Introduction
Overweight and obesity are ever more common these days, especially in developed countries. The reason why obesity is important in dentistry is because many studies indicate a link between body weight and certain dental diseases. There is evidence that intense adipose tissue accumulation may cause oral inflammatory diseases because hyper-inflammatory periodontal tissues react with an accentuated response to infection by periodontal pathogens and therefore, the incidence of periodontitis in the obese is greater than in the average population [
1].
Periodontitis is a multifactorial inflammatory disease which involves continuous destruction of tissues surrounding and supporting the teeth. The role of bacteria in the onset of periodontitis is essential; however, the development, clinical appearance, and level of progression of the disease are influenced by host-related factors. Examples of conditions associated with an increased risk of developing periodontitis include diabetes, smoking, elderly age, and stress [
2,
3]. Relative to bacteria, fungi such as various
Candida species make up a minor proportion of the oral and crevicular fluid flora. However, their numbers may increase in conditions of nutrient deficiency or reduced immune system function; examples of other factors predisposing to Candida growth include removable denture use, diabetes, and limited saliva production [
4,
5].
Healthy diet and exercise are an essential part of obesity treatment. If these fail to produce results, it is possible to perform body weight reduction surgery, especially when treating markedly severe obesity and its concomitant diseases (e.g., type 2 diabetes, hyperlipidemia, hypertension) [
6]. Several previous studies indicate that despite significant weight loss after surgery, the condition of periodontal tissues and the composition of crevicular fluid fail to improve; some studies have even found a deterioration in these outcomes [
7,
8].
In our study, we aimed to investigate the differences in crevicular gingival fluid microflora between patients in the obese group and the average (normal body weight) population, as well as to assess the effect of weight loss after bariatric surgery on the crevicular microflora.
Results
Of the total of 57 subjects in the study, 22 patients—13 women and 9 men—were in the normal control group, with a mean age of 33.9 (SD 9.24) years, ranging from 18 to 53 years and a mean body mass index (BMI) of 23.3 (SD 2.16) kg/m
2. Of the 35 obese subjects, 18 did not undergo surgery and had no change to their body weight; these 13 women and 5 men made up the obese control group, with mean age 44.1 (SD 10.79) years, ranging from 19 to 58 years and mean BMI 44.5 (SD 6.52) kg/m
2. Seventeen of the obese subjects underwent weight loss surgery (surgical patient group); the mean age of these 7 women and 10 men was 39.4 (SD 10.17) years, ranging from 21 to 54 years, and their mean BMI before surgery was 46 (SD 7.03) kg/m
2. Repeat sampling was performed an average 11.3 months after gastric bypass surgery, at which time a mean weight loss of 41.5 kg and a new mean BMI of 31.5 (SD 8.3) kg/m
2 was recorded (Table
1). There was no loss to follow-up in the surgery group.
Table 1
Descriptive statistics of age, gender, and BMI by study group
Age | 33.9 (9.24) [18–53] | 44.1 (10.79) [19–58]§ | 39.4 (10.17) [21–54] |
Male/female | 9/13 | 5/13 | 10/7 |
BMI at baseline | 23.3 (2.16) [19.8–29.5] | 44.5 (6.52) [35.0–58.0]§ | 46.0 (7.03) [34.5–60.0]§ |
BMI at follow-up | N/A | N/A | 31.5 (8.3)* |
Change in BMI | N/A | N/A | − 14.5 (4.45) |
As to periodontal conditions, no signs of inflammation were observed in any group, and no attachment loss greater than 3 mm or pathologically deep periodontal pockets were detected, including in subjects after surgery and weight loss.
Crevicular fluid samples included
Actinomyces,
Candida,
Capnocytophaga,
Eikenella,
Fusobacterium,
Granulicatella,
Haemophilus,
Lachnoanaerobaculum,
Lactobacillus,
Micrococcus,
Neisseria,
Prevotella,
Rothia,
Staphylococcus,
Streptococcus, and
Veillonella genera, as detailed in Table
2. Adjustment for age or sex proved unnecessary when comparing the study groups in terms of germ counts at baseline.
Table 2
Presence of bacterial genera in crevicular fluid samples by study group
Actinomyces | 1; 4.545 | 0; 0 | 1; 1.882 | 0; 0 |
Candida | 1; 454.5 | 2; 7.333 | 0; 0 | 5; 44,176§ |
Capnocytophaga | 1; 4.545 | 2; 11.11 | 0; 0 | 0; 0 |
Eikenella | 0; 0 | 0; 0 | 0; 0 | 1; 58.82 |
Fusobacterium | 4; 140.9 | 3; 1167 | 2; 647.0 | 3; 176.4 |
Granulicatella | 0; 0 | 0; 0 | 1; 588.2 | 0; 0 |
Haemophilus | 1; 4.545 | 6; 629.5* | 2; 70.58 | 4; 1824 |
Lachnoanaerobaculum | 1; 4.545 | 0; 0 | 0; 0 | 0; 0 |
Lactobacillus | 0; 0 | 1; 1.777 | 0; 0 | 0; 0 |
Micrococcus | 0; 0 | 1; 5.555 | 0; 0 | 0; 0 |
Neisseria | 1; 1.454 | 10; 11,906* | 10; 1606* | 4; 6718 |
Prevotella | 3; 590.9 | 11; 6783* | 7; 2529 | 11; 13,882 |
Rothia | 0; 0 | 1; 5.555 | 1; 58.82 | 1; 58.82 |
Staphylococcus | 2; 4547 | 0; 0 | 0; 0 | 2; 64.70 |
Streptococcus | 22; 25,270 | 18; 43,005* | 17; 23,257 | 17; 54,118§ |
Veillonella | 2; 456 | 2; 611.1 | 1; 588.2 | 2; 117.6 |
It can be observed that the average germ count increased after surgery and weight loss, albeit not significantly. In addition,
C. albicans and non-albicans
Candida species:
C. dubliniensis,
C. kefyr, and
C. lusitaniae emerged after surgery, both in terms of the proportion of subjects and a significant germ count surge. The proportion of patients with
Neisseria decreased significantly after surgery. A phenomenon of
Candida only emerging where
Neisseria was absent throughout or eliminated after surgery was also noticeable. Other genera affecting a considerably increased proportion of subjects upon weight loss included
Prevotella (Table
3).
