Contribution of lifestyle to the occurrence of gastric adenocarcinoma in Midwest Brazil: a case-control studyAbstract
Background: Gastric adenocarcinoma ranks as the fourth leading cause of cancer-related deaths worldwide.
Objective: This study aimed to evaluate the lifestyle of individuals and the risk of gastric adenocarcinoma.
Method: Conducted in Midwest Brazil from 2019 to 2021, this case-control study categorized participants into three groups: the case group (patients with a diagnosis of gastric adenocarcinoma confirmed by histology, ICD-O-3, C16), control 1 (dyspeptic patients without neoplasms), and control 2 (patients without gastric complaints).
Results: The study included 411 participants: 104 in the case group, 166 in control group 1, and 141 in control group 2. A greater risk of gastric adenocarcinoma was observed in the case group and control group 1 among individuals aged over 60 years (odds ratio=3.26, 95%CI 1.54–6.91) and those with a family history of cancer (odds ratio=2.03, 95%CI 1.16–3.56). Similarly, results showed a greater risk of gastric adenocarcinoma in males (odds ratio=2.25, 95%CI 1.15–4.40) and those aged over 60 (odds ratio=4.85, 95%CI 2.13–11.08) in the case and control group 2.
Conclusion: The factors associated with gastric adenocarcinoma included male sex, age over 60, and family history of cancer. In contrast, lower risk of gastric adenocarcinoma was observed in individuals with higher education and overweight.
Keywords:
stomach neoplasms; risk factors; epidemiology; case-control studies; Brazil
Resumo
Introdução: O adenocarcinoma gástrico é a quarta principal causa de morte relacionada ao câncer em todo o mundo.
Objetivo: Este estudo teve como objetivo avaliar o estilo de vida e as chances de adenocarcinoma gástrico.
Método: Realizado no Brasil Central de 2019 a 2021, este estudo caso-controle categorizou os participantes em três grupos: casos (pacientes com diagnóstico confirmado de adenocarcinoma gástrico por histologia, CID-O-3, C16), controle 1 (pacientes dispépticos sem neoplasias) e controle 2 (pacientes sem queixas gástricas).
Resultados: O estudo incluiu 411 participantes, sendo 104 casos, 166 do grupo controle 1 e 141 do grupo controle 2. Observou-se maior chance de adenocarcinoma gástrico nos grupos caso e controle 1 entre indivíduos com idade superior a 60 anos (razão de chances=3,26, IC95% 1,54–6,91) e aqueles com histórico familiar de câncer (razão de chances=2,03, IC95% 1,16–3,56). Da mesma forma, nos grupos caso e controle 2, foi observado maior risco de adenocarcinoma gástrico em homens (razão de chances=2,25, IC95% 1,15–4,40) e naqueles com mais de 60 anos (razão de chances=4,85, IC95% 2,13–11,08).
Conclusão: Os fatores associados ao adenocarcinoma gástrico incluíram sexo masculino, idade superior a 60 anos e história familiar de câncer. Em contrapartida, foram observadas menores chances de adenocarcinoma gástrico em indivíduos com ensino superior e com excesso de peso.
Palavras-chave:
neoplasias gástricas; fatores de risco; epidemiologia; estudos de casos e controles; Brasil
INTRODUCTION
Gastric cancer is the fifth most frequent neoplasm and the fourth leading cause of cancer-related deaths worldwide in 2020. The incidence and mortality rates of gastric cancer have decreased in recent decades, although it remains a major public health concern worldwide1. In Brazil, it is estimated that in 2020–2022, there will be more than 10 thousand deaths from gastric cancer and 21 thousand new cases per year, representing the sixth most frequent type of cancer, except for non-melanoma skin cancer2,3.
According to the World Cancer Research Fund and the American Institute for Cancer Research (WCRF/AICR), approximately one-third of cancers can be prevented through lifestyle changes4. Key risk factors associated with the development of gastric cancer include hereditary factors, Helicobacter pylori infection, and modifiable factors such as dietary habits, physical activity, smoking, and alcohol consumption5,6.
Smoking and consumption of alcoholic beverages are lifestyle habits that have a well-established causal link with various types of cancer7,8. As a result, tobacco and alcohol were classified by the International Agency for Research on Cancer (IARC) as Group 1 carcinogens9. Epidemiological studies have shown a positive association between the consumption of alcoholic beverages and smoking habits in the context of gastric cancer4,6. Despite this, some studies failed to report this association10,11, reinforcing the multifactorial nature of this neoplasm and emphasizing the necessity for regional studies.
