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Analysis between symptoms of the upper gastrointestinal tract and endoscopic findings of patients undergoing upper digestive endoscopy in a reference center in the interior of Maranhão, Brazil

ABSTRACT

Purpose:

To analyze clinical and endoscopic aspects of dyspeptic patients submitted to upper endoscopy in a reference center in the interior of Maranhão, Brazil.

Methods:

Observational, descriptive, and analytical research through interviews and endoscopic reports of 80 patients with dyspeptic complaints submitted to upper endoscopy.

Results:

Among the respondents, 66.25% were women, most were aged ≥ 40 years old and had epigastric pain as their main symptom, and 29.75% had no appropriate indication to perform upper endoscopy. Mild enanthematous gastritis of the antrum was the most frequent finding, and 92.5% had non-significant findings. Rapid urease test was positive in 25%. The following findings showed a statistically significant correlation (p < 0.05): age < 40 years old, female gender, and gastric lesion with positive urease test; smoking with gastric lesion and age less than 40 years old with normal examination. Patients with significant findings had appropriate indications for upper endoscopy.

Conclusions:

The correct indication of upper endoscopy is essential for satisfactory endoscopic yields and accurate diagnosis.

Key words:
Dyspepsia; Endoscopy; Helicobacter pylori

Introduction

Dyspepsia or dyspeptic syndrome can be characterized by a set of symptoms related to the upper digestive tract, such as epigastric pain, postprandial discomfort, early satiety, retrosternal pyrosis, regurgitation, and heartburn11 Colin-Jones DG, Bloom B, Bodemar G. Management of dyspepsia: Report of working party. Lancet. 1988;1(8585):576-9. . In this context, according to the Rome IV criteria, this syndrome can be classified as functional or organic. Organic dyspepsia is related to confirmed structural or histopathological changes, such as peptic ulcer disease, gastroesophageal reflux disease (GERD), gastric cancer, gastritis, and Helicobacter pylori infection. Functional dyspepsia, on the other hand, is defined by symptoms unrelated to structural disease, and upper gastrointestinal endoscopy (UGE) findings demonstrate normality or changes not compatible with the symptoms22 Moayyedi PM, Lacy BE, Andrews CN, Enns RA, Howden CW, Vakil N. ACG and CAG clinical guideline: management of dyspepsia. Am J Gastroenterol. 2017;112(7):988–1013. https://doi.org/10.1038/ajg.2017.154
https://doi.org/10.1038/ajg.2017.154...
.

Diagnosis and therapeutic management in these cases are essentially clinical, requiring complementary tests depending on the indications. UGE can be used to provide information for diagnosis and staging, differential diagnosis, investigation of complications, and treatment of gastrointestinal disorders22 Moayyedi PM, Lacy BE, Andrews CN, Enns RA, Howden CW, Vakil N. ACG and CAG clinical guideline: management of dyspepsia. Am J Gastroenterol. 2017;112(7):988–1013. https://doi.org/10.1038/ajg.2017.154
https://doi.org/10.1038/ajg.2017.154...
,33 Keren D, Rainis T, Stermer E, Lavy A. A nine-year audit of open-access upper gastrointestinal endoscopic procedures: results and experience of a single centre. Can J Gastroenterol. 2011;25(2):83–8. https://doi.org/10.1155/2011/379014
https://doi.org/10.1155/2011/379014...
. In this context, according to the IV Brazilian Consensus on H. pylori Infection, UGE should be performed in patients aged 40 years old or older with uninvestigated dyspepsia, patients who do not respond to empirical treatment with histamine H2 receptor blockers (H2), proton pump inhibitors (PPIs), or prokinetics, among others, and patients of any age with alarm signs, including unintentional weight loss, dysphagia, persistent vomiting, palpable abdominal mass, jaundice, bleeding, and a positive family history of gastric cancer in first-degree relatives44 Coelho LGV, Marinho JR, Genta R, Ribeiro LT, Passos MDC, Zaterka S, Assumpção PP, Barbosa AJA, Barbuti R, Braga LL, Breyer H, Carvalhaes A, Chinzon D, Cury M, Domingues G, Jorge JL, Maguilnik I, Marinho FP, Moraes-Filho JP, Parente JML, Paula-E-Silva CM, Pedrazzoli-Júnior J, Ramos AFP, Seidler H, Spinelli JN, Zir JV. IVth Brazilian consensus conference on Helicobacter pylori infection. Arq Gastroenterol. 2018;55(2):97–121. https://doi.org/10.1590/s0004-2803.201800000-20
https://doi.org/10.1590/s0004-2803.20180...
.

