
Infection may be the cause or the effect of obesity and the two phenomena are in a relationship of mutual interaction1). Obesity reduces the acquired immunity and induces changes in cellular immunity to cause infection2). There are claims that an increase in adipocytes aggravates chronic inflammation and that obesity itself is chronic inflammation3). On the contrary, the term ‘infectobesity’ was coined based on the observation that obesity could be induced by viral or bacterial infection4). Studies have reported that obesity increased upon the use of antibiotics5), or that the gut microbiota could be used in the treatment of obesity6).
Periodontal diseases are a form of chronic inflammation, and the relationship between obesity and periodontal diseases has been continuously investigated since the 1970s. Alveolar bone resorption in obese mice was reported7), and the alteration in macrophage function was observed in mice infected with
Periodontal diseases are fundamentally an inflammatory response caused via the infection of periodontal tissues by the Gram negative bacteria. However, only a few studies have reported on the influence or correlation of obesity on or with the oral microbiota. The presence of
The participants of this study were the same subjects as those of Park et al.10); the individuals in 20s who followed a 4-week program consisting of diet control and exercise training for weight loss. Prior to the program, those with body mass index (BMI) <23 kg/m2 or a missing value among the analytic indices were excluded to leave a total of 46 participants for analyses. Among the 46 participants, 32 were females (69.6%) and 14 were males (30.4%). Six individuals had BMI ≥23 kg/m2 and <25 kg/m2 (13.0%) and 40 individuals had BMI ≥25 kg/m2 (87.0%). The participants stayed in a camp for four weeks and performed each day two hours of aerobic exercise, three hours of weight training and a low salt-low fat diet (≤1,300 kcal/day).
The oral examination before and after weight control was performed by one dentist (SJH). Two indices were used; the dental plaque index and the gingival index. The dental plaque index was measured as the dental state after the usual brushing and was thus measured after brushing using the Sum of Turesky modification of the Quigley- Hein Index (STQHI). The gingival index was measures as the level of inflammation using the Sum of Löe-Silness Gingival Index (SLSGI).
Before and after weight control, the physical measurements were taken and after blood collection, the levels of low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglycerides, and C-reactive protein (CRP) were measured. The levels of MMP-8, MMP-9, and IL-1b in the GCF were also measured. The measurements using blood samples were performed at the Dept. of Laboratory Medicine of Konyang University Hospital (Daejeon, Korea) and to estimate the inflammatory indices in the GCF, the Human IL-1b ELISA Kit (Promokine, Heidelberg, Germany), Quantikine human MMP-8 (R&D systems, Minneapolis, MN, USA) and Quantikine human MMP-9 (R&D systems) were used. The blood and GCF samples were analyzed three times and the mean of triplicate was obtained as the representative values.
The saliva samples stored at −20°C were sent to the DocsMedi Laboratory of Appletree Dental Hospital (Ilsan, Korea) for the test of periodontal bacteria. The ExiPrepDx Bacteria Genomic DNA Kit (Bioneer, Daejeon, Korea) was used to extract the bacterial genomic DNA from the saliva. The RT-qPCR (ExicyclerTM 96, Bioneer) was used to detect the
For statistical analyses, the variation before and after weight control was analyzed by paired t-test and the correlation of each index was analyzed by the partial correlation analysis (PCA) after controlling the dental plaque index and the gingival index. The two indices were controlled as they could affect the bacterial indices, while this study mainly aimed to analyze the change in periodontal bacteria based on obesity control. All statistical analyses were performed using the IBM SPSS 20.0 (IBM Corp., Armonk, NY, USA) with the level of significance set to 0.05.
As shown in Table 1, the participants showed a significant fall in BMI through the 4-week program of exercise and diet control. The serum LDL was significantly reduced (p<0.001). The levels of MMP-8, MMP-9, and IL-1b in the GCF were also significantly reduced after the obesity control program (p<0.001). However, the plaque index was increased (p<0.001) and despite weight loss, the serum triglyceride was increased (p<0.001).
