Published online Mar 9, 2025. doi: 10.5409/wjcp.v14.i1.97543
Revised: October 21, 2024
Accepted: November 12, 2024
Published online: March 9, 2025
Processing time: 201 Days and 15.1 Hours
Disorders of gut-brain interaction (DGBI) are common, but knowledge about their physiopathology is still poor, nor valid tools have been used to evaluate them in childhood.
To develop a psycho-gastroenterological questionnaire (PGQ) to assess the psycho-gastroenterological profile and social characteristics of a pediatric population with and without DGBI.
One hundred and nineteen Italian children (age 11-18) were included: 28 outpatient patients with DGBI (Rome IV criteria) and 91 healthy controls. They filled the PGQ, faces pain scale revised (FPS-R), Bristol stool chart, ga
Compared to controls, patients had more medical examinations (35% of them went to the doctor more than five times), a higher school performance (23% vs 13%, P < 0.05), didn’t use tobacco (never vs 16%, P < 0.05), had early life events (28% vs 1% P < 0.05) and a higher percentage of pain classified as 4 in the FPS-R during the examination (14% vs 7%, P < 0.05).
Pediatric outpatients with DGBI had a higher prevalence of early life events, a lower quality of life, more medical examinations rising health care costs, lower anxiety levels.
Core Tip: Little is known with respect to the presence of psychological issues in association with gastrointestinal problems among children and adolescents with disorders of gut-brain interaction. The psycho-gastroenterological questionnaire could be useful to better identify such issues to tailor a possible psychological and pharmacological treatment.
- Citation: Giorgio V, Venezia I, Pensabene L, Blasi E, Rigante D, Mariotti P, Stella G, Margiotta G, Quatrale G, Marano G, Mazza M, Gasbarrini A, Gaetani E. Psycho-gastroenterological profile of an Italian population of children with disorders of gut-brain interaction: A case-control study. World J Clin Pediatr 2025; 14(1): 97543
- URL: https://www.wjgnet.com/2219-2808/full/v14/i1/97543.htm
- DOI: https://dx.doi.org/10.5409/wjcp.v14.i1.97543
According to Rome IV criteria, functional gastrointestinal disorders (FGIDs) are characterized by “gastrointestinal symptoms which cannot be attributed to another medical condition after appropriate medical evaluation”[1]. It has been well established that gut-brain axis disorders play a pivotal role in FGIDs physiopathology[2,3], as much as they should more appropriately mentioned as disorders of gut-brain interaction (DGBI). Recent studies have also demonstrated the important role of gut microbiota in DGBI development, since it is implied in the intestinal production of crucial neu
Biological (gastrointestinal symptoms), psychological [anxiety and depression, emotion dysregulation, insecure at
A prevalence study on DGBI based on Rome III criteria in the pediatric age, along the Mediterranean areas, was published in 2017. In the 4-year-old to 10-year-old group DGBI prevalence rate was 20.7% in comparison to a global prevalence of 26.6% observed in the 11-year-old to 18-year-old group. These data demonstrated how prevalent DGBI were in children and how these impacted on socio-economic aspects of health and life[20].
Therefore, in this case-control study, we aimed to evaluate the epidemiological and socio-demographic characteristics of children with irritable bowel syndrome (IBS) and functional constipation, compared to a control population; moreover, we aimed to study the gastrointestinal symptoms and the perceived health status of cases and controls in order to explore the psychological profile, particularly anxiety levels, alexithymia, the perceived self-efficacy in managing negative emotions and expressing positive ones. We finally described the QoL of these patients.
In this control-case study we consecutively screened all patients referred to the Pediatric Gastroenterology Outpatient Unit of Università Cattolica del Sacro Cuore of Rome, between February 2017 and February 2018. Among 956 screened patients, we enrolled 28 children aged 11-18 years diagnosed with DGBI according to Rome IV criteria. We excluded all patients with concomitant psychiatric conditions, type I and type II diabetes, thyroid diseases, history of abdominal surgery, connective tissue diseases or other gastrointestinal diseases other than DGBI. We also enrolled 91 sex and age-matched healthy controls attending the High School “Istituto Magistrale Tommaso Stigliani” of Matera (in Southern Italy).
