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Journal of Digestive Diseases 2015; 16; 337–341

doi: 10.1111/1751-2980.12246

Original article

Association between individual response to food taste and gastroesophageal symptoms Tomoyuki SHIBATA,* Masahiko NAKAMURA,† Takafumi OMORI,* Tomomitsu TAHARA,* Yuichiro ICHIKAWA,* Masaaki OKUBO,* Takamitsu ISHIZUKA,* Yoshihito NAKAGAWA,* Mitsuo NAGASAKA,* Masakatsu NAKAMURA,‡ Tomiyasu ARISAWA‡ & Ichiro HIRATA* *Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake, †Department of Gastroenterology, Namiki Hospital, Nagoya and ‡Department of Gastroenterology, Kanazawa Medical University School of Medicine, Kahoku, Japan

OBJECTIVE: Taste is an important element in food preferences. Gastroesophageal reflux disease (GERD) is related to lifestyles including eating habits. We aimed to investigate the relationship between responses to specific tastes and GERD. METHODS: Altogether 280 patients including 170 men with a mean age of 58.6 years were included in the study to determine the relationship between their liking for specific tastes and GERD using a new self-administered questionnaire (responses to various tastes and participants’ sensitivity to taste and hot food and on the frequency of stomatitis). Another self-administrated questionnaire was administrated for a diagnosis of GERD (the frequency scale for the symptoms of GERD cut-off score of 10). Furthermore, 142 of 280 patients who had received esophagogastroduodenoscopy (EGD) were investigated on the association between endoscopic esophagitis and their favorite tastes. KEY WORDS:

RESULTS: In the association analyses between responses to specific tastes and GERD, the group liking salty food and the group with a high frequency of stomatitis had a significantly higher incidence of GERD (salty food: odds ratio [OR] 2.059, 95% confidence interval [CI] 1.215–3.488, P = 0.0073; stomatitis: OR 2.861, 95% CI 1.558–5.253, P = 0.0007, respectively). In association analyses with endoscopic esophagitis, the groups liking salty and sour food had a significantly higher incidence rate of endoscopic esophagitis (salty: OR 2.718, 95% CI 1.330–5.555, P = 0.0061; sour: OR 3.267, 95% CI 1.491–7.160, P = 0.0031, respectively). CONCLUSIONS: Sensitivity and response to specific food taste were associated with GERD. The results of a preference to hot or salty food and endoscopic esophagitis suggest that physical stimuli are important for esophageal injuries.

food preferences, gastroesophageal, reflux, self-administrated questionnaire, taste.

INTRODUCTION Correspondence to: Tomoyuki SHIBATA, Department of Gastroenterology, Fujita Health University School of Medicine, 1–98, Dengakugakubo, Kutsukake-cho, Toyoake 470-1192, Japan. Email: [email protected] Conflict of interest: None. © 2015 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd

Mammalian taste is classified into the categories of sweet, salty, sour, bitter and umami. Different taste receptors have recently been identified,1–4 showing that taste receptors exist in the gastrointestinal (GI) tract in addition to those in the tongue5,6. Through these receptors, the gut responds to specific taste stimuli such as hot tastes or umami.7,8

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Gastroesophageal reflux disease (GERD) is a complex disease that is related with the individual’s lifestyle, including the food that one eats. Taste is one of the elements that correspond to food preferences. Some factors such as alcohol consumption, obesity, a highprotein diet and excess consumption of fat have been found to be the triggers of GERD symptoms.9–12 These reports mentioned the relationship between transient lower esophageal sphincter relaxation (TLESR) and the exposure of gastric acid reflux, suggesting that specific food or flavors may be the triggers for deteriorated GERD symptoms or endoscopic esophagitis (EE) because of the frequencies of TLESR. Although there have been many studies on the association between lifestyle and GERD symptoms, the relationship between the responses to specific tastes and GERD symptoms has not been widely clarified.

