Eat Weight Disord DOI 10.1007/s40519-013-0081-4
ORIGINAL ARTICLE
Habitual street food intake and subclinical carotid atherosclerosis Silvio Buscemi • Alessandro Mattina • Giuseppe Rosafio • Fatima M. Massenti Fabio Galvano • Giuseppe Grosso • Emanuele Amodio • Anna M. Barile • Vincenza Maniaci • Alice Bonura • Delia Sprini • Giovam B. Rini
•
Received: 14 July 2013 / Accepted: 7 October 2013 Ó Springer International Publishing Switzerland 2013
Abstract Street food (SF) is defined as out-of-home food consumption, and generally consists of energy-dense meals rich in saturated fats and poor in fibers, vitamins and antioxidants. Though SF consumption may have unfavorable metabolic and cardiovascular effects, its possible association with atherosclerosis has not been considered. The association between habitual SF consumption and asymptomatic carotid atherosclerosis, defined as the presence of plaques and/or increased intima-media thickness, was therefore investigated. One thousand thirty-five randomly selected adult participants without known diabetes and atherosclerotic cardiovascular diseases were crosssectionally investigated in Palermo, Italy. Each participant answered a food frequency questionnaire and underwent high-resolution ultrasonographic evaluation of both carotid arteries. Laboratory blood measurements were obtained in a subsample of 541 participants. A score of SF consumption was obtained by categorizing each of ten SFs consumed more or less than once a month. Participants were divided into three classes based on the tertiles of SF score distribution. Age, gender distribution, body mass index
S. Buscemi (&) A. Mattina G. Rosafio A. M. Barile V. Maniaci A. Bonura D. Sprini G. B. Rini Laboratorio di Nutrizione Clinica, Dipartimento Biomedico di Medicina Interna e Specialistica (DIBIMIS), P. Giaccone Policlinico, University of Palermo, Via del Vespro 129, 90127 Palermo, Italy e-mail: [email protected] F. M. Massenti Dipartimento di Scienze per la Promozione della Salute e Materno Infantile, University of Palermo, Palermo, Italy F. Galvano G. Grosso E. Amodio Dipartimento di Scienze del Farmaco, University of Catania, Catania, Italy
(BMI), prevalence of hypertension and of clinically silent carotid atherosclerosis (I tertile 20.8 %, II tertile 19.7 %, III tertile 19.0 %; P = 0.85) were not significantly different among the three groups. Clinically silent carotid atherosclerosis was independently associated with age, gender and hypertension. The score of SF consumption was significantly correlated with BMI (r = 0.10; P = 0.04), uric acid (r = 0.16; P = 0.002) and high-density lipoproteinscholesterol (r = -0.13; P = 0.009) blood concentrations. In conclusion, this study suggests that SF consumption is not associated with clinically silent carotid atherosclerosis. However, given the association of SF consumption with other cardiovascular risk factors, caution requires that this category of food should be limited in patients at high cardiovascular risk. Keywords Atherosclerosis Carotid intima-media thickness Hypertension Obesity Street food
Introduction Despite the fact that a Mediterranean diet is advised as part of a healthy diet to reduce the risk of cardiovascular disease, fast food consumption is greatly increasing worldwide, especially among younger age groups [1]. Fast food is generally perceived as unhealthy and consists of energy dense meals that are rich in saturated fats and poor in fibers, vitamins and antioxidants. Fast food outlets specialize in foods that are usually fried, such as hamburgers, chicken, French fries and pizza. These enterprises are usually indoors, and invest heavily in seating, air conditioning and bright decor. Marketing strategies are almost exclusively dependent on advertising, sponsorship and special offers that aim at creating brand loyalty. Owners
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typically have a franchise arrangement with a transnational company that also controls the provision of raw materials, the menu and the mode of preparation [2]. Frequent consumption of fast food promotes weight gain [3–5] and may have unfavorable cardiovascular effects [6]. As a result, strategies are actually under consideration for reducing the consumption of these foods [7]. Closely linked to fast food is another version of out-ofhome food consumption, termed street food (SF). Street food has old, historical roots, with complex socioeconomic and cultural implications [8]. SF reflects traditional local cultures. Vendors’ stalls are usually located outdoors or under a roof that is easily accessible from the street. They have low-cost seating facilities that are sometimes rudimentary. Their marketing success depends exclusively on location and word-of-mouth promotion. Street food businesses are usually owned and operated by individuals or families. Street food is found even in less developed countries and has occasionally been considered a hallmark in the early development of fast food [2, 9]. It is quickly available and consumed, and generally affordable for large parts of the population. Despite the emergence of modern fast food, traditional SF persists worldwide, especially in Europe and Mediterranean countries [10], contributing to the preservation of local traditions. However, differently from fast food, the question of the possible influences of SF on health, particularly cardiovascular, have not been considered. We recently investigated the possible effects of SF consumption on health in Palermo, the largest city in Sicily, Italy, and found that excessive SF consumption may be associated with such unfavorable cardiovascular risk factors as higher body mass index (BMI) and increased prevalence of hypertension [11]. Furthermore, endothelial function, which plays a central role in the development of atherosclerosis, and is a strong independent risk factor for future cardiovascular disease and mortality [12–14], has been found to be impaired in high SF consumers [15]. Though these findings suggest that high SF consumption may promote atherosclerosis, no study has ever considered the relationship between the two. On the other hand, there is evidence from epidemiological studies [16] and animal experiments [17] that dietary factors may influence atherosclerosis. Even when asymptomatic, carotid atherosclerosis has important clinical implications. Ultrasound-assessed plaques are independent predictors of cardiovascular events [18], and carotid intima-media thickness (c-IMT) is a wellvalidated surrogate marker of future coronary events [19]. This study was undertaken to determine whether SF consumed in Palermo was associated with atherosclerosis. We investigated habitual SF consumption and the prevalence of asymptomatic carotid atherosclerosis (plaques
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and/or increased IMT) in a large group of randomly selected adults without such potential confounders as known diabetes and atherosclerotic cardiovascular disease.