The prevalence of dyspepsia is high worldwide, with an estimated rate of 10 to 30%55 Mahadeva S, Goh KL. Epidemiology of functional dyspepsia: a global perspective. World J Gastroenterol. 2006;12(17):2661–6. https://doi.org/10.3748/wjg.v12.i17.2661
https://doi.org/10.3748/wjg.v12.i17.2661...
. In line with this, gastroesophageal reflux disease, one of the main causes of dyspepsia, motivates more than 5.6 million medical consultations each year66 Peery AF, Crockett SD, Murphy CC, Lund JL, Dellon ES, Williams JL, Jensen ET, Shaheen NJ, Barritt AS, Lieber SR, Kochar B, Barnes EL, Fan YC, Pate V, Galanko J, Baron TH, Sandler RS. Burden and cost of gastrointestinal, liver, and pancreatic diseases in the United States: update 2018. Gastroenterology. 2019;156(1):254–72 e11. https://doi.org/10.1053/j.gastro.2018.08.063
https://doi.org/10.1053/j.gastro.2018.08...
.

Considering the above, the present study aimed to analyze the clinical and endoscopic aspects of dyspeptic patients undergoing UGE at a reference center in the interior of Maranhão, Brazil.

Methods

Study type

This is an observational, descriptive, and analytical study of patients with dyspeptic complaints undergoing UGE at the Digestive Endoscopy Service of the Macrorregional Hospital Dra. Ruth Noleto in Imperatriz, Maranhão.

Inclusion and exclusion criteria

All patients aged 18 years old or older, of both sexes, with symptoms of the upper gastrointestinal tract, referred for UGE, and who agreed to participate in the research by signing the informed consent form (ICF) were included. Exclusion criteria were any indication for UGE other than dyspepsia, the use of antacids or gastric secretion inhibitors in the two weeks prior to endoscopic examination, pregnancy or lactation, age under 18 years old, surgical conditions such as vagotomy, previous gastric resection surgery, or pyloric stenosis. Additionally, those who did not sign the ICF were excluded.

Data collection

Clinical data were collected through an interview with the volunteer at the research site before undergoing endoscopic examination from October 2022 to February 2023. Data were filled in a semi-structured questionnaire with clinical and endoscopic variables of the patients included in the study. Variables collected included name, gender, age, clinical presentation, comorbidities, risk factors, history of previous endoscopies, and whether they had appropriate indications for UGE according to the IV Brazilian Consensus on Heliobacter pylori Infection.

Regarding risk factors, a family history of gastric cancer was defined as those reporting such pathology in a first-degree relative. Non-selective or high-dose use of nonsteroidal anti-inflammatory drugs, smoking, alcohol consumption, and daily coffee intake were considered as risk factors. The criteria for appropriate UGE indications were based on the IV Brazilian Consensus on Heliobacter pylori Infection.

Subsequently, the data were entered into a Microsoft Office Excel spreadsheet (365 version), in which the anatomical location of the lesion seen in UGE (esophageal lesion, gastric lesion, duodenal lesion, or normal examination) and the severity of the lesion were classified. The latter was categorized into significant or non-significant findings based on the classification by Wallace et al.7, defining a significant finding as the presence of ulcers, tumors, or strictures.

Sample size calculation

To be a finite sample, since the number of cases is small in relation to the total population, we use a calculation formula for a finite population that corresponds to Eq. 1:

n = n 0 1 + n 0 1 N (1)

no = sampling intensity; N = sample size in the population.

Where no is equal to Eq. 2:

n 0 = Z ( K ) 2 4 d 2 (2)

where: z(K)22 Moayyedi PM, Lacy BE, Andrews CN, Enns RA, Howden CW, Vakil N. ACG and CAG clinical guideline: management of dyspepsia. Am J Gastroenterol. 2017;112(7):988–1013. https://doi.org/10.1038/ajg.2017.154
https://doi.org/10.1038/ajg.2017.154...
= value in the Student’s t-test table with (n-1) degrees of freedom for the confidence interval; d = error.

Taking into account the research carried out by Oliveira et al.8, which found 1,730 cases, we have to:

Initially it was determined no (Eq. 3):

n 0 = 1 , 96 2 4 ( 0 , 05 ) 2 = 384 , 16 (3)

Replacing no, we have Eq. 4:

n = 384 , 16 1 + ( 384 , 16 1 ) 1730 = 315 (4)

If we understand that this work was carried out over a period of time corresponding to five months, taking into account the maintenance of case numbers, we will have a sample corresponding to 80 patients.