The study protocol was approved by Ethical Committee of Università Cattolica del Sacro Cuore di Roma (Prot. 46650/16 12339/17, ID: 1424). All patients and their parents/Legal guardians signed informed consent form.
All patients underwent clinical evaluation and personal and pathological history were collected. Anthropometric measurements [weight, height, BMI (kg/m2)], demographic characteristics, surgery history, number of clinical eva
Patients and controls filled out a psycho-gastroenterological questionnaire (PGQ), which included: Personal details (sex, year of birth, age), school information and performance, family member information (married/cohabitant/separated/divorced parents; siblings information), digital habits (computer, mobile phone, digital music, social network), smoking habits, numbers of clinical evaluations in hospital or at the general practitioner, surgical history, presence of comor
Faces pain scale revised: The faces pain scale revised (FPS-R) is characterized by different facial expressions to evaluate pain. This is a modified version of FPS which consists in six faces representing the level of pain. The range score is between 0 and 10 (0 = no pain, 2 = a little bit of pain, 3 = a little bit more of pain, 6 = even more pain, 8 = too much pain, 10 = the worst pain ever)[21].
Bristol stool chart: The Bristol stool chart (BSC) is a practical tool often used in the clinical studies to describe the intestinal habit expressing the type of patients’ faeces. A picture shows seven types of faeces: type 1 and 2 correspond to hard faeces related to constipation, type 3 and 4 correspond to a normal bowel habit, type 5 indicates the presence of soft stool, type 6 and 7 correspond to liquid faeces related to diarrhea[22].
Gastrointestinal symptoms rating scale: Gastrointestinal symptoms rating scale (GSCG) is a questionnaire extensively used in the clinical practice which studies the adverse impact of gastrointestinal symptoms on patients, investigating 15 symptoms evaluated by a Likert scale based on 4 points (from 0 = no symptoms to 3 = more noticeable symptoms)[23]. The overall score represents the global frequency and the severity of the gastrointestinal symptoms, which are gathered in five classes (abdominal pain syndrome, dyspepsia, diarrhea, constipation, reflux syndrome). The scoring is based on the sum of the score of each item: The higher the score, the worse the symptoms appear to be.
State-trait anxiety inventory: The state-trait anxiety inventory Y (STAI Y) form[24] is a questionnaire based on a Likert scale and the interviewed subject evaluates from 1 to 4 (1 = not at all and 4 = very much) how much some sentences match with his/her own behavior. There are 40 questions, 20 of them explore the state anxiety (Y1) and the other 20 questions the trait anxiety (Y2). The state anxiety indicates how the person feels in a precise moment. The trait anxiety indicates how the interviewed habitually feels, which characterizes the person regardless a particular situation. The state anxiety form is filled out as first because it is sensitive to the condition in which the patient feels during the questionnaire. Two scores are obtained, one for the state anxiety and another for the trait anxiety. A graduated score is used: Up to 20 corresponds to very low level of anxiety; 21-40 to low level; 41-60 to moderate level; 61-80 to high level of anxiety.
Toronto alexithymia scale 20: The Toronto alexithymia scale (TAS-20) is used to explore the inability to verbally express feelings to people we know and interact with. The questionnaire is composed by 20 sentences describing the difficulty in identifying and describing emotions, the thinking pointed to external reality, the difficulty in the contact or in using emotions. The scale allows to divide patients in three groups: Absence of alexithymia (score until 50); borderline alexithymia (score 50-60), alexithymia (score > 61)[25,26].
Perceived self-efficacy and APEN-G and APEP-G scales: Self-efficacy is the self-perception on what we can do, feel, express or be. A high perceived self-efficacy is associated to low anxiety levels. The APEN-G scale evaluates the perceived self-efficacy in the management of negative emotions including 8 items. The APEP-G scale evaluates the perceived self-efficacy in the expression of positive emotions including 7 items. Answers are based on a scale from 1 (Totally unable) to 5 (Totally able). The scoring for the APEN-G goes from 8 to 40; for the APEP-G from 7 to 35. Higher scores correspond to a greater ability to manage emotions[27].
