Educação Nutricional: uma Lacuna na Formação Médica Nutritional Education: a Gap in Medical Training

Introduction: The role of nutrition in medicine has changed from a passive function, from an adjuvant therapy, to a proactive and sophisticated therapy that prevents various health problems and changes the natural history of the disease. Recent studies show up that medical education does not sufficiently and efficiently address the patient’s nutritional aspects, thus training physicians who are not confident in providing nutritional care to their patients. This study aimed to analyze and describe scientific studies that have evaluated nutrition education in medical schools, seeking within this context to find nutrition topics important for undergraduate medical education. Methods: This research was conducted through a cross-sectional, descriptive, scoping review after searching for synonyms using MeSH (Medical Subject Headings) and DeCS (Health Sciences Descriptors) tools. Results: We initially found 1.057 publications that underwent sequential screening until reaching a total of 16 articles, which achieved the scope of this research. Most articles are from the United States of America (50%), assessed a total of 860 medical students and 243 medical schools using different approaches regarding the teaching of nutrition. Final considerations: In this review, we have shown that despite several studies ratifying the well-established association between nutrition and prevention/treatment of diseases that require outpatient care, or at the hospital level, nutrition education in undergraduate medical school has not accompanied this evidence and, for many years, the subject has been underestimated. In Brazil, no studies were found on this topic with the used descriptors. –


INTRODUCTION
Human nutrition involves cultural, psychological, educational, social, political and economic aspects. Recently, with advances in food technologies and zootechnics, the food scenario has become even more complex and, without a doubt, has an impact on the health of the population 1 .
Several authors have reported the impact that food has on the healthdisease process 2,3-6 . A study published in 2016 reported atherosclerotic cardiovascular disease as the main cause of preventable death in the United States of America (USA) and that dietary factors have shown to reduce the morbidity and mortality of this type of pathology 7 . Other chronic pathologies, such as type 2 diabetes and high blood pressure are also strongly influenced by nutritional practices 8 .
Hospital malnutrition is also a critical point. Malnourished patients remain hospitalized for longer periods, suffer from impaired respiratory and cardiac functions, decreased immune function and higher rates of morbidity and mortality 9 .
Regarding malnourished patients admitted to the intensive care unit (ICU), for instance, there is an increase in hospital length of stay, prolonged mechanical ventilation and higher mortality rates 10 . However, this remains a topic that is not even part of the medical undergraduate curriculum 1,11 .
Nowadays, the prevalence of malnutrition in hospitals varies according to the authors, from 20 to 60% 12,13 . Evidence shows that approximately 50% of patients are already experiencing some degree of malnutrition at the time of hospitalization, and at the end of the hospital length of stay, the performed nutritional assessment shows that this rate increases to 62% 5,13 . Han et al. (2016) 14 evaluated the knowledge and perception of nutrition in resident physicians acting in primary care and showed that 86% did not feel adequately trained to discuss nutrition with patients. However, nutrition is inseparable from all other therapeutic forms, whether clinical or surgical 15 . In spite of that, the doctors themselves report feeling unable to promote nutritional care 16,17 .
Some resident physicians recognize that there is a lack of training regarding this aspect in their residency programs 18,19 . Devries et al. (2017) 18 , in their study, found that 31% of cardiologists and 21% of cardiology residents do not remember having been taught subjects related to nutrition in their undergraduate courses, and 90% during their residency in cardiology.
Among the factors pointed out as causes of weakness in medical training, are a very dense and extensive curriculum, the difficulty in finding specialist professors in the area and defend the inclusion of these subjects, and the lack of a consensus on which nutritional issues should be addressed 16,20 .
In 1977, a survey was published in which only 19% of medical schools in the United States had a course on nutrition. A study carried out in 1985 with 45 medical schools in the USA showed that 60% of schools devoted less than 20 hours to nutritional education and 20% less than 10 hours to the subject 21 .
Moreover, it is observed that medical schools that include some nutritional content usually do so in the first years of medical school. The lack of clinical applicability of the subject tends to make students unaware of the subject importance 22,23 .
This lack of training in nutritional care is evident in the hospital environment 5,6 . Ferreira et al. 24 , in 2017, assessed the knowledge of doctors from different clinics on parenteral nutritional therapy (PNT) and found that 50% of them did not feel prepared to work with parenteral nutrition. Diet is the first item of the medical prescription in the hospital and it is a complex one, because it shows variations regarding the route of administration, presentation, composition and fractioning 25 .
Considering that the most accepted hypothesis for this medical insecurity in prescribing the diet is the insufficient teaching of this subject in the curriculum of the undergraduate medical course, this work aims to investigate the teaching of nutrition in medical schools according to the literature.