Statistical analysis

In data processing, the database was initially imported from the Microsoft Office Excel spreadsheet program (365 version) to the open-access statistical program R Studio. Categorical variables were expressed in frequencies (n) and percentages (%). The association between two categorical variables was performed using the Pearson χ22 Moayyedi PM, Lacy BE, Andrews CN, Enns RA, Howden CW, Vakil N. ACG and CAG clinical guideline: management of dyspepsia. Am J Gastroenterol. 2017;112(7):988–1013. https://doi.org/10.1038/ajg.2017.154
https://doi.org/10.1038/ajg.2017.154...
test or Fisher’s exact test, chosen based on the frequency of individuals in the cell. The statistical significance was established at p < 0.05.

Ethical aspects

Data collection was carried out after the signing of the ICF. This study followed the guidelines of Resolution no. 466/12 of the National Health Council, and data collection began after approval by the Research Ethics Committee of the Universidade Federal do Maranhão. All collected information was for exclusive use of this research, with no other purposes. Data privacy will be guaranteed, and the researcher is responsible for organizing the data to comply with ethical aspects. The study was approved by the Research Ethics Committee of the Universidade Federal do Maranhão under the number 5.693.609 and approval number Certificate of Presentation of Ethical Review 57473522.4.0000.5086 on the Brazil Platform, following the guidelines of Resolution No. 466 of December 12, 2012, of the National Health Council. The translation of this work was carried out with the help of artificial intelligence (AI). AI, represented by the GPT-3.5 language model developed by OpenAI, played a fundamental role in the transposition and accuracy of scientific content into the target language.

Results

Sociodemographic and clinical data

Data from 80 dyspeptic patients who underwent UGE at Macrorregional Hospital Dra. Ruth Noleto, from October 2022 to February 2023, were analyzed. As shown in Table 1, most patients were female (66.25%). The most prevalent age group was between 29 and 39 years old (36.25%), and most respondents were aged 40 years old or older when stratifying the minimum age for UGE (53.75%). Epigastric pain was the most frequent symptom, reported by 77.5% of patients. Most patients had two symptoms (23.75%), followed by three symptoms (22.5%). During the interviews, 29.75% of patients did not have an indication for UGE according to established criteria.

Table 1
Presentation of clinical features in patients with dyspepsia undergoing upper endoscopy.

Among the indication criteria, age 40 years old or older was the most prevalent, followed by symptoms refractory to treatment (17.5%) and unexplained weight loss (17.50%). Among all, 53.75% reported having undergone at least one previous UGE. Most patients had no comorbidities (65.82%), and among those who did, systemic arterial hypertension (20%) and type 2 diabetes mellitus (13.75%) were the most prevalent. Among the patients, 80% had risk factors, with coffee consumption being the most common (65%).

Examination results

According to Table 2, mild enanthematous antral gastritis was the most prevalent finding (21.25%), followed by mild enanthematous pangastritis (12.50%), and moderate enanthematous pangastritis (11.25%). Regarding the number of lesions presented by patients, 75% had one lesion, 20% had two, and 5% had three. Among the patients, 10% had UGE without alterations. The lesion location was gastric in 85% of patients, and in 92.5% the alterations were not significant. The urease rapid test was positive in 25% of patients.

Table 2
Endoscopic findings of patients with dyspepsia undergoing upper endoscopy.

Statistical correlations

According to Table 3, using Pearson and Fisher’s Exact correlation tests, there was a statistically significant correlation between age younger than 40 years old and a positive urease rapid test (p = 0.012), and female gender with a positive urease test (p = 0.041). There was no significant correlation between appropriate or inappropriate indication for UGE and urease test (p = 0.476).

Table 3
Correlation between clinical presentation and urease rapid test.

Table 4 describes the correlations between clinical data and the location of the lesion. Symptoms of pyrosis and regurgitation were related to esophageal lesions in only 12.8 (p = 0.711) and 17.5% (p = 0.724), respectively. A significant relationship was found between smoking and gastric lesions (p = 0.021). A normal endoscopic examination was significantly correlated with age younger than 40 years old (p = 0.022).

Table 4
Correlation between clinical presentation and anatomical site of lesion in upper endoscopy.

All patients with significant findings had appropriate indications for UGE (p = 0.175) (Table 5).

Table 5
Correlation between clinical presentation and severity of lesions in upper endoscopy.