Methods and procedures This observational, cross-sectional study was done in Palermo, which has a population of 663,173. From March 28 to April 10, 2011, groups composed of physicians (n = 5) and dieticians (n = 13) alternated their presence inside The Forum, a shopping mall in Palermo, from 9:00 a.m. until 9:00 p.m. There they contacted those customers who asked to participate in the study, which had been proposed by means of posters at the mall. The Forum is the largest shopping mall in Palermo, and customers come from all parts of the city, the suburbs and neighboring areas. Data provided by the Forum administration indicated that the characteristics of their habitual customers were heterogeneous in terms of gender (females 65 %, males 35 %), age (10–54 years of age 50 %, C55 years 50 %), education (college graduate = 14 %, high school = 37 %, middle school = 32 %, elementary school = 17 %) and employment status (housewife = 40 %, retired = 23 %, employed = 19 %, student = 8 %, unemployed = 6 %, manager/professional = 4 %). Inclusion criteria were age C18 years and residency in Palermo. No incentive was provided to the participants. Participants were asked to come to the Biomedical Department of Internal and Specialized Medicine’s Laboratory of Clinical Nutrition, at the University of Palermo, in the following weeks, and no later than July 15, 2011, to undergo blood sampling for assessment of blood chemistry and hormonal parameters. A serum sample was frozen and stored at -80 °C, and a sample was treated and stored for subsequent measurements. Each participant signed an approved informed consent form. Our internal review board approved the study protocol. Participants were interviewed and answered a questionnaire on demographic characteristics, the presence of chronic disease and pharmacologic treatment, physical activity, including questions on level of physical activity and weekly frequency, and daily time watching television, on the computer and playing video games. Half-quantitative habitual intakes of different foods during the past 12 months were assessed with the Food Frequency Questionnaire (FFQ) [20]. The response rate was 100 %. Specifically, participants were asked by trained dietitians about their consumption of 31 different food items. They were also asked to indicate their usual rate of consumption, choosing from nine frequency categories
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ranging from ‘‘never’’ or ‘‘less than once a week’’ to ‘‘7 times per week’’. The food items were listed as red meat, white meat, fish, cured meat, eggs, fried foods, milk, dairy products, cheese, legumes, bread, pasta/rice, fruit, vegetables, olive oil, seed oil, butter, margarine, sweets, soft drinks, coffee and alcohol. For coffee and alcoholic and soft drinks, the amount in terms of cups/glasses was specified. In addition, the consumption of traditional Palermo SF (panelle, rascatura, crocche`, arancine, focaccia with milza, sfincione, frittola, musso, quarume, stigghiole) was considered. A more complete gastronomic and nutritional description of Palermo SF has been given elsewhere [11] and is also available on the Internet at http://www. scribd.com/doc/60786261/Palermo-Street-Food. Participants were asked if they consumed any of these foods (yes/no), and reported frequency of consumption of each food was categorized as more or less than once a month. Following an investigation to test a group of 500 people interviewed on the street to assess their frequency of SF consumption, we chose to categorize the habitual consumption of each food as less than (rarely) or more than (frequently) once a month. The score of SF consumption was then arbitrarily calculated, as in our previous study [11]. So, the ten above-mentioned SFs were considered and each was assigned a score as follows: 0, never consumed; 1, once a month or less; 2, more than once a month. Thus, the sum of single scores could range from 0 to 20. Measurements Height and body weight were measured with participants lightly dressed and without shoes (SECA); the BMI was calculated as body weight (kg)/height2 (m2). Body circumference was measured at the umbilicus (waist circumference) and was used as an indirect index of body fat distribution. Systolic and diastolic arterial blood pressure (two measurements obtained at a 5-min interval in seated position) and heart rate were measured by physicians or dietitians according to standardized procedures (Omron M6; Omron Healthcare Co.; Matsusaka, Mie, Japan). Carotid intima-media thickness Images of the right and left extracranial carotid artery walls were obtained in several projections by using a high-resolution ultrasonographic 10-MHz linear array probe (Sonoline G50; Siemens, Germany) with participants in the supine position. The end-diastolic IMT of the far wall of both common carotid arteries was measured as described elsewhere [21], 10 mm caudal to the bulb, using twodimensional longitudinal sections of the vessel and the distance from the first echogenic line to the second
echogenic line (three values for each carotid artery using antero-posterior, laterolateral, and postero-anterior scans). The highest value was considered for calculations [22]. Two physicians were responsible for carrying out the carotid ultrasonographic examination. Images were video recorded. A single physician who was blinded to the study hypothesis read the images. The intra-observer coefficients of variations were 1.2 and 1.1 %, respectively. The interobserver coefficient of variation was 2.9 %. Clinically silent carotid atherosclerosis was diagnosed in the presence of an IMT C0.9 mm and/or plaques [23]. Laboratory analysis Capillary blood glucose concentrations were randomly assessed using a glucose reflectometer (Glucocard G meter; Menarini Diagnostics; Florence, Italy). Fasting plasma glucose, total cholesterol, high-density lipoproteins-cholesterol (HDL-c), triglycerides, uric acid and creatinine concentrations were ascertained by using standard clinical chemistry methods (Glucosio HK UV; Colesterolo tot. Mod P/D; Colesterolo HDL gen 3 mod P/917; Trigliceridi; Acido urico MOD P/917; Creatinina enzimatica; Roche Diagnostics, Monza, Italy). Basal insulin concentrations (Elecsys insulina; Roche Diagnostics; Monza, Italy) and glycated hemoglobin (HbA1c; HbA1c gen.3; Roche Diagnostics; Monza, Italy) were also measured. Low-density lipoprotein (LDL) cholesterol concentration was calculated with Friedewald’s formula [24]. Insulin resistance was considered on the basis of the homeostasis model assessment of insulin resistance (HOMA-IR) and calculated as described in Matthews et al. [25]. Statistical analysis Normal distribution of variables was tested on the basis of skewness, standard error of skewness, kurtosis and standard error of kurtosis. Participant characteristics were grouped in three classes according to the tertiles of the SF score to discriminate rare, average and frequent SF consumers. All data are presented as mean ± standard error of mean (SE) or as prevalence (%). Basal comparisons between groups were tested for statistical significance using the analysis of variance (ANOVA) or Pearson v2, when appropriate. Linear regression analysis assessed the relationships between SF score and different variables, including anthropometric, lipidemic and uric acid concentrations, since dietary factors may influence even uric acid concentrations that are associated with atherosclerosis, as well as with insulin resistance [26]. Multivariate logistic regression analyses were done to evaluate factors associated with subclinical carotid atherosclerosis. For subclinical carotid atherosclerosis, the
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Eat Weight Disord Table 1 Participant demographic and clinical characteristics categorized according to the tertile of street food score
P valuea
Street food score tertiles I (n = 372)
II (n = 422)
Gender (% male)
34.2
36.3
35.1
0.64
Age (years)
49.9 ± 0.7
49.2 ± 0.7
49.2 ± 0.9
0.75
Offspring (n)
1.7 ± 0.07
1.6 ± 0.06
III (n = 241)
1.7 ± 0.08
Education (%)
0.52 0.19
0–5 years
12.4
11.6
6–8 years
33.9
32.5
14.9 39.0
9–13 years
38.4
42.4
35.7
[13 years
15.3
13.3
10.8
Single
18.8
19.7
19.5
Married Divorced
73.4 4.3
73.0 3.3
75.9 2.1
Widow/er
3.5
3.8
2.9
Unemployed
58.9
59.9
59.3
Employed
35.8
30.3
35.3
4.6
9.2
5.8
Never smoked
18.0
23.0
18.2
Former smoker
59.5
56.8
54.9
Current smoker
22.5
20.2
26.9
29.0
27.0
25.6
Marital status (%)
0.84
Employment (%)
0.20
Manager/professional Smoking (%)
0.15
Participants on anti-hypertensives (%)
0.65
Use of anti-hypertensives (%) Diuretics Beta-blockers Use of statins (%) Physical activity (%) All values are presented as mean ± SE or percentages a
ANOVA or Pearson v2
7.3
7.5
0.83
7.8
7.1
0.34
8.9
6.2
5.8
0.36 0.41
None
49.5
46.2
48.1
Light
33.6
39.6
32.8
Moderate/heavy
16.9
14.2
19.1
following baseline covariates were tested: age, gender, BMI, waist circumference, hypertension and SF score tertile. Results of the logistic regression models are expressed as odds ratios (ORs) with their 95 % confidence intervals (CI). A two-tailed P value of\0.05 was considered statistically significant. All analyses were done using SYSTAT (Windows version 11.0; Systat Software Inc., San Jose, CA, USA).
