Abstract

Educative actions are an important component of health promotion in Brazil's primary healthcare program, the Family Health Strategy (FHS). The efficacy of these actions is evidenced by compliance with healthy behaviors and in the reduction of rates of mortality and morbidity. The objective of this study was to identify whether access to information regarding the prevention of oral cancer is greater among elders whose residences are registered with the FHS. SPSS^® was utilized to obtain estimates that were corrected for sample design, considering the magnitude of the associations between access to such information with personal determinants, the use and cost of healthcare, health-related behaviors and health outcomes. 58.9% of the 492 participating elders reported having access to such information. We verified that there was a greater chance for access among residents of houses registered by the FHS; those with greater per capita income (2.01/1.183.43); non-smokers (2.00/1.16-3.46); those that realized oral self-examination (6.35/3.46-11.64); and those that did not perceive discomfort in the mouth, head or neck (2.06/1.02-4.17). Access was greater among residents of homes registered by the FHS. Personal determinants of health, health-related behaviors and health outcomes are influenced or influence access to information regarding the prevention and management of oral diseases.

Keywords
Oral cancer; seniors; health literacy; primary healthcare; Family Health Strategy

Introduction

Brazilian elders are exposed to risk factors that increase their rates of morbidity and mortality as a result of chronic degenerative diseases¹1 Schmidt MI, Duncan BB, Silva GA, Menezes AM, Monteiro CA, Barreto SM, Chor D, Menezes PR. Doenças crônicas não transmissíveis no Brasil: carga e desafios atuais. Lancet 2011; 377(9781):2042-2053., especially cancer, which is considered a public health problem due to its high rate of mortality and fatality²2 Pisani P, Parkin DM, Bray F, Ferlay J. Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 1999; 83(1):18-29.,³3 Torres-Pereira CC, Angelim-Dias A, Melo NC, Lemos Júnior CA, Oliveira EMF. Abordagem do câncer da boca: uma estratégia para os níveis primário e secundário de atenção em saúde. Cad Saude Publica 2012; 28(Supl.):S30-S39.. Oral cancer generates high rates of mortality and fatality²2 Pisani P, Parkin DM, Bray F, Ferlay J. Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 1999; 83(1):18-29., and has a negative impact on people's quality of life⁴4 Andrade FP, Antunes JLF, Durazzo MD. Evaluation of the quality of life of patients with oral cancer in Brazil. Braz Oral Res 2006; 20(4):290-296.. According to global estimates from the Project Globocan 2012, by the International Agency for Research on Cancer, of the World Health Organization (WHO), there were 14.1 million new cases of cancer and 8.2 million deaths due to cancer in the world in 2012. The burden of cancer will continue to increase in developing countries and will rise even more in developed countries if preventive measures are not widely adapted. Oral cancer is an public health problem across the globe. In the case of Brazil, it has been estimated that in the year 2014, 11,280 new cases of this cancer were reported in men and 4,010 in women. These values correspond to an estimated risk of 11.54 new cases per 100,000 men and 3.92 new cases per 100,000 women. Not considering non-melanoma skin tumors, oral cancer in men is the fifth most common form and the eleventh most common form in women⁵5 Instituto Nacional do Câncer (INCA). Estimativa de incidência de câncer no Brasil para 2014. Rio de Janeiro: INCA; 2014. [acessado 2014 set 3]. Disponível em: http://www.inca.gov.br/estimativa/2014/sintese-deresultados-comentarios.asp
http://www.inca.gov.br/estimativa/2014/s... . In Brazil, the distribution of new cases of cancer is heterogeneous, with higher concentrations in the Southeastern and Southern regions⁶6 Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncology 2009; 45(45):309-316..

The rates of mortality for oral cancer stand out among the rates of mortality for other types of neoplasty⁷7 Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, Bernstein L, Schoenberg JB, Stemhagen A, Fraumeni Junior JF. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Research 1988; 48(11):3282-3287.

8 Franceschi S, Talamini R, Barra S, Barón AE, Negri E, Bidoli E, Serraino D, La Vecchia C. Smoking and Drinking in Relation to Cancers of the Oral Cavity, Pharynx, Larynx, and Esophagus in Northern Italy. Cancer Res 1990; 50(20):6502-6507.-⁹9 Jayalekshmi PA, Gangadharan P, Akiba S, Koriyama C, Nair R R K. Oral cavity cancer risk in relation to tobacco chewing and bidi smoking among men in Karunagappally, Kerala, India: Karunagappally cohort study. Cancer Sci 2011; 102(2):460-467.. Diet¹⁰10 Shanmugham JR, Zavras Athanasios I, Rosner B, Edward G. Alcohol-folate interactions in women's oral cancer risk: A prospective cohort study. Cancer Epidemiol Biomarkers Prev 2010; 19(10):2516-2524.,¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57., low income, education¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57. and infection by the Human papillomavirus (HPV)¹²12 Syrjänen K, Syrjänen S, Lamberg M, Pyrhönen S, Nuutinen J. Morphological and immunohistochemical evidence suggesting human papillomavirus (HPV) involvement in oral squamous cell carcinogenesis. Int J Oral Surg 1983; 12(6):418-424., as well as the synergy created by the concurrent use of tobacco and alcohol¹³13 Ko YC, Huang YL, Lee CH, Chen MJ, LM Lin, Tsai CC. Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. J Oral Med Pathol 1995; 24(10):450-453., are risk factors for diverse types of oral cancer. A randomized trial¹⁴14 Sankaranarayanan R, Ramadas K, Thomas G, Muwonge R, Thara S, Mathew B, Rajan B Effect of screening on oral cancer mortality in Kerala, India: a cluster-randomized controlled trial. Lancet 2005; 365(9475):1927-1933. was conducted in Kerala, India, with 167,741 participants over the course of nine years (1996 to 2004). The participants in the intervention group (87,655) participated in educative actions, during three distinct periods every three years, which included education regarding the harmful effects of tobacco and alcohol in terms of the risk for oral cancer and screenings conducted by trained professionals to identify cancerous lesions, as well as early diagnosis and immediate treatment of oral cancer. On the other hand, participants in the control group (80,086) were evaluated at the beginning and at the end of the study and received routine services from health services. The rates of mortality and fatality due to oral cancer were less in the intervention group than in the control group. The association between mortality rates and the intervention among all the participants was not statistically significant, however, among men who had drinking or smoking habits, the rates of mortality in the intervention group were lower¹⁴14 Sankaranarayanan R, Ramadas K, Thomas G, Muwonge R, Thara S, Mathew B, Rajan B Effect of screening on oral cancer mortality in Kerala, India: a cluster-randomized controlled trial. Lancet 2005; 365(9475):1927-1933.. This suggests that educative actions, especially among those with known risk factors, may minimize the rates of mortality and fatality due to oral cancer. In conclusion, health promotion strategies, including those aimed education at prevention, early diagnosis and treatment of oral cancer are important.