Table 3
Number and percentage of positive cultures for microorganisms in 17 surgery patients before and 6–12 months after bariatric surgery in decreasing order of pre-surgery values
Streptococcus | 17 | 100.0 | 17 | 100.0 | N/A |
Neisseria | 10 | 58.8 | 4 | 23.5 | 0.0339 |
Prevotella | 7 | 41.2 | 11 | 64.7 | 0.2482 |
Fusobacterium | 2 | 11.8 | 3 | 17.6 | 0.6547 |
Haemophilus | 2 | 11.8 | 4 | 23.5 | 0.4142 |
Veillonella | 1 | 5.9 | 2 | 11.8 | 0.5637 |
Granulicatella | 1 | 5.9 | 0 | 0.0 | 0.3173 |
Rothia | 1 | 5.9 | 1 | 5.9 | N/A |
Actinomyces | 1 | 5.9 | 0 | 0.0 | 0.3173 |
Staphylococcus | 0 | 0.0 | 2 | 11.8 | 0.1573 |
Candida | 0 | 0.0 | 5 | 29.4 | 0.0253 |
Eikenella | 0 | 0.0 | 1 | 5.9 | 0.3173 |
Discussion
In our study, no periodontal abnormalities were found either in the normal control or any of the obese groups. More and more studies suggest that excess weight is not a predisposing entity on its own, and periodontitis requires the simultaneous presence of other factors for its development. Saxlin et al. have also come to the conclusion that overweight and obesity are not substantial risk factors in the onset and pathogenesis of the periodontal disease (similarly, they studied a low-risk population) [
10].
No periodontitis was observed after postoperative weight loss in our obese patients either. Similar results were obtained by Sales-Peres et al. in 2017: during their 1-year follow-up of bariatric surgery, probing depth and the extent of attachment loss did not change significantly from the preoperative baseline (although increased gum bleeding was observed during the first 6 months) [
11].
Although periodontal status did not change remarkably after weight loss, changes did occur in the microflora of the crevicular fluid as the average germ count increased and new species such as non-albicans
Candida species emerged. A number of studies suggest that changes to the quantitative and qualitative composition of the crevicular fluid are more common in patients undergoing bariatric surgery. In 2015, Sales-Peres et al. investigated the quantitative relations of 4 periodontal pathogenic bacterial species,
Porphyromonas gingivalis,
Tannerella forsythia,
Treponema denticola, and
Prevotella intermedia, prior to and 6 and 12 months after bariatric surgery. They found that the
P. gingivalis count increased abruptly in the first 6 months and then decreased substantially; overall, the counts of other bacteria declined slightly over 12 months [
7]. In contrast, of these bacteria, only
Prevotella species were present in our study, and the proportion of subjects affected increased after weight loss.
Hashizume et al. investigated patients’ saliva sample levels of
Streptococcus,
Lactobacillus spp., and
C. albicans before and 6 months after bariatric surgery. They detected high
C. albicans levels both before and after the intervention and elevated
S. mutans levels 6 months after bariatric surgery. However, they also reported that the patients with obesity in their study suffered from a number of chronic systemic comorbidities such as diabetes, for which they were treated with various medications and were prosthesis users, all of which predispose to the expansion of
C. albicans [
12]. None of these predisposing factors was present in our study, yet in addition to
C. albicans, non-albicans
Candida species such as
C. dubliniensis,
C. kefyr, and
C. lusitaniae emerged after surgery. Typically, these non-albicans
Candida species can be isolated from the oral cavity of immunosuppressed patients, mainly those on chemotherapy for tumors, and HIV-infected individuals [
4,
5,
13,
14].
It was also observed in our study that the various
Candida species only emerged where
Neisseria species were absent throughout or eliminated after surgery. In 2017, Janus et al. investigated in vitro the effect of
C. albicans on oral biofilm. In a similar fashion to our study, they found that biofilms without
C. albicans contained more bacteria of aerobic and facultative anaerobic genera such as
Neisseria,
Rothia, and
Streptococcus [
15].
The strengths of our study include the fact that it provides a detailed picture of crevicular microflora changes following bariatric surgery. In contrast with previous research, our investigations were extended beyond bacteria to cover fungi as well, and we only included non-smoking subjects with good general health who had susceptibility factors neither for periodontal diseases nor for Candida infection. Nevertheless, our study has limitations: our findings are subject to more precise elucidation based on patient groups of greater sample sizes. In addition, the control groups could also be re-sampled to evaluate potential changes in crevicular fluid composition. Finally, a longer follow-up of several years could be undertaken to find out about the constant or variable nature of these results.
In conclusion, our study demonstrates that changes after bariatric surgery do affect the oral cavity and the periodontium as well; since the composition of crevicular gingival fluid changed 6 to 12 months after surgery, various non-albicans Candida species emerged, and the proportion of those affected by Prevotella increased. However, with an uninflamed periodontal condition before surgery, absence of predisposing factors, and good oral hygiene, periodontitis is highly unlikely to develop after surgery and weight loss even if changes to the crevicular microflora have taken place. For this reason, it would be important to assess the condition of the oral cavity and periodontium and to treat and eliminate possible inflammatory conditions in patients with obesity before surgery.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.