Consumption of foods according to their degree of processing in patients with established atherosclerosis disease

Este trabajo fue recibido el 13 de diciembre de 2018. Aceptado con modificaciones: 22 de agosto de 2019. Aceptado para ser publicado: 28 de octubre de 2019. ABSTRACT The aim of the present study was to analyze the consumption of foods according to their degree of processing in patients with established atherosclerosis disease. A cross-sectional study was performed with 74 patients of the BALANCE Program trial, a randomized, multicenter and national clinical trial occurring in Brazil. Body weight, height, waist circumference, blood pressure, lipid profile and fasting glucose were collected. Food intake was assessed with 24-h dietary recall. Consumption of nutrients was analyzed in quartiles of consumption of ultra-processed foods and their differences were obtained by one-way ANOVA with Tukey’s post hoc test. Half of consumed calories came from natural or minimally processed foods (50.9%), followed by ultra-processed food products (35.1%). The largest contribution in calories came from meats, cereals/roots/tubers, breads, and sweets. No significant difference was found in quartiles of consumption of ultra-processed foods. In this sample, consumption of processed/ultra-processed food was almost the same as natural/minimally processed foods. Preferential consumption of unprocessed/minimally processed foods should be more widely advocated by health professionals.


INTRODUCTION
Cardiovascular diseases (CVDs) are a major cause of death worldwide. In 2012, more than 17 million people died from CVDs, which represented 31% of all deaths 1 . The prevention of this group of pathologies must include proper control of risk factors such as improper eating, obesity, physical inactivity and harmful consumption of alcohol 1,2 .
Dietary factors, such as consumption of high amounts of salt and fat (particularly saturated and trans fatty acids), and an inadequate intake of fruits and vegetables, increase the risk of CVDs 1,2 . Therefore, governmental concern has increased in recent years, resulting in regulatory policies that aim to reduce fats and sodium use by the food industry, potentially contributing to a decrease in the consumption of these nutrients in the population 2 .
In 2014, new Dietary Guidelines were published in Brazil 3 . This edition contains a novel food classification, which evaluates the extent and purpose of the industrial processing applied to foodstuffs and divides foods into four groups: natural or minimally processed, processed culinary ingredients, processed foods and ultra-processed food products 3 . The ultra-processed group stands out for its unfavorable nutritional profile, due to high energy density and high levels of total fat, saturated fat, trans fat, free sugars and sodium 4,5 . Nevertheless, these products frequently have attributes that stimulate their consumption, such as high palatability, large portion sizes, durability, easy transport, being "ready-to-eat" and wide marketing and advertising 3 .
According to the Brazilian Ministry of Health 6 , in 2017, approximately 27% of deaths in Brazil were due to CVD. However, Moreira et al 7 estimated that 29% of CVD deaths could be avoidead if saturated fat, trans-fat, salt and added sugar were reduced from processed culinary ingredients and ultra-processed foods in the Brazilian diet.
Considering the potential association between the consumption of ultra-processed foods and CVDs, and the fundamental role of lifestyle adjustments, including a healthy diet for secondary prevention of atherothrombotic events, the objective of the present study was to analyze the consumption of foods, according to their degree of processing, in a sample of patients with established atherosclerosis disease, participants the Brazilian Cardioprotective Nutritional Program Trial (BALANCE Program Trial).