Discussion

Regarding the variable of gender in the patients analyzed in this study, there was compatibility with a study conducted in Belém, PA, Brazil, by Domingues et al.99 Domingues EP, Rymsza GP, Caldato C, de Melo Medeiros L, de Oliveira ACM. Avaliação dos resultados dos exames de Endoscopia Digestiva Alta realizadas em um hospital do município de Belém-PA no ano de 2019. Rev Eletr Acervo Saúde. 2023;23(4):12154. https://doi.org/10.25248/reas.e12154.2023
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, which indicated a higher prevalence of females (65%). A systematic review of gender-based prevalence studies showed inconsistent prevalence of dyspepsia in men and women1010 Ahlawat SK, Cuddihy MT, Locke GR. Gender-related differences in dyspepsia: a qualitative systematic review. Gend Med. 2006;3(1):31–42. https://doi.org/10.1016/s1550-8579(06)80192-0
https://doi.org/10.1016/s1550-8579(06)80...
. Thus, we postulate that women are more likely to seek medical attention for dyspepsia symptoms than men, explaining the higher number of endoscopies performed on female patients1111 Koloski NA, Talley NJ, Boyce PM. Epidemiology and health care seeking in the functional GI disorders: a population-based study. Am J Gastroenterol. 2002;97(9):2290–9. https://doi.org/10.1111/j.1572-0241.2002.05783.x
https://doi.org/10.1111/j.1572-0241.2002...
.

Regarding the age of the patients who underwent the examination, Batool et al.1212 Batool S, Sajid MU, Waris J, Satti SA, Hassan F, Aziz F. Endoscopic findings in patients presenting with dyspepsia and association of age and gender with organic dyspepsia. Pak Armed Forces Med J. 2021;71(2):567–70. https://doi.org/10.51253/pafmj.v71i2.4860
https://doi.org/10.51253/pafmj.v71i2.486...
found that 67% were in the age group > 40 years old, a higher value than the 53.75% found in this study. However, these findings are in line with some guidelines for UGE indication, such as the IV Brazilian Consensus on H. pylori Infection44 Coelho LGV, Marinho JR, Genta R, Ribeiro LT, Passos MDC, Zaterka S, Assumpção PP, Barbosa AJA, Barbuti R, Braga LL, Breyer H, Carvalhaes A, Chinzon D, Cury M, Domingues G, Jorge JL, Maguilnik I, Marinho FP, Moraes-Filho JP, Parente JML, Paula-E-Silva CM, Pedrazzoli-Júnior J, Ramos AFP, Seidler H, Spinelli JN, Zir JV. IVth Brazilian consensus conference on Helicobacter pylori infection. Arq Gastroenterol. 2018;55(2):97–121. https://doi.org/10.1590/s0004-2803.201800000-20
https://doi.org/10.1590/s0004-2803.20180...
. In addition, the upper gastrointestinal tract symptomatology presented by the patients is in line with Serra et al.1313 Serra MAA, Medeiros AT, Torres MD, Dias ICC, Santos CAA, Araújo MFM. Correlation between the symptoms of upper gastrointestinal disease and endoscopy findings: Implications for clinical practice. J Taibah Univ Med Sci. 2021;16(3):395–401. https://doi.org/10.1016/j.jtumed.2020.12.020
https://doi.org/10.1016/j.jtumed.2020.12...
, who demonstrated epigastric pain as the most prevalent (83%).

Regarding the appropriate or inappropriate indication of patients for UGE, there was variation in the literature depending on which guidelines the articles followed. In this study, 29.75% of patients were inappropriately indicated according to established criteria. In this context, the study by Meira et al.1414 Meira ATDS, Tanajura D, Viana ISS. Clinical and endoscopic evaluation in patients with gastroesophageal symptoms. Arq Gastroenterol. 2019;56(1):51–4. https://doi.org/10.1590/s0004-2803.201900000-16
https://doi.org/10.1590/s0004-2803.20190...
, which used American Society for Gastrointestional Endoscopy criteria, and the study by Gupta et al.1515 Gupta K, Groudan K, Jobbins K, Hans B, Singhania R. Single-center review of appropriateness and utilization of upper endoscopy in dyspepsia in the United States. Gastroenterol Res. 2021;14(2):81–6. https://doi.org/10.14740%2Fgr1370
https://doi.org/10.14740%2Fgr1370...
, using criteria from the American College of Gastroenterology and the Canadian Association of Gastroenterology, found 39.5 and 75.5%, respectively, of inappropriate indications. Furthermore, a systematic review by Hassan and Zullo1616 Zullo A, Manta R, De Francesco V, Fiorini G, Hassan C, Vaira D. Diagnostic yield of upper endoscopy according to appropriateness: A systematic review. Dig Liver Dis. 2019;51(3):335–9. https://doi.org/10.1016/j.dld.2018.11.029
https://doi.org/10.1016/j.dld.2018.11.02...
, which included 23 studies and 53,392 patients, showed that UGE was inappropriately indicated in 21.7% of cases, and, despite a decline in inappropriate indications during the period analyzed by the authors, this rate is still higher than 20%, which is in line with the present research.