The importance of health education, prevention, tracking, early diagnosis and treatment of oral cancer has been recognized by the WHO¹⁵15 Petersen PE. Oral cancer prevention and control – The approach of the World Health Organization. Oral Oncology 2009; 45(4-5):454-460.. Subsequently, policies supporting the promotion of health education and prevention regarding oral cancer were implemented¹⁶16 Antunes JLF, Toporcov TN, Wunsch-Filho V. Resolutividade da campanha de prevenção e diagnóstico precoce do câncer bucal em São Paulo, Brasil. Rev Panam Salud Publica 2007; 21(1):30-36., as part of primary health care (PHC). In Brazil, PHC is carried out through the Family Health Strategy (FHS), the strategy chosen for the reorganization of PHC within Brazil's “Unified System of Health” (SUS)¹⁷17 Pinto RM, Wall M, Yu G, Penido C, Schmidt C. Primary care and public health services integration in Brazil's unified health system. Am J Public Health 2012; 102(11):69-76.,¹⁸18 Alencar MN, Coimbra LC, Morais APP, Silva AAM, Pinheiro SRA, Queiroz RCS. Avaliação do enfoque familiar e orientação para a comunidade na Estratégia Saúde da Família. Cien Saude Colet 2014; 19(2):353-364.. Among the characteristics of SUS, comprehensive coverage stands out, with emphasis on health promotion strategies that are aimed at developing health education that focuses on the improvement of self-care by individuals¹⁹19 Brasil. Ministério da Saúde (MS). Saúde da Família: uma estratégia para a reorientação do modelo assistencial. Brasília: MS; 1997.. In the context of health promotion, educational health interventions have the objective of increasing the level of health literacy. Sorensen et al have proposed a theoretical model that presents variables that influence and are influenced by the level of health literacy²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80. (Figure 1).

The model identifies proximal and distal factors that determine or are determined by the levels of health literacy. Oval forms that are concentrically related to the nucleus of the model represent these factors. The following variables were considered in the identification of the levels of health literacy: previous knowledge regarding health issues; necessary competencies for self-care and motivation to access, understand, appraise and apply information related to health. Access, the first condition of health literacy, refers to the capacity to seek, find and obtain information regarding health; understanding refers to the capacity to comprehend health related information; appraise is considered to be the capacity to interpret, filter and judge this information; and apply refers to the capacity to communicate and use this information to make decisions that maintain and/or improve one's health status. The model also identifies factors dynamically associated to health literacy or, in other words, its principle determinants and/or consequences. These factors include distal determinants that can be social or environmental (demographics, culture, language, political forces and social systems), proximal determinants that can be social or situational (social support, the influence of family and colleagues, the use of media and the physical conditions of the environment) and personal determinants (age, sex, race, socioeconomic condition, marital status, formal education, occupation and salary). There are other factors that have been presented as possibly associated with health literacy (determinants or consequences): the use of health services, the cost of healthcare, health-related behaviors, health outcomes, the participation of people, empowerment, equity and maintenance. In this model, it is important to consider feedback relationships between the presented factors and health literacy²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.. The age and race of people are the only factors that do not present a feedback relationship, as increasing health literacy cannot modify them. In the context of health promotion, access to information related to health is essential to improving health literacy levels. Therefore, identifying the prevalence of access to information about the prevention of oral cancer and discovering if seniors living in residences registered by the FHS have more access to this information than those that are not registered may lead to improvements in health policies that prioritize elderly health. However, studies regarding this issue were not identified.

The FHS provides an adequate context for interventions related to the promotion of health, emphasizing health education and encouraging the implementation of health-related information and the adaption of healthy behaviors. As such, the objective of this study is to identify, based on the theoretical model of health literacy²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80., whether access to information regarding the prevention of oral cancer is greater among elders who residences are registered by the FHS.