IBS-QoL questionnaire: The IBS-QoL questionnaire explores patient’s QoL including patient’s feelings, experience of the disease and functional status related to a medical condition. It is composed by 34 questions regarding eight health fields (dysphoria, interference with activity, body image, health worry, food avoidance, social reaction, sexual, relationships, overall). The average scores are calculated for each health component from 0 (the worst QoL) to 100 (the best QoL). Then an overall score is calculated.
Differences among groups and within group in the mean values of each parameter were analyzed by Kruskal-Wallis one-way analysis of variance by ranks, followed by post hoc analyses using the Dunn’s Multiple. The Mann–Whitney U-test was applied to compare independent samples and the Wilcoxon signed rank test for relative samples. Chi-squared test or Fisher exact test were used when appropriate. All statistical tests were two tailed using 0.05 level of significance. The analysis was done by running the Prism software version 5.00 (GraphPad, San Diego, CA, United States). Data were expressed as mean ± SD, unless otherwise stated.
We enrolled 119 individuals (91 were assigned to the control sub-cohort and 28 to the case sub-cohort). The epidemiological characteristics are shown in Table 1. In the case sub-cohort more than 90% of patients were affected by IBS and they were assigned in the IBS subtypes, with the subtype diarrhea being predominant (IBS-diarrhea 50%, IBS-unspecified 29%, IBS with constipation 14%, Functional Constipation 7 %). Around 35% cases went to the doctor for gastrointestinal concerns more than 5 times during the study period.
| Cases | Controls | P value | |
| Total n | 28 | 91 | |
| Males n (%) | 18 (64,28) | 9 (9.89) | |
| Age, years (median and range) | 14 (13-16) | 16.5 (14-17) | Not significant |
| BMI, kg/m2 (mean ± SD) | 21 ± 5 | 21 ± 3 | Not significant |
We obtained data concerning school performance and smoking habit in 89 (98%) controls and 26 (93%) cases, level of digitalization in 87 (96%) controls and 26 (93%) cases. With respect to school performance, it was considered within standards in 75 (84%) controls and 20 (77%) cases, above standards in 12 (13%) controls and 6 (23%) cases, below standards in 2 (2%) controls and in none of the cases. None of the cases smoked whereas of 14 (16%) controls did (P < 0.05), with a number of cigarettes per day ranging from 1 to 5 in 66 (57%) of the whole sample, and 6 to 10 in 49 (43%). The population was for sure digitalized (Table 2) including both cases and controls. Concerning family members, using a semi-structured interview, we found out that in 1 (1%) control early life events occurred (identified as parents’ separation and the presence of mother’s partner) vs 8 (28%) cases (P < 0.05). 13 (14%) controls were a single son/daughter vs 6 (21%) of cases.
| Cases | Controls | ||||||
| Digitalization (h) | 0-2 | 2-6 | > 6 | 0-2 | 2-6 | > 6 | |
| Personal computer | 26 (100) | 0 | 0 | 85 (97.70) | 1 (1.14) | 1 (1.14) | |
| Internet | 14 (53.84) | 4 (15.38) | 8 (30.76) | 23 (26.43) | 20 (22.98) | 44 (50.57) | |
| Mobile phone | 10 (38.46) | 12 (46.15) | 4 (15.38) | 9 (10.34) | 23 (26.43) | 55 (63.21) | |
| Music | 16 (61.53) | 6 (23.07) | 4 (15.38) | 75 (86.20) | 7 (8.04) | 5 (5.74) | |
| Social network | 14 (53.84) | 8 (30.76) | 4 (15.38) | 25 (28.73) | 32 (36.78) | 30 (34.48) | |
Among cases, 20 (71%) children complained of mesogastric pain, followed by 4 (14%) with hypogastrium pain, 2 (7%) had epigastrium pain and left hip and right iliac fossa were painful in 2 samples (almost 7%). Concerning the perceived health status level according to the FPS-R, 14 (50%) cases had no pain when filling-in the questionnaire vs 59 (64%) controls; 10 (35%) cases had a “little bit of pain” (score 2 on the scale) vs 24 (26%) controls and 4 (14%) cases had “more pain” (score 4 on the scale) vs 6 (7%) controls (P < 0.05). Concerning the BSC, the most common feces type was type 3 in both cases (6 samples, 21%) and controls (40 samples, 45%).
