Introduction

Gastroesophageal reflux disease (GERD (is a health problem with a high prevalence and remarkable consequences such as esophageal stricture, gastrointestinal bleeding, or Barrett’s esophagus for those affected.¹ It is a pathologic condition of the esophagus caused by regurgitation of gastric- or gastroduodenal contents into the lumen of the esophagus.² Epidemiologic studies showed that the prevalence of GERD is between 10% to 48% in western countries and up to 5% in Asia³; however, an increasing trend is reported.⁴In Iran, according to a population-based study,⁵ it is estimated to be up to 33% among adults. The typical symptoms of reflux are heartburn (a retrosternal burning sensation) and acid regurgitation (a sour taste in the mouth).⁶

The symptoms ofGERD can trigger esophagitis to such an extent as to lessen the patient’s quality of life.⁷ Furthermore, GERD is a strong risk factor for Barrett’s esophagus⁸ and esophageal adenocarcinoma (EA).⁹ A systematic review on GERD indicated both absence from work and reduced productivity while at work.¹⁰ As the incidence of EA has increased in the world over the last 30 years,¹¹it is very important to identify factors which may affect the conditions leading to the development of GERD.

Despite the importance of GERD and remarkable knowledge of its pathogenesis,¹²risk factors remain poorly understood. However, there is considerable evidence that GERD occurs more commonly after meals.^13,14In this regard, majority of studies have been carried out from physiological,^15,16 but not dietary perspective. They have investigated the effect of fat on postprandial esophageal acid exposure,^17,18 or on lower esophageal sphincter (LES) motility.^19,20 In addition, they were mostly in patients with severe GERD and even hospitalized patients with esophagitis and EA.^21,22

Most of the physiological studies failed to establish the role of diet (most notably fat) on GERD or altering the competence of LES junction.^23,24 Even some suggested that recommending a low-fat diet to GERD patients is, however, an inappropriate approach.^20,24 In contrary, some of the prior investigators demonstrated the association of fat with GERD.^21,25 Therefore, relevant studies have often provided conflicting results.^26,27

Generally, studies investigating the effect of total dietary intake on GERD are scarce.^28,29 Amongst is a cross-sectional study by El-Serag et al²⁸ in 371 employees at Veteran Administration in which a significant association was reported between high fat intake and GERD symptoms; however, having adjusted the effect of body mass index (BMI), the association became non-significant; since there is a significant association between obesity and GERD symptoms.³⁰ A more recent study suggested that further work investigating the association between dietary fat intake and food sources of fat are needed for confirmation of these results.³¹

Present physiological studies on meal volume and caloric density in GERD are inconclusive. Iwakiri et al³²reported a decrease in postprandial GERD by reducing the volume of a liquid meal in healthy volunteers. Pehl et al³³showed that the amount of gastroesophageal reflux induced by ingestion of a meal seems to depend on the volume but not on the caloric density of a meal. In contrast, the study by Colombo et al²⁴indicated that advice on dietary habits in GERD patients should be concentrated on decreasing the caloric load of meals rather than their fat content. However, Esmaillzadeh et al³⁴ reported certain associations between dietary patterns and GERD, which may partly be modulated by body weight.

Health promotion of the population particularly those with GERD is important and to the best of our knowledge, the role of individual meals of diet on GERD has not been studied yet. Therefore, in the present study the association of total diet as well as individual meals was investigated to bridge the gap in this area.

Materials and Methods

Results

Out of 250 participants who filled out the GERD checklist, 217 returned their dietary records with complete and interpretable answers, among whom 106 (48.8%) had experienced GERD symptoms (case group) with a mean age (±SD) of 35.3 ± 12.6 years and 111 (51.2%) were controls with a mean age of 35.1 ± 13.2 years. Only education level differed significantly between cases and controls (P < 0.001; Table 1).

