Empty stomach sensation and Bothersome hunger sensation: Two Relevant Clinical Manifestations in Patients with Dyspepsia

doi:10.21203/rs.3.rs-4698597/v1

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Research Article

Empty stomach sensation and Bothersome hunger sensation: Two Relevant Clinical Manifestations in Patients with Dyspepsia

https://doi.org/10.21203/rs.3.rs-4698597/v1

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Background

Dyspepsia, characterized by symptoms in the gastroduodenal region, poses diagnostic challenges despite Rome IV criteria.

Aim

This study aimed to investigate the prevalence of two underreported symptoms, Empty Stomach Sensation and Bothersome Hunger Sensation, in dyspeptic patients, and their association with the disorder of gut-brain interaction.

Methods

A cross-sectional study surveyed 1,211 individuals in northwest Mexico, assessing dyspeptic symptoms with pictograms and a 7-point Likert scale. Logistic regression analyzed associations between dyspepsia, Empty Stomach Sensation, and Bothersome Hunger Sensation.

Results

Dyspepsia prevalence was 39.1%, being overlap syndrome the most common (42.7%) phenotypic presentation. Empty Stomach Sensation prevalence in dyspeptic patients was 43.8% versus 12.6% in non-dyspeptics (p < 0.001). Bothersome Hunger Sensation prevalence in dyspeptics was 25.4% compared to 5.6% in non-dyspeptics (p < 0.001). Both symptoms were associated with epigastric pain syndrome, postprandial distress syndrome, overlap syndrome, anxiety disorders and other gastroduodenal symptoms.

Conclusions

Empty Stomach Sensation and Bothersome Hunger Sensation, though prevalent in dyspeptic patients, are often overlooked. Strengths of this study include its large sample size and comprehensive assessment of symptoms. Limitations include the lack of diagnostic endoscopy and long-term follow-up. Future research should explore the underlying mechanisms of these symptoms and their implications for clinical management.

Disorders of gut-brain interaction

Functional dyspepsia

Postprandial distress syndrome

Hunger

Satiety

Anxiety

Dyspepsia is a syndrome encompassing symptoms originating in the gastroduodenal region, and according to Rome IV criteria, it is diagnosed based solely on the following symptoms: epigastric pain, epigastric burning, early satiety, and postprandial fullness. Based on these symptoms, it is subclassified into three subtypes: epigastric pain syndrome (primarily characterized by epigastric pain/burning), postprandial distress syndrome (manifested by early satiety and/or postprandial fullness) and overlap syndrome (epigastric pain syndrome and postprandial distress syndrome symptomatology)[1], [2]. Although there are well-established diagnostic criteria for functional dyspepsia (FD), the term remains confusing for both medical personnel and patients, complicating symptom expression (due to cultural and language differences) among the affected population. Additionally, despite being a syndrome with established criteria, there are other symptoms related to the gastroduodenal region that could be considered part of the clinical spectrum of dyspepsia, including those related to appetite such as empty stomach sensation and bothersome hunger sensation [3], [4], [5], [6], [7], [8].

Although Tack et al.'s study describes pictograms associated with dyspepsia well, there are other symptoms not represented, such as the sensation of epigastric void and painful hunger.

One established strategy for better understanding symptoms by both physicians and patients is the use of visual tools such as pictograms. These pictograms objectively exemplify symptoms that are difficult for patients to understand or describe, such as dyspeptic symptoms. In a study by Tack et al., assessing the clinical concordance of medical assessment with self-assessment by FD patients, it was reported that the use of questionnaires without pictograms had a concordance of 36%, which increased to 48% (p = < 0.001) with the addition of a pictogram to the assessment[9]. Although this study describes pictograms associated with dyspepsia well, there are other symptoms not represented, such as the empty stomach sensation and bothersome hunger sensation.

Therefore, the objective of this study was to determine the presence of two symptoms (using pictograms) commonly reported by Mexican patients, namely the empty stomach sensation and the bothersome hunger sensation, in patients with typical FD symptoms, as well as their association with this disorder of gut-brain interaction (DGBI).