The majority of analyzed patients had undergone previous endoscopic examinations (53.75%), which is in agreement with findings in the analyzed literature, such as the study by Meira et al.1414 Meira ATDS, Tanajura D, Viana ISS. Clinical and endoscopic evaluation in patients with gastroesophageal symptoms. Arq Gastroenterol. 2019;56(1):51–4. https://doi.org/10.1590/s0004-2803.201900000-16
https://doi.org/10.1590/s0004-2803.20190...
, in which this percentage was 61.4%. In this context, this fact may be related to the chronic nature of gastrointestinal diseases and the need for multifactorial treatment for better effectiveness, such as lifestyle changes1717 Haruma K, Kinoshita Y, Sakamoto S, Sanada K, Hiroi S, Miwa H. Lifestyle factors and efficacy of lifestyle interventions in gastroesophageal reflux disease patients with functional dyspepsia: primary care perspectives from the LEGEND study. Intern Med. 2015;54(7):695–701. https://doi.org/10.2169/internalmedicine.54.3056
https://doi.org/10.2169/internalmedicine...
.

The data on patients with comorbidities (35%) are in line with those found by Meira et al.1414 Meira ATDS, Tanajura D, Viana ISS. Clinical and endoscopic evaluation in patients with gastroesophageal symptoms. Arq Gastroenterol. 2019;56(1):51–4. https://doi.org/10.1590/s0004-2803.201900000-16
https://doi.org/10.1590/s0004-2803.20190...
(38%), demonstrating that the minority of dyspeptic patients had comorbidities. These facts can be explained by comparing the small number of patients (13.75%) aged 62 years old or older in this study and in Silva and Breda’s study1818 Silva LB, Breda D. A prevalência e distribuição de comorbidades envolvidas nos pacientes idosos em uma Unidade de Saúde do município de Cascavel-PR. Res Soc Dev. 2023;12(4):e24612441215. https://doi.org/10.33448/rsd-v12i4.41215
https://doi.org/10.33448/rsd-v12i4.41215...
, which showed a higher prevalence of comorbidities in elderly patients. Furthermore, regarding risk factors, daily coffee consumption in the Japanese study by Haruma et al.1717 Haruma K, Kinoshita Y, Sakamoto S, Sanada K, Hiroi S, Miwa H. Lifestyle factors and efficacy of lifestyle interventions in gastroesophageal reflux disease patients with functional dyspepsia: primary care perspectives from the LEGEND study. Intern Med. 2015;54(7):695–701. https://doi.org/10.2169/internalmedicine.54.3056
https://doi.org/10.2169/internalmedicine...
was 32.9% of patients and lower than that found in this study, reflecting this common habit in Brazil and the high number of patients with risk factors.

The percentage of normal endoscopic reports was higher than indicated in the national literature. Normal endoscopic reports were higher (10%) compared to national literature. Domingues et al.99 Domingues EP, Rymsza GP, Caldato C, de Melo Medeiros L, de Oliveira ACM. Avaliação dos resultados dos exames de Endoscopia Digestiva Alta realizadas em um hospital do município de Belém-PA no ano de 2019. Rev Eletr Acervo Saúde. 2023;23(4):12154. https://doi.org/10.25248/reas.e12154.2023
https://doi.org/10.25248/reas.e12154.202...
, in a study conducted in the state of Pará, and Rolim Junior et al.1919 Rolim Junior RAS, Barreto ASM, de Carvalho Nascimento E, de Lima Mota M, de Lima FS, Soares ACGM. Prevalência dos achados endoscópicos em Sergipe. Res Soc Dev. 2021;10(13):e567101321705. https://doi.org/10.33448/rsd-v10i13.21705
https://doi.org/10.33448/rsd-v10i13.2170...
, in Sergipe, Brazil, found a prevalence of normal exams of 1.8 and 6.5%, respectively. This can be explained by analyzing whether the indication was appropriate or not for the exam, such as Keren et al.’s study33 Keren D, Rainis T, Stermer E, Lavy A. A nine-year audit of open-access upper gastrointestinal endoscopic procedures: results and experience of a single centre. Can J Gastroenterol. 2011;25(2):83–8. https://doi.org/10.1155/2011/379014
https://doi.org/10.1155/2011/379014...
, which found that a normal endoscopic finding was less frequent when American Society for Gastrointestinal Endoscopy indications were followed (p < 0.001).