Methods

Cross-sectional study conducted with a complex probabilistic sample organized by conglomerate in two stages of elders from Montes Claros, a Brazilian city with a high population, situated in the Northern region of the state of Minas Gerais. For the purposes of this study, elders were considered to be people between the ages of sixty-five and seventy-four, as recommended by the WHO²¹21 World Health Organization (WHO). Oral health surveys: basic methods. 4th Ed. Geneva: WHO; 1997.. In the sample calculation, the estimate for the proportion of occurrence of events or illnesses was considered to be 50% of the population, with an error of 5.5%, a rate of non-response of 20%, the guarantee of proportionality by sex and a design effect (deff) of 2.0. In this way, a sample of 740 elders was estimated²²22 Martins AMEBL, Santos-Neto PE, Batista LHS, Nascimento JE, Gusmão AF, Eleutério NB, Guimarães ALS, Paula AMB, Haikal DS, Silveira MF, Pordeus IA. Plano amostral e ponderação pelo efeito de desenho de um levantamento epidemiológico de saúde bucal. RUC 2012; 14(1):15-29.. Conglomerates, census tracts and blocks were selected by simple random sampling and the collection was conducted in the homes of the participants. The diagnostic criteria of oral conditions were those recommended by the WHO in 1997²¹21 World Health Organization (WHO). Oral health surveys: basic methods. 4th Ed. Geneva: WHO; 1997.. Twenty-four trained and calibrated dentists conducted oral exams in the homes of participants in an open environment under natural light, using a sterilized mirror and CPI (Community Periodontal Index) probe²¹21 World Health Organization (WHO). Oral health surveys: basic methods. 4th Ed. Geneva: WHO; 1997.. Additionally, twenty-four interviewers (students) and twenty-four dentistry trained and calibrated²³23 Martins AMEBL, Haikal DS, Santos-Neto PE, Alves SFF, Eleutério NB, Oliveira, PHA, Gomes GP, Guimarães BL, Ferreira RC, Silveira MF, Pordeus IA. Calibração de examinadores do Levantamento epidemiológico das condições de saúde bucal da população de Montes Claros, MG - Projeto SBMOC. RUC 2012; 14(1):43-56. participated in the collection of data (the Kappa coefficient of inter-rater correlation was above 0.60)²⁴24 Cicchetti DV, Volkmar F, Sparrow SS, Cohen D, Fermanian J, Rourke BP. Assessing the reliability of clinical scales when the data have both nominal and ordinal features: proposed guidelines for europsychological assessments. J Clin Exp Neuropsychol 1992; 14(5):673-686.. Handheld computers with specially-designed a software program, entitled “Program for the Collection of Health Data”²⁵25 Martins AMEBL, Rodrigues CAQ, Haikal DAS, Silveira MF, Mendes DC, Oliveira MP, Andrade AF, Freitas CV, Pordeus IA. Desenvolvimento de um programa de computador para levantamentos epidemiológicos sobre condições de saúde bucal. RUC 2012; 14(1):30-42. allowed for the simultaneous collection of data and building of the database.

Among those that agreed to participate in the study, those that related never having accessed dental services and those that did not respond to the question regarding access to information on how to prevent oral cancer were excluded from the study. The construction of the dependent variable – access to information on how to prevent oral cancer – was obtained only from elderly who did not present cognitive problems. The identification of cognitive problems was carried out using a version of the mini-exam of mental status (MEEM)²⁶26 Bertolucci PHF, Brucki SMD, Campacci SR, Juliano Y. O mini-exame do estado mental em uma população geral: impacto da escolaridade. Arq Neuropsiquiatr 1994; 52(1):1-7. that has been validated for use in Brazil, taking into account the level of education of the elder²⁷27 Kochhann R, Varela JS, Lisboa CSM, Chaves MLF. The Mini Mental State Examination: review of cutoff points adjusted for schooling in a large Southern Brazilian sample. Dement Neuropsychol 2010; 4(1):35-41.. Those who responded positively to the question “Have you received information regarding how to avoid oral cancer from your dental service provider?” were considered to be elders that had access to information on how to avoid oral cancer.

Adapting the model of Sorensen et al., 2012²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80., as a theoretical reference, the independent variables were organized in five groups: 1) access to health-related information (the initial condition for heath literacy), 2) personal determinants of health, 3) use of health services/ health costs, 4) health-related habits and behaviors, and 5) health outcomes²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80..

The personal determinants considered in this study were age in years, self-declared race, sex, marital status, schooling in years of study and per capita income (reported as number of monthly minimum wages earned). The variables related to health services and health costs were dental services utilized, registration of residence with the FHS, time since the last dental use and motive for using dental services.

The health-related behaviors considered in this study were presence of past or current habitual use of tobacco, presence of past or current use of alcohol and practice of oral self-examination. It is important to note that, for the purposes of our study, past users of tobacco were grouped with current users. Regarding health outcomes, two subgroups were considered: 1) self-reported general health in terms of the presence of diseases and the use of medications and 2) normative and subjective conditions of oral health. Normative conditions of oral health included alterations in the oral soft tissues and the use of removable dental prostheses. The subjective conditions of oral health were self-perception, considering the perception of the need for treatment, the perception of pain in the teeth and gums in the last six months, the perception of discomfort in the mouth, head or neck and the identification of the possible consequences (impacts) of oral disorders, using the validated Brazilian version of the Oral Health Impact Profile (OHIP)²⁸28 De Oliveira BH, Nadanovsky P. Psychometric properties of the Brazilian version of the oral Health Impact Profile-Short form. Community Dent Oral Epidemiol 2005; 33(4):307-314.. All of the individuals that affirmed the presence of dental issues (by indicating repeatedly or always) for at least one of the fourteen questions on the OHIP, are considered to have reported some negative consequence, impact or outcome related to their condition of oral health.

SPSS^® 18.0 was used to analyze the collected data. We adjusted for estimated sample design effects in the analysis of data. The descriptive analysis included relative frequencies with corrections for the sample design effect, standard error (SE) and conglomerate effect (Deff) for the categorical variables. For the quantitative variables, the mean, SE and Deff were estimated. Bivariate analyses were conducted to select the variables (p < 0.20) that were included in the multivariate analyses. During the bivariate and multiple analyses (logistic regression), the odds ratio and confidence intervals were estimated as 95% (OR/IC 95%). In the final model the variables associated (p < 0.05) with access to information regarding the prevention of oral cancer were maintained. This study was approved by the relevant Institutional Review Boards and adhered to the ethical principles of Resolution 196/96 of the Brazilian National Council for Health²⁹29 Brasil. Ministério da Saúde (MS). Conselho Nacional de Saúde. Resolução nº 196 de 10 de outubro de 1996. Diretrizes e Normas Regulamentadoras de Pesquisas Envolvendo Seres Humanos. Diário Oficial da União 1996; 16 out..