Results A total of 1,231 (465 males and 766 females) participants were evaluated; 196 participants were excluded because of the presence of diabetes (types 1 and 2), clinically known atherosclerotic diseases (coronary heart disease, previous stroke, carotid or peripheral atherosclerosis) or chronic renal failure. Laboratory blood measurements were obtained in 541 participants and random capillary blood
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7.5 10.5
glucose in 991 participants. Based on the tertile of SF score, the 1,035 participants (age 49.5 ± 13.8; range 18–90 years) were divided into three groups: 372 (I tertile, SF score 0–2), 422 (II tertile, SF score 3–5) and 241 (III tertile, SF score C6). Demographic, anthropometric and clinical characteristics of the three groups of SF consumers are reported in Tables 1 and 2. The frequency of consumption of different foods in the three groups of SF score tertiles is reported in Table 4. From tertile I to III, there was a significant trend toward eating vegetables less frequently, and pasta/rice, bread, cured meats, eggs, cheese, seeds oil and fried foods more frequently. Age, gender distribution, BMI and prevalence of hypertension were not significantly different among the three groups, nor was the prevalence of clinically silent carotid atherosclerosis (P = 0.85) and the c-IMT (P = 0.16) (Table 2). Multivariate logistic regression analysis showed that clinically silent carotid atherosclerosis was independently associated
Eat Weight Disord Table 2 Anthropometric, echographic and laboratory data of participants categorized according to the tertile of street food score P valuea
Street food score tertiles I (n = 372)
II (n = 422)
III (n = 241)
Body weight (kg)
73.3 ± 0.8
73.5 ± 0.8
75.4 ± 1.0
0.22
BMI (kg/m2)
27.8 ± 0.3
27.9 ± 0.3
28.3 ± 0.3
0.39
Waist (cm)
97.1 ± 2.9
94.2 ± 0.8
95.3 ± 1.0
0.52
Systolic BP (mmHg)
128 ± 1
130 ± 1
129 ± 1
Diastolic BP (mmHg) Heart rate (beats/min) Carotid-IMT (mm) Carotid atherosclerosis (%)
78 ± 0.5
79 ± 0.5
79 ± 0.7
0.11 0.77
74 ± 0.6
74 ± 0.6
74 ± 0.8
0.91
0.59 ± 0.01 20.8
0.61 ± 0.01 19.7
0.60 ± 0.01 19.0
0.16 0.85
Random capillary blood glucose (mg/dl)
88 ± 1.1 (n = 359)
88 ± 1.0 (n = 401)
89 ± 1.3 (n = 231)
0.81
Glycated hemoglobin (%)
5.6 ± 0.01 (n = 194)
5.6 ± 0.03 (n = 227)
5.6 ± 0.05 (n = 120)
0.53
Fasting blood concentration of Glucose (mg/dl)
90 ± 0.8
90 ± 0.8
92 ± 1.1
0.12
Insulin (lU/mL)
8.7 ± 0.4
9.8 ± 0.4
10.0 ± 0.6
0.07
Cholesterol (mg/dl)
0.85
214 ± 3
212 ± 3
214 ± 3
HDL-cholesterol (mg/dl)
62 ± 1
60 ± 1
57 ± 1
0.038
Triglycerides (mg/dl)
97 ± 3
102 ± 3
105 ± 5
0.39
LDL-cholesterol (mg/dl)
132 ± 35
131 ± 38
137 ± 34
0.18
Uric acid (mg/dl)
4.9 ± 0.1
4.9 ± 0.1
5.2 ± 0.1
0.046
Creatinine (mg/dl)
0.83 ± 0.02
0.82 ± 0.01
0.84 ± 0.02
0.80
2.0 ± 0.1
2.6 ± 0.3
2.4 ± 0.2
0.26
HOMA-IR
All values are presented as mean ± SE or percentages BMI body mass index, BP blood pressure, HDL high-density lipoproteins, HOMA-IR homeostasis model assessment of insulin resistance, IMT intima-media thickness, LDL low-density lipoproteins a
ANOVA or Pearson v2
with age, gender and hypertension, while no significant association was observed in the SF tertile, BMI and waist circumference (Table 3). The score of SF consumption was significantly correlated with BMI (r = 0.10; P = 0.04), uric acid (r = 0.16; P = 0.002) and HDL-c blood concentrations (r = -0.13; P = 0.009). Among the laboratory variables considered, the HDL-cholesterol blood concentrations decreased significantly (P = 0.038) from the I to III tertile group, while those of uric acid increased (P = 0.046).