Among 106 cases, 69 (65.1%) had at least weekly symptoms while 37 (34.9%) complained of monthly symptoms. Total diet and individual meals of the participants are summarized in Table 2. Cases and controls showed statistically non-significant differences. Even though cases reported further total energy intake when compared to controls (median, 1922.5 kcal vs. 1882 kcal), however, their difference did not reach a significant level. Both groups consumed similar amounts of carbohydrates (median, 265.7 g vs. 272.1 g), protein (median, 60.6 g vs. 63.7 g), and fat (median, 62.4 g vs. 61.4 g). Similarly, the intake of other nutrients was more or less the same. Meanwhile, total caloric density, total meal volume and frequency did not differ significantly between the two groups (Table 3). In contrast, statistically significant differences were observed between participants with and without GERD at lunch and evening snack for the following dietary items; at lunch: amount of fat (P = 0.04) and meal volume (P = 0.02), and at evening snack: energy intake (P = 0.01), amount of protein (P = 0.01), fat (P = 0.01), and sugar (P = 0.03), and percentage of energy from carbohydrates (P = 0.02). Amount of carbohydrates and caloric density at evening snack were marginally significant (P = 0.05).

Results of multivariate logistic regression revealed significant associations between GERD and percentage of energy from protein (OR = 0.89; 95% CI: 0.81-0.98) in total diet; amount of fat (OR = 1.02; 95% CI:1.00-1.05) at lunch; amount of sugar (OR = 0.95; 95% CI:0.91-0.99) and energy intake (OR = 0.99; 95% CI:0.99-1.00) at evening snack with GERD after adjusting for BMI and education level (Table 4).

Discussion

Because GERD is an important health problem and modification of dietary behavior appears to play a role in its prevention, we studied the association of total diet as well as individual meals (including large meals and snacks) with GERD. The results showed that among total dietary factors, only percentage of energy from total protein was significantly associated with GERD.

To the best of our knowledge, this is a preliminary study that examined the association of total diet as well as individual meals (including large meals and snacks) with GERD. Our study demonstrated that total dietary intakes of cases and controls did not differ significantly. In addition, total dietary factors had no significant association with GERD, except for percentage of energy from total protein. It could be in part explained by the fact that protein increases the LES pressure and stimulates gastrin secretion which promotes stomach emptying.^41,42 Prior investigators have postulated a pathophysiologic relationship between delayed gastric emptying,⁴³ decreased LES pressure²⁵ and GERD.

El-Serag et al²⁸ reported significantly higher daily intakes of total fat, saturated fatty acids, percentage of energy from fat, and average fat servings in GERD patients comparing with healthy subjects. Moreover, there was a dose-response relationship between GERD and fatty acids and cholesterol. Though after adjusting for BMI, the association between fat and GERD was non-significant, however, in their study food intake was only evaluated by a food frequency questionnaire which is prone to recall bias, whereas in our study a 3-day food record was obtained, the gold standard tool of dietary assessment.⁴⁴

In another study,³³performed on 60 patients with reflux, perceived reflux event was significantly associated with higher intakes of cholesterol, saturated fatty acids, and calories from fat.This study demonstrated that BMI did not correlate with having a sensed reflux event. However, their study suffered not only from a small number of patients, but also it lacked control group. In contrary, our study had adequate power to detect the differences between the two groups and had control group as well. In a study by Nandurkar et al,²⁹no significant association was found between diet and reflux symptoms in 211 community subjects.

In our study, there was a great variability in reported amount of foods consumed particularly at meals in both groups (Table 2). In addition, it is unknown whether GERD patients had altered their diet at the time of the study, since GERD patients are often advised to adjust their dietary habit, e.g. by minimizing the intake of high-fat meals or excluding offending foods to avoid symptoms. Nonetheless, some of the patients with non-severe GERD were reluctant to change their diet despite persisting symptoms; perhaps, because of the pleasure of eating those foods. Besides, it is not clear whether patients were exposed to symptoms at the time of food record, or it influenced the type and amount of the food consumed. The above mentioned factors may interfere with significant associations between total diet and GERD.