Evaluated Population

A cross-sectional study was conducted with consecutive sampling in an open population (individuals in areas such as malls, parks, and entertainment centers) in northwest Mexico from October 2017 to January 2018. The subjects evaluated participated voluntarily, and with prior verbal and paper based informed consent expressed by the evaluator, they agreed to be evaluated.

All subjects completed a questionnaire (previously validated) including the collection of sociodemographic data, comorbidities, medications in use, eating pattern, gastroduodenal symptomatology, as well as Rome IV criteria for dyspepsia diagnosis and the Hospital Anxiety and Depression Scale (HADS)[9], [10], [11], [12]. The evaluation was conducted by general practitioners previously trained by a certified gastroenterologist (Flores A.R).

Dyspeptic symptoms were assessed with pictogram support, and severity was evaluated using a 7-point Likert scale.[9]

The evaluated symptoms were: postprandial fullness, early satiety, epigastric pain, epigastric burning, bloating, nausea, vomiting, regurgitation, empty stomach sensation and bothersome hunger sensation[9]. Online Resource 1.

Empty stomach sensation was defined as the sensation of having an empty, void, or absence of intrabdominal content in the epigastric location, exemplified with a pictogram, clarifying that this sensation was not equivalent to hunger or appetite and that it was uncomfortable and impacted the patient's quality of life. Appendices 1. Bothersome hunger sensation was defined as the presence of appetite or hunger sensation causing pain or more intense epigastric discomfort than usual, considered bothersome and impacting the patient's quality of life. Online Resource 2.

FD diagnosis was considered for those who met Rome IV criteria, with the limitation that organic etiology was not ruled out, and diagnostic endoscopy was not performed. Regarding anxiety and depression, a diagnosis was considered with an HADS score ≥ 11 in the respective items for each psychiatric disorder.

With the collected information, the studied population was divided into two groups: a group of patients meeting Rome IV criteria for FD and subjects who did not meet these criteria.

Statistical Analysis

A consecutive non-probabilistic sampling technique was used. Continuous variables were expressed as means with standard deviation, and categorical variables as proportions. Group comparison was performed using multivariate logistic regression analysis with chi-square test for qualitative variables, expressing the results in odds ratios with 95% confidence intervals and considering a value of p < 0.05 statistically significant. Quantitative variables were subjected to a distribution analysis with Shapiro-Wilk test and Levene test for variance equality. Variables were analyzed according to their distribution, homoscedasticity or heteroscedasticity, using Student's t-test with or without Welch transformation, expressing the results in means with standard deviation or Mann-Whitney U test, expressing the results in medians and interquartile range. In both tests, a statistically significant result was considered when a p-value of < 0.05 was obtained. Statistical analysis was performed using IBM® SPSS Statistics 28.0.1 software.

Ethical Considerations

The development of this protocol adheres to the guidelines established in the Universal Declaration on Bioethics and Human Rights on October 19, 2005, at the UNESCO General Conference, and there are no known or unforeseen risks for the subjects participating in the research protocol, carefully safeguarding both the confidentiality of the participating subjects and the obtained information.

Demographic Characteristics and Associated Factors

A total of 1,211 subjects were evaluated, with a mean age of 36 years (standard deviation ± 14); 56% (n = 678) were female, and 44% (n = 533) were male. The diagnosis of FD was established in 39.1% (n = 473, 95% CI: 0.36–0.41) of cases. The overlap syndrome was present in 42.70% (n = 202, 95% CI: 0.38–0.47), followed by postprandial distress syndrome and epigastric pain syndrome with 33.4% (n = 158, 95% CI: 0.29–0.37) and 23.9% (n = 113, 95% CI: 0.21–0.26), respectively.

Table 1 shows the sociodemographic characteristics among patients with FD and subjects without FD. There were no differences in age (FD: 33 years [IQR: 24–47] vs. Without FD: 31 years [IQR: 23–50], p = 0.439) and sex when comparing both groups (female, 56% vs. Without FD: Female, 51.9%. p = 0.160). Regarding comorbidities, patients with FD presented non-gastrointestinal chronic pain more frequently (FD: Chronic pain, 10.6% vs. Without FD: Chronic pain, 7.0%. p = 0.017), as well as substance use such as smoking (FD: Smoking, 20.9% vs. Without FD: Smoking, 15.6%. p = 0.017), and alcohol consumption (FD: Alcohol consumption, 57.9% vs. Without FD: Alcohol consumption, 47.4%. p = < 0.001).