Table 3 Multivariate odds ratios (OR) and 95 % confidence intervals (CI) of clinically silent carotid atherosclerosis determined by age, gender, body mass index, waist circumference, hypertension and tertile of habitual street food consumption Effect
OR
95 % CI
Age (years)
0.89
0.88–0.91
Gender (male vs. female)
1.68
1.15–2.46
BMI
1.00
0.96–1.05
Waist circumference
1.00
0.99–1.01
Hypertension (yes vs. no)
2.17
1.46–3.21
Street food score tertile
Discussion In this cross-sectional study, frequent consumers of SF were found to also frequently consume pasta/rice, bread, cured meats, eggs, cheese, seeds oil and fried foods, and rarely consume vegetables. This dietary pattern is generally considered unhealthy and is almost the opposite of a traditional, healthy Mediterranean diet [27]. This finding supports the hypothesis that SF may be a proxy indicator of other components of an unhealthy lifestyle [28]. We also found that with increased levels of habitual SF
I vs. III
0.89
0.54–1.45
II vs. III
0.95
0.59–1.55
BMI body mass index
consumption, the HDL-cholesterol blood concentrations decreased and those of uric acid rose, two conditions that are associated with atherosclerosis and increased cardiovascular risk [29]. Nonetheless, we found no significant association between habitual SF consumption and the prevalence of asymptomatic carotid atherosclerosis,
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Eat Weight Disord Table 4 Participants’ mean habitual intake of different foods categorized according to the tertile of street food score Food intake (days a week) Pasta, rice Bread Fruit Vegetables Legumes Fish Red meat White meat Cured meats Eggs Milk Dairy products Cheese Olive oil Seed oil Butter Margarine Fried foods Sweets
P valuea
Street food score tertiles I (n = 372)
II (n = 422)
III (n = 241)
5.5 5.9 6.0 5.4 1.5 1.4 1.7 2.0 1.5 1.1 3.9 2.3 2.9 6.6 0.2 0.2 0.1 0.4 1.9
5.8 6.3 5.8 4.9 1.6 1.4 1.8 1.9 1.8 1.3 3.6 2.7 3.3 6.7 0.4 0.2 0.1 0.8 2.2
6.1 6.3 5.8 4.8 1.5 1.3 1.9 1.9 1.8 1.4 3.5 2.7 3.8 6.7 0.7 0.3 0.04 1.0 2.2
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.04 0.04 0.02 0.04 0.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.05 0.04 0.02 0.1 0.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.2 0.2 0.1 0.09 0.05 0.02 0.1 0.2
0.003 0.015 0.32 \0.001 0.33 0.66 0.16 0.73 0.045 0.011 0.312 0.098 \0.001 0.34 \0.001 0.63 0.31 \0.001 0.08
All values are presented as mean ± SE a ANOVA
defined as the presence of carotid plaques and/or increased IMT, in participants without clinically known atherosclerotic diseases. Multivariate analysis confirmed that other traditional cardiovascular risk factors, such as age, gender and hypertension, are independently associated with clinically silent carotid atherosclerosis. Therefore, our study seems to indicate that, at least in participants with no history of cardiovascular disease or diabetes, dietary factors in terms of habitual SF consumption have little or no impact on carotid atherosclerosis. These results are in agreement with other studies that failed to find a definite significant role of dietary factors in cardiovascular primary prevention, while the beneficial effects of a healthy diet have been substantially demonstrated in secondary prevention [30]. We previously observed that endothelial dysfunction, a predisposing condition to atherosclerosis, characterizes frequent consumers of SF [15]. However, our results seem to suggest that habitual SF consumption does not induce atherosclerosis beyond that already produced by age, gender and hypertension. Therefore, the relationship between SF consumption, endothelial function and atherosclerosis is yet to be elucidated. Furthermore, despite the fact that we confirmed a positive correlation between the SF score and BMI, neither adiposity (BMI) nor fat distribution (waist circumference) was an independent predictor of carotid atherosclerosis in our study. The
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participants included in this study were clinically healthy and had a mean age of 50 years. Income and education were found to be inversely related with atherogenic diets [31], and even neighborhood factors, sometimes indicated as local food environment, have been suggested as influences on dietary patterns [32]. However, in this study we obtained no adequate data to infer neighborhood factors. This study has some intrinsic limitations. First, the sample size is relatively small, which may have blunted the statistical power of the observed associations. Given the characteristics of this study, results cannot be generalized and they must be referred only to local people whose nutritional habits include different degrees of SF consumption. Whether our results parallel similar food practices in other countries is unknown, but could be a subject of further investigation. The SF score has other intrinsic limitations. For instance, someone who eats SF most days of the week, but only eats one item would only have a score of 2. We could, however, consider this an extreme situation that is expected to have no high influence on the results, given the relatively high number of participants included in this study. In general, both the number of SF specialties consumed and the frequency of their consumption may influence the SF score. Two points of the SF score correspond to the habitual consumption of two specialties of SF once a month or less or, alternatively, to the consumption of one specialty of SF more than once a month. Therefore, the SF score likely reflects a tendency toward a nutritional style rather than the amount of habitual energy intake. The calculated SF score was not validated, but did provide interesting information. Indeed, we calculated the SF score using the same criteria for describing habitual SF consumption that we have previously adopted [11], so that comparisons between the two studies are possible. We acknowledge that further validation studies would be needed for an accurate interpretation of what an elevated SF score means. Even the FFQ we used in this study was not validated. However, we present generic half-quantitative data on habitual consumption of different foods and not amounts of energy intake or quantitative amounts of each food. This probably reduces inaccuracy. As we did not enroll a representative cohort of the Palermo population, some bias might be associated with the sampling technique. However, the composition of the cohort we recruited was similar to that reported for the shopping mall customers. The characterization of study participants and the use of a strict ultrasound procedure by two operators that probably helped reduce possible biases are points of strength. In conclusion, this cross-sectional study shows that SF consumption has no significant impact on carotid atherosclerosis in participants with no history of cardiovascular
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disease or diabetes. Only adequate longitudinal studies and interventional trials can definitively clarify the role of SF consumption in influencing atherosclerosis. Nevertheless, given the association of SF consumption with other cardiovascular risk factors, caution requires that this category of food should be limited in patients at high cardiovascular risk. Further studies are also needed to determine whether the nutritional characteristics of SF in other geographic regions are associated with unfavorable cardiovascular and metabolic conditions. Acknowledgments Palermo, Italia.
