Introduction

Heart Burn Syndrome (HBS) is a highly prevalent condition affecting a wide range of people in the world [1]. HBS has become very common in the past three decades [2]. In the US, almost half of adult people experience reflux symptoms monthly [3]. In western nations, 10–20% of adult populations are affected [4]. Although the prevalence in Asian countries is comparatively low, recent estimates indicated the increasing trend of this condition [5]. In Iran, 1.9–52% of adult population has been reported to have the condition based on different definitions [6]. HBS is associated with several complications including esophagitis, esophageal ulcer, upper GI bleeding and Barrett esophagus [7]. Furthermore, it affects quality of life and imposes a great burden on the health care system [8].

The exact etiology of HBS is still unknown. Besides genetic predisposition, it seems that lifestyle factors greatly contribute to this condition [9]. Among several lifestyle-related factors, poor sleep quality, smoking, alcohol drinking, short meal-to-sleep interval and irregular dietary habits have been reported as strong determinants [10]. Although some studies have been conducted to identify the diet-related factors in HBS [11, 12], limited information is available about the relationship between breakfast consumption and HBS. In a cross-sectional study in Japan, it has been found that irregular dietary habits and breakfast skipping could strongly contribute to HBS symptoms; such that the effects of breakfast skipping were even stronger than smoking and alcohol consumption [13]. However, participants in that study were among wealthy peoples with specific dietary habits. Therefore, this finding might not completely reflect the population-based data from Asian people. In the current study, we hypothesized that breakfast skipping might contribute to HBS because skipping meals might exacerbate gastric acidity, a phenomenon that is observed in patients with HBS [14, 15]. Furthermore, prior studies have indicated a significant association between breakfast skipping and obesity [16, 17]. The link between obesity and the prevalence of HBS has also been shown [9]. Therefore, breakfast skipping might contribute to HBS through its effects on obesity. Given the limited evidence of the relationship between breakfast consumption and HBS as well as the increasing trend of HBS in the Asian countries, including Iran, we examined the association between breakfast skipping and prevalent HBS among a large group of Iranian adults.

Methods

Study population

This cross-sectional study was performed among general adult population of Isfahan. The study was conducted in the framework of SEPAHAN (the study on the epidemiology of psychological, alimentary health and nutrition) project that has been designed to investigate the epidemiological aspects of functional gastrointestinal disorders (FGIDs) and their relationship with different lifestyle and psychological factors [18]. Briefly, this study was conducted among nonacademic staff working in 50 different health centers affiliated to the Isfahan University of Medical Sciences (IUMS) in Isfahan province, Iran. These participants worked in hospitals, university campuses, and health centers. The required sample size was determined based on the proposed formula for cross-sectional studies [19]. We hypothesized the prevalence of FGDIs as 15%. So, considering the type I error of 5% and the study power of 80%, and desired confidence interval of 0.03, we reached the minimum required sample size of 1387 subjects. In the SEPAHAN project, data collection was done in two main phases. In the first and second phases of the project, 10,087 and 9652 questionnaires were sent to subjects aged 18–55 years, respectively. The questionnaire in the first phase included questions on demographic information, lifestyle and nutritional factors. Totally, 8691 subjects returned the completed questionnaire (response rate: 86.16%). The questionnaire is the second phase included questions on gastrointestinal disorders; which 6239 subjects completed and returned questionnaires (response rate: 64.64%). The national identification number of participants was used to merge the questionnaires from two phases. We were unable to use 1476 questionnaires in the final analysis, due to incomplete questionnaires or lack of having national identification number in phase 1 or 2 as well as having missing information on exposure or outcome of interest. Finally, data on 4763 subjects, who had complete data on related variables, were analyzed (Fig. 1). Ethical approval of the study was provided by the Medical Research Ethics Committee of Isfahan University of Medical Sciences (IUMS). All participants provided informed written consent.

Fig. 1
figure 1

Flow diagram of the study population

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Assessment of breakfast skipping

We asked a question from participants to assess patterns of breakfast eating: 1) “How frequently do you eat breakfast during a week?” Participants were able to respond as: "never or 1 day/wk", "2–4 days/wk", "5–6 days/wk", "every day".

Assessment of HBS

A Persian version of validated self-administered modified ROME III questionnaire was applied to assess the functional gastrointestinal disorders [18]. As the rating scales used in ROME III (never, less than 1 day a month, 1 day a month, 2–3 days a month, 1 day a week, more than 1 day a week, every day) were hard to be discriminated by most participants during the face validation of the questionnaire, we modified the rating scale of the original questionnaire into a four-item rating scale (never or rarely, sometimes, often, always). In the current study, HBS was defined as the presence of reflux attack sometimes, often or always. The validity and reliability of Persian version of ROME III questionnaire in Iranian population has earlier been shown [18].