METHODOLOGY
This cross-sectional, descriptive study was carried out at Universidade do Estado do Pará with a convenience sample, using a scoping review, based on the search for accessible, indexed and readily available studies in the databases hosted at PubMed (US National Library of Medicine/ National Institute of Health), Eric (Education Resources Information Center), BIREME (Latin American and Caribbean Health Sciences Information Center) and Google Scholar, starting 10 years before July 31, 2019, the last day of data collection. After searching for synonyms using the MeSH (Medical Subject Headings) and DeCS (Health Sciences Descriptors) terms, the descriptors were defined. To improve the accuracy of the search for relevant articles, the following filters were applied: 10 years of publication (2009 -2019), human subjects, and English, Portuguese and Spanish languages.
As for the formulas used for the study and their respective Boolean operators, they were carried out in three different ways: :"Nutrition" AND "Medical Education" OR "Medical School" AND "Curriculum" AND "Nutrition Science" AND "Nutrition Therapy", published in the last 10 years, involving human beings, written in English, Portuguese and Spanish; "Nutrition" AND "Medical Education" OR "Medical School" AND "Curriculum" AND "Nutrition Science" AND "Nutrition Therapy", with a 10-year time filter and "Nutrição" AND "Educação Médica" OR "Escolas Médicas" AND "Currículo" AND "Ciências Nutricionais" AND "Terapia Nutricional".
The articles were selected based on the pool of articles obtained with the descriptors defined by the research. Some words and/or terms were defined as excluding, as they deviate from the study objective, such as: "veterinary medicine", "early childhood education", "pre-school nutrition" and "education policy".
Studies that did not evaluate the population of interest or did not analyze at least one of the defined outcomes, were excluded from the review.
The outcomes defined for this research were: • Focus on Medical Schools: Evaluation of nutrition teaching in medical schools; • Focus on the student: Perception and/or evaluation of the medical student regarding nutritional education; • Relevant topics: Topics in nutrition education most frequently recommended to be part of the medical curriculum.

Statistical analysis
The collected data were tabulated in the Microsoft Excel program spreadsheets, treated by descriptive statistical methods based on the following information collected from the studies: study design, studied sample, study site, performed interventions and reported outcomes.

RESULTS
The total number of articles found in the chosen databases comprised 1057 articles referenced up to July 31, 2019 Regarding the distribution of these manuscripts by databases, when the formula "Nutrition" AND "Medical Education" OR "Medical School" AND "Curriculum" AND "Nutrition Science" AND "Nutrition Therapy" was applied, 1012 manuscripts were collected, only from the PUBMED platform, with no findings in the others. On the other hand, when the formula "Nutrition" AND "Medical Education" OR "Medical School" AND "Curriculum" AND "Nutrition Science" AND "Nutrition Therapy" was applied, 16 studies were identified in the BIREME platform and 28 in the Google Scholar platform, totaling 44 manuscripts for this operation. Finally, when the search was carried with the formula "Nutrição" AND "Educação Médica" OR "Escolas Médicas" AND "Currículo" AND "Ciências Nutricionais" AND "Terapia Nutricional", no work was identified in any of the databases.
The synthesis of this selection can be seen in the flowchart of Figure 1.

Characteristics of included studies
The search resulted in studies from 7 countries and 3 multicenter studies (1 Global, 1 European, 1 African), with 50% of the studies (8) carried out in the United States.
After the screening and reading of the full articles, they were classified according to their research design. Of the total of 16 articles, the majority, 7 (43.75%), were cross-sectional, and the second most frequent type of study was the "before and after" study, represented by 3 articles (18.75%) (Graphic 1).
It is noteworthy that some studies had more than one outcome. Among the outcomes defined and analyzed in the studies that were part of the research scope are: • Outcome 1: Outcome found in 31.25% of the evaluated studies.
Focus on medical schools. Of the 243 evaluated medical schools, more than 50% had less than 25 hours of nutritional training in their curriculum. • Outcome 2: Outcome found in 50% of the evaluated studies.
Focus on the Student. Of the 860 students questioned during the research of the different articles, more than half reported that they did not feel confident in handling issues related to nutrition.

Synthesis of studies
The selection of the 16 articles used in this research, with their main characteristics, is shown in Table 1.

DISCUSSION
The role of nutrition in medicine has changed from a passive function to a proactive and complex therapy, which prevents numerous health problems and has changed the natural history of the disease 30 . Even so, the most prevalent causes of morbidity and mortality in developed and developing countries are directly or indirectly related to the diet 2 .
Continue...  In the hospital environment, the problem is a latent one. A national study, involving 4,000 patients and published in 2001, showed a hospital malnutrition rate of 48%. After more than 15 years, a meta-analysis published in 2017, with a sample of 29,474 patients from 12 countries in Latin America, including 57.7% Brazilian patients, showed an even higher hospital malnutrition rate of up to 60% 31,32 .