Results

Among the 740 elders evaluated (the response rate was 92%), 492 elders were included in the study as they fit the inclusion criteria. Of these, 58.9% reported that they had access to information regarding the prevention of oral cancer. The mean age of the elders was 68.35 years, SE=0.16 and Deff=1.47. A majority self-reported age as between 65 and 68 years old, race as mixed “brown”, sex as female and being married or in a stable civil union. The mean number of years of formal education was 5.07, SE = 0.36, Deff = 4.04; the mean per capita monthly income in Brazilian currency was R$ 404.17, SE = 34.37, Deff = 2.65. A majority reported residing in a home registered by the FHS and most seniors reported favorable health-related behaviors regarding tobacco and alcohol. A majority reported having a chronic disease diagnosed by a physician. Most elders did not have alterations in the oral soft tissues, used removable prostheses and did not report negative consequences, impacts or outcomes related to the condition of oral health (Table 1).

In the bivariate analysis, the following variables showed association (p ≤ 0,20) with access to information on the prevention of oral cancer: self-declared race, marital status, formal education, per capita income, registration of residence by the FHS, presence of past or present tobacco habit, practice of oral self exam, presence of chronic disease, self-reported perception of discomfort in the mouth, head or neck and impact on various aspects of oral health (Table 2).

In the multiple analysis, access to information regarding the prevention of oral cancer was associated with: personal determinants of health, the use and costs of health services, health-related behaviors and health outcomes (Table 3).

Discussion

Evaluation of the level of health literacy is a relatively new approach in the field of health promotion, as it is based on a conception of health education that goes beyond the offer of information, focusing on the capacity of people to effectively access, understand, evaluate and apply this information. Improvement in health literacy rates depends on several variables, among these, empowerment²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80. stands out. It refers to social actions that promote the participation of individuals, organizations and communities in controlling their own destinies and the destiny of society. In this way, people create or are given opportunities to care for their own health, through a series of experiences through which they learn to see a more direct relationship between their objectives and a sense of how to reach them, and, in this way, they obtain more access and control over their own resources and over public and community resources available through governmental or non-governmental organizations that seek to promote health and prevent disease³⁰30 Wallerstein N, Bernstein E. Empowerment education: Freire's ideas adapted to health education. Health Educ Q 1988; 15(4):379-394..

The prevalence of access to information (the initial condition for oral health literacy) regarding the prevention of oral cancer, was 58.9%. The odds of self-reporting such access was approximately three times greater among elders registered with the FHS than those who were not registered by the FHS, even after controlling for personal determinants of health, health-related behaviors and health outcomes. The odds of access to this information was greater among those with a higher per capita income, that did not smokers, that did oral self-examiners, and those that did not perceive discomfort in the mouth, head or neck. We were not able to directly compare the findings of our study in Montes Claros with similar studies in other cities as articles with directly comparable results were not found in the recent relevant literature. However, related studies that consider degrees of knowledge or awareness regarding oral cancer, its determining factors and preventive measures were identified³¹31 Quirino MRS, Gomes FC, Marcondes MS, Balducci I, Anbinder AL. Avaliação do conhecimento sobre o câncer de boca entre participantes de campanha para prevenção e diagnóstico precoce da doença em Taubaté – SP. Rev Odontol UNESP 2006; 35(4):327-333.

32 Ribeiro R, Martins MAT, Fernandes KPS, Bussadori SK, Miyagi SPH, Martins MD. Avaliação do nível de conhecimento de uma população envolvendo câncer oral. ROBRAC 2008; 17(44):104-109.

33 Peker I, Alkurt MT. Nível de conscientização do público sobre câncer bucal em um grupo de pacientes odontológicos. J Contemp Pract Dent 2010; 11(1):49-56.-³⁴34 Elango KJ, Anandkrishnan N, Suresh A, Iyer SK, RamaIyer SK, Kuriakose MA. Mouth self-examination to improve oral cancer awareness and early detection in a high-risk population. Oral Oncology 2011; 47(7):620-624..

More than a third of the evaluated elders reported not having any type of access to information regarding the prevention of oral cancer provided their health professional, a worrisome fact, considering that the acquisition of consistent information regarding oral cancer, its determining factors and preventive measures can support the adoption of healthy habits and contribute to the prevention and early diagnosis of this type of cancer²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.,³¹31 Quirino MRS, Gomes FC, Marcondes MS, Balducci I, Anbinder AL. Avaliação do conhecimento sobre o câncer de boca entre participantes de campanha para prevenção e diagnóstico precoce da doença em Taubaté – SP. Rev Odontol UNESP 2006; 35(4):327-333.

32 Ribeiro R, Martins MAT, Fernandes KPS, Bussadori SK, Miyagi SPH, Martins MD. Avaliação do nível de conhecimento de uma população envolvendo câncer oral. ROBRAC 2008; 17(44):104-109.

33 Peker I, Alkurt MT. Nível de conscientização do público sobre câncer bucal em um grupo de pacientes odontológicos. J Contemp Pract Dent 2010; 11(1):49-56.

34 Elango KJ, Anandkrishnan N, Suresh A, Iyer SK, RamaIyer SK, Kuriakose MA. Mouth self-examination to improve oral cancer awareness and early detection in a high-risk population. Oral Oncology 2011; 47(7):620-624.