Associazione
Onlus
Nutrizione
e
Salute,
Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest.
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ORIGINAL ARTICLE
Habitual street food intake and subclinical carotid atherosclerosis Silvio Buscemi • Alessandro Mattina • Giuseppe Rosafio • Fatima M. Massenti Fabio Galvano • Giuseppe Grosso • Emanuele Amodio • Anna M. Barile • Vincenza Maniaci • Alice Bonura • Delia Sprini • Giovam B. Rini
•
Received: 14 July 2013 / Accepted: 7 October 2013 Ó Springer International Publishing Switzerland 2013
Abstract Street food (SF) is defined as out-of-home food consumption, and generally consists of energy-dense meals rich in saturated fats and poor in fibers, vitamins and antioxidants. Though SF consumption may have unfavorable metabolic and cardiovascular effects, its possible association with atherosclerosis has not been considered. The association between habitual SF consumption and asymptomatic carotid atherosclerosis, defined as the presence of plaques and/or increased intima-media thickness, was therefore investigated. One thousand thirty-five randomly selected adult participants without known diabetes and atherosclerotic cardiovascular diseases were crosssectionally investigated in Palermo, Italy. Each participant answered a food frequency questionnaire and underwent high-resolution ultrasonographic evaluation of both carotid arteries. Laboratory blood measurements were obtained in a subsample of 541 participants. A score of SF consumption was obtained by categorizing each of ten SFs consumed more or less than once a month. Participants were divided into three classes based on the tertiles of SF score distribution. Age, gender distribution, body mass index
S. Buscemi (&) A. Mattina G. Rosafio A. M. Barile V. Maniaci A. Bonura D. Sprini G. B. Rini Laboratorio di Nutrizione Clinica, Dipartimento Biomedico di Medicina Interna e Specialistica (DIBIMIS), P. Giaccone Policlinico, University of Palermo, Via del Vespro 129, 90127 Palermo, Italy e-mail: [email protected] F. M. Massenti Dipartimento di Scienze per la Promozione della Salute e Materno Infantile, University of Palermo, Palermo, Italy F. Galvano G. Grosso E. Amodio Dipartimento di Scienze del Farmaco, University of Catania, Catania, Italy
(BMI), prevalence of hypertension and of clinically silent carotid atherosclerosis (I tertile 20.8 %, II tertile 19.7 %, III tertile 19.0 %; P = 0.85) were not significantly different among the three groups. Clinically silent carotid atherosclerosis was independently associated with age, gender and hypertension. The score of SF consumption was significantly correlated with BMI (r = 0.10; P = 0.04), uric acid (r = 0.16; P = 0.002) and high-density lipoproteinscholesterol (r = -0.13; P = 0.009) blood concentrations. In conclusion, this study suggests that SF consumption is not associated with clinically silent carotid atherosclerosis. However, given the association of SF consumption with other cardiovascular risk factors, caution requires that this category of food should be limited in patients at high cardiovascular risk. Keywords Atherosclerosis Carotid intima-media thickness Hypertension Obesity Street food
Introduction Despite the fact that a Mediterranean diet is advised as part of a healthy diet to reduce the risk of cardiovascular disease, fast food consumption is greatly increasing worldwide, especially among younger age groups [1]. Fast food is generally perceived as unhealthy and consists of energy dense meals that are rich in saturated fats and poor in fibers, vitamins and antioxidants. Fast food outlets specialize in foods that are usually fried, such as hamburgers, chicken, French fries and pizza. These enterprises are usually indoors, and invest heavily in seating, air conditioning and bright decor. Marketing strategies are almost exclusively dependent on advertising, sponsorship and special offers that aim at creating brand loyalty. Owners
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typically have a franchise arrangement with a transnational company that also controls the provision of raw materials, the menu and the mode of preparation [2]. Frequent consumption of fast food promotes weight gain [3–5] and may have unfavorable cardiovascular effects [6]. As a result, strategies are actually under consideration for reducing the consumption of these foods [7]. Closely linked to fast food is another version of out-ofhome food consumption, termed street food (SF). Street food has old, historical roots, with complex socioeconomic and cultural implications [8]. SF reflects traditional local cultures. Vendors’ stalls are usually located outdoors or under a roof that is easily accessible from the street. They have low-cost seating facilities that are sometimes rudimentary. Their marketing success depends exclusively on location and word-of-mouth promotion. Street food businesses are usually owned and operated by individuals or families. Street food is found even in less developed countries and has occasionally been considered a hallmark in the early development of fast food [2, 9]. It is quickly available and consumed, and generally affordable for large parts of the population. Despite the emergence of modern fast food, traditional SF persists worldwide, especially in Europe and Mediterranean countries [10], contributing to the preservation of local traditions. However, differently from fast food, the question of the possible influences of SF on health, particularly cardiovascular, have not been considered. We recently investigated the possible effects of SF consumption on health in Palermo, the largest city in Sicily, Italy, and found that excessive SF consumption may be associated with such unfavorable cardiovascular risk factors as higher body mass index (BMI) and increased prevalence of hypertension [11]. Furthermore, endothelial function, which plays a central role in the development of atherosclerosis, and is a strong independent risk factor for future cardiovascular disease and mortality [12–14], has been found to be impaired in high SF consumers [15]. Though these findings suggest that high SF consumption may promote atherosclerosis, no study has ever considered the relationship between the two. On the other hand, there is evidence from epidemiological studies [16] and animal experiments [17] that dietary factors may influence atherosclerosis. Even when asymptomatic, carotid atherosclerosis has important clinical implications. Ultrasound-assessed plaques are independent predictors of cardiovascular events [18], and carotid intima-media thickness (c-IMT) is a wellvalidated surrogate marker of future coronary events [19]. This study was undertaken to determine whether SF consumed in Palermo was associated with atherosclerosis. We investigated habitual SF consumption and the prevalence of asymptomatic carotid atherosclerosis (plaques
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and/or increased IMT) in a large group of randomly selected adults without such potential confounders as known diabetes and atherosclerotic cardiovascular disease.