Change in BMI, Inflammatory Index in Serum, Inflammatory Index in GCF, Plaque Index, and Gingival Index through 4-Week Weight Control Program (n=46)
Index | Baseline | After 4-week weight control | p-value |
---|---|---|---|
BMI (kg/m2) | 27.83±2.88 | 25.54±2.33 | <0.001 |
CRP in serum (mg/dL) | 0.21±0.22 | 0.29±1.28 | 0.674 |
LDL in serum (mg/dL) | 123.04±24.61 | 87.87±17.59 | <0.001 |
HDL in serum (mg/dL) | 54.30±9.51 | 54.32±10.19 | 0.984 |
Triglyceride (mg/dL) | 58.11±13.40 | 71.94±13.77 | <0.001 |
MMP-9 in GCF (ng/mL) | 10.52±5.54 | 5.80±5.12 | <0.001 |
MMP-8 in GCF (ng/mL) | 8.08±6.36 | 3.31±4.19 | <0.001 |
IL-1b in GCF (pg/mL) | 101.59±63.36 | 39.55±41.39 | <0.001 |
Plaque index | 50.65±17.08 | 72.26±31.47 | <0.001 |
Gingival index | 22.63±52.88 | 20.61±31.39 | 0.744 |
BMI: body mass index, GCF: gingival crevicular fluid, CRP: C-reactive protein, LDL: low-density lipoprotein, HDL: high-density lipoprotein, MMP: matrix metalloproteinase, IL: interleukin.
aPaired t-test.
As shown in Table 2, no significant change was found after the obesity control program for the total bacterial count in saliva or for
Change in the Amount of Periodontal Bacteria through 4-Week Weight Control Program (n=46)
Bacteria | Baseline | After 4-week weight control | p-value |
---|---|---|---|
Total bacteria | 1.4846×106±1.3634×106 | 1.5865×106±1.3382×106 | 0.369 |
2,680.17±4,085.66 | 4,345.52±10,354.82 | 0.313 | |
2,196.24±6,056.90 | 4,839.61±17,168.15 | 0.370 | |
169.52±506.18 | 315.22±585.34 | 0.140 | |
66.39±198.98 | 64.97±102.57 | 0.956 | |
174.50±288.88 | 138.28±278.88 | 0.382 | |
359.04±331.32 | 959.09±2,005.59 | 0.044 | |
705.70±1197.96 | 1,012.76±1,519.37 | 0.143 | |
Ratio of |
19.30±23.50 | 21.76±24.93 | 0.639 |
Ratio of |
11.54±28.98 | 15.78±47.50 | 0.295 |
Ratio of |
0.85±2.74 | 2.33±5.38 | 0.069 |
Ratio of |
0.35±0.97 | 0.33±0.89 | 0.864 |
Ratio of |
0.80±1.56 | 0.57±1.62 | 0.414 |
Ratio of |
3.00±3.57 | 5.30±6.59 | 0.025 |
Ratio of |
6.61±10.12 | 7.11±12.18 | 0.777 |
Values are presented as mean±standard deviation.
Ratio of each bacteria=amount of each bacteria/amount of total bacteria.
aPaired t-test.
As shown in Table 3, no correlation was found between serum lipid indices and GCF inflammatory indices in the PCA controlled for the plaque index and the gingival index based on the pre-intervention data. The BMI was negatively correlated with the total bacterial count and Fn. The plasma CRP showed a weak positive correlation with
Relationship between Obesity Index, Inflammation Index in GCF, and Periodontal Bacteria in Saliva at Baseline
BMI | CRP | LDL | HDL | Triglyceride | MMP-9 | MMP-8 | IL-1β | |
---|---|---|---|---|---|---|---|---|
CRP | 0.202 | |||||||
LDL | 0.101 | 0.105 | ||||||
HDL | −0.150 | −0.199 | 0.228 | |||||
Triglyceride | 0.389 |
0.125 | 0.313 | −0.286 | ||||
MMP-9 | −0.250 | −0.211 | −0.049 | 0.063 | 0.017 | |||
MMP-8 | −0.089 | −0.110 | 0.023 | 0.197 | 0.127 | 0.780 |
||
IL-1b | −0.041 | −0.388 |
−0.043 | 0.109 | −0.077 | 0.555 |
0.360 |
|
−0.301 |
0.330 |
0.270 | 0.210 | −0.097 | 0.017 | −0.113 | 0.082 | |
0.000 | 0.447 |
−0.093 | 0.128 | −0.209 | −0.135 | −0.171 | −0.148 | |
−0.037 | −0.089 | 0.008 | 0.145 | −0.127 | 0.247 | 0.260 | 0.231 | |
0.060 | −0.091 | −0.042 | 0.113 | −0.120 | 0.141 | 0.118 | 0.244 | |
−0.007 | −0.049 | −0.085 | 0.145 | −0.1048 | 0.124 | 0.161 | 0.148 | |
−0.240 | 0.384 |
0.101 | 0.098 | −0.008 | 0.054 | 0.053 | 0.073 | |
0.002 | −0.163 | 0.089 | 0.209 | −0.221 | 0.116 | 0.184 | 0.264 | |
Total bacteria | −0.344 |
−0.057 | 0.086 | 0.336 |
−0.261 | 0.167 | −0.017 | 0.164 |
Ratio of |
−0.147 | 0.396 |
0.261 | 0.101 | −0.065 | −0.100 | −0.094 | −0.027 |
Ratio of |
−0.033 | 0.081 | −0.054 | 0.090 | 0.134 | −0.049 | −0.079 | −0.042 |
Ratio of |
−0.135 | −0.222 | 0.011 | 0.146 | −0.105 | 0.348 |
0.333 |
0.304 |
Ratio of |
0.214 | −0.172 | −0.127 | 0.265 | −0.168 | 0.075 | 0.091 | 0.435 |
Ratio of |
−0.090 | −0.143 | 0.041 | 0.016 | 0.118 | 0.212 | 0.186 | 0.148 |
Ratio of |
0.000 | 0.313 |
−0.044 | −0.163 | 0.011 | 0.007 | −0.057 | 0.075 |
Ratio of |
0.098 | −0.107 | 0.030 | 0.076 | −0.154 | 0.054 | 0.092 | 0.273 |
GCF: gingival crevicular fluid, BMI: body mass index, CRP: C-reactive protein, LDL: low-density lipoprotein, HDL: high-density lipoprotein, MMP: matrix metalloproteinase, IL: interleukin,
*p<0.05 adjusted by plaque index and gingival index.
