Effects of pork vs veal consumption on serum lipids in healthy subjects

Efecto del consumo de cerdo y de ternera sobre el perfil lipídico de sujetos sanos

J. A. Rubio^*, M. A. Rubio^**, L. Cabrerizo^**, P. Burdaspal^***, R. Carretero^***, J. A. Gómez-Gerique^****,
M. T. Montoya^****, M. L. Maestro^*****, M. T. Sanz^***** y C Fernández^******

*Department of Endocrinology and Nutrition. Príncipe de Asturias University Hospital. Alcalá de Henares. Madrid.
**Department of Endocrinology and Nutrition. San Carlos University Hospital. Madrid. ]]> ***Department of Bromatology. Carlos III Institute of Health. Madrid.
****Department of Biochemistry. Jiménez Díaz Foundation. Madrid.
*****Tumoral Biology Section. Department of Clinical Analysis. San Carlos University Hospital. Madrid.
******Department of Clinical Epidemiological Research. San Carlos University Hospital. Madrid. España.

Correspondencia

ABSTRACT

AIMS: To analyse the influence of lean pork (P) and veal (V) consumption on the lipid profile of healthy subjects within the framework of a healthy diet comprising low levels of total fat (TF), saturated fatty acids (SFA) and cholesterol.
DESIGN: Double-crossover, randomized and controlled trial ]]> SUBJECTS: 44 healthy individuals (22 male and 22 female), recruited voluntarily from the University Complutense of Madrid. The weight and lipid profiles of these volunteers were normal and their dietary patterns were typical for people in our area.
INTERVENTIONS: The study comprised 4 phases: stabilisation phase (5 weeks), the participants followed their normal diet; second phase (6 weeks), half of the subjects, were randomised to lean pork or veal consumption, 150 g per day, for their main meal of the day; washout period (5 weeks) and final phase, which was the second phase of intervention (6 weeks). During the intervention stages, only the main meal of the day was taken in the Hospital. The rest of the subjects' diets consisted of different fortnightly menus designed in accordance with the recommendations of the Spanish Society of Arteriosclerosis (SEA).
RESULTS: After both stages of intervention had been completed, there was a mean reduction of 5.5% in lowdensity lipoprotein cholesterol. However, after each intervention there were no significant differences between those who had consumed P, 2.62 (0.55) mmol/L and those who had consumed V, 2.71 (0.47) mmol/L. No differences were observed in any of the other parameters between those who had consumed P and those who had consumed V.
CONCLUSIONS: Lean pork and veal produces similar effects on the lipid profiles of healthy subjects. Its consumption, as part of the saturated fat and cholesterolcontrolled diet, could therefore be included in food guidelines, both for normal and therapeutic diets.

Palabras clave: Cerdo. Ternera. Buey. Carne roja. Lipoproteínas. Lípidos séricos.

RESUMEN

OBJETIVO: Analizar la influencia del consumo de carne magra de cerdo (P) y de ternera (V) en el perfil lipídico de sujetos sanos, cuando se realiza dentro de un patrón de dieta saludable con bajo contenido en grasa total (TF), ácidos grasos saturados (SFA) y en colesterol.
DISEÑO: Ensayo cruzado doble, aleatorizado y controlado.
SUJETOS: 44 sujetos sanos (22 varones y 22 mujeres), reclutados de forma voluntaria de la Universidad Complutense de Madrid. Los pesos y los perfiles lipídicos de estos voluntarios y su patrón de alimentación eran típicos de las personas de nuestra área.
INTERVENCIONES: El estudio consta de 4 fases: fase de estabilización (5 semanas), los participantes seguían su dieta normal; segunda fase (6 semanas), la mitad de los sujetos se randomizaron para que consumieran carne magra de cerdo o de ternera, 150 g al día, durante la principal comida del día; periodo de lavado (5 semanas) y fase final, que era la segunda fase de intervención (6 semanas). Durante las fases de intervención, sólo la principal comida se realizaba en el hospital. El resto de las dietas de los sujetos estaba constituida por menús diferentes para 2 semanas que seguían las recomendaciones de la Sociedad Española de Arteriosclerosis (SEA). ]]> RESULTADOS: Tras ambas intervenciones, hubo una reducción media de un 5,5% en el LDL colesterol. Sin embargo, después de cada intervención no encontramos diferencias significativas entre los que consumieron P, 2.62 (0.55) mmol/L y estos que consumieron V, 2.71 (0.47) mmol/L. No se observó diferencias en el resto de los parámetros analizados entre los que consumieron P y los que consumieron V.
CONCLUSIONES: El consumo de P y B produce efectos similares sobre el perfil lipídico de sujetos sanos. Su consumo, formando parte de dietas controladas en grasa saturada y colesterol, podrían incluirse en pautas alimentarias, tanto de dietas normales como terapéuticas.