MATERIALS AND METHODS
A cross-sectional study was conducted. This work represents a subanalysis of the BALANCE Program Trial, a randomized, multicenter and national clinical trial, conducted by the Hospital do Coração (HCor) in partnership with the Unified Health System (SUS) (PROADI-SUS) of the Ministry of Health, to reduce events and risk factors inn secondary prevention for CVD. The pilot and protocol studies have been published previously 8,9 . The data presented were collected from patients in one of the participating centers, Pelotas-RS, at baseline. The study included patients aged 45 years or older, with evidence of established atherosclerosis disease in the preceding 10 years. a) coronary disease (defined by previous myocardial infarction, stable or unstable angina, history of atherosclerotic stenosis ≥70% of the diameter of any coronary artery on conventional or computed tomographic (CT) coronary angiography, or history of angioplasty, stenting, or coronary artery bypass surgery); (b) previous stroke; (c) peripheral vascular disease (ankle/arm ratio <0.9 of systolic blood pressure in either leg at rest, angiography or Doppler demonstrating >70% stenosis in a cardiac artery, intermittent claudication, vascular surgery for atherosclerotic disease, amputation due to atherosclerotic disease, or aortic aneurysm). The exclusion criteria were: neurocognitive or psychiatric conditions; life expectancy less than 6 months; pregnancy or lactation; liver failure with a history of encephalopathy or anasarca; renal failure with indication for dialysis; congestive heart failure; previous organ transplantation; wheelchair use; or any restrictions to receiving an oral diet. Eligible subjects were selected from cardiology outpatient clinic and teaching hospital, in the period of August 2013 to December 2014. The study was approved by the local ethics committee (nº 287.722) and all participants provided written informed consent prior to inclusion.
Body weight and height were measured using a digital calibrated scale with a coupled stadiometer (Filizola ® ), with an accuracy of 0.1 kg and 0.1 cm, respectively. Waist circumference was obtained by inelastic tape measure, at midway between the lowest rib and the iliac crest using an anthropometric tape, with an accuracy of 0.1 cm. Body mass index (BMI) was calculated from weight (kg) divided by squared height (m) and categorized in groups according to World Health Organization criteria for subjects under 60 years (underweight, BMI<18.5kg/ m²; normal weight, BMI18.5 to 24.9kg/m²; overweight, 25 to 29.9 kg/m²; and obesity, BMI>30 kg/m²) or Pan American Health Organization criteria for the elderly (underweight, BMI<23kg/m²; normal weight, BMI 23 to 27.9 kg/m²; overweight, BMI 28 to 29.9 kg/m²; and obesity, BMI>30 kg/m²) 10,11 .
Blood pressure was assessed using the auscultatory method. Total cholesterol, HDL cholesterol, triglycerides and glucose were determined by enzymatic colorimetric dry chemistry method (Ortho-Clinical Diagnostics VITROS 5.1), in venous blood, and LDL cholesterol was estimated using the Friedewald equation 12 . Clinical history was collected from patient records and complemented by interview when necessary.
Food intake was assessed with one 24-h dietary recall per patient, performed by trained dietitians. The subjects described their average portion sizes for food items in terms of household measurements, the standard weights of food items and validated food portion photographs of known weights. To quantify energy intake, data were entered into the Nutriquanti ® diet system, an online computer program that is based on the Brazilian food database. All cited foods in the 24-h dietary recalls were classified according to the new food classification system proposed by Brazilian Dietary Guidelines 3 : natural or minimally processed foods, processed culinary ingredients, processed foods and ultraprocessed food products.
Natural foods are obtained directly from plants or animals and do not undergo any alteration following their removal from nature, and minimally processed are natural foods that have been submitted to cleaning, removal of inedible or unwanted parts, fractioning, grinding, drying, fermentation, pasteurisation, cooling, freezing, or other processes that may subtract part of the food but do not add oils, fats, sugar, salt or other substances (e.g. meat, milk, eggs, grains, legumes, and fruits). Processed culinary ingredients are products extracted from natural foods or from nature by processes such as pressing, grinding, crushing, pulverising, and refining (e.g. vegetable oils, butter, sugar and salt). Processed foods are products manufactured by industry with the use of salt, sugar, oil or other substances added to natural or minimally processed foods (canned vegetables, fruits in sugar, cheeses and breads made of wheat µour, yeast, water, and salt). Ultra-processed foods are industrial formulations made entirely or mostly from substances extracted from foods, derived from food constituents or synthesised in laboratories from food substrates or other organic sources (e.g. biscuits, chocolates, chips and soft drinks) 3 .
Economic level were categorized according to the Brazilian Criteria of Economic Classification of the Brazilian Research Institute in A, B, C, D and E 13 . Education was evaluated by years of study in the following way: low education level, elementary school (complete or incomplete), high school (complete or incomplete) and college (complete or incomplete).
Continuous variables were expressed as the mean ± standard error or medians and interquartile ranges, depending on their normality, and categorical data were expressed with frequencies. Consumption of micro and macronutrients was analyzed in quartiles of relative contribution of ultraprocessed foods to total energy. Differences between quartiles were obtained by one-way ANOVA with Tukey's HSD post hoc test. All analyses were carried out using GraphPad ® Prism 5.

RESULTS
The sample consisted of 74 subjects. As shown in  Table 1). The mean daily energy consumption was 1,429 kcal. Roughly half of calories came from natural or minimally processed foods (50.9%), followed by ultra-processed food products (35.1%), processed foods (11.1%) and processed culinary ingredients (2.9%). The foods that most contributed in calories can be seen in table 2. The largest contribution in calories came from meats and cereals/roots/tubers, both from the group of minimally processed foods. Next, from the processed food group, came bread, followed by sweets and biscuits, both from the ultra-processed food group.
The consumption of nutrients and biochemical parameters distributed in quartiles of ultra-processed intake are presented in table 3. No significant difference was found.

