Pictograms to assess bloating and distension symptoms in the general population in Mexico: Results of The Rome Foundation Global Epidemiology Study

There is no term for bloating in Spanish and distension is a very technical word. “Inflammation”/“swelling” are the most frequently used expressions for bloating/distension in Mexico, and pictograms are more effective than verbal descriptors (VDs) for bloating/distension in general GI and Rome III‐IBS patients. However, their effectiveness in the general population and in subjects with Rome IV‐DGBI is unknown. We analyzed the use of pictograms for assessing bloating/distension in the general population in Mexico.

individuals were surveyed in each country that was included in the RFGES with a predefined demographic in each country of 50% female and 50% male individuals, and 40% for 18-39 years, 40% for 40-64 years, and 20% for 65+ years. 5 The Survey was conducted by Qualtrics, Inc., a global market research company with partner survey companies in multiple countries. The enrolled participants had already registered to participate in various Internet surveys. As the members of those survey-taker panels had known demographic profiles, Qualtrics's sub-vendors were able to quickly access individuals with the required demographic characteristics to fill the study quotas in each country, such as in Mexico, and ensure geographical distribution within the country. Potential study participants were invited via e-mail in multiple waves until all quota categories were filled. The survey participants were entirely anonymous to the RFGES investigators, as the data were collected in a fully deidentified manner by design. 10 The following variables were assessed using data from the RFGES The question of the Rome IV Questionnaire on the frequency of bloating and distension symptoms, that was analyzed was: "In the last 3 months, how often did you feel bloated or noticed that your belly looked unusually larger?" The answer options were: 0 = never, 1 = less than one day a month, 2 = one day a month, 3 = two to three days a month, 4 = once a week, 5 = two to three days a week, 6 = most days, 7 = every day, 8 = multiple times per day or all the time. It is important to mention, that this is the only question of the Rome IV Questionnaire that specifically asks about the presence of bloating and/or distension. The bloating/distension pictograms ( Figure 1) were preceded by the following instruction: "Please mark if you have any of the following manifestations." They are also intended to investigate about the presence of bloating and distension at that specific moment. The pictograms are generic in nature, that is, they do not depict any body parts, and include a normal abdomen, one representing bloating depicting a red balloon inside the tummy, one representing distension which shows an increment in the abdominal F I G U R E 1 Pictograms for assessing abdominal bloating and/or distension. Bloating/distension pictograms. The pictograms included four pictorial representations: one representing a normal abdomen only depicting the silhouette of a human being, one representing bloating depicting a red balloon inside the tummy, one representing distension which shows an increment in the abdominal girth with arrows detailing that increment, and one with both bloating and distension. They were preceded by the following instructions: Please mark if you have any of the following manifestations. Below each pictogram, there was a box for subjects to mark their manifestations.

Normal
BloaƟng Distension BloaƟng/Distension girth with arrows detailing that increment, and one with both bloating and distension. 3  It is important to mention that we considered the answer "never" to the Rome IV question about the frequency of bloating or an unusually larger belly during the previous 3 months, to also be a VD for a normal abdomen (i.e., not having abdominal bloating and/or distension); while answer options 1-8 (i.e., "less than one day a month", to "multiple times per day or all of the time"), would be VDs representing the presence of bloating and/or distension at any time. Also, the normal abdomen pictogram would be the pictorial representation of the absence of bloating and/or distension by the VDs, while the pictograms representing abdominal bloating, distension, or both, would be the representation of the VDs of "inflammation"/"swelling" and/ or abdominal distension.