Key words: Pork. Veal. Beef. Read meat. Lipoproteins. Serum lipids.

Introduction

Evidence that the mediterranean diet is associated with a low risk of cardiovascular disease, and the effects of each nutrient on lipid profiles, have led to the establish-ment of a dietary model whose basic aim is to reduce the consumption of total fat (TF) and saturated fatty acids (SFA). This model was outlined in a consensus document published by the Spanish Society of Arteriosclerosis¹ which recommended a TF consumption< 35%, an SFA consumption < 10%, a polyunsaturated fat (PUFA) consumption < 7%, and a dietary cholesterol < 300 mg/day. These recommended levels are illustrated in a pyramid structure², where many of the recommended foods are limited in both the normal diet of a healthy population and in therapeutic diets,so maintaining such a diet long-term maybe difficult.

In the last few years, it has been shown that the hyperlipaemic effect of meats is more due to the type of fat contained than to the protein source itself. Therefore, we would not expect lean cuts of meat to have a negative effect on the lipid profile of consumers who are following a fat- and cholesterol-controlled diet^3,4. It has been shown both for normolipaemic subjects^5-8 and for hyperlipaemic subjects^9-11 that the lipid profiles of consumers of lean red meats (beef and pork) who are following a fat-controlled diet are similar to those of consumers of white meats (basically chicken and/or fish). However, not much is known about the effects of consuming lean pork as opposed to lean veal on serum lipid concentrations.

This is important in European diet. So, in Spain, where the consumption of meat of pork (13.3 kg per capita per year), is the second one after the meat of poultry (16.7 kg), and followed by the veal (9.02 kg)¹². The consumption of processed pork (cooked and dry cured products), which has a long tradition, is also important (15.8 kg). Dietary recommendations for preventing hyperlipaemia usually restrict the overall consumption of both lean and processed pork.

This paper compares how lean pork consumption and lean veal consumption, as part of the fat- and cholesterol- controlled diet recommended by the Spanish Society of Arteriosclerosis, affect the lipid profiles of healthy subjects.

Subject

One hundred and twenty-six healthy subjects responded to a public announcement by the Complutense University of Madrid inviting volunteers to participate in the study.

Sample size was calculated for an expected reduction in LDL cholesterol concentrations around 0.25 mm/L (8.3 %), considering a type I error probability of 0.05, statistical power of 90 % and a prediction of drop-outs in the follow-up up to of 30 %; so, the sample size calculated was 44 individuals.

Inclusion criteria comprised normal weight subjects (Body Mass Index between 18.5-25 kg/m²), both sexes, and without evidence of any systemic disease or taking any medication. Individuals with total cholesterol concentration ≥ 6.2 mmol/L or < 3.87 mmol/L, low-density lipoprotein (LDL) cholesterol ≥ 4.13 mmol/L or < 2.06 mmol/L, triglycerides ≥ 2.25 mmol/L or high-density lipoprotein (HDL) cholesterol< 0.9 mmol/L were excluded. Regular alcohol consumption> 20 g/day and /or tobacco consumption >10 cigarettes/day, as well as physical exercise > 4186 kJ per week or an evidence for energy consumption < 6279 kJ per day or < 30% of energy in TF were also excluded from the study to avoid a possible bias due to its influence on lipid metabolism.

Of the 126 subjects, 44 subjects (22 men and 22 women) met all inclusion criteria. Informed written consent was obtained from all subjects and the Protocol was approved by the Hospital Ethics Committee.

Study design

This was a double-crossover, randomised and controlled trial to compare the effects on LDL cholesterol concentrations, of consuming lean pork with the effects of consuming lean veal. The null hypothesis would be meet if the LDL cholesterol concentrations of subjects who consumed lean pork and subjects who consumed lean veal showed no significant differences.

During the subjects' first visit, we recorded their case histories, collected anthropometric data and blood samples were obtained in order to check the criteria for inclusion and exclusion. During the five-week stabilisation phase, the participants were asked to follow their normal diet. This diet was to be typical of the diet of the general population¹². During the intervention phase, 22 subjects were randomly allocated to consume lean pork (P) and the other 22 were to consume lean veal (V) for their main meal of the day, which was prepared in the San Carlos University Hospital. Subjects received dietary counselling, which included a rotatory system of menus every fortnight and a food exchange list. These menus were designed in accordance with the main recommendations of the SEA1. Meat was only consumed during the main meal of the day. After this first phase of intervention, the subjects were asked to again follow their normal diet for 5 weeks. This was the washout phase. Finally, during the second phase of intervention, which lasted 6 weeks, the subjects who had consumed pork during the first phase of intervention now consumed veal, and viceversa. By means of this crossover system, each subject acted as his or her own control.