35 Souza LRB, Ferraz KD, Pereira NS, Martins MV. Conhecimento acerca do câncer bucal e atitudes frente à sua etiologia e prevenção em um grupo de horticultores de Teresina (PI). Rev Bras Cancerol 2012; 58(1):31-39.-³⁶36 Ratzan SC, Parker RM. Introduction. In: Selden CR, Zorn M, Ratzan SC, Parker RM, editors. National Library of Medicine current bibliographies in medicine: health literacy. Bethesda: NLM; 2000.. Among participants in the Campaign for the Prevention and Early Diagnosis of Oral Cancer, in one Brazilian municipality (Taubaté in the state of São Paulo), knowledge about oral cancer was evaluated in the years 2001, 2003 and 2005. Reported knowledge regarding the causes of this type of cancer varied between 32.68% – 40.52%. In 2001, 16.52% reported knowing what is an oral self-examination, in 2003, 31.97% and in 2005, 22%³¹31 Quirino MRS, Gomes FC, Marcondes MS, Balducci I, Anbinder AL. Avaliação do conhecimento sobre o câncer de boca entre participantes de campanha para prevenção e diagnóstico precoce da doença em Taubaté – SP. Rev Odontol UNESP 2006; 35(4):327-333., demonstrating a low prevalence of knowledge regarding this preventive measure among those interviewed³¹31 Quirino MRS, Gomes FC, Marcondes MS, Balducci I, Anbinder AL. Avaliação do conhecimento sobre o câncer de boca entre participantes de campanha para prevenção e diagnóstico precoce da doença em Taubaté – SP. Rev Odontol UNESP 2006; 35(4):327-333.. Possibly, as proposed by the theoretical model of Sørensen et al.²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80., the low rate of knowledge might be influenced by the rates of previous knowledge and by the competence and motivation of people who have had access to health-related information. Improvements also depend on the degree of understanding of this information in a context of vast demographic, cultural and educational diversity as well as a variety of situational and personal factors that may facilitate or prevent the application of health-related knowledge²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80..

In the context of health promotion, educative actions influence perceptions regarding oral conditions, support self-diagnosis and self-care in search of preventing and/or curing oral diseases in their initial stages³⁷37 Silva SRC, Fernandes RAC. Autopercepção das condições de saúde bucal por idosos. Rev Saude Publica 2001; 35(4):349-355.. A majority of Brazilian elders perceived their oral health as satisfactory, even though they presented oral health issues³⁸38 Martins AMEBL, Barreto SM, Pordeus IA. Auto-avaliação de saúde bucal em idosos: análise com base em modelo multidimensional. Cad Saude Publica 2009; 25(2):421-435.. Perhaps, due to this positive perception of oral health, elders do not feel it is necessary to seek information about oral health, compromising their access to information on how to prevent oral cancer. Alternately, in studies conducted in the United States, some dentists have justified not providing orientation regarding oral diseases, including cancer, due to lack of time³⁹39 Horowitz AM, Siriphant P, Sheikh A, Child, WL. Perspectives of Maryland dentists on oral cancer. JADA 2001; 132(1):65-72., often explaining that they do not feel it is necessary or that they are not paid for such services⁴⁰40 Gajendra S, Cross GD, Kumar JV. Oral cancer prevention and early detection: knowledge, practices and opinions of carers oral health in New York State. J Cancer Educ 2006; 21(3):157-162.. Furthermore, the compliance of health professionals with permanent education strategies is associated with the appropriateness of physical space, multidisciplinary approaches and epidemiological characteristics of the population⁴¹41 d’Ávila LS, Assis LN, Melo MB, Brant LC. Adesão ao Programa de Educação Permanente para médicos de família de um Estado da Região Sudeste do Brasil. Cien Saude Colet 2014; 19(1):1-16.. Perhaps employment issues, such as time and financial compensation, and other professional development factors, such as the available quality and content of accessible education for appropriate health professionals, can explain the fact that dentists do not ensure that their patients have access to information regarding the prevention of oral cancer.

In one study that was conducted in a rural location in the South of Brazil, more than half of the participants (65%) reported receiving information on how to avoid oral problems. However, although a vast majority (83%) was satisfied with what they received, 42.6% felt that the dentist could have provided more information. This study revealed that this educative measure is not always carried out with satisfactory quality⁴²42 Mialhe FL, Oliveira CSR, Silva DD. Acesso e avaliação dos serviços de saúde bucal em uma localidade rural da região sul do Brasil. Arq Cien Saude Unipar 2006; 10(3):145-149.. Health professionals, upon passing out information regarding health, need to previously know the level of health literacy of the patients and their relatives in order to refine educational strategies to meet the needs of the population being served. Perhaps the collection and analysis of more information regarding the health literacy and empowerment of study participants²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.,³⁶36 Ratzan SC, Parker RM. Introduction. In: Selden CR, Zorn M, Ratzan SC, Parker RM, editors. National Library of Medicine current bibliographies in medicine: health literacy. Bethesda: NLM; 2000.,⁴³43 Coulter A, Ellins J. Effectiveness of strategies for informing, educating, and involving patients. BMJ 2007; 335(7609):24-27. could provide explanations for the absence of associations between access to information on how to avoid oral cancer and some of the variables considered in this attempt to operationalize the theoretical model²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.. Probably, the professionals that carried out the treatment of these elders did not consider all of the variables proposed in the adapted theoretical model, indicating a need for health education initiatives within the context of health promotion²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80..