Journal of Digestive Diseases 2015; 16; 337–341 criteria were: patients with malignant diseases, peptic ulcer, submucosal tumors, post-operation of the abdomen and severe systematic diseases. At the same time, another questionnaire on the symptoms for the diagnosis of GERD were administrated using the frequency scale for the symptoms of GERD (FSSG) designed by Kusano et al.13 with a cut-off score set at 10. This study was conducted in accordance with the ethical principles stated in the Declaration of Helsinki. The protocol was approved by the Fujita Health University. Written informed consent was obtained from all patients who agreed to participate in this investigation before their enrollment. Endoscopic evaluation

In this study, we aimed to determine the relationship between specific taste or food preferences and GERD using a new self- questionnaire, together with a wellestablished questionnaire for the diagnosis of GERD on the participants’ favorite taste and their GERD symptoms or endoscopic esophagogastric findings. PATIENTS AND METHODS Questionnaires A new self-administered questionnaire was developed for this study on the participants’ responses to various tastes, such as sour, spicy and salty, and their sensitivity to taste and hot stuffs was also inquired. Additionally, we asked about the frequencies of stomatitis (Table 1). The questionnaire was administered to 280 patients who visited our Endoscopy Unit in Fujita Health University Hospital (Toyoake, Japan) for GI endoscopic screening with esophagogastroduodenoscopy (EGD) or colonoscopy. The exclusion Table 1. taste

Self-administered questionnaire on individual

Question 1 Question 2 Question 3 Question 4 Question 5 Question 6 Question 7 Question 8 Question 9

Do you like salty tastes (for example, table salt, etc.)? Do you dislike salty tastes? Do you like sour tastes? Do you dislike sour tastes? Do you like spicy tastes (for example, pepper)? Do you dislike spicy tastes? Do you have stomatitis often? Do you have a keen sense of taste? Are you sensitive to hot food?

In all, 142 of 280 patients who underwent EGD were included in the analysis on the association of the endoscopic findings of the esophagogastric junction (EGJ) and the patients’ various tastes in food, their sensitivity to taste and piquant food, and the frequencies of stomatitis, which were collected on the basis of the self-administrated questionnaire. EE was classified according to the Los Angeles grading,14 and minimal change was considered as endoscopypositive esophagitis.15,16 Two expert endoscopists who were blinded to the results of the self-administered questionnaire determined the endoscopic diagnosis of EE. Statistical analyses Continuous variables were expressed as mean ± standard deviation or medians and ranges, whereas discrete variables were expressed as numbers and percentages or frequencies. Logistic regression analysis were performed and odds ratios (OR) and 95% confidence interval (CI) were calculated to determine the association between the patients’ tastes and their GERD symptoms or findings. All analyses were performed using JMP 10.0 (SAS Institute Inc., Cary, NC, USA). P < 0.05 was regarded as statistically significant. RESULTS The association between FSSG and the preferences to taste Altogether 280 patients, including 170 men and 110 women, with a mean age of 58.6 ± 14.4 years were

© 2015 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd

Journal of Digestive Diseases 2015; 16; 337–341 Table 2.

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The analyses based on frequency scale for the symptoms of gastroesophageal reflux disease (FSSG)

Like salty taste, n (Y/N) Dislike salty taste, n (Y/N) Like sour taste, n (Y/N) Dislike sour taste, n (Y/N) Like spicy taste, n (Y/N) Dislike spicy taste, n (Y/N) Stomatitis, n (Y/N) A keen sense of taste, n (Y/N) Sensitive to hot tastes, n (Y/N)

FSSG ≥ 10 (N = 94)

FSSG < 10 (N = 186)

OR

95% CI

P value

58/36 33/61 59/35 28/66 62/32 29/65 33/61 50/44 34/60

88/98 67/119 101/85 47/139 112/74 50/136 26/160 86/100 66/120

2.059 0.903 1.342 1.383 1.210 1.208 2.861 1.407 1.123

1.215–3.488 0.528–1.546 0.795–2.264 0.784–2.441 0.707–2.076 0.683–2.135 1.558–5.253 0.845–2.345 0.661–1.908

0.0073 NS NS NS NS NS 0.0007 NS NS

CI, confidence interval; N, no; NS, not significant; OR, odds ratio; Y, yes.