Table 1

Baseline characteristics: Functional Dyspepsia vs. Non-Functional dyspepsia.
Variable	Functional Dyspepsia = 473	Non-Functional Dyspepsia = 738	p
Age, median (IQR) 18–34 years, n (%) 35–49 years, n (%) 50–64 years, n (%) ≥65 years, n (%)	33 (24–47) 254 (53.7) 77 (16.3) 125 (26.4) 17 (3.6)	31 (23–50) 414 (56.1) 97 (13.1) 180 (24.4) 47 (6.4)	0.439 0.413 0.129 0.426 0.035
Sex Female, n (%) Male, n (%)	265 (56) 208 (44)	383 (51.9) 355 (48.1)	0.160 0.160
Comorbidities Diabetes, n (%) Hypertension, n (%) Non-gastrointestinal Chronic pain, n (%)	46 (9.7) 81 (17.1) 50 (10.6)	53 (7.2) 99 (13.4) 52 (7)	0.115 0.077 0.031
Substance use Alcohol, n (%) Tobacco, n (%)	274 (57.9) 99 (20.9)	350 (47.4) 115 (15.6)	< 0.001 0.017
Dyspeptic symptoms Epigastric pain, n (%) Epigastric burning, n (%) Postprandial fullness, n (%) Early satiety, n (%)	248 (52.4) 257 (54.3) 232 (49) 199 (42.1)	45 (6.1) 88 (11.9) 87 (11.8) 77 (10.4)	< 0.001 < 0.001 < 0.001 < 0.001
Other upper gastrointestinal symptoms Globus, n (%) Heartburn, n (%) Regurgitation, n (%) Belching, n (%) Nausea, n (%) Vomiting, n (%) Bloating, n (%) Empty stomach sensation, n (%) Bothersome hunger sensation, n (%)	48 (10.1) 225 (47.6) 198 (41.9) 114 (24.1) 108 (22.8) 40 (8.5) 238 (50.3) 207 (43.8) 120 (25.4)	11 (1.5) 102 (13.8) 95 (12.9) 64 (8.7) 61 (8.3) 5 (0.7) 111 (15) 93 (12.6) 41 (5.6)	< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001
HADS* Total score Anxiety cutoff, n (%) Anxiety score, media (DS) Depression cutoff, n (%) Depression score, media (DS)	11 (6–16) 194 (41) 6 (3–10) 82 (17.3) 4 (2–6)	6 (3–10) 106 (14.4) 3 (1–6) 37 (5.0) 3 (1–4)	< 0.001 < 0.001 < 0.001 < 0.001 < 0.001
HADS: Hospital Anxiety and Depression Scale

Dyspepsia and Empty stomach sensation

Among patients with FD, 43.8% (n = 207, 95% CI: 0.39–0.48) reported experiencing an Empty stomach sensation, while in subjects without FD, this symptom was only present in 12.6% (95% CI: 0.10–0.15). p = < 0.001) Table 1, Fig. 1. When assessing the proportion of this symptom in the FD syndromic subgroups, it was more prevalent in patients with overlap syndrome being present in 54.9% (n = 111, 95% CI: 0.47–0.61), followed by postprandial distress syndrome and epigastric pain syndrome with 34.4% (n = 40, 95% CI: 0.26–0.44) and 35.5% (n = 56, 95% CI: 0.28–0.43), respectively. Table 1, Fig. 2.