The anatomical location of the lesion in UGE is in accordance with Rolim Junior et al.’s study1919 Rolim Junior RAS, Barreto ASM, de Carvalho Nascimento E, de Lima Mota M, de Lima FS, Soares ACGM. Prevalência dos achados endoscópicos em Sergipe. Res Soc Dev. 2021;10(13):e567101321705. https://doi.org/10.33448/rsd-v10i13.21705
https://doi.org/10.33448/rsd-v10i13.2170...
, who found gastric lesions as the main location in 64%. Regarding the most prevalent finding in the UGE report, this study found that mild enanthematous gastritis of the antrum was present in 21.25% of patients and is in accordance with Domingues et al.’s study99 Domingues EP, Rymsza GP, Caldato C, de Melo Medeiros L, de Oliveira ACM. Avaliação dos resultados dos exames de Endoscopia Digestiva Alta realizadas em um hospital do município de Belém-PA no ano de 2019. Rev Eletr Acervo Saúde. 2023;23(4):12154. https://doi.org/10.25248/reas.e12154.2023
https://doi.org/10.25248/reas.e12154.202...
, but in a lower proportion, as they found 72.9% of people with enanthematous antral gastritis. Such discrepancies in values can be explained by the classification made by these authors, as they grouped all enanthematous antral gastritis, without specifying if it was mild or moderate.

Regarding significant findings (7.5%), the data found are similar to the recent study by Abdeljawad et al.2020 Abdeljawad K, Wehbeh A, Qayed E. Low prevalence of clinically significant endoscopic findings in outpatients with dyspepsia. Gastroenterol Res Pract. 2017;2017:3543681. https://doi.org/10.1155/2017/3543681
https://doi.org/10.1155/2017/3543681...
, which found 10.2%. However, they are lower than those found by Wallace et al.77 Wallace MB, Durkalski VL, Vaughan J, Palesch YY, Libby ED, Jowell PS, Nickl NJ, Schutz SM, Leung JW, Cotton PB. Age and alarm symptoms do not predict endoscopic findings among patients with dyspepsia: a multicentre database study. Gut. 2001;49(1):29–34. https://doi.org/10.1136/gut.49.1.29
https://doi.org/10.1136/gut.49.1.29...
(21%), an older study. We postulate that these results are lower due to the easier access to medications nowadays, the widespread use of PPIs in clinical practice, and the reduced prevalence of H. pylori infection2121 Scarpignato C, Gatta L, Zullo A, Blandizzi C; SIF-AIGO-FIMMG Group; Italian Society of Pharmacology, the Italian Association of Hospital Gastroenterologists, and the Italian Federation of General Practitioners. Effective and safe proton pump inhibitor therapy in acid-related diseases–A position paper addressing benefits and potential harms of acid suppression. BMC Med. 2016;14(1):179. https://doi.org/10.1186/s12916-016-0718-z
https://doi.org/10.1186/s12916-016-0718-...
.

Regarding the result of the positive urease rapid test (25%), there was variation in prevalence when compared to national literature. In this sense, Vaz et al.2222 Vaz AFC, Belarmino DAA, Ferreira JGG, Frade RI, Silva RO. Prevalência de infecção por Helicobacter Pylori em pacientes submetidos à endoscopia digestiva alta do Centro de Especialidades Médicas da cidade de Itabirito/MG. NBC-Periódico Cient do Núcleo de Biociências [Internet]. 2021 [accessed on Sept. 2023];11(21). Available in: https://www.metodista.br/revistas-izabela/index.php/bio/article/view/2276
https://www.metodista.br/revistas-izabel...
found 44.54% positive tests in patients undergoing UGE in Itabirito, MG, Brazil, and Frugis et al.2323 Frugis S, Czeczko NG, Malafaia O, Parada AA, Poletti PB, Secchi TF, Degiovani M, Rampanazzo-Neto A, D’Agostino MD. Prevalência do helicobacter pylori há dez anos comparada com a atual em pacientes submetidos à endoscopia digestiva alta. ABCD. Arq Bras Cir Dig. 2016;29(3):151–4. https://doi.org/10.1590/0102-6720201600030006
https://doi.org/10.1590/0102-67202016000...
, in a study conducted in São Paulo, SP, Brazil, found 17% positive results in a retrospective analysis of 10 years of patients undergoing UGE. These factors can be explained by the great variation in national territory of risk factors related to H. pylori infection, such as poor home conditions and low educational levels2424 Moosazadeh M, Lankarani KB, Afshari M. Meta-analysis of the prevalence of Helicobacter pylori infection among children and adults of Iran. Int J Prev Med. 2016;7:48. https://doi.org/10.4103%2F2008-7802.177893
https://doi.org/10.4103%2F2008-7802.1778...
.