DISCUSSION
Consumption of ultra-processed products has significantly increased in the Brazilian diet, as seen in metropolitan areas since the 1980s and confirmed at a national level in the 2000s 14 . A similar increase has also been observed in Sweden 15 and Canada 16 . In our sample of patients with established atherosclerotic disease, we found a high contribution of ultra-processed foods to total caloric intake.
Obesity presented a high prevalence and the mean of waist circumference was elevated. Previous studies associated ultra-processed products consumption with the risk of metabolic syndrome in adolescents 17 , while a dietary pattern high in fruit and dairy and low in white bread, processed meat, margarine and soft drinks may help prevent abdominal fat accumulation in adults 18 . In addition, people with high consumption of ultra-processed foods had a significantly higher BMI and higher odds of being obese, compared with those with the lowest consumption 19,20 .
The majority of our sample (60.8%) presented dyslipidemia with low levels of HDL cholesterol, but this profile was not significantly associated with baseline ultra-processed consumption. Importantly, patients in our sample received guideline-recommended therapy for CVD disease, including statins in 96% of cases, and that may have influenced the results of this study. Corroborating these findings, Stewart et al. 21 , evaluated more than 15,000 patients with stable coronary heart disease and did not observe an association between LDL and HDL cholesterol and the Western dietary pattern that includes consumption of refined grains, sweets, fried foods and sugared drinks. Authors also believe that the use of preventive medications may decrease the ability to detect modest effects of diet on these risk factors. In our study, mean daily energy consumption was 1,430 kcal. About half of calories came from natural or minimally processed foods, followed by ultra-processed food products. Louzada et al. 20 , studying more than 30,000 adults and adolescents, found a similar consumption of ultra-processed foods (30%). However, other studies exhibit different results.
For example, one study with 32,898 Brazilians (aged 10 years or older) identified that natural or minimally processed foods contributed with approximately 70% of the calories 22 , while, a cohort study with 4,202 young adults in the city of Pelotas-Brazil, showed a relatively higher intake of ultraprocessed foods (51.2% of total calories) 23 . Patients in our study belong to a different demographic stratum (older and lower socioeconomic status), and already had established CVD, which may explain the different pattern of consumption as compared to the cited studies. These results demonstrate the need for more studies using different age groups, as this may influence food consumption choices. In Canada, over 60% of dietary energy came from ultra-processed products and the average diet exceeded WHO upper limits for fat, saturated fat, free sugars and sodium density, with less fiber than recommended 5 . Highly processed foods contributed 61% of mean energy intake in Spain, and 78-79% in the Netherlands and Germany 24 . A recent study performed in a Brazilian urban area described factors associated with preferential acquisition of minimally processed foods: the habit of buying fruits and vegetables at farmer´s markets or group-specific markets, walking as the principal means of transportation to buy food, and the perception of availability of fresh fruits and vegetables in the neighborhood 25 .
In a previous study, increased consumption of ultra-processed foods was positively correlated with the consumption of fat, cholesterol, sodium, iron, calcium, and calories, and negatively correlated with the consumption of carbohydrates, protein, and dietary fiber; the main source of ultra-processed food were sweets, breads and snacks 23 .
In our sample, we evaluated all food processing groups and we analyzed impact on total caloric intake. The major contribution in calories came from natural or minimally processed foods, mainly by meats and cereals/roots/tubers, followed by processed (breads) and ultra-processed foods (sweets). Overall, in the Brazilian diet, rice and beans represent about 25% of the energy consumed throughout the day, followed by red meat (9.3% of total energy), fruits (6.9%), and cereals other than rice (5.9%) and, among ultraprocessed foods, the top ones are industrialized breads (9.2%), pizzas, hamburgers and sandwiches (4.7%), and cakes and cookies (3.0%) 20 . Although we did not find a difference between quartiles of ultra processed food intake, patients in the highest quartile did not reach the recommendations for most nutrients, more  26,27,28,29,30 . This inadequacy in the consumption of nutrients involved in the development of CVD shows the importance of controlling the intake of ultra-processed foods for better secondary prevention. The latest edition of the Dietary Guidelines for the Brazilian Population advises that natural or minimally processed foods should be the basis of diet. However, it does not indicate a referential value. Thus, further studies are needed in order to establish an appropriate consumption value of foods according to their degree of processing. In our study, close to half of dietary calories came from natural or minimally processed foods. However, as exposed before, the diet of our sample was not nutritionally adequate.
There are some limitations of our study. The dietary survey was not designed specifically to classify foods according to the characteristics of industrial processing, and this could limit the ability to detect associations and complicate classification of some preparations into groups. In addition, 24h recall can underestimate real portions, a characteristic intrinsic of this instrument. Recall was performed for only one day and thus may not reflect habitual consumption. Furthermore, we do not know if patients in our study had received nutritional recommendations after the cardiovascular event, reflected in a healthier diet, detected in our analysis.
To our knowledge, this is the first study to address the relative contribution of foods according to their degree of processing in patients with atherosclerotic disease. Larger studies with the power to investigate the association of this novel food classification system with cardiovascular events could bring important contributions to our understanding of the role of dietary counseling in the treatment of atherosclerotic diseases.

CONCLUSION
In this sample of patients with established atherosclerotic disease, consumption of processed/ultra-processed food was almost the same as natural/minimally processed. Preferential consumption of natural/minimally processed foods should be advocated by health professionals, as recommended by the Dietary Guidelines for the Brazilian Population. Further experimental and clinical studies are recommended to assess the possible association between these foods and cardiovascular biomarkers and events.