Bariatric surgery did not have a significant effect on oral health nor on the perception of quality of life influenced by oral conditions.
Guy Weinberg DMD1, Leon Bilder DMD1, Jacob Horwitz DMD1,2*, Moti Pupko DMD1, Ahmad Mahajna MD2,3, Eli Machtei DMD1,2 and Ahmad Assalia DMD2,3
1Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, Haifa, Israel
2Faculty of Medicine, Technion (I.I.T.), Haifa, Israel
3Department of General Surgery, Rambam Health Care Campus, Haifa, Israel
*Corresponding Author: Jacob Horwitz, School of Graduate Dentistry, Department of Periodontology, Rambam Health Care Campus, Haalya Hashnya 8, Haifa 3525408, Israel; Tel: +972 4 8542983; Fax: +972 4 7773429; E-mail: j_horwitz@rambam.health.gov.il
ABSTRACT
Bariatric surgery did not have a significant effect on oral health nor on the perception of quality of life influenced by oral conditions.
Keywords: Obesity; Bariatric Surgery; Oral Health; Quality of Life
INTRODUCTION
Obesity is defined as having too much body fat and a weight greater than what’s considered healthy for an individual’s height, built and age. It is usually a preventable condition caused by excessive food intake, lack of physical activity, and genetic susceptibility [1]. Medically, people are considered obese when their body mass index – BMI (kg/m2) is equal or greater than 30, whereas BMI equal or greater than 40 indicates morbid obesity.
Obesity is a scourge of the 21st century. According to the World Health Organization (WHO), worldwide obesity has more than doubled since 1980. In 2014 more than 1.9 billion adults (39%) were overweight, of these more than 600 million (13%) were obese [2]. It is more prevalent in the United States where up to 30% of the population are obese and 6% have morbid obesity [3].
Conservative treatments include lifestyle changes (diet, physical activities) and sometimes medications. Another very effective therapy measure is bariatric surgery [4,5].
Bariatric surgery induces weight loss by reducing the size of the stomach, restricting the amount of food that can be eaten and absorbed. It includes a variety of procedures such as: gastric band, sleeve gastrectomy, biliopancreatic diversion with duodenal switch, and gastric bypass.
In the last two decades there was a significant increase in bariatric surgeries performed in the United States and in Israel. According to the American Society for Metabolic and Bariatric Surgery, there was an increase in the number of procedures performed from 16,000 in the early 1990s to more than 103,000 in 2003, and 220,000 in 2008 [6]. Similarly, in Israel, the ministry of health reported of an increase from 1001 surgeries performed in 2004 to 3615 in 2009 [7] and 9308 surgeries in 2015 [8].
Bariatric surgeries are considered safe and effective procedures. Various short and long-term potential risks were reported which include: excessive bleeding, infections, lung or breathing problems, gastrointestinal adverse reactions, hernias, hypoglycemia, malnutrition, vitamins and minerals deficiency, anemias, and on rare occasion even fatality [9,10].
The effects of these surgeries on general health are considered to be very significant [11] and include less risks of stroke and heart attacks, the complete reversal of type II diabetes and decreased risks for some types of cancer and liver disease not connected with alcohol. In addition, there is improved hypertension and dyslipidemia control, less sleep apnea and improved fertility.
Furthermore, as reported by Adams et al. in the New England Journal of Medicine [12], obese people (defined as BMI equal or up to 45) who underwent gastric bypass surgeries had significantly lower mortality rates compared to those who did not undergo surgeries.
In a recent review of the existing literature, it appears that bariatric surgeries related oral outcomes had only been studied scarcely7 with somewhat contradictory results [13-15].
Having in mind these dramatic changes and the reduced systemic inflammatory response, our hypothesis was that bariatric surgery outcomes may influence oral health as well.
Thus, the aim of this study was to analyze the effect of bariatric surgery on periodontal and dental health and the impact of these changes on quality of life.
