Gastric emptying rate before and after orthodontic treatment examined with the [ 13C] breath test: A pilot study


Orthodontic patients with malocclusion have significantly lower masticatory and gastrointestinal digestive function than persons with normal occlusion. Although several studies have suggested that masticatory function is improved after orthodontic treatment, the relationship between such improvement and change in gastrointestinal symptoms has not been quantitatively evaluated. In this study, we aimed to investigate the change in masticatory function and the gastric emptying rate in patients with malocclusion, before and after orthodontic treatment.


Seven women with malocclusion, before (pretreatment group) and after orthodontic treatment (posttreatment group), and 7 healthy dentate female volunteers (control group) underwent a 13 C-acetate breath test ( 13 CO 2 ) with a liquid meal and the color changeable gum test, along with completing the frequency scale for symptoms of gastroesophageal reflux and a questionnaire on food intake. Between-group differences were evaluated.


The pretreatment group had significantly longer maximum 13 CO 2 exhalation time and lower masticatory function, quantified using a higher red-color value on the gum test and the questionnaire on food intake, than did the posttreatment and control groups. No significant differences were identified between the posttreatment and the control groups.


We provide evidence of improvement of masticatory function after orthodontic treatment, which was associated with a faster rate of gastric emptying.


  • Subjects with malocclusion have a significantly slower gastric emptying rate.

  • Orthodontic treatment provided subjective improvement of masticatory function.

  • Improvement of masticatory function increased gastric emptying rates.

  • After orthodontic treatment, gastric emptying became faster.

In the oral cavity, food is processed into transportable and digestible pieces during mastication by the teeth. Simultaneously, the tongue and salivary glands moisten and lubricate the food particles and bind them into a coherent bolus that can be easily swallowed. After mastication and swallowing, the food bolus is transported to the stomach, where its size is further reduced mechanically by vermicular movement and chemically by gastric acid into small particles. Before the food bolus exits the pylorus, it must be reduced to particles less than 2 mm in size. Based on this mechanism, it has been postulated that functional depression of mastication and reduced exposure to saliva cause impairment in bolus formation, inadequate secretion of gastric acid, and overall digestive disorders.

Several studies have examined the relationship between mastication and digestion. Farrell reported the effect of mastication on digestion for various types of food, providing evidence that some foods are better digested with mastication, whereas others are equally well digested without mastication. Mercier and Poitras found that approximately 60% of patients with an edentulous mandible reported digestive complaints, such as burning sensation, bloating, cramps, constipation, and diarrhea. These complaints improved in 85% of these patients after insertion of functional dental prostheses.

Impairment of masticatory function in patients with malocclusion has been associated with higher rates of gastrointestinal tract symptoms. Several studies have examined the relationship between malocclusion and masticatory function, suggesting that orthodontic treatment can improve masticatory function by improving occlusal relationships, in addition to improving esthetics. Togawa et al and Kusano et al evaluated the relationship between malocclusion and digestive symptoms using the self-report frequency scale of symptoms of gastroesophageal reflux disease (FSSG). Quantitative techniques have also been used to evaluate masticatory function, with the color-changeable chewing gum test widely used as a simple method. This technique has been used to demonstrate the differential effects of different types of malocclusion on masticatory function. Several methods are also available to evaluate gastrointestinal function, including measurement of esophageal pressure, inspection of stomach secretion, and measurement of gastroesophageal pH. Recently, the rate of gastric emptying has been measured using the stable isotope [ 13 C], which is rapidly absorbed by the duodenum and is present in the expired air or blood after gastric emptying of a test meal. The [ 13 C] breath test is a reliable and noninvasive method for assessing the rate of gastric emptying without radiation exposure, and its accuracy is well supported by several studies that reported a strong correlation between the [ 13 C] breath test and scintigraphy, which is the gold standard for measuring gastric emptying. Using this technique, Pera et al described a relationship between malocclusion, mastication, and digestion, with a reduction in the number of masticatory cycles leading to delays in gastric emptying of identical test meals. Based on their findings, Pera et al concluded that comminution of food significantly influences gastric emptying rates. Moreover, using the [ 13 C] breath test, Koike et al reported a delay in gastric emptying of a liquid meal in patients with malocclusion, compared with those with normal occlusion, indicating that suppression of gastric function is linked to malocclusion. It is probable that chronic insufficient comminution of food in daily life in patients with malocclusion causes higher functional stress on the gastrointestinal system than in persons with normal occlusion.

It is well known that orthodontic treatment can improve masticatory function. However, the relationship between orthodontic treatment and changes in gastrointestinal function has yet to be fully clarified. Therefore, we aimed to evaluate the change in gastrointestinal function, using the [ 13 C] breath test with a liquid test meal, before and after orthodontic treatment, in patients with malocclusion, and to investigate the relationship between occlusion, mastication, and gastrointestinal function to test the hypothesis that gastrointestinal function improves with orthodontic treatment of malocclusion.