In the comparative analysis of both groups using a multivariate logistic regression model, an association of FD with the presence of Empty stomach sensation was found (OR 1.87, 95% CI: 1.19–2.95, p = 0.007). Table 2. When assessing the association of Empty stomach sensation with different FD phenotypes, an association was found between Empty stomach sensation and epigastric pain syndrome (OR 1.88, 95% CI: 1.12–3.15, p = 0.016), postprandial distress syndrome (OR 2.22, 95% CI: 1.43–3.45, p = < 0.001), and overlap syndrome (OR 3.45, 95% CI: 2.20–5.40, p = < 0.001). Table 3, Fig. 2.Table 2

Multivariable analysis: Functional Dyspepsia vs. Non-Functional dyspepsia.
Variable	OR	IC 95%	p
Age 18–34 years 35–49 years 50–64 years ≥65 years	1.08 1.05 1.47 0.78	0.40–2.87 0.36-3.00 0.56–3.82 0.30–1.98	0.875 0.925 0.425 0.606
Sex Female Male	1.06 0.96	0.72–1.55 0.65–1.41	0.751 0.852
Comorbidities Diabetes Hypertension Non-gastrointestinal Chronic pain	1.18 1.32 1.50	0.57–2.45 0.74–2.37 0.75–3.03	0.639 0.343 0.248
Substance use Alcohol Tobacco	1.62 1.78	1.08–2.42 1.09–2.93	0.020 0.021
Dyspeptic symptoms Epigastric pain Epigastric burning Postprandial fullness Early satiety	9.32 3.85 7.36 4.31	5.84–14.89 2.48–5.99 4.76–11.3 2.73–6.78	< 0.001 < 0.001 < 0.001 < 0.001
Other upper gastrointestinal symptoms Globus Heartburn Regurgitation Belching Nausea Vomiting Bloating Empty stomach sensation Bothersome hunger sensation	1.67 2.50 2.06 1.40 0.68 7.87 2.79 1.87 1.78	0.64–4.31 1.61–3.90 1.31–3.23 0.83–2.38 0.38–1.20 2.09–29.6 1.83–4.23 1.19–2.95 1.03–3.07	0.290 < 0.001 0.002 0.201 0.184 0.002 < 0.001 0.007 0.038
HADS* Anxiety Depression	1.34 2.67	0.84–2.15 1.37–5.20	0.216 0.004
HADS: Hospital Anxiety and Depression Scale

Table 3

Multivariable analysis: Empty stomach sensation vs. Non-Empty Stomach sensation.
Variable	OR	IC 95%	p
Age 18–34 years 35–49 years 50–64 years ≥65 years	1.38 1.99 1.28 0.70	0.59–3.18 0.83–4.72 0.57–2.88 0.32–1.55	0.448 0.119 0.545 0.385
Sex Female Male	1.37 0.72	1.00-1.89 0.52–0.99	0.048 0.048
Comorbidities Diabetes Hypertension Non-gastrointestinal Chronic pain	2.00 0.93 0.80	1.14–3.50 0.57–1.52 0.46–1.40	0.015 0.791 0.443
Substance use Alcohol Tobacco	0.87 0.77	0.63–1.22 0.50–1.18	0.440 0.236
Dyspeptic symptoms Epigastric pain Epigastric burning Postprandial fullness Early satiety	1.03 2.45 1.39 1.56	0.71–1.48 1.71–3.50 0.98–1.98 1.10–2.22	0.873 < 0.001 0.059 0.013
Functional dyspepsia Epigastric pain syndrome Postprandial distress syndrome Overlap syndrome	1.88 2.22 3.45	1.12–3.15 1.43–3.45 2.20–5.40	0.016 < 0.001 < 0.001
Other upper gastrointestinal symptoms Globus Heartburn Regurgitation Belching Nausea Vomiting Bloating Bothersome hunger sensation	1.21 1.85 0.78 1.57 1.54 1.19 1.89 2.57	0.65–2.26 1.30–2.64 0.54–1.13 1.06–2.33 1.02–2.32 0.57–2.49 1.36–2.64 1.72–3.84	0.536 0.001 0.192 0.023 0.040 0.638 0.016 < 0.001
HADS* Anxiety Depression	1.60 0.99	1.11–2.31 0.59–1.64	0.011 0.974
HADS: Hospital Anxiety and Depression Scale

Empty stomach sensation was also associated with female sex (OR 1.37, 95% CI: 1.00-1.89, p = 0.048), comorbidities such as diabetes (OR 2.00, 95% CI: 1.14–3.50, p = 0.015), esophageal symptoms such as heartburn (OR 1.85, 95% CI: 1.30–2.64, p = 0.001) and belching (OR 1.57, 95% CI: 1.06–2.33, p = 0.023), other gastroduodenal symptoms such as nausea (OR 1.54, 95% CI: 1.02–2.32, p = 0.040), bloating (OR 1.89, 95% CI: 1.36–2.64, p = < 0.001), bothersome hunger sensation (OR 2.57, 95% CI: 1.72–3.84, p = < 0.001), and psychiatric disorders such as anxiety (OR 1.60, 95% CI: 1.11–2.31, p = 0.011). Table 3.