Assessment of other variables

Information on age, sex, marital status, smoking, existence of diabetes, supplement use, and Oral Contraceptive Pill (OCP) use were obtained by demographic and medical history questionnaires. The General Practice Physical Activity Questionnaire (GPPAQ) was used to assess participants’ physical activity [20]. As previous investigations have shown that even 1 h of walking per week may reduce the risk of chronic diseases [21], we classified participants as: physically active (≥ 1 h/week) and inactive (< 1 h/week). In addition, anthropometric measures including weight, height, and waist circumference (WC) were assessed using a validated self-administered questionnaire [22]. Then, body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. Furthermore, information on dietary habits including number of meals per day, chewing behaviors, eating speed, meals to sleep intervals, and consumption of spicy foods were also examined.

Statistical analysis

Participants were classified into four categories based on their frequencies of breakfast consumption "never or 1 day/wk", "2–4 days/wk", "5–6 days/wk", "every day". One-way ANOVA and Chi-square test were used to compare general characteristics of study subjects across different categories of breakfast consumption for continuous and categorical variables, respectively. Multivariable logistic regression in different models was used to find the relation between breakfast consumption and odds of HBS presence. First, we adjusted for age (years) and sex (male/female). Findings were additionally adjusted for smoking (yes/no), presence of chronic conditions (yes/no), and physical activity (less/more than 1 h per week) in Model 2. Further control for number of meals per day (one/two/three), chewing quality (not very well/well/more than adequate), quick eating (yes/no), meal to sleep interval (less than 2 h as short/more than 2 h as adequate), and spicy foods consumption (˂3/4–6/ ≥ 7 times/week) was done in the third model. Finally, additional adjustment was done for BMI (kg/m2). The first category of breakfast consumption (never or 1 day/wk) was considered as reference in the analyses. We considered the categories as ordinal variable to calculate the trend of odds ratios across increasing categories of breakfast consumption. To determine the association of breakfast consumption with severity of heartburn syndrome, we applied multivariable ordinal logistic regression. P values less than 0.05 were considered as statistically significant. All analyses were performed using Statistical Package for Social Sciences (SPSS Corp, version 18, Chicago, IL, USA).

Results

General Characteristics of study participants across various categories of frequency of breakfast consumption is shown in Table 1. Compared with those who had breakfast ≤ 1 time/wk, individuals who consumed breakfast daily were older, more likely to be females and physically active. No significant differences were found in terms of mean weight, BMI as well as distribution of smokers, supplement users and obesity across various categories of breakfast intake.

Table 1 General characteristic of study participants across categories of breakfast consumption1
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Distribution of participants in terms of diet-related behaviors across different categories of breakfast intake is provided in Table 2. Compared to those who had breakfast ≤ 1 time/wk, lower percentage of people who had breakfast daily, consumed one meal a day and a greater percentage of them had three meals per day. Greater percentage of subjects who had breakfast daily reported well chewing of foods compared with those who had breakfast ≤ 1 time/wk. Quick eating was highly prevalent among those with frequent breakfast intake. Breakfast consumers were less likely to have a short meal-to-sleep interval than breakfast skippers.

Table 2 Distribution of participants in terms of diet-related practices across categories of breakfast intake
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Multivariable-adjusted odds ratios for having HBS across various categories of breakfast intake are indicated in Table 3. Daily intake of breakfast was associated with a reduced risk of HBS; such that those who consumed breakfast everyday had 43% lower risk (OR 0.57; 95% CI 0.45–0.72) for having HBS as compared with those who had breakfast ≤ 1 times/wk. Adjustment for potential confounders including age, gender, smoking and physical activity did not significantly attenuate the association. Even after adjusting for all confounders, including diet-related behaviors and BMI, there was still a significant inverse association between breakfast intake and risk of HBS (OR 0.57; 95% CI 0.41–0.80). The prevalence of heart burn syndrome across categories of breakfast intake is shown in Fig. 2.

Table 3 Multivariable—adjusted odds ratios for heart burn syndrome across categories of breakfast intake1
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Fig. 2
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The prevalence of heart burn syndrome across categories of breakfast intake; heart burn

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Multivariable-adjusted odds ratios for frequency of HBS across various categories of breakfast intake are shown in Table 4. When the analysis was done for the whole population, we found a significant inverse relationship between breakfast consumption and frequent HBS (OR 0.55; 95% CI 0.44–0.70). After controlling for potential confounders, including BMI, those who had breakfast everyday were 45% less likely to have frequent HBS than those who had breakfast ≤ 1 times/wk (OR 0.57; 95% CI 0.40–0.77). When the analysis was confined to those with HBS, the association disappeared (OR 0.56; 95% CI 0.28–1.13).

