et al. [12] reported that obese individuals were prone to showing higher clinical attachment loss compared to none-obese individuals, suggesting an increased risk for the progression of alveolar bone loss. Additionally, the presence of subgingival calculus, visible Plaque Index, bleeding on probing, and PPD > 4 mm were also shown to be higher in obese children and adolescents [15]. A more recent study found that a higher consumption of sweets (candy), combined with poor hygiene habits and increased rates of gum inflammation, worsened periodontal tissue status (PPD, CAL) in obese adults [29]. Therefore, gingival and periodontal health and unsatisfactory oral hygiene status appeared to manifested more often in obese children, adolescents, and adults. In turn, obese individuals were observed to anticipate higher odds of any tooth loss or edentulism [17]. However, the evidence is not robust enough due to the heterogeneity of study designs and uncontrolled confounding variables.
The association between obesity and periodontitis in different ethnic and age groups is reasonably well demonstrated in the aforementioned studies. However, the causal—effect relationship and the direction of this causality have not been clarified, and potential biological/pathological mechanisms have not been evaluated or determined. Based on the current evidence, it can be speculated that the connection between both diseases is of a casual nature, and that this relationship would be bidirectional. Further laboratory-based and longitudinal population/cohort studies are warranted to establish this bidirectional causal relationship. 

3. How Does Obesity Influence Bone Quality?

Patients with obesity are also at a higher risk of metabolic complications including hypertension, T2DM, heart disease, non-alcoholic fatty liver, kidney disease, polycystic ovary syndrome, and cancer [30]. Over the past decade, a growing number of studies have indicated that obesity is associated with osteopenia and osteoporosis, suggesting a negative impact of obesity on bone quality, including the jawbone [31].

3.1. Obesity-Drives Disruptive Bone Homeostasis

Bone is a dynamic organ that is permanently in a process of resorption followed by remodeling/reconstruction as its major biological process throughout life [32]. Bone homeostasis involves a balance between bone formation and resorption, which are engineered by osteoblasts and osteoclasts [33]. The very first belief was that obesity correlated with increased bone mass, and long-term weight-bearing is beneficial for bone formation [34]. However, more recent studies have revealed links between excess fat and osteoporosis, making bone more fragile [35][36]. In some cohorts, the percentage of total fat mass is strongly and inversely associated with bone mineral density (BMD) and total bone mineral content [37][38]. Obesity exerts a detrimental effect on bone homeostasis by impairing the balance of osteoblast and osteoclast activities and increasing bone resorption. Reasons for this effect could be that excess fat in bone marrow, with an enlarged adipocyte number and size, leads to altered bone marrow stem cells (BMSCs) differentiation with decreased osteoblasts, thus harming bone integrity [7][39]. However, some studies have suggested that this effect is probably more complex and site-dependent, with a higher risk for only certain types of bone to fracture [4].

3.2. Systemic Bone Loss

Early studies support the favorable role of obesity in regulating BMD and bone mass due to the positive effect of weight-bearing exercise on bone quality [40]. Previous longitudinal studies have observed that BMD changes at some sites were positively related to the changes of fat mass [41]. By contrast, a multinational survey in 2011, for the first time, reported a higher prevalence of bone fragility fractures in postmenopausal women with obesity [42]. Of interest, Liu and colleagues enrolled 471 women in a cross-sectional study; after categorizing them into lean, overweight, and obese groups, the researchers observed that body fat < 33% showed positive association with bone density, while those with body fat > 33% showed the opposite effect for most of the skeletal sites that followed [43]. Despite the conflicting positive and negative actions of obesity on bone mass, which may be explained by heterogeneity in population and measurements, the current common view favors the idea that obesity is associated with poor bone quality [3]. Ample evidence from animal studies also implies the adverse effects of obesity on bone mass. The high fat diet (HFD) obesity model is most commonly used in studying the influence of adiposity [44]. Tencerova et al. [45] observed significant and consistent trabecular and cortical bone loss in 12-week HFD-fed mice, alongside bone marrow adipose tissue expansion, suggesting that bone mass reduction could be a biological consequence of coherent adiposity mechanisms. Another study showed critical deterioration in trabecular bone micro-architecture at the early stage of HFD-fed mice, leading to decreased trabecular bone density [46]. In the murine spines, HFD also resulted in significantly less trabecular bone volume in the lumbar vertebrae [47].

3.3. Periodontal Bone Loss

Compared to studies focusing on systemic bone, only a few reports have investigated the role of obesity on alveolar bone. Obesity appeared to be an established risk indicator for periodontitis (Table 1). Animal studies have consistently shown that increased body weight could exacerbate alveolar bone loss in periodontitis [48]. One study used a long-term cafeteria (high-fat/high-carbohydrate) diet in Wistar rats, and reported that obesity and hyperlipidemia could further increase alveolar bone loss in ligature-induced periodontitis [49]. Muluke et al. [50] found that a palmitic acid (PA)-enriched HFD contributed to more bone loss in Porphyromonas gingivalis-induced periodontitis, and together with increased free fatty acids in serum, suggested a possible (but yet unclarified) role of PA promoting alveolar bone loss. Li et al. [51] also described increased periodontal inflammatory response and bone loss, which were both observed after local injection of bacterial lipopolysaccharides in the jaws of obese animals fed on a HFD, compared to a normal control diet.
Of interest, it was reported that alveolar bone density loss could be triggered by obesity without the necessity of periodontitis induction, (i.e., pathogenic microorganism inoculation or ligature) in both mature and growing animals to facilitate the development of periodontal disease. A previous investigation showed that an increase in weight gain can result in decreased alveolar bone crest height, suggesting obesity as a putative risk factor, even in a clinically healthy periodontium [52]. In the development of diet-induced obesity, another animal study showed impaired trabecular bone architecture and retarded periosteal bone formation in the early stage of HFD treatment (4 weeks), followed by a decrease in cortical bone density in the alveolar bone area with increased serum leptin levels [53]. All of these findings suggest that systemic alternations induced by obesity could have an impact on alveolar bone integrity.

This entry is adapted from the peer-reviewed paper 10.3390/biom12070865

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