Table 3.

The analyses of endoscopic findings of gastroesophageal reflux disease (GERD)

Like salty taste, n (Y/N) Dislike salty taste, n (Y/N) Like sour taste, n (Y/N) Dislike sour taste, n (Y/N) Like spicy taste, n (Y/N) Dislike spicy taste, n (Y/N) Stomatitis A keen sense of taste, n (Y/N) Sensitive to hot tastes, n (Y/N)

GERD-positive (N = 67)

GERD-negative (N = 75)

OR

95% CI

P value

41/26 19/48 45/22 16/51 42/25 17/50 9/58 34/33 15/52

28/47 36/39 36/39 20/55 36/39 27/48 16/59 34/41 30/45

2.718 0.427 3.267 0.634 1.533 0.646 0.726 1.631 0.406

1.330–5.555 0.204–0.892 1.491–7.160 0.276–1.458 0.755–3.114 0.301–1.386 0.286–1.842 0.800–3.327 0.185–0.890

0.0061 0.0236 0.0031 NS NS NS NS NS 0.0243

CI, confidence interval; N, no; NS, not significant; OR, odds ratio; Y, yes.

included in the study. The details of the association between the FSSG and taste preferences are shown in Table 2. In association analyses with responses to specific tastes and GERD, the group liking salty food had significantly higher incidence of GERD (OR 2.059, 95% CI 1.215–3.488, P = 0.0073). In the same analyses, based on FSSG, the group with a high frequency of stomatitis had a significantly higher incidence of GERD compared with those without (OR 2.861, 95% CI 1.558–5.253, P = 0.0007).

The details of the association between endoscopic GERD findings and taste preferences are shown in Table 3. In association analyses with endoscopic GERD in the absence of esophagitis, the group liking salty and sour food had significantly higher incidence of GERD (salty: OR 2.718, 95% CI 1.330–5.555, P = 0.0061; sour: OR 3.267, 95% CI 1.491–7.160, P = 0.0031). In contrast, in the analysis based on FSSG no significant association was observed between stomatitis and GERD.

The association between endoscopic evaluation and taste preferences

The group disliking hot or salty taste had a significantly lower incidence of GERD (hot food: OR 0.406, 95% CI 0.185–0.890, P = 0.0243; salty food: OR 0.427, 95% CI 0.204–0.892, P = 0.0236).

In all, 142 patients including 84 men and 58 women with a mean age 59.1 ± 14.6 years underwent EGD only. Based on the endoscopic evaluations, 67 (47.2%) cases were diagnosed as GERD and the other 75 (52.8%) were negative for GERD. Among all endoscopically GERD positive cases, grade M was the most frequent group (n = 53, 79.1%), followed by grade A (n = 5, 7.5%), grade B (n = 3, 4.5%), Barrett epithelium (n = 3, 4.5%), grade D (n = 2, 3.0%) and grade C (n = 1, 1.5%).

DISCUSSION This is the first study to investigate the relationship between specific tastes and the incidence of GERD. We found that a specific taste sensation (liking salty things) was related to GERD symptoms as well as being stomatitis based on FSSG analyses. Moreover, the group liking salty food had a significantly higher

© 2015 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd

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Journal of Digestive Diseases 2015; 16; 337–341

incidence of endoscopic GERD than those disliking salty food. Additionally, liking sour tastes was significantly related to endoscopic GERD. Interestingly, disliking hot or salty tastes was protective against the development of endoscopic GERD.

observed; however, the difference was not significant (data not shown). These results might be due to the small sample size or the different mechanism of the development of stomatitis and esophagitis. Further studies are needed to discern this relationship.