Denise Bitar Vasconcelos Villacorta et al.
Mass education is understood as the best way to modify the nutritional habits that occur with the disease process. This fact is clear in Law n. 13.666/2018, which makes food and nutrition education mandatory in the school curricula of elementary and high school students from public and private education institutions throughout Brazil 33 .
Paradoxically, there are no regulations regarding how much nutritional knowledge a doctor in training has to obtain for it to become a modifying agent of this reality. And the lack of studies published in Brazil on nutritional education in medical schools suggests that the discussion regarding this fragility has not even started. A recent, randomized and controlled study demonstrated the potential positive impact on patients who participated in a nutritional education course taught by medical students 34 .
Despite the growing importance of the nutritional aspects in the therapeutic management of the patient, and the fact that the physician is in the front line to raise awareness about healthier eating habits, this competence has not been attained by schools that train medical professionals around the world, so much that a global study led by ESPEN (European Society for Clinical Nutrition and Metabolism), with representation from 57 countries, demonstrated that nutritional education in medical courses is heterogeneous and insufficient 2,11 .
A study carried out in Australia with medical students found that 99% of the students considered nutritional education important and the degree of confidence they mentioned in managing nutritional care ranged between 12 and 64 35 .
The concern with nutritional education in schools is not a recent phenomenon outside Brazil. In 1985, the National Academy of Sciences (NAS), through its Committee on Nutrition in Medical Education, presented to society the work entitled 'Nutrition Education in US Medical Schools' , considered a milestone in medical literature on this topic 36 .
Driven by this study, the Nutrition Academic Award (NAA) was launched, which promoted the integration of nutritional content in the medical curriculum and produced guidelines on how to achieve this integration. However, in 2005, resources for this program were suspended, limiting its impact to only 21 American medical schools. After 3 decades of the national assessment organized by the NAS, nutrition in medical schools is still an issue to be resolved 21 .
The relevance of the topic for the American public health is clear when one considers that the main health problems in North Americans are obesity, cardiovascular diseases, diabetes and cancer, which are directly related to dietary factors and lifestyle habits and, therefore, potentially preventable 9 .
While international authors have been discussing the deficiency in nutritional education in medical schools and residency programs for over 30 years, proposing specific actions and conferences for this topic 37 , no studies were found that were carried out in Brazil among the researched literature using the descriptor formula. This is a matter of concern, since in Brazil, recent surveys have shown that more than 50% of the population is overweight and that the prevalence of hospital malnutrition can affect up to 60% of hospitalized patients 38,39 .
Quaresma et al 40 , in 2019, evaluated on-duty doctors at an intensive care unit in a public hospital in Brazil and found that 65% of the respondents have difficulty recognizing patients at nutritional risk.
Among the described barriers for advancing the teaching of nutrition in medical schools are the low clinical applicability, the perception that nutritional care is not the doctor' s responsibility, lack of knowledge of the medical school in clinical nutrition, lack of motivation by professors in teaching the subject, and an overcrowded curriculum, among others 17 .
In the last decade (2009-2019), the focus of this research, it was identified that the majority (43.75%) of the selected studies were crosssectional ones. This suggests that medical education managers seek to increase the discussion on the topic, initially working to define a situational diagnosis and thus lead the process to more vigorous actions.
Other studies were of the 'before and after' type, 18.75%, having as interventions courses dedicated to clinical nutrition that were not part of the regular medical undergraduate curriculum. It is perfectly understandable that a curricular change is not a simple task to achieve, since more advanced classes, for instance, would not benefit from the curricular insertions only in the first semesters of the course.
Although old, the minimum recommendation of 25 hours of nutrition education in the medical curriculum is the starting point and the reference for most interventions. Nutrition courses have been described in the following formats: only 5 lectures; others with a workload of 13 hours; 2 weeks in length and also those that are included for 3 years in the undergraduate clinical cycle 34,[41][42][43] .
Regarding the population evaluated in each selected study, two different populations were found: the medical school and the student. The medical schools were evaluated through questionnaires sent to the institutions' coordinators and managers, a fact that may constitute a selection bias, since the person responsible for answering the form was the one with the most interest in offering a more "adequate" picture than the actual reality.
Of the 243 schools evaluated in the several added studies, in 40 of them it was not possible to identify how many hours of nutritional education were administered. Among those of which workload was possible to be evaluated, more than 50% offered less than the minimum of 25 hours recommended by the National Academy of Sciences 36 , ranging from 4.2 to 19.6 hours. When one considers that a medical course has a minimum workload of 7,200 hours, it is evident that the time for the teaching of nutrition is negligible.