Methods and procedures This observational, cross-sectional study was done in Palermo, which has a population of 663,173. From March 28 to April 10, 2011, groups composed of physicians (n = 5) and dieticians (n = 13) alternated their presence inside The Forum, a shopping mall in Palermo, from 9:00 a.m. until 9:00 p.m. There they contacted those customers who asked to participate in the study, which had been proposed by means of posters at the mall. The Forum is the largest shopping mall in Palermo, and customers come from all parts of the city, the suburbs and neighboring areas. Data provided by the Forum administration indicated that the characteristics of their habitual customers were heterogeneous in terms of gender (females 65 %, males 35 %), age (10–54 years of age 50 %, C55 years 50 %), education (college graduate = 14 %, high school = 37 %, middle school = 32 %, elementary school = 17 %) and employment status (housewife = 40 %, retired = 23 %, employed = 19 %, student = 8 %, unemployed = 6 %, manager/professional = 4 %). Inclusion criteria were age C18 years and residency in Palermo. No incentive was provided to the participants. Participants were asked to come to the Biomedical Department of Internal and Specialized Medicine’s Laboratory of Clinical Nutrition, at the University of Palermo, in the following weeks, and no later than July 15, 2011, to undergo blood sampling for assessment of blood chemistry and hormonal parameters. A serum sample was frozen and stored at -80 °C, and a sample was treated and stored for subsequent measurements. Each participant signed an approved informed consent form. Our internal review board approved the study protocol. Participants were interviewed and answered a questionnaire on demographic characteristics, the presence of chronic disease and pharmacologic treatment, physical activity, including questions on level of physical activity and weekly frequency, and daily time watching television, on the computer and playing video games. Half-quantitative habitual intakes of different foods during the past 12 months were assessed with the Food Frequency Questionnaire (FFQ) [20]. The response rate was 100 %. Specifically, participants were asked by trained dietitians about their consumption of 31 different food items. They were also asked to indicate their usual rate of consumption, choosing from nine frequency categories
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ranging from ‘‘never’’ or ‘‘less than once a week’’ to ‘‘7 times per week’’. The food items were listed as red meat, white meat, fish, cured meat, eggs, fried foods, milk, dairy products, cheese, legumes, bread, pasta/rice, fruit, vegetables, olive oil, seed oil, butter, margarine, sweets, soft drinks, coffee and alcohol. For coffee and alcoholic and soft drinks, the amount in terms of cups/glasses was specified. In addition, the consumption of traditional Palermo SF (panelle, rascatura, crocche`, arancine, focaccia with milza, sfincione, frittola, musso, quarume, stigghiole) was considered. A more complete gastronomic and nutritional description of Palermo SF has been given elsewhere [11] and is also available on the Internet at http://www. scribd.com/doc/60786261/Palermo-Street-Food. Participants were asked if they consumed any of these foods (yes/no), and reported frequency of consumption of each food was categorized as more or less than once a month. Following an investigation to test a group of 500 people interviewed on the street to assess their frequency of SF consumption, we chose to categorize the habitual consumption of each food as less than (rarely) or more than (frequently) once a month. The score of SF consumption was then arbitrarily calculated, as in our previous study [11]. So, the ten above-mentioned SFs were considered and each was assigned a score as follows: 0, never consumed; 1, once a month or less; 2, more than once a month. Thus, the sum of single scores could range from 0 to 20. Measurements Height and body weight were measured with participants lightly dressed and without shoes (SECA); the BMI was calculated as body weight (kg)/height2 (m2). Body circumference was measured at the umbilicus (waist circumference) and was used as an indirect index of body fat distribution. Systolic and diastolic arterial blood pressure (two measurements obtained at a 5-min interval in seated position) and heart rate were measured by physicians or dietitians according to standardized procedures (Omron M6; Omron Healthcare Co.; Matsusaka, Mie, Japan). Carotid intima-media thickness Images of the right and left extracranial carotid artery walls were obtained in several projections by using a high-resolution ultrasonographic 10-MHz linear array probe (Sonoline G50; Siemens, Germany) with participants in the supine position. The end-diastolic IMT of the far wall of both common carotid arteries was measured as described elsewhere [21], 10 mm caudal to the bulb, using twodimensional longitudinal sections of the vessel and the distance from the first echogenic line to the second
echogenic line (three values for each carotid artery using antero-posterior, laterolateral, and postero-anterior scans). The highest value was considered for calculations [22]. Two physicians were responsible for carrying out the carotid ultrasonographic examination. Images were video recorded. A single physician who was blinded to the study hypothesis read the images. The intra-observer coefficients of variations were 1.2 and 1.1 %, respectively. The interobserver coefficient of variation was 2.9 %. Clinically silent carotid atherosclerosis was diagnosed in the presence of an IMT C0.9 mm and/or plaques [23]. Laboratory analysis Capillary blood glucose concentrations were randomly assessed using a glucose reflectometer (Glucocard G meter; Menarini Diagnostics; Florence, Italy). Fasting plasma glucose, total cholesterol, high-density lipoproteins-cholesterol (HDL-c), triglycerides, uric acid and creatinine concentrations were ascertained by using standard clinical chemistry methods (Glucosio HK UV; Colesterolo tot. Mod P/D; Colesterolo HDL gen 3 mod P/917; Trigliceridi; Acido urico MOD P/917; Creatinina enzimatica; Roche Diagnostics, Monza, Italy). Basal insulin concentrations (Elecsys insulina; Roche Diagnostics; Monza, Italy) and glycated hemoglobin (HbA1c; HbA1c gen.3; Roche Diagnostics; Monza, Italy) were also measured. Low-density lipoprotein (LDL) cholesterol concentration was calculated with Friedewald’s formula [24]. Insulin resistance was considered on the basis of the homeostasis model assessment of insulin resistance (HOMA-IR) and calculated as described in Matthews et al. [25]. Statistical analysis Normal distribution of variables was tested on the basis of skewness, standard error of skewness, kurtosis and standard error of kurtosis. Participant characteristics were grouped in three classes according to the tertiles of the SF score to discriminate rare, average and frequent SF consumers. All data are presented as mean ± standard error of mean (SE) or as prevalence (%). Basal comparisons between groups were tested for statistical significance using the analysis of variance (ANOVA) or Pearson v2, when appropriate. Linear regression analysis assessed the relationships between SF score and different variables, including anthropometric, lipidemic and uric acid concentrations, since dietary factors may influence even uric acid concentrations that are associated with atherosclerosis, as well as with insulin resistance [26]. Multivariate logistic regression analyses were done to evaluate factors associated with subclinical carotid atherosclerosis. For subclinical carotid atherosclerosis, the
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Eat Weight Disord Table 1 Participant demographic and clinical characteristics categorized according to the tertile of street food score
P valuea
Street food score tertiles I (n = 372)
II (n = 422)
Gender (% male)
34.2
36.3
35.1
0.64
Age (years)
49.9 ± 0.7
49.2 ± 0.7
49.2 ± 0.9
0.75
Offspring (n)
1.7 ± 0.07
1.6 ± 0.06
III (n = 241)
1.7 ± 0.08
Education (%)
0.52 0.19
0–5 years
12.4
11.6
6–8 years
33.9
32.5
14.9 39.0
9–13 years
38.4
42.4
35.7
[13 years
15.3
13.3
10.8
Single
18.8
19.7
19.5
Married Divorced
73.4 4.3
73.0 3.3
75.9 2.1
Widow/er
3.5
3.8
2.9
Unemployed
58.9
59.9
59.3
Employed
35.8
30.3
35.3
4.6
9.2
5.8
Never smoked
18.0
23.0
18.2
Former smoker
59.5
56.8
54.9
Current smoker
22.5
20.2
26.9
29.0
27.0
25.6
Marital status (%)
0.84
Employment (%)
0.20
Manager/professional Smoking (%)
0.15
Participants on anti-hypertensives (%)
0.65
Use of anti-hypertensives (%) Diuretics Beta-blockers Use of statins (%) Physical activity (%) All values are presented as mean ± SE or percentages a
ANOVA or Pearson v2
7.3
7.5
0.83
7.8
7.1
0.34
8.9
6.2
5.8
0.36 0.41
None
49.5
46.2
48.1
Light
33.6
39.6
32.8
Moderate/heavy
16.9
14.2
19.1
following baseline covariates were tested: age, gender, BMI, waist circumference, hypertension and SF score tertile. Results of the logistic regression models are expressed as odds ratios (ORs) with their 95 % confidence intervals (CI). A two-tailed P value of\0.05 was considered statistically significant. All analyses were done using SYSTAT (Windows version 11.0; Systat Software Inc., San Jose, CA, USA).