MATERIALS AND METHODS
This prospective longitudinal cohort study included patients who were recruited from July 2014 to March 2016 and followed for a period of one year.
Inclusion criteria were: patients scheduled for all types of bariatric surgeries (gastric band, sleeve gastrectomy, biliopancreatic diversion with duodenal switch or gastric bypass) in the unit of advanced laparoscopic and bariatric surgery within the department of general surgery at Rambam Health Care Campus. Exclusion criteria included patients under the age of 18, patients who have received periodontal treatment 6 months prior to the baseline evaluation and pregnant women.
The study was initially approved by the Helsinki research ethics Committee (approval No. 0131-14-RMB) and all patients signed a written informed consent.
Data was collected and recorded twice: pre-operatively (baseline examination) and 12 months after surgery.
Detailed medical history including updated blood workups, medication intake, BMI and smoking habits were initially recorded.
Clinical evaluations
All patients attended the periodontal department for oral clinical evaluations.
Caries experience was assessed by the decayed, missing, and filled teeth (DMFT) index [16]. The periodontal examination was performed using the 6 Ramfjord index teeth [17] and included plaque index (PI) [18] probing pocket depth (PPD), bleeding on probing (BOP) and presence of calculus [19,20]. Additionally, the presence and condition of removable dentures and changes in oral soft tissues were recorded.
In addition, the Impact of this procedure and its outcome on the quality of life of the patients were evaluated using the Self-reported Oral Health Impact Profile – 14 questionnaires (OHIP-14) [21,22].
Statistical analysis
Statistical analysis was performed using Minitab Express software (Minitab, Ltd. Coventry, United Kingdom). Changes in systemic and oral variables following bariatric surgery were analyzed using Paired student’s t-test. Pearson correlation test was used to evaluate the association between systemic (BMI, HbA1c) and oral (DMFT, mean PPD, OHIP-14 score) variables, and simple regression analysis was performed to investigate how changes in predictor variables may predict the level of change in outcome variables. Finally, 2-sample t-test was used to compare two independent groups in order to see if their means are different. A 5% significance level was used.
RESULTS
Eighty patients were initially recruited and examined for this study; of these 50 were available for the final examination and are included in this analysis. Six patients were excluded because they did not undergo surgeries, and 24 did not attend the follow-up examinations. Most of the drop-outs were due to the decision of the patients to be followed-up at community clinics rather than at our medical center where they had the surgery done.
Patients were examined before and after surgery, with a mean follow-up period of 11.8 ± 2.6 months (range 6-18). Mean age at baseline was 37.5 ± 12.1 years (range 18-60); 26 were females (52%) and 24 males (48%). 12 patients (24%) were smokers and the rest none or former smokers. Demographic characteristics and medical status of the study population is presented in Table 1.
Table 1: Demographic characteristics and medical status of the study population.
|
Total n=50 (%) |
Gender Male Female |
24 (48) 26 (52) |
Education level High school or below Professional Academic |
30 (60) 4 (8) 16 (32) |
Married Yes No |
33 (66) 17 (34) |
Religion Jewish Not Jewish |
36 (72) 14 (28) |
Smoking habits Yes No |
12 (24) 38 (76) |
Diabetes treated patients Yes No |
10 (20) 40 (80) |
Calcium Channel Blockers medication Yes No |
4 (8) 46 (92) |
Vitamins intake Yes No |
18 (36) 32 (64) |
Table 2: Changes in Systemic Variables Following Bariatric Surgery.