The National Curricular Guidelines (NCG) of the medical course, published in 2014, practically do not contain any line on the nutritional care of the patient. In subsection I, which deals with the Attention to Individual Health Needs, Article 13, which comments on therapeutic plans, mentions as one of its objectives the "establishment, based on clinical-epidemiological reasoning in specific contexts, of therapeutic plans contemplating the dimensions of promotion, prevention, treatment and rehabilitation". In this context, planning the therapeutic intervention means being prepared for all items such as dietary care, as it can constitute both prevention and treatment of some pathologies 44 .
Recently, Neumann et al (2019) 45 adapted and improved the competencies for medical internship students to the Portuguese language, based on the assessment of 15 EPAs (Entrustable Professional Activities). We highlight 2 EPAs that are strongly related to nutritional education: To collaborate as a member of a multiprofessional team, and; educating patients: disease management, health promotion and preventive medicine.
The medical student' s assessment was similar to that of medical schools, using questionnaires of perception and, sometimes, of knowledge; the students were selected and assessed by researchers from their own educational institution, favoring evaluation bias.
Of the 860 students questioned in the selected studies, more than half reported not feeling prepared to handle patient nutritional care. Frantz et al. (2016) 46 performed a survey of 122 medical school internship students, where 71% reported feeling inadequately prepared to practice clinical nutrition.
In an attempt to solve this deficiency, some courses introduced nutrition based on basic topics, such as the study of macro and micronutrients, energy expenditure and nutritional needs in the first two years of the course, called pre-clinics 42 . However, with the emergence of evidence that chronic diseases such as cardiovascular diseases, diabetes, hypertension and cancer are directly influenced by diet, and that, therefore, medical treatment was necessary to treat them, the subject started to be included in the first four years of the medical course, with a more clinical focus in the third and fourth years, seeking to develop skills in nutritional management of patients and using problem-based learning methods 47 .
In this study, 50% of the articles presented outcome n. 3, related to the most frequently mentioned topics and considered more relevant to be part of the medical curriculum. The subjects were congregated in three groups.
The topics of basic nutrition were mentioned by all articles, since this knowledge is essential for the understanding of the pathophysiology of nutritional disorders, thus making clinical applicability feasible. Among them, the knowledge about macro and micronutrients, nutritional needs, nutritional assessment and energy expenditure stands out. Data from VIGITEL/Ministry of Health published in 2017 showed that only 24.9% to 49.8% of Brazilians regularly consume fruits and vegetables, information that suggests the population' s inadequate awareness of the main healthy sources of macro and micronutrients 48 .
The nutritional management of chronic diseases influenced by the diet was also frequently mentioned. The examples include cardiovascular diseases, which constitute one of the main causes of death worldwide; hypertension, directly related to the consumption of salt and processed foods; diabetes, which has as its main support an adequate consumption of carbohydrates; some types of cancer, which can be triggered by oncogenic factors present in food; and finally, obesity, which is directly influenced by the population' s dietary pattern 17,49,50 .
Finally, a topic that took on greater proportions in the 1970s, when the first publications on hospital malnutrition appeared, and continues to rise to the present day, was nutritional therapy for hospitalized patients. This topic deserves to be highlighted, as it involves the care of patients in borderline pathological situations. And unlike other practice environments, the physician is the trigger for nutritional care through its indication and prescription. It requires specific knowledge, considering the types of nutritional therapies, such as enteral and parenteral nutrition, which in addition to significantly higher costs to the hospital, are permeated by greater risks and possible complications during its implementation process.
Aiming to regulate the use of this type of therapy, norms were created in Brazil by the Ministry of Health that regulate the entire process of using enteral and parenteral nutrition, from its indication to its administration, going through quality controls, transportation and handling 51,52 .

FINAL CONSIDERATIONS
In this scope review, we show that despite the several studies endorsing the well-established association of nutrition, both in the prevention and treatment of chronic diseases that require outpatient care, as in pathologies that depend on therapies at the hospital level, nutritional education in medical training has not followed this evidence and, for many years, the subject has been underestimated. Currently, it has been increasingly discussed outside Brazil.
The absence of Brazilian research in this area makes it possible to develop new studies aiming to diagnose the national reality and later search for strategies consistent with the identified context. At the moment, as in other countries, extracurricular courses can be an alternative to provide the knowledge and skills that are not being delivered by medical schools.