Results A total of 1,231 (465 males and 766 females) participants were evaluated; 196 participants were excluded because of the presence of diabetes (types 1 and 2), clinically known atherosclerotic diseases (coronary heart disease, previous stroke, carotid or peripheral atherosclerosis) or chronic renal failure. Laboratory blood measurements were obtained in 541 participants and random capillary blood
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7.5 10.5
glucose in 991 participants. Based on the tertile of SF score, the 1,035 participants (age 49.5 ± 13.8; range 18–90 years) were divided into three groups: 372 (I tertile, SF score 0–2), 422 (II tertile, SF score 3–5) and 241 (III tertile, SF score C6). Demographic, anthropometric and clinical characteristics of the three groups of SF consumers are reported in Tables 1 and 2. The frequency of consumption of different foods in the three groups of SF score tertiles is reported in Table 4. From tertile I to III, there was a significant trend toward eating vegetables less frequently, and pasta/rice, bread, cured meats, eggs, cheese, seeds oil and fried foods more frequently. Age, gender distribution, BMI and prevalence of hypertension were not significantly different among the three groups, nor was the prevalence of clinically silent carotid atherosclerosis (P = 0.85) and the c-IMT (P = 0.16) (Table 2). Multivariate logistic regression analysis showed that clinically silent carotid atherosclerosis was independently associated
Eat Weight Disord Table 2 Anthropometric, echographic and laboratory data of participants categorized according to the tertile of street food score P valuea
Street food score tertiles I (n = 372)
II (n = 422)
III (n = 241)
Body weight (kg)
73.3 ± 0.8
73.5 ± 0.8
75.4 ± 1.0
0.22
BMI (kg/m2)
27.8 ± 0.3
27.9 ± 0.3
28.3 ± 0.3
0.39
Waist (cm)
97.1 ± 2.9
94.2 ± 0.8
95.3 ± 1.0
0.52
Systolic BP (mmHg)
128 ± 1
130 ± 1
129 ± 1
Diastolic BP (mmHg) Heart rate (beats/min) Carotid-IMT (mm) Carotid atherosclerosis (%)
78 ± 0.5
79 ± 0.5
79 ± 0.7
0.11 0.77
74 ± 0.6
74 ± 0.6
74 ± 0.8
0.91
0.59 ± 0.01 20.8
0.61 ± 0.01 19.7
0.60 ± 0.01 19.0
0.16 0.85
Random capillary blood glucose (mg/dl)
88 ± 1.1 (n = 359)
88 ± 1.0 (n = 401)
89 ± 1.3 (n = 231)
0.81
Glycated hemoglobin (%)
5.6 ± 0.01 (n = 194)
5.6 ± 0.03 (n = 227)
5.6 ± 0.05 (n = 120)
0.53
Fasting blood concentration of Glucose (mg/dl)
90 ± 0.8
90 ± 0.8
92 ± 1.1
0.12
Insulin (lU/mL)
8.7 ± 0.4
9.8 ± 0.4
10.0 ± 0.6
0.07
Cholesterol (mg/dl)
0.85
214 ± 3
212 ± 3
214 ± 3
HDL-cholesterol (mg/dl)
62 ± 1
60 ± 1
57 ± 1
0.038
Triglycerides (mg/dl)
97 ± 3
102 ± 3
105 ± 5
0.39
LDL-cholesterol (mg/dl)
132 ± 35
131 ± 38
137 ± 34
0.18
Uric acid (mg/dl)
4.9 ± 0.1
4.9 ± 0.1
5.2 ± 0.1
0.046
Creatinine (mg/dl)
0.83 ± 0.02
0.82 ± 0.01
0.84 ± 0.02
0.80
2.0 ± 0.1
2.6 ± 0.3
2.4 ± 0.2
0.26
HOMA-IR
All values are presented as mean ± SE or percentages BMI body mass index, BP blood pressure, HDL high-density lipoproteins, HOMA-IR homeostasis model assessment of insulin resistance, IMT intima-media thickness, LDL low-density lipoproteins a
ANOVA or Pearson v2
with age, gender and hypertension, while no significant association was observed in the SF tertile, BMI and waist circumference (Table 3). The score of SF consumption was significantly correlated with BMI (r = 0.10; P = 0.04), uric acid (r = 0.16; P = 0.002) and HDL-c blood concentrations (r = -0.13; P = 0.009). Among the laboratory variables considered, the HDL-cholesterol blood concentrations decreased significantly (P = 0.038) from the I to III tertile group, while those of uric acid increased (P = 0.046).