Regarding the correlation between the symptoms presented by patients and the anatomical locations of lesions in UGE, although it did not show statistically significant correlation, symptoms of heartburn and regurgitation were related to esophageal lesions in only 12.8 (p = 0.711) and 17.5% (p = 0.724), respectively. These data are interesting to reaffirm that the diagnosis of GERD is clinical, since in up to 70% of cases it is non-erosive reflux disease, in which there are no signs of mucosal damage via endoscopy2525 Quigley EM. Non-erosive reflux disease: part of the spectrum of gastro-oesophageal reflux disease, a component of functional dyspepsia, or both? Eur J Gastroenterol Hepatol. 2001;13(Suppl.1):S13–8. . Furthermore, a significant relationship was found between smoking and gastric lesions (p = 0.021), reaffirming the involvement of smoking in peptic lesions, such as gastritis, through various mechanisms, including vasoconstriction in the mucosa1717 Haruma K, Kinoshita Y, Sakamoto S, Sanada K, Hiroi S, Miwa H. Lifestyle factors and efficacy of lifestyle interventions in gastroesophageal reflux disease patients with functional dyspepsia: primary care perspectives from the LEGEND study. Intern Med. 2015;54(7):695–701. https://doi.org/10.2169/internalmedicine.54.3056
https://doi.org/10.2169/internalmedicine...
.

Normal endoscopic examination was significantly correlated with age under 40 years old (p = 0.022). In this context, these data are in line with the study by Batool et al.1212 Batool S, Sajid MU, Waris J, Satti SA, Hassan F, Aziz F. Endoscopic findings in patients presenting with dyspepsia and association of age and gender with organic dyspepsia. Pak Armed Forces Med J. 2021;71(2):567–70. https://doi.org/10.51253/pafmj.v71i2.4860
https://doi.org/10.51253/pafmj.v71i2.486...
, which found a significant finding between age over 40 years old and a higher incidence of organic dyspepsia (p <0.01).

Although there was no statistically significant association between significant findings and appropriate UGE indication criteria (p = 0.175), all patients with significant findings had appropriate indications for UGE. In this context, the study by Abdeljawad et al.20 found an association between significant findings and alarm signs, demonstrating the importance of these signs in identifying more serious pathologies in patients. Additionally, the study by Crouwel et al..2626 Crouwel F, Meurs-Szojda MM, Klemt-Kropp M, Fockens P, Grasman ME. The diagnostic yield of open-access endoscopy of the upper gastrointestinal tract in the Netherlands. Endoscopy Int Open. 2018;6(4):E383–E394. https://doi.org/10.1055/s-0043-123185
https://doi.org/10.1055/s-0043-123185...
suggested that patients under 40 years old can be treated without UGE, with a very low risk of missing a curable malignancy. On the other hand, these data demonstrate the low frequency of significant findings in patients without appropriate indications for UGE. In this regard, due to the high prevalence of dyspepsia, an immediate endoscopy for each dyspeptic patient is not a practical approach, as this will lead to high costs and low endoscopy yield2020 Abdeljawad K, Wehbeh A, Qayed E. Low prevalence of clinically significant endoscopic findings in outpatients with dyspepsia. Gastroenterol Res Pract. 2017;2017:3543681. https://doi.org/10.1155/2017/3543681
https://doi.org/10.1155/2017/3543681...
.

A significant relationship was found between age under 40 and positive urease rapid test (p = 0.012). These values are in line with those found by Singh et al.2727 Singh SKR, Kamendu A, Kishor A. A study on the prevalence of helicobacter pylori infection by rapid urease test in patients undergoing upper gastro intestinal endoscopy for dyspepsia in a tertiary care hospital of Southern Bihar. Int J Health Clin Res. 2020;3(4):103–8., who found a high incidence of H. pylori infection in patients aged 20 to 30 years old and a decreasing incidence in the age group above 50 years old (p = 0.0242). That said, studies show that H. pylori infection in the elderly is easier to eradicate, as there is atrophy of the stomach mucosa with aging, making colonization by the bacteria unviable2828 Israel DA, Peek RM. Pathogenesis of Helicobacter pylori-induced gastric inflammation. Aliment Pharmacol Ther. 2001;15(9):1271–90. https://doi.org/10.1046/j.1365-2036.2001.01052.x
https://doi.org/10.1046/j.1365-2036.2001...
.