Analysis of diet, meats and menus

These bromatological data were used to design the various diets. The menus were then prepared using the food composition tables of Wander-Novartis Health Consumer S.A.¹⁵. Energy estimates were made in accordance with data on calorie consumption obtained from the food records obtained at the subject-selection stage. These were then adjusted to match the energy estimates proposed by the WHO¹⁶. All food except the main meal of the day (lunch), which was prepared and eaten in the Hospital, was consumed at home (under free-living conditions) following the rotatory system of menus. In the lunch, lean read meats, pork or veal (150 g) was consumed. Subjects were allowed to make rational exchanges of the ingredients within each food group.

To make sure that the theoretical estimates matched those of our study, bromatological analysis of the menus prepared in the hospital kitchens was carried out in triplicate according to the same official procedure as that used to analyse the meats.

Compliance

Study compliance was determined using the records of assistance of the subjects to the programmed visits and to the main meal of the day in the Hospital. Diet compliance was realized by quantitative (computerized)analysis of seven-day diet records (by means a nutritional software: Wander-, Novartis Nutrition, Barcelona, Spain).

Blood analysis

After 12 hour overnight fast, blood samples were drawn to determine total cholesterol, triglycerides, HDL cholesterol and apolipoproteins (apo A-I and B) concentrations at the subject-recruitment phase, in the fifth weeks of the stabilisation and washout phases, and in the fifth and sixth weeks of both phases of intervention. Total choles-erol was determined by the CHOD-PAP enzymatic method of Boehringer, Mannheim, Germany¹⁷ and triglycerides were determined by the GPO-PAP enzymatic method of Boehringer, Mannheim, Germany¹⁸. HDL cholesterol was determined by precipitation of VLDL and LDL using phosphotungstic acid-Mg⁺⁺ and quantification of the cholesterol concentration in the supernatant, Boehringer, Mannheim, Germany19. Inter-assay variation coefficients were < 3% for total cholesterol, triglycerides and HDL-cholesterol. LDL-cholesterol was estimated by the Friedewald formula²⁰. Apo A-I and Apo B were determined by the nephelometric method²¹ and the interassay variation coefficients were 5%.

The genotype of the apo E obtained from total blood was also determined by the standard Quiagen_ method (Izasa, Madrid, Spain) and PCR using allele-specific oligonucleotide probes to detect the cysteine-arginine interchanges at residues 112 and 158 that distinguish the three common isoforms of apo E: E2, E3 and E4²².

Statistical analysis

We compared the means of the variables at the beginning and at the end of both phases of intervention using the paired Student t-test. Multivariate variance was analysed for repeated measurements with one or two factors (type of meat assigned, time and gender). The level of significance was p < 0.05.

Results

Subjects

The two groups of subjects were well matched with regard to baseline characteristics (table I). The subjects' weights did not change during the various phases of the study: men +0.1 (1.17) kg (p = 0.625); women +0.1 (1.03) kg, (p = 1). Subject participation was high: 100 % in programmed visits, blood analyses and nutritional records. Ninety seven of percentage came along at the hospital for the main meal. All the subjects completed the study.

Analysis of meats and menus

Table II shows that the fat contents of the lean cuts of pork and lean cuts of veal were low and that there were no differences between the two types of meat. However the content of oleic acid was significantlyhigher in pork than in veal (51.1% as opposed to 40.7%; p = 0.036), though there was no significant differences in total MUFA content between pork and veal. Neither bromatologic analysis of menus revealed significant differences in nutrients between both types of meats (table III).

Serum lipids and lipoproteins

Lipid and lipoprotein concentrations are shown intable V, which shows the changes in lipid concentrations after each intervention, where we found no significant differences between pork consumption or veal consumption.

If there were significant differences in the total cholesterol and LDL cholesterol after both pork consumption (-5.2% and -6.5%, respectively) and veal consumption (-4.3% and -4.1%, respectively). The reduction in triglycerides was significant only after veal consumption. There were also significant decrease in the concentrations of apo A-I after both pork consumption (-8.48%) and veal consumption (-10.2%). (table V)

Multivariate analysis revealed no differences between changes to lipid concentrations after each intervention (i.e. after the first or second phase of intervention) or according to gender.