In fact, risk factors related to gastric cancer are unevenly distributed worldwide1. Brazil, as a country with continental proportions, exhibits significant social and cultural variances across its geographic regions. The Brazilian Midwest has cultural peculiarities where lifestyle can add characteristics that favor the carcinogenesis of gastric adenocarcinoma (GAC). Understanding the role of these factors and their association with GAC may contribute to preventing, screening high-risk individuals, and diagnosing GAC early. Thus, this study aimed to analyze the sociodemographic characteristics and lifestyle regarding alcohol consumption, smoking, and the presence of GAC in a population in Midwest Brazil.
METHODS
Study population
This was a hospital-based case-control study of patients with GAC conducted from March 2019 to June 2021. Data were collected through interviews with patients recruited at Hospital das Clínicas da Universidade Federal de Goiás, Associação de Combate ao Câncer em Goiás — Araújo Jorge Hospital, Instituto do Aparelho Digestivo, and Centro Brasileiro de Radioterapia, Oncologia e Mastologia, in the city of Goiânia, Goiás, Brazil.
The cases were patients of both sexes and aged 18–75 years who had been diagnosed with GAC within the past two years, as confirmed by histopathological examination and categorized according to the International Classification of Diseases (ICD-10, C16)12.
Controls were divided into two groups: control group 1, including dyspeptic patients undergoing upper digestive endoscopy; and control group 2, including patients who did not have gastric complaints, treated in the departments of gynecology, orthopedics, and ophthalmology. Controls were patients of both sexes aged 18–75 years.
Among the cases, patients with advanced neoplasms in the terminal stage without a therapeutic proposal and those unable to answer the questionnaire were excluded. In the control groups, patients with intestinal metaplasia and previous malignancies, except for non-melanoma skin cancer, were excluded.
Data collection
Information was collected from interviews conducted by trained health professionals and stored in a computerized database, Research Electronic Data Capture (REDCap™) EPGC Version 10.6.9. During the interview, participants completed an epidemiological questionnaire containing details on sociodemographic characteristics (sex, age, education, and marital status), lifestyle habits (alcohol and tobacco consumption), assessment of body mass index (BMI, in kg/m2), and personal and family medical history. Information on the histopathology of the cases was provided by the clinical pathology laboratories of the specialized centers included in the study.
The variables used for analysis were sex, age (≤45 years, 46–59 years, ≥60 years), marital status (married and unmarried), level of education (illiterate, elementary school, high school, and higher), ethnicity (white and non-white), BMI (underweight/eutrophic, overweight, and obese), family history of cancer, and alcohol and tobacco consumption. Alcohol consumption status was classified as follows: never consumed alcohol, alcoholic (drinking alcohol for at least six months in the last year), and former alcoholic (drinking alcohol for at least six months in a period prior to one year). Meanwhile, tobacco consumption status was categorized as: never smoked, smoker (smoked for at least six months in the last year), and former smokers (smoked for at least six months in a period prior to one year).
Nutritional status was classified according to the World Health Organization (WHO) using the BMI13. The adult population was categorized as either underweight (<18.5 kg/m2), eutrophic (18.5≤BMI<24.9 kg/m2), overweight (25.0≤BMI<29.9 kg/m2), and obese (≥30 kg/m2). The elderly population (>60 years old) was categorized according to the Pan American Health Organization (PAHO) as either underweight (<23 kg/m2), eutrophic (23≤BMI<28 kg/m2), overweight (28≤BMI<30 kg/m2), and obese (≥30 kg/m2)14.
Statistical analysis
Descriptive analysis of categorical variables was performed using absolute and relative frequencies; for continuous variables, the mean and standard deviation (SD) were calculated. Pearson’s χ2 test of association was performed for categorical variables and the Kruskal-Wallis test for continuous variables, with a significance level of 5%. Univariate and multiple binary logistic regression models were used in the analysis of odds ratios (ORs) and their respective 95% confidence intervals (95%CI). The multiple model was built using univariate analyses with a value of p≤0.20, based on the likelihood ratio test. The stepwise method (stepwise forward) was used to adjust the model, including the variables in decreasing order of significance; variables that were not significant and hindered a good adjustment of the model were excluded. In the multiple analysis, variables with p<0.05 and those considered as adjustment remained. Residual analysis was performed using the Hosmer–Lemeshow test. All analyses were performed using the STATA 15 program.