As shown in Table 4, the pre-intervention PCA showed significant correlations among 15 out of 28 bacterial strains. A positive correlation was shown by
Relationship between Periodontal Bacteria in Saliva at Baseline
0.208 | |||||||
0.049 | 0.285 | ||||||
0.034 | 0.215 | 0.840 |
|||||
0.014 | 0.362 |
0.905 |
0.743 |
||||
0.447 |
0.372 |
0.434 |
0.424 |
0.430 |
|||
−0.031 | 0.078 | 0.372 |
0.203 | 0.366 |
0.214 | ||
Universal | 0.617 |
0.229 | 0.308 |
0.205 | 0.353 |
0.311 |
0.016 |
*p<0.05 adjusted by plaque index and gingival index.
As shown in Table 5, no correlation was found between serum lipid indices and GCF inflammatory indices in the PCA controlled for the plaque index and the gingival index based on the post-intervention data. A weak positive correlation was shown by BMI with IL-1b (r=0.388) and ratio of
Relationship between Obesity Index, Inflammation Index in GCF, and Periodontal Bacteria in Saliva after 4-Week Weight Control Program
BMI | CRP | LDL | HDL | Triglyceride | MMP-9 | MMP-8 | IL-1β | |
---|---|---|---|---|---|---|---|---|
CRP | −0.023 | |||||||
LDL | −0.204 | 0.195 | ||||||
HDL | −0.340 |
−0.215 | 0.006 | |||||
Triglyceride | 0.187 | 0.054 | 0.057 | −0.106 | ||||
MMP-9 | 0.111 | 0.196 | −0.197 | −0.062 | 0.022 | |||
MMP-8 | 0.191 | 0.259 | 0.018 | 0.121 | −0.079 | 0.519 |
||
IL-1b | 0.388 |
0.223 | −0.133 | 0.058 | −0.185 | 0.363 |
0.801 |
|
−0.070 | −0.022 | 0.008 | −0.022 | −0.081 | −0.140 | −0.192 | −0.164 | |
0.051 | −0.118 | 0.210 | −0.140 | −0.020 | −0.139 | −0.200 | −0.085 | |
−0.108 | −0.019 | 0.062 | 0.008 | −0.194 | 0.047 | 0.017 | −0.007 | |
0.032 | −0.102 | −0.428 |
−0.073 | −0.338 |
0.237 | 0.110 | 0.274 | |
−0.128 | −0.011 | −0.217 | 0.060 | −0.109 | 0.130 | 0.125 | 0.117 | |
0.071 | 0.016 | −0.080 | −0.144 | 0.006 | −0.026 | −0.065 | 0.017 | |
0.175 | −0.033 | −0.273 | −0.063 | −0.140 | 0.175 | 0.180 | 0.248 | |
Total bacteria | −0.042 | −0.007 | −0.095 | −0.055 | −0.025 | −0.101 | −0.271 | −0.224 |
Ratio of |
0.054 | −0.075 | −0.034 | −0.159 | −0.036 | −0.115 | −0.147 | −0.082 |
Ratio of |
0.039 | −0.116 | 0.189 | −0.149 | −0.045 | −0.142 | −0.189 | −0.061 |
Ratio of |
−0.001 | −0.005 | 0.115 | −0.042 | −0.119 | 0.140 | 0.098 | 0.033 |
Ratio of |
0.192 | −0.060 | −0.335 |
−0.035 | −0.251 | 0.291 | 0.269 | 0.539 |
Ratio of |
0.063 | −0.038 | −0.329 |
0.035 | −0.144 | 0.291 | 0.327 |
0.369 |
Ratio of |
0.040 | −0.004 | −0.043 | −0.243 | 0.025 | 0.006 | 0.044 | 0.165 |
Ratio of |
0.327 |
−0.068 | −0.230 | −0.047 | −0.106 | 0.311 |
0.345 |
0.460 |
GCF: gingival crevicular fluid, BMI: body mass index, CRP: C-reactive protein, LDL: low-density lipoprotein, HDL: high-density lipoprotein, MMP: matrix metalloproteinase, IL: interleukin,
*p<0.05 adjusted by plaque index and gingival index.