Variable |
Before Surgery (Mean ± SD) |
After Surgery (Mean ± SD) |
Change (Mean ± SD) |
P-Value* |
BMI (kg/m2) |
42.7 ± 5.4 |
28.7 ± 5.1 |
14 ± 4.3 |
< 0.0001 |
HbA1c (%) |
6.3 ± 1 |
5.4 ± 0.7 |
0.9 ± 0.9 |
0.001 |
HbA1c among Diabetic treated Patients (%) |
6.9 ± 1.1 |
5.7 ± 0.9 |
1.2 ± 1.3 |
0.048 |
Fasting Glucose (mg/dl) |
114.1 ± 47.6 |
90 ± 15 |
24.1 ± 46.7 |
0.002 |
Fasting Glucose among Diabetic treated Patients (mg/dl) |
166 ± 91.5 |
104.7 ± 25.4 |
61.2 ± 97.4 |
0.118 |
* Paired student’s t-test
Table 3: Changes in Oral Variables Following Bariatric Surgery.
Variable |
Value Before (Mean ± SD) |
Value After (Mean ± SD) |
Change (Mean ± SD) |
P-Value* |
D |
1.3 ± 1.7 |
1.3 ± 2.1 |
0 ± 1.6 |
0.861 |
M |
2.3 ± 4.1 |
2.6 ± 4.2 |
-0.3 ± 0.6 |
0.003 |
F |
7.4 ± 5.3 |
8.2 ± 5.6 |
-0.8 ± 2.1 |
0.008 |
DMFT |
11 ± 6.8 |
12.1 ± 7 |
-1.1 ± 1.8 |
< 0.0001 |
Mean PI |
1.56 ± 0.9 |
1.54 ± 0.7 |
0.01 ± 0.9 |
0.928 |
Teeth with Calculus (%) |
38 ± 34.2 |
35.9 ± 29.3 |
2.1 ± 30.6 |
0.63 |
Mean PPD (mm) |
2.46 ± 0.7 |
2.37 ± 0.8 |
0.08 ± 0.5 |
0.259 |
Teeth with BOP (%) |
61 ± 37.6 |
68.3 ± 33.7 |
-7.3 ± 52.7 |
0.33 |
OHIP - 14 |
1.6 ± 0.5 |
1.5 ± 0.5 |
0.08 ± 0.5 |
0.236 |
OHIP Q5 |
2.3 ± 1.3 |
1.9 ± 1.1 |
0.5 ± 1.5 |
0.037 |
* Paired student’s t-test
Bariatric surgeries significantly improved systemic variables (Table 2).
BMI values (kg/m2) decreased significantly from 42.7 ± 5.4 to 28.7 ± 5.1 one year post-operatively (p<0.001). 72% of the patients were considered to have morbid obesity (BMI≥40) before surgery, while postoperatively, only 1 patient (2%) still had morbid obesity. Thirty patients (60%) had BMI<30 at the end of the study.
Similar metabolic effect was also observed. HbA1c level (%) was significantly reduced from 6.3 ± 1 to 5.4 ± 0.7 (p=0.001), and fasting glucose values (mg/dl) decreased from 114.1 ± 47.6 to 90 ± 15 (p=0.002). The prevalence of type II diabetes among these patients were 20% before surgery compared to only 6% of the study population still diagnosed and treated for diabetes one year later. When analyzing the difference in HbA1c levels specifically among diabetic treated patients, a significant mean decreases of 1.2 ± 1.3 was found (p=0.048).
When age was used as a predictor variable, a slight correlation was found only with BMI, again with weak but significant correlation (r=0.28, p=0.05). Older age may be associated with less decrease in BMI values after bariatric surgery
Caries experience was analyzed by comparing DMFT values before and after surgery. DMFT significantly increased from 11 ± 6.8 to 12.1 ± 7 (p<0.0001). However, changes in the number of active caries wasn't noted (mean change 0 ± 1.6, p=0.861); To the contrary, the number of fillings and missing teeth significantly increased by 0.8 ± 2.1 (p=0.008) and 0.3 ± 0.6 (p=0.003), respectively.