Table 4 Multivariable-adjusted odds ratios for frequency of heart burn syndrome across categories of breakfast intake
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Multivariable-adjusted odds ratios for severity of HBS across different categories of breakfast intake among individuals with HBS are provided in Table 5. We observed an inverse association between regular breakfast consumption and severity of HBS in crude model (OR 0.57; 95% CI 0.37–0.87). However, when potential confounders were taken into account, this relationship became non-significant (OR 0.57; 95% CI 0.31–1.05). When the model was adjusted for BMI, we observed a trend toward inverse association between breakfast intake and severity of HBS (OR 0.56; 95% CI 0.31–1.04).

Table 5 Multivariable-adjusted odds ratios for severity of heart burn syndrome categories of breakfast intake among those with HBS*
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Discussion

In this cross-sectional study, an inverse association was found between frequency of breakfast consumption and odds of HBS as well as HBS severity among adults. This association remained significant even after controlling for a wide range of potential confounders. To the best of our knowledge, limited information is available about the relationship between breakfast consumption and HBS. Heartburn is the classic and most common symptom of GERD. However, the diagnosis of GERD usually was done by upper gastrointestinal endoscopic examination or using the GERD Symptom Assessment Scale (GSAS). In our study, we used a modified ROME III questionnaire that contain some questions about the presence of heartburn symptoms. So, we did not perform endoscopic examination. This is why we did not use GERD as the outcome instead of heartburn syndrome.

Totally gastrointestinal problems are highly prevalent among adult population which can affect quality of life [8]. Lifestyle-related factors, including dietary habits and dietary intakes might influence their occurrence and severity [23,24,25]. We found that breakfast intake was inversely associated with HBS in the Iranian adult population. In line with ours, a cross-sectional study in Japan reported a strong inverse association between breakfast consumption and HBS symptoms [13]. The direct association of breakfast skipping with HBS symptoms was also reported in another study on 1840 junior high school students in Japan [26]. However, in a cohort study on 817 Japanese patients with type 2 diabetes, the authors did not find a significant relationship between breakfast skipping and HBS. However, participants of the latter study were patients with type 2 diabetes mellitus who had been treated for diabetes for several years [27]. Therefore, many of them might have changed their eating behaviors to control hyperglycemia. Overall, it seems that breakfast consumption, along with other dietary habits, can be recommended as a preventive measure to HBS.

Breakfast is among the most important meals which provide micro- and macro-nutrients [28]. It has been shown that breakfast skippers were more likely to have a poor diet quality compared with breakfast consumers [29, 30]. The exact mechanism through which breakfast consumption might affect HBS has not been understood. However, breakfast skipping might exacerbate gastric acidity which has been considered as an important risk factor of HBS development [31, 32]. Furthermore, breakfast skipping was associated with overweight and obesity [33, 34], which is in turn associated with an elevated risk of HBS [33,34,35]. Poor dietary quality and physical inactivity which are commonly observed among breakfast skippers might explain the high prevalence of obesity in these individuals [29, 36]. Furthermore, breakfast consumption has been found to alter inflammation, mainly due to change in levels of gastrointestinal peptides [37, 38]. Changing in gastrointestinal inflammatory environment has been also linked to HBS development [39]. In addition, we found that participants with frequent breakfast intake were more likely to have some healthy diet-related behaviors including good chewing of foods and adequate meal-to-sleep interval than breakfast skippers. Imperfect chewing of foods and short meal-to-sleep interval were also found to increase HBS severity [40].

Several strengths of the study should be highlighted. This is the first study from the Middle Eastern countries with a large sample size investigating the association of breakfast consumption with HBS among adults. A wide range of potential confounders were controlled for to reach an independent association between breakfast consumption and HBS. In addition, diet-related behaviors were taken into account in the current study. Given these strengths, some limitations should also be considered. Due to the cross-sectional design of the study, it is impossible to confer causality. Further studies, in particular of prospective design, are needed to discover causality and to confirm our findings. Symptoms of HBS were examined based on a self-administrated questionnaire in this study. Although validated questionnaires were used, misclassification of study participants cannot be excluded. In addition, the study was conducted on a population from Isfahan province, therefore, generalizing the findings to Iranian adults should be done cautiously.

Conclusions

In conclusion, findings from this cross-sectional study showed an inverse association between frequency of breakfast consumption and odds of HBS and frequency of HBS among adult populations. Further prospective studies, in particular from Middle-Eastern countries, are required to confirm these findings.

What is already known on this subject?

Several lifestyle-related factors are contributed to the etiology of HBS. Among them, irregular dietary habits have been reported as strong determinants. Some studies shown that breakfast skipping increased the odds of gastrointestinal diseases while others reported no significant association. In addition, most publications in this regard were from western countries and few information are accessible from the Middle-East.

What does this study add?

We estimated that 32.4% of the participants consumed breakfast less than one time per week. We also found subjects who consumed breakfast everyday had 43% lower risk for having HBS as compared with those who had breakfast less than one time per week.