Dyspepsia and Bothersome Hunger Sensation

The prevalence of Bothersome Hunger Sensation in patients with FD was 25.4% (n = 120, 95% CI: 0.21–0.29), while in subjects without FD, it was 5.6% (95% CI: 0.04–0.07). p = < 0.001) Table 1, Fig. 3. When assessing the proportion of this symptom in FD syndromic subgroups, it was more prevalent in patients with overlap syndrome at 32.7% (n = 66, 95% CI: 0.47–0.61), followed by epigastric pain syndrome and postprandial distress syndrome at 23.9% (n = 27, 95% CI: 0.26–0.39) and 17.1% (n = 27, 95% CI: 0.11–0.23), respectively. Figure 2.

Similarly to empty stomach sensation, in the multivariate analysis, an association was found between FD and bothersome hunger sensation (OR 1.78, 95% CI: 1.03–3.07, p = 0.038). Table 2. Bothersome hunger sensation also showed an association with all three dyspeptic syndromes, being associated with epigastric pain syndrome (OR 4.02, 95% CI: 2.17–7.45, p = < 0.001), postprandial distress syndrome (OR 2.53, 95% CI: 1.43–4.48, p = 0.001), and overlap syndrome (OR 5.30, 95% CI: 3.07–9.16, p = < 0.001). Table 4, Fig. 2.

Table 4

Multivariable analysis: Bothersome hunger sensation vs. non-bothersome hunger sensation.
Variable	OR	IC 95%	p
Age 18–34 years 35–49 years 50–64 years ≥65 years	2.26 1.46 0.87 0.78	0.74–6.85 0.46–4.61 0.29–2.60 0.27–2.20	0.148 0.510 0.814 0.646
Sex Female Male	2.11 0.459	1.41–3.17 0.30–0.69	< 0.001 < 0.001
Comorbidities Diabetes Hypertension Non-gastrointestinal Chronic pain	1.13 1.66 1.07	0.53–2.42 0.87–3.14 0.53–2.18	0.741 0.120 0.839
Substance use Alcohol Tobacco	0.98 0.89	0.65–1.47 0.53–1.49	0.932 0.661
Dyspeptic symptoms Epigastric pain Epigastric burning Postprandial fullness Early satiety	2.70 1.77 1.04 1.18	1.77–4.13 1.14–2.75 0.67–1.61 0.76–1.82	< 0.001 0.011 0.836 0.450
Functional dyspepsia Epigastric pain syndrome Postprandial distress syndrome Overlap syndrome	4.02 2.53 5.30	2.17–7.45 1.43–4.48 3.07–9.16	< 0.001 0.001 < 0.001
Other upper gastrointestinal symptoms Globus Heartburn Regurgitation Belching Nausea Vomiting Bloating Empty stomach sensation	0.46 0.82 1.81 1.24 1.96 0.59 0.75 2.67	0.20–1.03 0.53–1.27 1.19–2.77 0.77-2.00 1.22-3-15 0.25–1.37 0.49–1.15 1.78–3.98	0.061 0.392 0.006 0.366 0.005 0.222 0.190 < 0.001
HADS* Anxiety Depression	1.59 0.87	1.03–2.44 0.48–1.56	0.034 0.644
HADS: Hospital Anxiety and Depression Scale

Bothersome hunger sensation was also associated with female sex (OR 2.17, 95% CI: 1.44–3.28, p = < 0.001), esophageal symptoms such as regurgitation (OR 1.81, 95% CI: 1.19–2.77, p = 0.006) and belching (OR 1.57, 95% CI: 1.06–2.33, p = 0.023), other gastroduodenal symptoms such as nausea (OR 1.96, 95% CI: 1.22–3.15, p = 0.005) and empty stomach sensation (OR 2.67, 95% CI: 1.78–3.98, p = < 0.001), as well as the diagnosis of anxiety (OR 1.59, 95% CI: 1.03–2.44, p = 0.034). Table 4.