The compared analysis of the explored Psycho-gastroenterological items showed that: The global score was si
The TAS-20 scale demonstrated that 9 (36%) cases and 32 (36%) controls had a positive score for indeterminate Alexithymia. The APEP-G scale did not show significant differences between the two groups. Data are summarized in Table 3 and Table 4.
| Cases | Controls | P value | |||
| Pathological score | Non-pathological score | Pathological score | Non-pathological score | ||
| STAI Y1 | 6 (21.42) | 22 (78.57) | 71 (78.02) | 20 (21.97) | < 0.05 |
| STAY Y2 | 12 (42.85) | 16 (57.14) | 67 (73.62) | 24 (26.37) | < 0.05 |
| TAS-20 | 4 (14.28) | 24 (85.71) | 22 (24.17) | 69 (75.82) | < 0.05 |
| APEN-G | 18 (64.28) | 10 (35.71) | 80 (87.91) | 11 (12.08) | < 0.05 |
| APEP-G | 18 (64.28) | 10 (35.71) | 57 (62.63) | 34 (37.36) | Not significant |
| Cases | Controls | P value | |
| GSCG | 12.2 ± 8.1 | 6.9 ± 4.0 | < 0.05 |
| STAI Y-1 | 33.5 ± 12.1 | 48.6 ± 10.9 | < 0.05 |
| STAY Y-2 | 39.3 ± 10.7 | 47.4 ± 10.6 | < 0.05 |
| TAS-20 | 48.2 ± 8.0 | 51.8 ± 11.4 | < 0.05 |
| APEN-G | 24.3 ± 6.8 | 22.1 ± 5.0 | < 0.05 |
| APEP-G | 29.2 ± 2.9 | 28.8 ± 4.8 | Not significant |
| IBS-QoL | |||
| Dysphoria | 83.4 ± 12.8 | 96.3 ± 8.8 | < 0.05 |
| Interference with activity | 73.2 ± 17.3 | 95.3 ± 8.4 | < 0.05 |
| Body image | 87.0 ± 10.6 | 94.8 ± 9.4 | < 0.05 |
| Health worry | 83.9 ± 14.5 | 93.6 ± 11.3 | < 0.05 |
| Food avoidance | 66.0 ± 17.7 | 89.7 ± 17.5 | < 0.05 |
| Social reaction | 81.2 ± 17.8 | 95.7 ± 9.6 | < 0.05 |
| Sexual | 99.11 ± 3.2 | 98.9 ± 6.0 | Not significant |
| Relationships | 78.5 ± 21.2 | 96.3 ± 7.8 | < 0.05 |
| Overall | 80.5 ± 12.0 | 95.2 ± 7.7 | < 0.05 |
Our study suggests that the psycho-gastroenterological profile of pediatric patients with DGBI enrolled according to Rome IV criteria displays peculiar features, and that their QoL is significantly reduced compared to healthy age and sex-matched people; as a matter of fact DGBI have an important impact on QoL, causing sleep disorders, school truancy, more medical examinations, endoscopies, therapy changes and laboratory testing[28] leading to significant health care costs, while the final outcome on remission is minimal[29].
It is widely acknowledged that DGBI arise from intricate and bidirectional interactions between biological, psychological, and social factors, rather than being the result of a simple, single cause etiopathogenetic process. According to the biopsychosocial model of DGBI, both genetic and environmental factors, such as early life experiences, trauma, and social learning, impact the brain and gut, which then communicate with each other through the autonomic nervous system and the Hypothalamic-Pituitary-Adrenal axis. The combined effects of altered physiology and the individual’s psychosocial state ultimately shape their experience of the illness and the resulting clinical outcome. Moreover, these outcomes will influence the severity of the disorder. This suggests that psychosocial elements play a crucial role in understanding the pathophysiology of DGBI and in developing an effective treatment approach[30].
On the other hand, the microorganisms in the gut –well known as gut microbiota- communicate back and forth with the brain through neural, hormonal, and immune pathways, which can have major effects on behavioral issues such as anxiety, depression, cognitive disorders, and chronic gastrointestinal disorders, drawing the complex microbiota-gut-brain-axis[4].
As far as we know, these observations are mainly based on in vitro studies or in-vivo clinical adult studies[31].