Material and methods

Seven Japanese women who visited the orthodontic clinic at Tokyo Medical and Dental University Dental Hospital for orthodontic treatment for malocclusion were randomly selected to form the malocclusion group. Prospective subjects were screened on the following inclusion criteria: 18 to 39 years old; normal body mass index (BMI); chief complaint of malocclusion, with a need for orthodontic treatment; no cleft lip or palate, or other craniofacial syndrome; no history of abdominal surgery; no use of medications, including gastrointestinal prokinetic agents, calcium antagonists, and selective serotonin reuptake inhibitors; absence of a current disease; no habitual heavy smoking or alcohol consumption; and no current or possible pregnancy. Based on these inclusion criteria, we recruited 7 subjects to form our malocclusion group, 26.7 ± 5.5 years old, with a BMI of 20.0 ± 2.9 kg per square meter. Using the same inclusion criteria, with the exception of the presence of malocclusion, 7 women were recruited to form the control group, 25.4 ± 1.0 years old, with a mean BMI of 19.2 ± 1.4 kg per square meter. Some subjects in our malocclusion and control groups were participating in another study. There were no significant differences in the mean age and BMI between the 2 groups.

We chose to include only women in our study based on the findings of Hellmig et al of a significant difference in gastric emptying between men and women. Moreover, Klingensmith et al reported the range of gastric emptying time, as a function of age and sex, to be narrower for women than for men. All subjects provided written informed consent after receiving a full explanation of the goals and structure of our study, and our methods were approved by the ethical committee of Tokyo Medical and Dental University (number 655) and conducted in accordance with the Declaration of Helsinki.

Outcome variables were measured in the malocclusion group before the orthodontic treatment (pretreatment) and at 1 month after the end of active orthodontic treatment (posttreatment), with a duration of active orthodontic treatment of 28 ± 6.1 months. Outcomes were measured in the control group at 2 time points, 30 months apart.

Measurements were taken as below, according to our previous study.

Gastric emptying was assessed using the [ 13 C]-labeled acetate breath test with a liquid test meal that had been stored at room temperature (22°C-26°C). Gastric emptying tests were performed at 9:00 am , after an overnight fast. All subjects ingested the liquid meal (RACOL; Otsuka Pharmaceuticals, Tokyo, Japan) (200 g, 200 mL, 200 kcal) labeled with 100 mg sodium [ 13 C] acetate (1- 13 C, 99%; Cambridge Isotope Laboratories, Andover, Mass) as quickly as possible within 1 minute. Breath samples were collected using special sampling bags (Otsuka Pharmaceuticals), before ingestion of the test meal, at 5-minute intervals over the first 20 minutes after ingestion, then at 10-minute intervals over the next 40 minutes, and thereafter every 15 minutes over a final 30-minute period. The concentration of 13 C in the collected breath sampling bags was measured using an infrared spectrophotometer (POCone; Fukuda Denshi, Tokyo, Japan). The maximum 13 CO 2 excretion time was evaluated as an indicator of gastric emptying time, with excretion time (minutes) determined directly from the [ 13 CO 2 ]% dose per hour curve.

Masticatory function was assessed using color-changeable chewing gum (Masticatory Performance Evaluating Gum Xylitol; Lotte, Saitama, Japan; 70 × 20 × 1 mm, 3.0 g) and a self-report questionnaire on food intake. All subjects were instructed to chew the gum for 80 strokes, without restriction on chewing frequency. The gum was collected immediately after chewing and compressed with a thickness of 1.5 mm in a polyethylene film between 2 glass plates. The gum was then removed from the glass plates, and its color was measured through the polyethylene film at 5 points (at the center of the compressed gum and at approximately 3 mm above, below, and to the right and left) with a colorimeter (CR-13; Konica-Minolta, Tokyo, Japan). The CIE L*a*b* color system was used to record the color and, specifically, to measure the a* value representing the degree of red coloring. We then calculated the mean a*value (points) for each trial.

The questionnaire on food intake included 51 foods ( Table I ). Subjects evaluated those foods based on the following 6 choices: 1, you are able to chew this food easily; 2, you are able to chew this food, but with difficulty; 3, you are not able to chew this food; 4, you do not eat this food, due to personal taste; 5, you are not able to eat this food due to physical problems, such as allergy; 6, you have never eaten this food. Choices 1, 2, and 3 were rescored as 0, 1, and 2 for analysis, with choices 4 through 6 not included in the analysis. To calculate a score of chewing difficulty from responses provided by each subject, the total score for all foods was divided by the number of foods scored, using the methods previously described by Saito et al.