Although the definition of dyspepsia is well established, there are symptoms associated with this disorder that have a high prevalence in the affected population, such as empty stomach sensation and bothersome hunger sensation. In this study, a prevalence of empty stomach sensation in the population with FD of 43.8% (n = 207, 95% CI: 0.39–0.48) was reported, while in subjects without FD, the prevalence was 12.6% (95% CI: 0.10–0.15).

There are symptoms associated with FD that share pathophysiological mechanisms such as visceral hypersensitivity, delayed gastric emptying, alterations in fundic accommodation, and central pain processing [13], [14], [15], [16]. In this study, an association between empty stomach sensation and symptoms that are part of the spectrum of clinical manifestations, which through gastroduodenal physiological tests have been shown to be related to visceral hypersensitivity, such as epigastric burning, bloating, and belching, was demonstrated. It was also associated with early satiety, which is the clinical manifestation of inadequate fundic accommodation, and an association was found with symptoms related to delayed gastric emptying such as nausea and vomiting.

Regarding painful hunger sensation, an association was found only with a symptom related to visceral hypersensitivity, which was epigastric pain, and like empty stomach sensation, an association was found with symptoms related to delayed gastric emptying such as nausea and regurgitation[17], [18], [19], [20]. Unlike empty stomach sensation, bothersome hunger sensation was not associated with symptoms related to fundic accommodation.

In both symptoms, an association with anxiety disorder was found, a frequent finding in patients diagnosed with FD, and its role in the pathophysiological mechanism of this DGBI has even been demonstrated[21], [22]. Hunger sensation is modulated by the hormone ghrelin, which has a positive effect on gastric emptying and is also decreased in its active form in patients with postprandial distress type FD, as demonstrated in a study by Akamizu T. et al., where ghrelin infusion in these patients could stimulate hunger sensation.[23]. It has also been shown that ghrelin plays an important role in anxiety regulation since it has been reported that in humans with anxiety, ghrelin levels may be elevated[24].

From this study, it can be concluded that epigastric void sensation and painful hunger sensation are frequent symptoms in the population with FD. Despite their high prevalence, there are no studies related to this symptomatology in FD, so the pathophysiological mechanism of this emerging symptomatology is unknown, which is why it is important to conduct gastroduodenal physiology studies, endoscopy with gastroduodenal biopsies, and studies assessing brain activity related to pain processing to understand the pathophysiological relationship of these symptoms with FD^25,26. As a hypothesis based on the recognition of anxiety as a risk factor for FD, as well as the relationship of ghrelin with hunger regulation and dysregulation in anxiety, this hormone could also be part of the pathophysiological mechanism of empty stomach sensation and bothersome hunger sensation[24].

Statement ethics

This study protocol was reviewed and approved by the ethics committee of the Instituto de Investigaciones Médico-Biológicas, Universidad Veracruzana, approval number IIMB-008-2017.

Conflict of interest statement

The authors have no conflicts of interest to declare.

Funding sources

This study was not supported by any sponsor or funder.

Author Contributions

Angel Ricardo Flores Rendon and Francisco Alejandro Felix Tellez were responsible for the organization and planning of the study, Angel Ricardo Flores Rendon also responsible for training doctors Francisco Alejandro Felix Tellez, Ana Luisa Mateos Viramontes, and Alex Rene Sandoval Aviles for the application of surveys and medical assessment of the studied population. Jose Maria Remes Troche, José Antonio Velarde Ruiz Velasco and Hector Ricardo Alvarez Ordaz were in charge of the statistical analysis and manuscript writing.

Data Availability Statement

The data underpinning the findings of this study cannot be accessed publicly as they include sensitive information that may compromise the privacy of research participants. Interested parties may obtain access to these data by contacting the corresponding author and submitting a reasonable request.

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No competing interests reported.

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Empty stomach sensation and Bothersome hunger sensation: Two Relevant Clinical Manifestations in Patients with Dyspepsia

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