The periodontal status of these patients did not change between baseline and one year. Baseline PI scores at baseline and 1 year were 1.56 ± 0.9 and 1.54 ± 0.7, respectively (p=0.928). The % of teeth with calculus (38 ± 34.2 to 35.9 ± 29.3, p=0.63) were similar before and after bariatric surgery. Additionally, no changes in mean PPD (-0.08 ± 0.5mm, p=0.259) nor in the % of teeth with BOP (7.3 ± 52.7%, p=0.33) were acknowledged.
The perception of the impact of oral conditions on quality of life, as assessed by OHIP-14 questionnaires did not seem to be influenced by bariatric surgery. Mean overall score change from 1.6 ± 0.5 to 1.5 ± 0.5 did not reach statistical significance (p=0.236). However, when comparing each score of the questionnaire separately, question 5 “Have you been self-conscious because of your teeth, mouth, or dentures” showed a significant improvement with mean score decreasing from 2.3 ± 1.3 to 1.9 ± 1.1, p=0.037.
BMI and HbA1c changes were analyzed as possible predictors of the level of changes in the following outcome variables: DMFT, PI, PPD, BOP and OHIP-14 score. Neither BMI nor HbA1c were correlated with any of these (P≥0.05). However, changes in HbA1c were found to have a moderate correlation with OHIP-14 score change (r=0.45, p=0.05).
Additionally, genders were compared using 2-Sample t-test analysis. No significant differences were found between males and females in mean changes of BMI, HbA1c, DMFT PPD and BOP (P≥0.05). Females, though, had a slight decrease in mean PPD of 0.2 ± 0.6 mm, compared to males with a mean PPD increase of 0.04 ± 0.4 mm after surgery (p=0.09). Further Pearson correlations performed for females only between BMI changes and oral variables didn’t lead to any significant correlation either.
Moreover, 2-Sample t-test was also used to explore possible differences in mean PPD between different ethnicities. No significant differences were found between Jewish and non-Jewish patients (p≥0.05).
DISCUSSION
In this study, bariatric therapy was significantly associated with decreased BMI levels (mean BMI dropping from 42.7 ± 5.4 to 28.7 ± 5.1 kg/m2, p<0.0001) at one year. These results are in agreement with previous studies reporting on the effects of these procedures on general health. In a review and meta-analysis published by Buchwald et al. (2004) [10]11, BMI reduction following all types of bariatric surgeries was assessed in 8232 patients. According to their findings, a weighted mean decreases of 14.01 kg/m2 was found (95% CI, 10.77-17.3, ranging from 4.1 to 27.0 kg/m2), and in most cases, weight loss outcomes did not differ significantly for assessments at 2 years or less compared with those at more than 2 years. Similarly, in a 7-18 month postoperative follow up performed by Maffazioli et al. (2016)27 the mean drops in BMI ranged from 12.6 ± 1.7 to 15.9 ± 1.1 kg/m2.
This drop in BMI was accompanied by a concomitant improvement in HbA1c levels. The mean decrease was 0.9 ± 0.9% (p=0.001) for all participants, and 1.2 ± 1.3% (p=0.048) among patients that were previously diagnosed with diabetes. These significant reductions are also in accordance with the literature. In a systematic review by Maggard-Gibbons et al. (2013) [23], bariatric surgical procedures performed on obese adults with diabetes were significantly associated with improved glycemic control and HbA1c reduction ranging from 0.9 to 1.43%, at one to two years postoperatively. Likewise, Buchwald et al. (2004) [10] 11 in a similar systematic review and meta-analysis reported a weighted mean drop in HbA1c of 0.3% (range 0 to 0.65) for all patients evaluated, and of 2.7% (range 0.7 to 5.0%) among diabetic patients. In their study, complete resolution of type II diabetes was defined as being able to discontinue all diabetes-related medications and maintain blood glucose levels within the normal range. According to their findings, improvement was found for all of types of surgery and complete resolution was achieved in 76.8% (range 70.7% to 82.9%) of the patients. Our present study demonstrated a similar reduction of 70% in the prevalence of diabetes.