There is a possibility that the sensitivity to salty tastes is associated with the onset of GERD. The association between food and GERD has been studied during the past decades.9–12,17,18 Nilsson et al.17 found for the first time that an increased use of extra table salt in regular meals was associated with an increased risk of reflux in a dose-dependent manner. The additional use of salt is related to a preference to salty food. Wu et al.18 also reported that a high intake of meat, oils, salt and calcium was associated with an increased risk of reflux esophagitis. The mechanism of salt intervention on the development of GERD remains unclear; however, it has been suggested that there is a relationship between TLESR and the intake of salty food.17,19 Furthermore delayed gastric emptying and increased pancreaticobiliary secretion after a high salt intake was also found.20

The group disliking hot and salty tastes in the analyses of endoscopic findings was negatively correlated with the onset of GERD, suggesting that this relationship was closely correlated with physical stimuli. If individuals who are sensitive towards hot food were hyposensitive esophageal mucosa would be injured easily. Drewes et al. reported that patients with esophagitis were hyposensitive to mechanical stimuli compared with the age-matched group.28 Detailed examinations are needed to confirm this result.

The relationship between GERD symptoms and endoscopic GERD findings were somewhat different. In our study, there might have been a sampling bias in the endoscopic evaluation. Since the GERD symptom and endoscopic findings,21,22 we performed endoscopic examinations in this study as well as a diagnosis of GERD based on the questionnaire. Our new selfadministered questionnaire suggested that GERD symptoms were related with stomatitis. We added stomatitis to this questionnaire in order to evaluate the participants’ oral environment. Moreover, there have been reports on the association between GERD and recurrent aphthous stomatitis,23 together with that between stomatitis and salivary secretion24–26. Another report suggested that the salivary flow was impaired in GERD patients.27 Based on these findings, we hypothesized that there would be associations among GERD, salivary flow and stomatitis, and therefore, we asked about the frequency of stomatitis as one of the parameters of oral conditions. And our results supported this hypothesis. Initially, we asked about the tendency to tooth decay besides stomatitis in this questionnaire. However, no sufficient answers were obtained and therefore, this item was excluded from the questionnaire. We found that stomatitis was not associated with endoscopic GERD. In the endoscopically minimal change group, a weak tendency to stomatitis were

From these results, the evidence is not sufficient to lead to the recommendations on the modification of lifestyles, but advice on the need for abandoning bad habits may be effective for the amelioration of GERD symptoms at a constant rate.29 In conclusion, food preferences and responses to specific tastes were associated with GERD symptoms, this suggesting that these factors are associated with the development of GERD symptoms. The results of food preferences to hot or salty stimuli and endoscopic GERD suggest that physical stimuli are important for esophageal injuries in addition to gastric acid. Investigations of oral condition may also contribute to the clarification of the complex pathophysiology of GI response including nonerosive reflux disease. ACKNOWLEDGMENT We thank all medical staffs of the Endoscopy Unit at Fujita Health University Hospital for taking the questionnaire. REFERENCES 1 Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS. A novel family of mammalian taste receptors. Cell 2000; 100: 693–702. 2 Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS. The receptors and cells for mammalian taste. Nature 2006; 444: 288–94. 3 Nelson G, Chandrashekar J, Hoon MA et al. An amino-acid taste receptor. Nature 2002; 416: 199–202. 4 Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A 2002; 99: 4692–6. 5 San Gabriel AM, Maekawa T, Uneyama H, Yoshie S, Torii K. mGluR1 in the fundic glands of rat stomach. FEBS Lett 2007; 581: 1119–23.

© 2015 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd

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© 2015 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd

Association between individual response to food taste and gastroesophageal symptoms.

Taste is an important element in food preferences. Gastroesophageal reflux disease (GERD) is related to lifestyles including eating habits. We aimed t...
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