Table 3 Multivariate odds ratios (OR) and 95 % confidence intervals (CI) of clinically silent carotid atherosclerosis determined by age, gender, body mass index, waist circumference, hypertension and tertile of habitual street food consumption Effect
OR
95 % CI
Age (years)
0.89
0.88–0.91
Gender (male vs. female)
1.68
1.15–2.46
BMI
1.00
0.96–1.05
Waist circumference
1.00
0.99–1.01
Hypertension (yes vs. no)
2.17
1.46–3.21
Street food score tertile
Discussion In this cross-sectional study, frequent consumers of SF were found to also frequently consume pasta/rice, bread, cured meats, eggs, cheese, seeds oil and fried foods, and rarely consume vegetables. This dietary pattern is generally considered unhealthy and is almost the opposite of a traditional, healthy Mediterranean diet [27]. This finding supports the hypothesis that SF may be a proxy indicator of other components of an unhealthy lifestyle [28]. We also found that with increased levels of habitual SF
I vs. III
0.89
0.54–1.45
II vs. III
0.95
0.59–1.55
BMI body mass index
consumption, the HDL-cholesterol blood concentrations decreased and those of uric acid rose, two conditions that are associated with atherosclerosis and increased cardiovascular risk [29]. Nonetheless, we found no significant association between habitual SF consumption and the prevalence of asymptomatic carotid atherosclerosis,
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Eat Weight Disord Table 4 Participants’ mean habitual intake of different foods categorized according to the tertile of street food score Food intake (days a week) Pasta, rice Bread Fruit Vegetables Legumes Fish Red meat White meat Cured meats Eggs Milk Dairy products Cheese Olive oil Seed oil Butter Margarine Fried foods Sweets
P valuea
Street food score tertiles I (n = 372)
II (n = 422)
III (n = 241)
5.5 5.9 6.0 5.4 1.5 1.4 1.7 2.0 1.5 1.1 3.9 2.3 2.9 6.6 0.2 0.2 0.1 0.4 1.9
5.8 6.3 5.8 4.9 1.6 1.4 1.8 1.9 1.8 1.3 3.6 2.7 3.3 6.7 0.4 0.2 0.1 0.8 2.2
6.1 6.3 5.8 4.8 1.5 1.3 1.9 1.9 1.8 1.4 3.5 2.7 3.8 6.7 0.7 0.3 0.04 1.0 2.2
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.04 0.04 0.02 0.04 0.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.05 0.04 0.02 0.1 0.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.2 0.2 0.1 0.09 0.05 0.02 0.1 0.2
0.003 0.015 0.32 \0.001 0.33 0.66 0.16 0.73 0.045 0.011 0.312 0.098 \0.001 0.34 \0.001 0.63 0.31 \0.001 0.08
All values are presented as mean ± SE a ANOVA
defined as the presence of carotid plaques and/or increased IMT, in participants without clinically known atherosclerotic diseases. Multivariate analysis confirmed that other traditional cardiovascular risk factors, such as age, gender and hypertension, are independently associated with clinically silent carotid atherosclerosis. Therefore, our study seems to indicate that, at least in participants with no history of cardiovascular disease or diabetes, dietary factors in terms of habitual SF consumption have little or no impact on carotid atherosclerosis. These results are in agreement with other studies that failed to find a definite significant role of dietary factors in cardiovascular primary prevention, while the beneficial effects of a healthy diet have been substantially demonstrated in secondary prevention [30]. We previously observed that endothelial dysfunction, a predisposing condition to atherosclerosis, characterizes frequent consumers of SF [15]. However, our results seem to suggest that habitual SF consumption does not induce atherosclerosis beyond that already produced by age, gender and hypertension. Therefore, the relationship between SF consumption, endothelial function and atherosclerosis is yet to be elucidated. Furthermore, despite the fact that we confirmed a positive correlation between the SF score and BMI, neither adiposity (BMI) nor fat distribution (waist circumference) was an independent predictor of carotid atherosclerosis in our study. The
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participants included in this study were clinically healthy and had a mean age of 50 years. Income and education were found to be inversely related with atherogenic diets [31], and even neighborhood factors, sometimes indicated as local food environment, have been suggested as influences on dietary patterns [32]. However, in this study we obtained no adequate data to infer neighborhood factors. This study has some intrinsic limitations. First, the sample size is relatively small, which may have blunted the statistical power of the observed associations. Given the characteristics of this study, results cannot be generalized and they must be referred only to local people whose nutritional habits include different degrees of SF consumption. Whether our results parallel similar food practices in other countries is unknown, but could be a subject of further investigation. The SF score has other intrinsic limitations. For instance, someone who eats SF most days of the week, but only eats one item would only have a score of 2. We could, however, consider this an extreme situation that is expected to have no high influence on the results, given the relatively high number of participants included in this study. In general, both the number of SF specialties consumed and the frequency of their consumption may influence the SF score. Two points of the SF score correspond to the habitual consumption of two specialties of SF once a month or less or, alternatively, to the consumption of one specialty of SF more than once a month. Therefore, the SF score likely reflects a tendency toward a nutritional style rather than the amount of habitual energy intake. The calculated SF score was not validated, but did provide interesting information. Indeed, we calculated the SF score using the same criteria for describing habitual SF consumption that we have previously adopted [11], so that comparisons between the two studies are possible. We acknowledge that further validation studies would be needed for an accurate interpretation of what an elevated SF score means. Even the FFQ we used in this study was not validated. However, we present generic half-quantitative data on habitual consumption of different foods and not amounts of energy intake or quantitative amounts of each food. This probably reduces inaccuracy. As we did not enroll a representative cohort of the Palermo population, some bias might be associated with the sampling technique. However, the composition of the cohort we recruited was similar to that reported for the shopping mall customers. The characterization of study participants and the use of a strict ultrasound procedure by two operators that probably helped reduce possible biases are points of strength. In conclusion, this cross-sectional study shows that SF consumption has no significant impact on carotid atherosclerosis in participants with no history of cardiovascular
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disease or diabetes. Only adequate longitudinal studies and interventional trials can definitively clarify the role of SF consumption in influencing atherosclerosis. Nevertheless, given the association of SF consumption with other cardiovascular risk factors, caution requires that this category of food should be limited in patients at high cardiovascular risk. Further studies are also needed to determine whether the nutritional characteristics of SF in other geographic regions are associated with unfavorable cardiovascular and metabolic conditions. Acknowledgments Palermo, Italia.
Associazione
Onlus
Nutrizione
e
Salute,
Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest.
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