| Demographics
The study population included a total of 2001 survey participants, half women and half men with a mean age of 44.7 ± 16.5 years. The majority lived in cities larger than >50,000 inhabitants (

| Bloating and distension according to verbal descriptors (VDs) and pictograms in subjects with Rome IV DGBI and without them
Having bloating or distension from less than once a month to all the time based on the Rome IV questionnaire was reported by 90.7% of those with any esophageal disorder, 92.1% with any gastroduodenal disorder, 90.0% with any bowel, and 91.6% with any anorectal disorder. These frequencies were higher than the presence of any form of bloating/distension by the pictograms for those with any bowel disorders (79.8%) and any anorectal disorders (86.2%), but not for those with any esophageal (84.7%) or any gastroduodenal disorder (88.1%).
The frequency of the VDs "inflammation" or "swelling" and/or abdominal distension in Spanish, and for a normal abdomen, bloating, distension, or both bloating and distension by the pictograms in subjects with or without DGBI, and in the specific DGBI of interest, are depicted in Table 2. Accordingly, both "inflammation"/"swelling" and abdominal distension, were reported twofold by subjects meeting criteria for at least one DGBI (34.3%) compared to those without them (17.2%). In addition, "inflammation"/"swelling" were somewhat similarly reported by those meeting criteria for any esophageal, gastroduodenal, and anorectal disorders compared to those with any bowel disorders who reported a lower frequency. The same was the case for the reported frequency of abdominal distension ( Table 2).
Regarding our specific DGBI of interest, subjects fulfilling criteria for functional abdominal bloating/distension followed by those with IBS, were the ones more frequently reporting "inflammation"/"swelling", followed by those with functional dyspepsia, and functional constipation. In contrast, only half of those with functional diarrhea reported "inflammation"/"swelling", compared to subjects meeting criteria for the other disorders of interest, which drives the lower frequency of reporting these VDs in those with any bowel disorder. Overall, abdominal distension was less frequently reported by subjects meeting criteria for the DGBI of interest compared to "inflammation"/"swelling" (34.3% vs. 73.1%). Also, the latter VDs were more frequently reported by those with IBS (63%) while those with Functional Constipation (30.9%) were the ones who less commonly reported them ( Table 2).
As for the pictograms, most subjects (59.5%) not meeting criteria for any DGBI selected the normal abdomen pictogram compared to only 22.1% of those meeting criteria for any DGBI. In contrast, any form of bloating/distension by the pictograms was reported by 40.5% of those without any DGBI compared to 77.9% of those meeting criteria for at least one DGBI. Also, reporting a normal abdomen by the pictograms was more frequent in subjects meeting criteria for any bowel disorders compared to those with any esophageal, gastroduodenal, and anorectal disorders. In contrast, subjects meeting criteria for any gastroduodenal disorders were the ones more frequently reporting any form of bloating/distension with the pictograms ( Table 2). Among subjects with the specific DGBI of interest, those with IBS were the ones more frequently reporting any form of bloating/distension by the pictograms (93.8%), in contrast to only half of those with Functional Diarrhea ( Table 2).
Regarding the meaning of the VDs "inflammation"/"swelling" or abdominal distension, there did not seem to be any difference between those fulfilling Rome IV criteria for DGBI compared to those without them, with roughly a third of subjects in both groups reporting that these VDs meant a "sensation of distension/inflammation or that the abdomen swells", a third reporting that it meant "an increase in the abdominal volume, girth or the need to loosen their belt", and a third reported that it meant both of the above. Not having any of those symptoms and/or not understanding them was scarcely reported ( Table 3).

| Bloating and/or distension by the pictograms in subjects not reporting or not understanding the VDs "inflammation"/"swelling" or abdominal distension
Any form of bloating and/or distension according to the pictograms in subjects not reporting "inflammation"/"swelling" or abdominal distension or not understanding these VDs, are depicted in Table 4A,B. In subjects without "inflammation"/"swelling", a normal abdomen by the pictogram was more commonly selected by those without DGBI compared to those with at least one DGBI, while any form of bloating and/or distension by the pictograms was almost double in those with at least one DGBI (38.3%, 95% CI: 31.7, 44.9) compared to subjects without any DGBI (14.5%, 95% CI: 12.0, 17.0). These figures were somewhat similar across subjects without "inflammation"/"swelling" that met criteria for any esophageal, gastroduodenal, bowel and anorectal disorders, and for subjects with the specific DGBI of interest, except for IBS, the group reporting the highest frequency of any form of bloating and/or distension according to the pictograms, although it was a very small group. Also, the reporting of bloating and/or distension with the pictograms in subjects not understanding the VDs "inflammation"/"swelling" was five times more frequent in subjects with DGBI compared to those without them (Table 4A) Finally, the prevalence rates of bloating and/or distension by pictograms in subjects not reporting "inflammation"/"swelling" by VDs, increased in the presence of two, three, or more DGBI, while it did not change in subjects not comprehending those expressions, however, the number of subjects was too small (only 9) to draw any conclusions.
TA B L E 2 Frequency of bloating and/or distension by verbal descriptors (VDs) in subjects meeting criteria for DGBI according to anatomical distribution and in the specific disorders of interest.