Among elders in Montes Claros, the prevalence of the offer of educational measures related to the prevention of oral cancer by dentists was not investigated. Perhaps a greater proportion of elders had access to preventive information, but as the access achieved did not lead to the acquisition and retention of knowledge, they do not remember having received this information. Additionally, those that were oriented and obtained understandings may or may not have put them to practice, considering their appraise of the information and/or due to their level of empowerment²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80..

Elders in residences registered by the FHS have a greater chance of accessing information regarding the prevention of oral cancer. Perhaps this is due to the greater emphasis on actions for health promotion and the prevention of disease in the context of the FHS as a public primary care system⁴⁴44 Paim J, Travassos C, Almeida C, Bahia L, Macinko J. The Brazilian health system: history, advances, and challenges. Lancet 2011; 377(9779):1778-1797.. The continuing education of professionals that work in this sector may also contribute to this result. This finding deserves recognition and suggests advancements in the performance of public oral healthcare services, a fact that should be recognized. However, 48.3% of elders that live in residences registered in the FHS report not having access to such information, and this also deserves attention. While advances in public policies have been registered in the past few years, such as the inclusion of oral healthcare providers in the FHS, efforts for vast policies to reduce social inequalities in the access and process of care, as well as in the evaluation of results in the area of oral health, are still necessary⁴⁵45 Rocha RACP, Goes PSA. Comparação do acesso aos serviços de saúde bucal em áreas cobertas e não cobertas pela Estratégia Saúde da Família em Campina Grande, Paraíba, Brasil. Cad Saude Publica 2008; 24(12):2871-2880., because dentists play a fundamental role in the sharing of preventive measures³²32 Ribeiro R, Martins MAT, Fernandes KPS, Bussadori SK, Miyagi SPH, Martins MD. Avaliação do nível de conhecimento de uma população envolvendo câncer oral. ROBRAC 2008; 17(44):104-109.. Health services, especially governmental services, have to contribute to achieving the desired principles of equitable and universal care, utilizing the clinical environment to offer more opportunities for learning and seeking to assure that all citizens have access to the necessary resources to ensure that dental care is treated as a human right in Brazil⁴⁶46 Narvai PC. Collective oral health: ways from sanitary dentistry to buccality. Rev Saude Publica 2006; 40(Spec nº):141-147.. It is important to point out that the vast diversity of circumstances should be considered in the development of strategies that aim to improve health literacy rates, especially with regard to the per capita income.

The odds of accessing information on how to prevent oral cancer was greater among elders with a higher per capita income, this association may reveal inequality in access to such information. Among patients in one Brazilian teaching hospital, oral cancer was associated with worse social conditions, such as low-income levels and less formal education¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57.. In one case control study in Kerala in India, a lower chance of pre-cancerous lesions was found among those with better socioeconomic conditions⁴⁷47 Hashibe M, Jacob BJ, Thomas G, Ramadas K, Mathew B, Sankaranarayanan R, Zhang ZF. Socioeconomic status, lifestyle factors and oral premalignant lesions. Oral Oncology 2003; 39(7):664-671.. The results presented in that study⁴⁷47 Hashibe M, Jacob BJ, Thomas G, Ramadas K, Mathew B, Sankaranarayanan R, Zhang ZF. Socioeconomic status, lifestyle factors and oral premalignant lesions. Oral Oncology 2003; 39(7):664-671. may be related to greater access to information regarding oral cancer prevention, as well as, a greater possibility of putting into practice such information among those with a greater per capita income. However, previous studies show that dentists are mostly concerned with ensuring that socio-economically disadvantaged individuals have access to health information because they assume that poor people are less informed¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57.,⁴⁷47 Hashibe M, Jacob BJ, Thomas G, Ramadas K, Mathew B, Sankaranarayanan R, Zhang ZF. Socioeconomic status, lifestyle factors and oral premalignant lesions. Oral Oncology 2003; 39(7):664-671.. Our findings suggest that, in Montes Claros, most of dentists do not consider low socioeconomic status to be a prerequisite for the provision of health-related information. In the context of health promotion, health education strategies that consider the socioeconomic conditions of the people are important in planning how the population will be approached regarding the prevention of oral cancer¹⁰10 Shanmugham JR, Zavras Athanasios I, Rosner B, Edward G. Alcohol-folate interactions in women's oral cancer risk: A prospective cohort study. Cancer Epidemiol Biomarkers Prev 2010; 19(10):2516-2524., considering that disadvantaged citizens, many of whom are elders, may have difficulty understanding, evaluating and applying the information provided²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.. In summary, a greater prevalence of access to information about the prevention of oral cancer among elders in Montes Claros is called for, especially considering that a majority of study participants presented unfavorable socioeconomic conditions that have been associated with the development of oral cancer¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57.,⁴⁷47 Hashibe M, Jacob BJ, Thomas G, Ramadas K, Mathew B, Sankaranarayanan R, Zhang ZF. Socioeconomic status, lifestyle factors and oral premalignant lesions. Oral Oncology 2003; 39(7):664-671..