As shown in Table 6, the post-intervention data varied from the pre-intervention data; the post-intervention PCA showed significant correlations among 13 out of 28 bacterial strains.
Relationship between Periodontal Bacteria in Saliva at Baseline
0.332 |
|||||||
0.091 | 0.036 | ||||||
0.049 | −0.115 | 0.307 | |||||
0.555 |
−0.052 | 0.505 |
0.457 |
||||
0.278 | 0.166 | 0.005 | 0.008 | 0.180 | |||
0.478 |
−0.046 | 0.293 | 0.509 |
0.717 |
0.332 |
||
Universal | 0.634 |
0.334 |
0.041 | −0.029 | 0.425 |
0.632 |
0.332 |
*p<0.05 adjusted by plaque index and gingival index.
Recently, an increasing number of studies are investigating the relationship between obesity and periodontal bacteria compared to the past. In the study by Tam et al.14), conducted on Type II diabetes patients, the diversity and composition of oral microbiota significantly varied between the group with BMI ≥30 kg/m2 and the group with BMI <30 kg/m2. Thomas et al.15) conducted microbial analyses on 19 patients with periodontitis and showed that the periodontal state in obese subjects was far more deteriorated with a larger number of missing tooth and a higher score of periodontal-support loss as well as a higher level of the
In a preceding study, the present investigator reported a fall in inflammatory indices of periodontal health achieved through an obesity control program consisting of physical activity and diet control10). The study10) had not applied other interventions such as oral health education or periodontal treatment and thus showed the direct effect of controlling the obesity indices on the other indices examined in the study, compared to previous cross-sectional studies. The results in this study were obtained through additional analyses of the periodontal bacteria in saliva from the same subjects as with the preceding study10), and the focus of the study was on identifying the correlations among physical obesity indices, serum lipid levels, CRP indices, GCF inflammatory indices and periodontal bacteria. Contradictory to the prediction, however, the bacteria in saliva fluctuated in the mean values of
Correlation analyses were performed on each index in this study at the base line and after the 4-week obesity control program, as it was necessary to investigate the correlation of the periodontal bacteria in saliva and other indices. While no intervention on oral health had been provided, the dental plaque index showed an increase following the program so that the respective index was excluded in the PCA. The periodontal bacteria showed a positive correlation with serum CRP inflammatory indices;
In a study by Maciel et al.19), normal weight subjects with periodontitis showed a positive correlation between the WHR and the proportions of
As the subjects of this study were in their 20s with relatively healthy periodontal states and obesity control relied on a short, 4-week intervention without a control group, precise determination of the variations in periodontal bacteria could be difficult. Nevertheless, this study is significant in having conducted an intervention study rather than a cross-sectional study and verified the possibility that obesity control could be used to adjust the relationship between gingival inflammatory indices and periodontal bacteria. Further studies should be conducted by including a control group in the design as well as various additional periodontal states.
We would like to thank Docsmedi Research Center at Apple Tree Dental Hospital for conducting an experiment to measure periodontal bacteria in saliva, which is the most important experiment for this study. The sequences of primers and probes used for bacterial measurement are not provided in this paper because of the confidentiality of Docsmedi Research Center.
No potential conflict of interest relevant to this article was reported.
This study was approved by the Institutional Review Board of Konyang University Hospital (No. KYUH 13-89).
Conceptualization: Soo-Jeong Hwang. Data acquisition: Soo-Jeong Hwang. Supervision: Soo-Jeong Hwang. Statistics: Min-Seock Seo and Soo-Jeong Hwang. Writing – original draft: Min-Seock Seo and Soo-Jeong Hwang. Writing – review & editing: Min-Seock Seo and Soo-Jeong Hwang.