TA B L E 3
Comprehension of the expressions "inflammation"/"swelling" and abdominal distension in subjects meeting criteria for DGBI and those without them.
Subjects that answered to either having "inflammation"/"swelling" and/or abdominal distension with the VDs (n/ total meeting criteria for DGBI)

Verbal descriptors (VDs)
Meaning of the VDs

Yield of bloating/distension by pictograms
Normal pictograms in those without "inflammation" /"swelling" by VDs Any form of bloating/ distension pictograms in those without "inflammation" /"swelling" by VDs   In contrast, the frequency of bloating and/or distension by pictograms in individuals not reporting abdominal distension by VDs did not change according to the presence of two, three, or more DGBI, while it did increase in a stepwise manner in those not comprehending that expression if they had two, three, for or more DGBI (Table S3).

| DISCUSS ION
There is no term for bloating in Spanish and abdominal distension is a very technical expression for people to understand, making it very difficult to investigate these symptoms in Spanish-speaking populations like in Mexico. 1 Therefore, we previously validated the use of pictograms to assess the presence of bloating and/or distension in patients from a general gastroenterology clinic and with IBS by Rome III criteria in this country. 3 In these studies, we found that "inflammation" was the most frequent VD used by the patients and distension was commonly interpreted as a sensation ("inflammation") and/or an increase in abdominal girth. 3 In addition, 82.2% of the general GI patients and 89.6% with IBS-Rome III without bloating/ distension by VDs, reported the presence of these symptoms by the Pictograms. Also, these pictograms were more sensitive and specific than the VDs, supporting their usefulness in the clinic and research studies. 3 However, their effectiveness in the general population and in subjects fulfilling Rome IV criteria for DGBI, is unknown.
In the RFGES, besides the Rome IV Questionnaire for DGBI and the other standard questionnaires that were included in all of the surveyed countries, there were questions and other instruments added that were specific for each country according to local research needs. 11 Therefore, in Mexico, we included questions about the presence of "inflammation"/"swelling" and distension in Spanish (VDs), their understanding, as well as the validated bloating/distension pictograms. 3 This analysis was run for all 2001 subjects that were surveyed, as well as in subjects meeting criteria for at least one DGBI by Rome IV, DGBI based on anatomical regions (esophageal, gastroduodenal, bowel and anorectal), and in those DGBI of interest because they are known to have bloating and/ or distension even if they do not meet symptom-based criteria for them, which we report herein. Accordingly, the findings of this study can be summarized as follows: 1. "Inflammation"/"swelling" in Spanish is reported by more than half of the subjects while abdominal distension is only reported by more than 23% in the general population in Mexico; 2.
Overall, the pictograms detected any form of bloating and/or distension in more than 42% of subjects not reporting or understanding the VDs    Note: The breakdown of the yield of the pictograms in subjects not reporting or not understanding the VDs abdominal "inflammation"/"swelling" according to the number of DGBI, is depicted in Table S3.