Given the scant data in the pediatric population, in our study we wanted to explore the anxiety levels, alexithymia, the perceived self-efficacy in managing negative emotions and expressing positive ones in children with DGBI, through specific and validated scales.
In the GSCG, STAI Y1, STAI Y2, TAS-20 e APEN-G scales we observed differences in the study groups (cases vs controls). In particular, in the GSCG the mean score of cases was doubled compared to controls (12 vs 6.9, P < 0.05), while in the STAI Y-1 we surprisingly observed that 78% of controls obtained a pathological score (> 40) vs 21% of cases. Moreover, the STAI Y-2 showed that 73% of controls had a pathological score compared to 43%. Our hypothesis to explain these findings is that children of the case sub-cohort were more used to face doctors and health care professionals, being more adapted in tolerating anxiety compared to age-matched healthy children. Controls, enrolled by doctors during school hours and being asked to answer medical question, might have felt stressed by the circumstances in which the scales were filled in. We observed within cases a consistent number of patients with trait anxiety (43%), suggesting that these adolescents had an independent anxious condition related to the circumstances in which the STAI was administered. If we hypothesize that cases have developed an ability to control anxiety, in particular the state anxiety, we would have expected a higher percentage of cases capable of managing emotions; indeed, in the APEN-G, even if both cases and controls had pathological scores (64% vs 87%, respectively), there was a higher percentage of cases capable of managing negative emotions compared to controls.
Concerning the TAS-20, both cases (85%) and controls (75%) had a score compatible with negative or indeterminate alexithymia, suggesting that the emotional analphabetism wasn’t spread. It seems important to start a follow-up for patients with indeterminate alexithymia (36% in controls vs 36% in cases) to avoid worsening of the condition in the near future.
Concerning the IBS-QoL, there was a significantly lower QoL in patients with DGBI compared to controls (P < 0.05), except for the sexual item. This result reflects what is already known in the literature[18].
In the case sub-cohort, constipation (type 6 and types 6 + 7) was present in 22% of children with a perceived health level as “more pain” (score 4 on the FPS-R) in 14% compared to 7% of controls (P < 0.05). In the control sub-cohort, 51% of healthy adolescents spent more hours on the internet (over 6 hours) than cases, while cases had a higher school performance compared to controls (23.07 vs 13.48; P < 0.05).
Almost all children in the case sub-cohort listened to digital music (86% cases vs 61% controls, P < 0.05), while there was no significant difference in the use of social network between the two groups. None of the cases smoked compared to 15% of controls (P < 0.05), and this outcome could be explained as the cases had a greater attention to health (as we saw in the IBS QoL questionnaire’s subscale “Health Worry”).
To our knowledge, no data concerning listening to music and social network use are available in the literature of pediatric DGBI. Related to smoking, there is only one study from 2022 that identified smoking as a risk factor in an adult and pediatric population for abdominal pain-related disorders of gut-brain interaction[32].
An important observed feature was the presence of early life events within cases (28% vs 1%, P < 0.05), highlighting the association between life events occurred in childhood and a higher incidence of chronic diseases in adulthood[33] and psychiatric disorders[34]. It is known that psychological distress is a significant risk factor in the onset of DGBI and, when it occurs, can worsen or prolong symptoms. Additionally, it can strain the doctor-patient relationship and adversely affect treatment results[30].
In the drop-out register there is one 16-year-old girl who, despite the given consent while she was filling in the questionnaire, decided to stop as the questions hit her weak points and she did not feel to continue.
This is the first pilot study dealing with a PGQ applied in a pediatric population with DGBI. The strength of our study drives from the fact is that it specifically designed to explore psycho-physical health areas which are difficult to evaluate in childhood. The main limit is the small sample considered.
The pediatric gastroenterologist every day faces patients with DGBI, and therapeutic management is complex and often troubling, particularly in children and adolescents. The PGQ could be a useful tool in routine daily practice. Our study has shown that there is a relevant decreased QoL in children with DGBI, highlighting the need to find a therapeutic plan of action in these categories of patients. There is a need to conduct a large-scale prevalence study on DGBI in pediatric populations using suitable methods to be validated in children and adolescents.
We would like to thank in advance all the children and adolescents who will take part in the study and their parents.
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