During this year, there was a statistically significant increase in the mean DMFT of all patients (from 11 ± 6.8 to 12.1 ± 7, p<0.0001). A more in-depth examination of this phenomenon indicates that this was the result of an increase in the number of fillings (from 7.4 ± 5.3 to 8.2 ± 5.6, p=0.008) and extractions (from 2.3 ± 4.1 to 2.6 ± 4.2, p=0.003). This may indicate that, following bariatric surgery, these patients have taken the initiative to improve their dental status by seeking dental treatment. According to Heling et al. (2006) [9], 34% of the patients after bariatric surgery reported increased frequency of visits to the dentist. Early case report studies have highlighted an association between higher caries prevalence and teeth erosions after bariatric therapy [24,25]. Their hypothesis was that the increased risk may be associated with post-surgical cariogenic meal patterns, along with nutrient deficiencies, gastrointestinal reflux, and lower salivary production & buffering capacity. In addition, 37% of the treated patients questioned about their nutritional habits following weight loss surgeries have reported an increase in the intake of sweet beverages and food [9]. Additional analysis performed in a longitudinal cohort study up to 6 months by a Brazilian group (Marsicano et al. 2011) [13] also reported a significant increase in non-treated dental caries (p=0.004) and in teeth wear (p=0.012). However, when DMFT was compared between a control group of obese patients who did not undergo surgeries and patients after bariatric procedures, no significant differences were found (mean DMFT was 16.06 ± 6.29 and 16.11 ± 5.19, respectively) [12]. Moreover, no significant differences in salivary flow could be established (p>0.05) [13] [24].
The periodontal status of participants was unchanged at 1 year post-operatively. This might be attributed to the lack of overall awareness to periodontal disease among patients and providers alike. However, the same Brazilian group reported contradictory results in a series of publications: de Moura-Grec et al. (2014) [24] found an increased prevalence of periodontal pockets (p=0.02) and a mean pocket depth increase of about 0.5 mm (p<0.001). Similarly, Marsicano et al (2012) [12] reported an increase in the number of periodontal pockets associated with bariatric surgery (OR = 3.29. 95%CI 1.16-9.33, p=0.039). In a more recent study by de Carvalho Sales-Peres et al. (2015), 50 patients who underwent bariatric surgery were examined at 12 months. They found a statistically significant increase in the mean PPD and CAL (PPD from 1.84 ± 0.47 to 2.07 ± 0.43, CAL from 1.96 ± 0.61 to 2.15 ± 0.52). In the same period, the amount of P. gingivalis increased (p=0.028) and was associated with PPD and gingival bleeding (p=0.03 and p=0.004 respectively).
Finally, the present study failed to show an effect of bariatric procedures on the impact of oral conditions on their quality of life (mean OHIP-14 score change from 1.6 ± 0.5 to 1.5 ± 0.5, p=0.236). Conversely, Marsicano et al. (2011) [13] reported a significant decrease in the impact of oral health on quality of life 6 months after surgery (p<0.05). While it is well accepted that bariatric therapy itself has in general positive influence on the quality of life [26], it seems reasonable to assume that oral outcomes may not be an influencing factor.
A major disadvantage of the present study is associated with the large dropout (30 out of the 80 patients). The main reason for this dropout was a patient preference to attend follow up at their respective community health care clinics and not to return to the hospital. According to a systematic review reporting on long-term follow-ups after bariatric procedures [27], compliance among the original cohort is rarely achieved. The authors concluded that protocols for handling and maintaining subjects in order to reduce the drop-outs should be developed and adopted in weight loss studies. Hence, while it is unlikely that these patients had a different response to therapy, this phenomenon should be noted.
CONCLUSIONS
Bariatric surgery did not have a significant effect on oral health nor on the perception of quality of life influenced by oral conditions, in spite of significant weight loss and improvements in general health parameters.
REFERENCES
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