Furthermore, when we relate gender to urease, there was a statistically significant relationship between female gender and positive urease (p = 0.041). In this context, these values differ from those found by R. M. and Shashidhara2929 RM SS, Shashidhara P. Prevalence of Helicobacter pylori infection by rapid urease test among patients with dyspeptic symptoms who underwent upper gastrointestinal endoscopy in a secondary care hospital. Int Surg J. 2022;9(3):563–6. https://doi.org/10.18203/2349-2902.isj20220398
https://doi.org/10.18203/2349-2902.isj20...
, who demonstrated a higher prevalence of positive results in males. The explanation for this could be verified by the higher number of women in the current research and a higher prevalence of men in comparative studies, interfering with the results. Thus, when comparing with studies by Vaz et al.2222 Vaz AFC, Belarmino DAA, Ferreira JGG, Frade RI, Silva RO. Prevalência de infecção por Helicobacter Pylori em pacientes submetidos à endoscopia digestiva alta do Centro de Especialidades Médicas da cidade de Itabirito/MG. NBC-Periódico Cient do Núcleo de Biociências [Internet]. 2021 [accessed on Sept. 2023];11(21). Available in: https://www.metodista.br/revistas-izabela/index.php/bio/article/view/2276
https://www.metodista.br/revistas-izabel...
and Frugis et al.2323 Frugis S, Czeczko NG, Malafaia O, Parada AA, Poletti PB, Secchi TF, Degiovani M, Rampanazzo-Neto A, D’Agostino MD. Prevalência do helicobacter pylori há dez anos comparada com a atual em pacientes submetidos à endoscopia digestiva alta. ABCD. Arq Bras Cir Dig. 2016;29(3):151–4. https://doi.org/10.1590/0102-6720201600030006
https://doi.org/10.1590/0102-67202016000...
, which had more women in their research, there was a higher prevalence of positive urease rapid test results in females, 66.32 and 59.25%, respectively.

Moreover, although there was no statistically significant relationship between patients with appropriate or inappropriate indication for UGE and urease test (p = 0.476), 35% of positive urease results were from patients inappropriately indicated for UGE. Thus, according to various guidelines, when the patient does not meet the criteria for appropriate UGE indication, the test and treat strategy should be employed with non-invasive H. pylori tests, such as the 13C-urea breath test, which is more cost-effective and reduces the demand for UGE. However, this test has not yet been incorporated into daily clinical practice in Brazil due to national authorities’ restrictions on the substrate44 Coelho LGV, Marinho JR, Genta R, Ribeiro LT, Passos MDC, Zaterka S, Assumpção PP, Barbosa AJA, Barbuti R, Braga LL, Breyer H, Carvalhaes A, Chinzon D, Cury M, Domingues G, Jorge JL, Maguilnik I, Marinho FP, Moraes-Filho JP, Parente JML, Paula-E-Silva CM, Pedrazzoli-Júnior J, Ramos AFP, Seidler H, Spinelli JN, Zir JV. IVth Brazilian consensus conference on Helicobacter pylori infection. Arq Gastroenterol. 2018;55(2):97–121. https://doi.org/10.1590/s0004-2803.201800000-20
https://doi.org/10.1590/s0004-2803.20180...
. Thus, this lack of non-invasive alternatives for H. pylori diagnosis drives the need for UGE in young dyspeptic patients without alarm signs3030 Cheddie S, Manneh CG, Owczarek BM, Moodley Y. Age is a predictor of significant endoscopic findings in dyspepsia patients in South Africa. S Afr J Surg. 2020;58(1):14–7.. This fact implies, for example, whether the criteria for appropriate UGE indication should be reformulated in Brazil or there is a need for greater encouragement of non-invasive H. pylori tests.

Conclusion

The study allowed us to assert that most patients undergoing UGE due to symptoms in the interior of Maranhão were female, aged 40 or older, presenting more than two symptoms, with epigastric pain being the main one. Many did not have a proper indication for UGE according to the criteria of the IV Brazilian Consensus Conference on H. pylori Infection. Most had no comorbidities, and many had risk factors. Furthermore, the main finding in UGE was mild enanthematous gastritis of the antrum, the stomach being the main site affected, and the majority was non-significant alterations. The rapid urease test had results that differ from other regions of Brazil, with a relationship between age under 40 and female gender with a positive urease result. Finally, smoking was related to gastric lesions, and a normal endoscopic exam was related to age under 40.

Acknowledgements

We appreciate the High Digestive Endoscopy Service of the Macrorregional Hospital Dr. Ruth Noleto for providing access to patients and examinations.

  • Research performed at Universidade Federal do Maranhão and Endoscopy Service of Macrorregional Hospital Ruth Noleto, Imperatriz (MA), Brazil.
  • Funding

    Not applicable.

Data availability statement

All data sets were generated or analyzed in the current study;

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Edited by

Section editor: Marcelo Moura Linhares https://orcid.org/0000-0002-9540-5937

Publication Dates

  • Publication in this collection
    30 Sept 2024
  • Date of issue
    2024

History

  • Received
    14 Feb 2024
  • Accepted
    15 July 2024
Sociedade Brasileira para o Desenvolvimento da Pesquisa em Cirurgia https://actacirbras.com.br/ - São Paulo - SP - Brazil
E-mail: actacirbras@gmail.com