Table I
Fifty-one foods used for the questionnaire on food intake
Zoni Raw tuna
Pudding Chicken (fried)
Rice Fried pork cutlet
Boiled kelp Meatball
Sweetened and jellied bean paste Ham
Banana Sausage
Buckwheat noodles Crackers
Burdock (boiled) Cabbage (raw)
Shiitake mushroom (boiled) Chicken (roasted)
Lettuce Chinese cabbage (pickled)
Pineapple Octopus (boiled)
Bread Roast beef
Beef (boiled) Pork (roasted)
Chicken (boiled) Apple
Gum Beef steak
Cabbage (boiled) Yellow pickled radish
Spinach (boiled) Cubic rice crackers
Short neck clam (boiled) Lotus root
Eggplant (pickled) Carrot (raw)
Carrot (boiled) Peanuts
Boiled fish paste Raw cuttlefish
Cucumber Rice cracker
Konnyaku Abalone
Gummi candies French bread
Jellyfish Dried cuttlefish
Beef jerky

All subjects completed the FSSG, The FSSG consists of 12 questions ( Table II ) on dyspeptic and dysmotility symptoms. The frequency of symptoms was measured on the following scale: 0, never; 1, occasionally; 2, sometimes; 3, often; and 4, always.

Table II
Frequency scale for the symptoms of gastroesophageal reflux disease (GERD) questionnaire
Do you have any of the following symptoms?
If so, please circle the appropriate response below.
1 Do you get heartburn?
2 Does your stomach get bloated?
3 Does your stomach ever feel heavy after meals?
4 Do you sometimes subconsciously rub your chest with your hand?
5 Do you ever feel sick after meals?
6 Do you get heartburn after meals?
7 Do you have an unusual (eg, burning) sensation in your throat?
8 Do you feel full while eating meals?
9 Do some things get stuck when you swallow?
10 Do you get bitter liquid (acid) coming up into your throat?
11 Do you burp a lot?
12 Do you get heartburn if you bend over?

Statistical analysis

For the control group, values for all outcome variables obtained at the 2 time points of measurement were comparable; therefore, the mean value of the 2 measurements was used in the analysis. The Steel-Dwass test was used to evaluate between-group differences at the 2 time points of measurements for the malocclusion group: pretreatment/control and posttreatment/control. The Wilcoxon signed rank test was used to evaluate changes in gastric emptying rates, a*values, chewing difficulty score, and FSSG scores, before and after orthodontic treatment. All statistical analyses were performed using SPSS statistical software (version 20; IBM, Armonk, NY), with statistical significance established at a P <0.05.


The classification of malocclusion (Angle Class I through Class III) for subjects who received active orthodontic treatment is summarized in Table III . Maximum excretion time was significantly longer in the pretreatment group (median, 50 minutes; range, 40-70 minutes) than in the control group (median, 40 minutes; range, 35-50 minutes; P = 0.049), with no difference between the control group and the posttreatment group (median, 40 minutes; range, 30-50 minutes; P = 0.623; Fig 1 ). In the malocclusion group, maximum excretion time was significantly longer in the pretreatment group (median, 50 minutes; range, 40-70 minutes) than in the posttreatment group (median, 40 minutes; range, 30-50 minutes; P = 0.027; Fig 2 ). The 13 C breath excretion curve for the pretreatment and posttreatment groups is shown in Figure 3 . 13 CO 2 excretion (% dose/h) was more elevated in the pretreatment group than in the posttreatment group, with significant differences identified at the following time points after meal ingestion: 10 minutes ( P = 0.004), 15 minutes ( P = 0.013), 30 minutes ( P = 0.013), 40 minutes ( P = 0.047), 60 minutes ( P = 0.035), 75 minutes ( P = 0.035), and 90 minutes ( P = 0.035).

Table III
Characteristics of subjects
Subject Type of malocclusion SNA (°) SNB (°) ANB (°) Md plane angle (°) U1 to SN (°) L1 to Md plane (°) Over bite (mm) Overjet (mm) Discrepancy (Mx, mm) Discrepancy (Md, mm) BMI (kg/m 2 )
1 Mandibular prognathism, facial asymmetry 80.8 86.1 −5.3 41.7 131.3 87.4 −8.0 8.0 −1.0 −3.0 20.0
2 Maxillary protrusion 84.6 83.4 1.2 35.6 124.7 100.7 −8.0 8.0 −1.5 −0.5 18.0
3 Maxillary protrusion, open bite 80.7 78.9 1.8 45.3 114.3 89.1 1.0 2.0 −8.0 −6.0 19.4
4 Facial asymmetry 81.4 80.0 1.4 35.2 99.7 71.0 −1.5 3.0 −2.0 −2.0 26.8
5 Maxillary protrusion, facial asymmetry 82.7 75.6 7.1 27.3 112.0 91.3 0.0 −2.0 −3.0 −3.0 18.4
6 Mandibular prognathism, facial asymmetry 80.1 86.0 −5.9 18.2 120.7 86.2 1.5 3.0 −5.5 0.0 18.3
7 Maxillary protrusion, open bite 77.9 77.3 0.6 38.3 109.5 105.0 −2.5 8.0 0.0 −3.0 19.1
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Dec 12, 2018 | Posted by in Orthodontics | Comments Off on Gastric emptying rate before and after orthodontic treatment examined with the [ 13C] breath test: A pilot study
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