TA B L E 4 (Continued)
"inflammation"/"swelling"/distension by VDs, was much more frequent in subjects meeting criteria for any DGBI compared to those without them.
We found that "inflammation"/"swelling" were reported by more than two-thirds of subjects meeting criteria for any DGBI, and only by 37.6% of those without DGBI, supporting the fact that these symptoms are common in subjects with these disorders. This finding is in agreement with our previous study that "inflammation" is the most common expression used by patients in Mexico to report the presence of bloating and/or distension. 2 In contrast, the lower rates of distension in subjects with DGBI and the even lower rates among those without DGBI compared to that of "inflammation"/"swelling" can be explained by the possibility that abdominal distension is less common than bloating, at least it seems that 75% of subjects with IBS and bloating have associated distension. 12 Alternatively, the lower rates of distension may reflect the lack of understanding of that VD. In fact, we found that almost 41% of individuals meeting criteria for any DGBI who reported that they did not understand adversely to different visual stimuli and was proposed by these researchers based on a study that examined the reactivity to images in health and IBS. 13 In their study, 12 "IBS images" were analyzed: pregnancy, a red balloon inside the tummy, hands squeezing the colon, knife stabbing the side of the stomach, toilets, vice tightly clenching the stomach, a knotted colon, volcanic bubbles, a volcano inside a tummy, sore intestines, rotting moss, mushrooms and fungi in the colon, and a laughing gremlin in the squat position. There were also four "neutral images" to compare with the 12 IBS images, including a sunset, fluffy clouds, a landscape, and an abstract purple landscape. The IBS patients reacted very differently from controls to those images in relation to bloating; the strength of association was most marked for the pregnancy image and the red balloon inside the tummy and a significant proportion of patients even saw bloating in the neutral images. 13 This is further supported by our finding that a normal abdomen by the pictograms was more commonly reported by individuals without DGBI compared to those meeting criteria for at least one DGBI. In other words, visual hypersensitivity may be much less frequent in subjects without DGBI.
Finally, the differences in the yield of the pictograms for bloating and/or distension in some of the specific DGBI of interest should be mentioned. On the one hand, the highest detection of these symptoms by the pictograms in subjects not reporting "inflammation"/"swelling", was in those meeting criteria for IBS (83% There are limitations in our study. First, this is a cross-sectional study without medical validation of participants' reports, nor investigations or chart reviews to rule out organic diseases; therefore, the diagnosis of DGBI or not is based solely on questionnaires. However, in our previous pictogram validation study among patients from a GI clinic, we found the same pictogram effectiveness for assessing bloating and or distension both in patients with IBS and those with organic and other GI disorders. 3 Therefore, we believe that the current findings support the use of pictograms for assessing bloating and/or distension in general population-based epidemiological studies in Mexico. Second, the results cannot be extrapolated to other Spanish-speaking countries in Latin America or Spain, as there might be differences in the local language that is used for expressing bloating and distension, and cultural differences may influence the perception of these symptoms. 2 Accordingly, the current results need to be replicated in other Spanish-speaking populations.
We recently conducted a study in El Paso Texas at the US-Mexico border where 82.9% of residents identify themselves as Hispanic with a high rate of acculturation. Using the Rome IV questionnaire in Spanish or English based on subject preferences, we found that bloating and/or distension was reported by pictograms in 30% of those not reporting them by the Rome IV Questionnaire, without any differences between Hispanics and Non-Hispanics, or the rate of acculturation. Also, reporting bloating and/or distension with the pictograms was more frequent among individuals reporting bloating/distension at least once a week compared to less frequently by the Rome IV questionnaire. 17 Another limitation is the lack of a comparison group that includes VDs added to the bloating/distension pictograms as in the Bristol Stool Scale. 18 Our bloating/distension pictograms have already been used in Malaysia where there is only one expression for bloating and distension, so adding the pictograms to VDs improved the diagnostic sensitivity of a recently developed Bloating Diagnostic Questionnaire in the Malay language. 19 In conclusion, we have found that pictograms are more effective than VDs in Spanish for detecting and assessing the presence of bloating and/or distension in the general population in Mexico, both in subjects meeting Rome IV criteria for DGBI and in those who do not.
Therefore, these pictograms should be incorporated in questionnaires that are used for studying the epidemiology of bloating and/or disten-

ACK N OWLED G M ENTS
This study was conducted under the auspice of The Rome Foundation.

CO N FLI C T O F I NTER E S T S TATEM ENT
No competing interests declared.