Ethical considerations
The study was conducted in accordance with the Ethical Standards of the Brazilian National Committee of Ethics in Human Research, which adheres to the principles of the Declaration of Helsinki. The research was approved by the Research Ethics Committee of the Antônio Prudente Foundation, under number 3.174.666 (CAAE: 53166915.9.1001.5432). All participants provided their informed consent.
RESULTS
A total of 449 patients were recruited from 2019 to 2021: 104 cases, 191 in control group 1, and 154 in control group 2. However, 25 patients from group control 1 and 13 from group control 2 were excluded. Finally, 104 participants in the case group, 166 in control group 1, and 141 in control group 2 were included in this study (Figure 1).
Flowchart of elegibility of cases and controls of the study conducted from 2019 to 2021 in Goiânia, Goiás, Brazil.
In the case group, 53.8% (56/104) were men, while in control groups 1 and 2, 62.7% (104/166) and 71.6% (101/141), respectively, were women (p=0.001). The mean age (56.3 years±10.1 SD) and the age group above 60 years (45.2%) were higher in the case group (Table 1).
Sociodemographic characteristics and lifestyle habits among cases and controls in the gastric adenocarcinoma study conducted from March 2019 to July 2021 in Goiânia, Goiás, Brazil
Married marital status was the most prevalent in all groups, particularly in the case group (72.1%). Regarding education level, the majority of participants in the case group (48.1%) and control group 1 (53.0%) reached elementary school, while those in control group 2 (65.3%) had completed high school or higher education. Moreover, 69.2% of the cases, 44.6% of control 1, and 47.5% of control 2 were underweight or eutrophic. A family history of cancer was more frequent in the case groups (57.7%) (Table 1).
The habit of consuming alcoholic beverages was more prevalent in control 2 (36.9%); however, 28.8% of the cases were former alcoholics. Among participants in the case group, tobacco consumption was observed in 32.7% and 17.3% were smokers and former smokers, respectively. Cases (62.8%) had a higher prevalence of consuming more than 20 pack-years compared to controls 1 (32.8%) and 2 (20.5%) (Table 1).
In the univariate analysis between the case group and control group 1, there was a higher risk of GAC in male patients (OR=1.95, 95%CI 1.19–3.22), patients aged over 60 years (OR=4.63, 95%CI 2.35–9.14), patients with a family history of cancer (OR=2.23, 95%CI 1.35–3.67), and smokers (OR=1.85, 95%CI 1.05–3.29). A lower risk of GAC was observed in unmarried patients (OR=0.44, 95%CI 0.26–0.74) and obese patients (OR=0.34, 95%CI 0.17–0.67) (Table 2).
Univariate and multiple logistic regression analysis of cases with gastric adenocarcinoma and control group 1, March 2019 to July 2021 in Goiânia, Goiás, Brazil
In the multiple analysis between the case group and control group 1, there was a higher risk of GAC in individuals aged over 60 years (OR=3.26, 95%CI 1.54–6.91) and those with a family history of cancer (OR=2.03, 95%CI 1.16–3.56). Conversely, a lower risk of GAC was observed in unmarried patients (OR=0.41, 95%CI 0.22–0.75) and overweight patients (OR=0.32, 95%CI 0.15–0.68), with the model adjusted for sex and alcohol and tobacco consumption (Table 2).
In the univariate analysis performed between the case group and control group 2, there was a greater risk of GAC in men (OR=2.94, 95%CI 1.73–5.01), patients aged over 60 years (OR=9.28, 95%CI 4.50–19.14), former alcoholics (OR=3.04, 95%CI 1.49–6.19), and smokers (OR=2.44, 95%CI 1.32–4.50). A lower risk of GAC was observed among unmarried patients (OR=0.57, 95%CI 0.33–0.98), patients who had completed high school or higher education (OR=0.08, 95%CI 0.23–0.31), and overweight patients (OR=0.37, 95%CI 0.19–0.71) (Table 3).
Univariate and multiple analysis of cases with gastric adenocarcinoma and control group 2, March 2019 to July 2021 in Goiânia, Goiás, Brazil
In the multiple analysis between the case group and control group 2, a higher risk of GAC was observed in male patients (OR=2.25, 95%CI 1.15–4.40) and patients aged over 60 years (OR=4.85, 95%CI 2.13–11.08). In contrast, a lower risk of GAC was observed among patients who had completed high school or higher education (OR=0.18, 95%CI 0.38–0.82) and obese patients (OR=0.42, 95%CI 0.18–0.98) (Table 3).