Among the information that should be shared in efforts that aim to improve health literacy rates, the impact of habitual tobacco use stands out. Tobacco use is an important risk factor related to the occurrence of oral cancer⁷7 Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, Bernstein L, Schoenberg JB, Stemhagen A, Fraumeni Junior JF. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer Research 1988; 48(11):3282-3287.,³⁹39 Horowitz AM, Siriphant P, Sheikh A, Child, WL. Perspectives of Maryland dentists on oral cancer. JADA 2001; 132(1):65-72., however, the evaluation of the association between access to information regarding oral cancer prevention and this risk factor in cross-sectional studies is complex. If on one hand it is expected that the dentist is motivated to pass on this information, especially among those with risk behavior (greater access to information among tobacco users). On the other hand it is expected that the person who has access to information about risky behavior for their health behavior change by adopting healthier habits (access leads to a quit attempt, greater access to information among no tobacco users). Among elders in Montes Claros, access to information regarding oral cancer prevention was greater among those that were non-smokers, noting once again that for the purposes of this study, ex-smokers were included in the group of tobacco users, and, thus, the possibility that these individuals may have abandoned this habit, as a result of greater access to preventive information, cannot be disregarded. Additionally, current tobacco users may report a lack of access to preventive information as a defense mechanism, since changing habits is difficult and information alone may not be capable of changing habitual behaviors. Tobacco and alcohol users who have removable dental prostheses may present injuries in the oral mucosa or precancerous lesions. This observation is in accordance with the hypothesis that the recurring physical irritation of the oral mucosa contributes to the topical carcinogenic effect of tobacco in the mouth, which should be taken into consideration in the planning of strategies for the promotion of health and health education, especially in promoting preventive and curative dental services¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57.. Tobacco users may tend to be less concerned with their health as exhibited by not abandoning a harmful habit and this may suggest that they may be less concerned with obtaining an early diagnosis of oral cancer. On the other hand, tobacco users with high levels of health literacy that are not able to abandon this harmful habit, may be more concerned with early diagnosis of tobacco-related diseases. One study found that delays in the early diagnosis of this type of cancer were greater among those that did not use tobacco⁴⁸48 Pitiphat W, Diehl SR, Laskaris G, Cartsos V, Douglass CW, Zavras AI. Factors Associated with Delay in the Diagnosis of Oral Cancer. J Dent Res 2002; 81(3):192-197., observing therefore association between tobacco use and early diagnosis of oral cancer, which may be preceded by oral self-examination.

Despite the lack of studies that prove an association between oral self-examination and a reduction in rates of mortality and fatality due to oral cancer, in one randomized trial, it was found that these rates decrease when there is screening by health professionals trained in identifying suspect lesions for oral cancer, timely confirmation of such suspicions by pathological examinations and follow-up through immediate treatment¹⁴14 Sankaranarayanan R, Ramadas K, Thomas G, Muwonge R, Thara S, Mathew B, Rajan B Effect of screening on oral cancer mortality in Kerala, India: a cluster-randomized controlled trial. Lancet 2005; 365(9475):1927-1933.. The early diagnosis of oral cancer may occur during a regularly scheduled dental appointment or as a result of screenings and appointments sought out after the identification of suspect lesions during an oral self-examination. There are places where screening is not carried out and there are other places where such procedures are carried out periodically in various intervals of time. If everyone learned and carried out oral self-examinations, especially in between regularly scheduled dental appointments or screenings, the possibility of early diagnosis and treatment would be maximized. Furthermore, in places where screening is not a regular policy, or where this policy has not been deployed, and even when screening is part of regularly scheduled treatment, the practice of appropriate self-examination can minimize morbidity and mortality related to oral cancer. This situation is full of importance, as access to information regarding the prevention of oral cancer is associated with oral self-examination and follow-up through an oral examination by a health professional, and, thus, increases the odds of early diagnosis of oral cancer. The odds of having access to information regarding the prevention of oral cancer among those who carry out self-examinations was six times greater than that of those who do not carry out self-examinations, even after controlling for other variables. Among elders who carry out oral examinations, more than 70% confirm having access to information regarding oral cancer prevention. This suggests that the directions given were effective and may have generated changes in habits of self-care or reinforced healthy behaviors if healthy behaviors were adopted after gaining access to information on preventive practices. One should also consider the possibility of feedback in this association, since the identification of changes in the oral cavity during self-examination may lead people to seek information related to oral health.

Research carried out in Germany⁴⁹49 Klosa K, Wiltfang J, Wenz HJ, Koller M, Hertrampf K. Opinions and practices of dentists in oral cancer prevention and early detection in Northern Germany. Eur J Cancer Prev 2011; 20(4):313-319.and the United States⁵⁰50 Choi Y, Dodd V, Watson J, Tomar SL, Logan HL, Edwards H. Perspectives of African Americans and dentists concerning dentist-patient communication on oral cancer screening. Patient Educ Couns 2008; 71(1):41-51. shows that a majority of dentists agree that preventive exams for oral cancer are important, but less than half discuss this information about these issues with their patients. In Montes Claros, especially among dentists that don't work in the FHS, there is a need for improvements in the continuing education of health professionals, especially with respect to the importance of oral health literacy. There is also a need to increase health promotion and education actions related to the prevention and early diagnosis of oral cancer. Governmental dental care, particularly the care of seniors, needs to be reevaluated. There is a need to develop health policies that include actions of health promotion and education geared towards self-diagnosis and self-care, as well as preventive actions, maintenance and rehabilitation³⁷37 Silva SRC, Fernandes RAC. Autopercepção das condições de saúde bucal por idosos. Rev Saude Publica 2001; 35(4):349-355.. Furthermore, lack of insatisfaction with dental services may be associated with problems accessing preventive information on how to avoid dental problems⁵¹51 Martins AMEBL, Jardim LA, Souza JGS, Rodrigues CAQ, Ferreira RC, Pordeus IA. Is the negative evaluation of dental services among the Brazilian elderly population associated with the type of service? Rev Bras Epidemiol 2014; 17(1):71-90.. Contrary to our findings among elders in Montes Claros, in a prospective intervention study with people above the age of 40 in Italy, there was more knowledge in the group that was instructed on the prevention of oral cancer than in the control group, however, this knowledge did not lead to a significant increase in self-examination in the instructed group⁵²52 Petti S, Scully C. Oral cancer knowledge and awareness: Primary and secondary effects of an information leaflet. Oral Oncology 2007; 43(4):408-415.. This suggests that the intervention applied in Italy may not have considered issues beyond access to information that are posed by the health literacy approach²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80.,³⁰30 Wallerstein N, Bernstein E. Empowerment education: Freire's ideas adapted to health education. Health Educ Q 1988; 15(4):379-394., or perhaps that for those participants other issues are more important than changing habits in order to prevent diseases. Cross-sectional studies on Brazil also demonstrate that, despite having knowledge about oral cancer and about risk factors, many people continue to practice habits harmful to health and do not conduct self-examinations³⁵35 Souza LRB, Ferraz KD, Pereira NS, Martins MV. Conhecimento acerca do câncer bucal e atitudes frente à sua etiologia e prevenção em um grupo de horticultores de Teresina (PI). Rev Bras Cancerol 2012; 58(1):31-39.,⁵³53 Dias GF, Fernandes DR, Mestriner SF, Júnior WM. Autocuidados na prevenção do câncer bucal. Rev Científica da Universidade de Franca 2005; 5(1/6):14-20.. As such, there is a need for the use and evaluation of diverse strategies, that consider the issues proposed in the theoretical model of health literacy²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80., among these is the need to empowerment patients³⁰30 Wallerstein N, Bernstein E. Empowerment education: Freire's ideas adapted to health education. Health Educ Q 1988; 15(4):379-394., promoting the acquisition of knowledge and practices that are aimed at controlling health problems.