Although it was revealed that there is almost no significant association between total dietary intake and GERD, several food items consumed at certain meals were found to be associated. For example, as expected, a significant association was found at lunch for amount of fat and marginally for meal volume. Lunch comprised the largest and main meal among most individuals. In addition, an enhanced volume might increase GERD via an enhanced gastric distension; thereby, triggering transient LES relaxations (TLESRs), considered the predominant mechanisms of reflux events in healthy subjects and reflux patients.³³ On the other hand, extracellular fats are widely used at lunch. Therefore, fat consumption at lunch might contribute to postprandial GERD symptoms.

Unlike lunch, it appears that evening snack is more likely to show a protective effect of energy, protein, fat, and sugar on GERD, regardless of the type and the food consumed. More interestingly, fat consumed at lunch provokes GERD symptoms; whilst at evening snack alleviates the symptoms. However, the mechanism (s) for such an effect is unclear; but as fat is consumed in different forms (e.g. intracellular vs. extracellular fat) and in varying proportions with other macronutrients, hence, the physiologic response to fat ingestion may potentially vary from one meal/snack to another.⁴⁵ In our study, fat was used in extracellular form at lunch, while it was ingested in intracellular form at evening snack, i.e. in the form of sweets, cakes, biscuits and junk foods. Therefore, the form of the consumed fat (e.g. intracellular vs. extracellular fat) might explain the present finding.

Given that sweets have been regarded as causing reflux because of their high osmolality and high fat content, it is expected to have more links with GERD at evening snack. However, it seems to be unlikely at least in our study; since this snack had minor volume of fat, sugar, carbohydrates, and so on, especially in GERD patients (Table 4); that is why the effect is more likely to be reversed. Although snacking may promote energy imbalance resulting in obesity among different age groups,⁴⁶ our results suggest evening snacking might protect GERD patients against the disease.

Conclusion

In conclusion, to promote health among population, particularly patients with GERD, dietary modification through following dietary guidelines and meal management and having appropriate food choices in each meal play an important role in the management of GERD. Our results indicate the protective effect of the percentage of energy from protein in total diet. It also shows that lunch and evening snack are associated with GERD symptoms. Seemingly, amount of fat at lunch positively affects GERD, whereas amount of macronutrients at evening snack reduces the symptoms, provided that the meal volume be low. Therefore, recommending a low-fat meal, particularly at lunch, to GERD patients sound reasonable. This is clinically important and may be suggested in the guideline for management of GERD. The increasing prevalence of patients with GERD along with inappropriate dietary habits merits evaluation of a proper dietary intervention for GERD and its symptoms. Large-scale studies are required to evaluate the impact of total diet as well as individual meals on symptoms.

The recommendation for practical implications and policy making

Regarding the important effect of diet in the management of GERD, it seems sound to accentuate more on dietary items in the current guidelines of GERD.

Ethical approval

The Ethics Committee of Tabriz University of Medical Sciences approved the protocol for the study (Reference Number: 5/4/11127).

Competing interests

The authors report no competing interests.

Authors’ contribution

EM M contributed in the study design, data interpretation, and appraised the manuscript. S S helped with data analysis and commented on the draft of the manuscript. AH SR contributed in the study design and appraised the manuscript. K M helped with the study design, acquisition of data, and reviewing the draft of the manuscript. SA M participated in the study design, acquisition of data, questionnaire development, data analysis and interpretation, drafting and editing the manuscript. All authors approved the final version for submission.

Funding

The present study was funded by Research Vice-Chancellor, Tabriz University of Medical Sciences, Tabriz, Iran.

Acknowledgements

We acknowledge all the participants as well as the staff of the specialized clinic of Tabriz University of Medical Sciences for their kind cooperation.

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