DISCUSSION
In this study, which analyzed GAC in two control groups, we observed that being male, married, and over 60 years of age increased the risk of GAC. According to the National Health Survey, data from the Brazilian Institute of Geography and Statistics, men consume almost three times more alcoholic beverages and smoke almost twice as much as women15. Female sex hormones such as estrogens, late menopause, and increased fertility may contribute to protection against gastric cancer in women16,17.
In this study, individuals aged over 60 years were more likely to have GAC. According to data from the United States Surveillance, Epidemiology, and End Results Program (SEER), from 2014 to 2018, approximately 27% of gastric cancer cases occurred in the age group of 65 to 74 years18,19. Although the incidence rates of gastric cancer in the elderly remain high, there has been an increased incidence in younger adults and women20. In Brazil, an increase in the incidence of gastric cancer was observed in women born in the 1960s21.
The risk of GAC was twice as high in patients with a family history of cancer (first-degree relatives) when compared to endoscopic control patients. Yaghoobi et al.22 reported that a family history of gastric cancer was associated with twofold or threefold risk of this neoplasm. The association between a family history of cancer and GAC is due to the existence of inherited genetic factors and family exposure to the same risk factors, including infection by H. pylori bacteria in the family environment, exposure to carcinogens from unhealthy eating habits, and lifestyle factors such as consumption of alcoholic beverages and smoking22,23.
Education level is a factor associated with economic development24. A higher educational level can contribute to access to health information, healthier eating habits, and healthier lifestyles25. In this study, a lower risk of GAC was observed in patients with high school or higher education; however, no difference was observed in the risk of GAC among illiterate people or people with elementary or high school, corroborating other studies25,26,27.
Excess body weight may be associated with an increased risk of gastric cancer, especially GAC, in the cardia region. In addition, obesity may be associated with other factors, including H. pylori infection, which may contribute to an increased risk of gastric cancer27,28,29. However, in this study, low weight was considered a lower risk factor for GAC. This can be attributed to reverse causality, which is common in case-control studies30.
Alcohol consumption can contribute to the development of GAC, since ethanol is soluble in fat, causing damage to the gastric mucosa from the entry of carcinogenic compounds. In addition, its metabolite acetaldehyde has a local toxic effect, which increases the risk of GAC28,31. A systematic review with meta-analysis performed by Ma et al.31 reported that alcohol consumption can increase the risk of gastric cancer, even at low levels.
Li et al.32 reported that alcohol consumption increases the risk of gastric cancer in a dose-response manner. However, some studies did not show a relationship between alcohol consumption status and gastric cancer, and this association was observed only in high-dose consumption33,34,35. The present study corroborates these results, where no association was found between alcohol consumption and GAC.
Tobacco smoke contains carcinogenic chemical compounds that contribute to GAC carcinogenesis through mutations, oxidative stress, epigenetic changes, and DNA binding36. The risk of gastric cancer can increase by approximately 1.5- to 2.5-fold for current and former smokers, by up to 60% in men and 20% in women who smoke, compared to non-smokers8,37. In addition, the number of cigarettes per day, packs per year, or duration of smoking increases the risk of gastric cancer in smokers38,39. However, in this study, there was no association between the tobacco consumption status and GAC. More complex analyses are required, including the number of pack-years and a larger sample size.
This study has limitations, such as the sample size and the lack of pairing between cases and controls. A potential limitation inherent to case-control studies concerns memory bias. Cases may be more likely to remember unhealthy lifestyle habits than controls. However, some strengths of this study need to be mentioned, including the utilization of a standardized questionnaire and the conduction of interviews by duly trained health professionals. Moreover, the recruitment of two hospital controls adds to the robustness of the study. To the best of our knowledge, this is the first case-control study in the Midwest region of Brazil to incorporate two controls. Another relevant aspect concerns the standardization of remote interviews, which characterizes a novelty in the scientific community, given that this resource is still underutilized. During the pandemic caused by the SARS-CoV-2 virus, the WHO recommended social isolation40. Consequently, adapting and standardizing remote interviews were indispensable for the continuity of this research.
CONCLUSION
The main factors associated with higher risk of GAC were male sex, age over 60 years, and a family history of cancer. Conversely, higher education and overweight individuals exhibited a lower risk of GAC. Nevertheless, studies with a larger number of cases and controls are necessary to include other risk factors, such as occupational exposure, physical activity, diet, and H. pylori infection.
ACKNOWLEDGEMENTS
We thank all patients who believed in our work and gave us their time to carry out the interviews.
DATA AVAILABILITY STATEMENT
The datasets generated and/or analyzed during the current study are not publicly available due to ethical and privacy restrictions but are available from the corresponding author upon reasonable request.
Funding:
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