The odds of access to preventive information regarding oral cancer were greater among those that did not report discomfort in the mouth, head or neck. There is a possibility for feedback in this association, as discomfort might lead a person to seek out information. Likewise, such information might increase the level of health literacy of individuals who can then identify a non-symptomatic lesion as a discomfort. Longitudinal studies may better elucidate this association, as the presence of discomfort should stimulate a greater concern on the part of health professionals to provide preventive information. An association between recurring oral ulcers due to poorly adjusted dentures and oral cancer has been proven¹¹11 Vaccarezza GF, Antunes JL, Michaluart-Júnior P. Recurrent sores by ill-fitting dentures and intra-oral squamous cell carcinoma in smokers. J Public Health Dent 2010; 70(1):52-57.,⁵⁴54 Marques LA, Eluf-Neto J, Figueiredo RA, Góis-Filho JF, Kowalski LP, Carvalho MB, Abrahão M, Wünsch-Filho V. Oral health, hygiene practices and oral cancer. Rev Saude Publica 2008; 42(3):471-479., further suggesting the importance of access to information related to oral discomfort and oral cancer.

It is probable that additional unfavorable conditions are present among those that have less access to health-related information, as access to this information was less among those with less income, among those that presented worse health behaviors and among those that reported the presence of discomfort. A previous study confirmed that individuals with less socioeconomic status were less likely to use dental services, and, when they did use such services, they were less likely to receive more conservative treatment, less information was received and they reported less understanding of treatments that could prevent the loss of teeth⁵⁵55 Gilbert GH, Duncan RP, Shelton BJ. Social Determinants of Tooth Loss. Health Serv Res 2003; 38(6 Pt 2):1843-1862.. These results suggest a paradox related to inequality in the oral health care of the elderly. On one hand, this indicates inequality, as less access was found to be associated with lower income. On the other hand, greater access was observed among residents of homes registered with the FHS, that are possibly those with less income, since the publicly funded services provided by the FHS should be a priority among those most in need of free health care.

Increasing health literacy may be a promising approach to educational programs and strategies developed and applied by health professionals to prevent disease and promote health by encouraging people to adapt healthy practices and routine preventive self-care. However, the adoption of the theories proposed in the model of Sørensen et al.²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80. presents challenges that have not yet been explored. In the context of health literacy, the specific cognitive qualities that are attained depend on both the quality of the information provided²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80. and the individual motivation and conscience of each individual³⁰30 Wallerstein N, Bernstein E. Empowerment education: Freire's ideas adapted to health education. Health Educ Q 1988; 15(4):379-394..

Some variables considered in the theoretical model proposed by Sorensen et al.²⁰20 Sørensen K, Van den Broucke S, Fullam J, Doyle G, Pelikan J, Slonska Z, Brand H. Health literacy and public health: a systematic review and integration of definitions and models. BMC Public Health 2012; 12:80. were not evaluated among elders in Montes Claros. On the other hand, this study followed the methodological rigor required in a cross-sectional study: planning sample, calibration and statistical analysis with correction for design effect.

Conclusions

A majority of the elders had access to information on how to prevent oral cancer, the prevalence was greater among residents registered with the FHS. There is a need to increase the provision of this preventive information by oral healthcare professionals, especially among those that did not live in registered residences, among those that are socially disadvantaged, among tobacco users, among those who do not conduct self-examinations and among those that report discomfort in the mouth, head and neck. Practical implementation of acquired knowledge is recommended, in the context of the adopted theoretical model of health literacy, regarding the use of tobacco, the importance of oral self-examination and the existence of a possible association between oral cancer and the presence of discomfort in the mouth. It is also important to note associations between access to information regarding oral cancer prevention and the use of tobacco, the implementation of oral self-examinations and reports of discomfort in the mouth, all of which should be evaluated considering the possibility of feedback mechanisms.

Acknowledgements

The Project was funded by FAPEMIG and the Mayor's Office of Montes Claros and received logistical support from the State University of Montes Claros – Unimontes, the Dental School of UFMG and the Unified Colleges of Northern Minas Gerais – FUNORTE. AMEBL Martins is a post-doctorate fellow with funding from the CNPQ; IA Pordeus, EF Ferreira and SM Barreto are productivity fellows with funding from the CNPQ. The authors would like to acknowledge the contributions of Dr. Kimberly Marie Jones (SOEBRAS) in her translation of this manuscript from the original version in Portuguese.

References

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