Genotype of the apo

E Thirty-four subjects (77.2%) in the study had genotype E3/E3, 8 subjects (18.2%) had genotype E4/E3, and 2 subjects (4.6%) had genotype E2/E3. When we analysed the concentrations of lipids according to genotype (see table VI), we found that the subjects with genotype E3/E3 had higher concentrations of triglycerides and LDL cholesterol than subjects with genotype E4/E3 at the baseline, but the changes observed after both interventions (pork and veal consumption) were similar for both of these genotypes.

Discussion

We had a great control over the variables that could affect the results of the study. The meats used in the study contained low levels of fat (4.5% for pork; 5.5% for veal). The same analysis showed that the cuts of pork contained slightly greater contents of PUFA and MUFA than the cuts of veal, but the only significant differences involved the greater content of oleic acid in the pork. These results are widely documented in the literature²⁴. The pig crossbreed used in this study was a Landrace-Large White pig, which was fed a mixture of barley, wheat, corn and soy meal. This meat, which is marketed under the brand name Porcidiet (TM) and commercialized by Vaquero Meat Industries has a low intramuscular fat content (<3 %) and low cholesterol (46 mg/100g)²⁵.

However, these differences in fatty acids profile disappeared when we analysed the nutrients and fat contents of the diets designed for the study and the nutritional composition of the menus prepared in the Hospital kitchens. We can therefore state that on a macronutrient point of view, the two types of intervention (pork and veal consumption) were similar except for the protein origin of the meats themselves.

When we analysed the subjects' nutritional records, we found that during both phases of intervention there was a decrease in energy consumption, however it was not associated with loss of weight, so energy balance was maintained. The reductions in the consumption of TF, SFA and cholesterol were similar for both phases of intervention. Studies comparing changes in serum lipid concentrations after the consumption of red meat, white meat and fish have varied greatly in the degree of control they have exercised over the variables involved. Most of these studies only controlled intake through foods records. Few of them analysed the nutritional composition of the meats^6,7,10,26 or menus^10,27 used.

The compliance at different level of participation in our study was practically 100%, so we can state with a fair degree of certainty what percentage of subjects complied with the dietary intervention designed for the study. In most studies we have checked, the meats were prepared at home by the subjects themselves. This introduces variability factors, such as menu preparation by the subjects and the real percentage of consumption, which depend on the subjects themselves.

Our findings show that there were no changes to serum lipid concentrations after the consumption of pork and veal, by what the null hypothesis was fulfilled. These results are similar to those of other authors who compared the consumption of red meats (beef and pork) and the consumption of fish and/or white meat (chicken) in healthy normolipaemic subjects^5-8,27. Only one study (29) found a greater decrease in LDL cholesterol concentrations in subjects who had consumed fat fish than in subjects who had consumed red meat. However, during the period of study (six weeks), they found that the intake of SFA of those who had consumed red meat increased, while that of those who had consumed fat fish decreased. The beneficial effect of consuming fish as opposed to red meat is therefore probably due to a reduction in SFA intake. None of the above studies analysed the effects on serum lipids after the consumption of veal or pork; though the study by Flynn et al.⁷, found that the concentrations of LDL cholesterol after pork consumption and after beef consumption were similar. However, this study has some methodological bias, like the absence of controlling fat intake and the lack of a washout period between the phases of intervention.

Similar results have been found with regard to hyperlipaemic subjects in studies comparing the consumption of red meat and the consumption of white meat (chicken or fish)^9-11,30, where the overall reductions in total cholesterol and LDL cholesterol after both interventions (4-6%) is attributable to the intake reduction of TF, SFA and dietary cholesterol^31,32 and non by the consumption of meat. Our results are agreed in the same direction that these studies.

The reductions we found in the concentrations of apo A-I after the consumption of pork (-8.5%) and veal (-10.2%) were not different and were as expected following the reduction in total cholesterol and LDL cholesterol due to dietary intervention. The reduction in apo A-I was similar to those reported in studies involving changes from a normal diet to a diet rich in MUFA³³.

Analysis of serum lipids according to the most common genotypes of apo E (E3/E3 and E4/E3) showed that the concentrations of triglycerides and LDL cholesterol were greater for the E3/E3 genotype than for the E4/E3 genotype. This result did not agree with previous reports³⁴ , which found high cholesterol concentrations for E4 allele, intermediate concentrations for E3 and low concentrations for E2. This was probably due to the small sample of genotype E4/E3 (n = 8) used in our study. Changes to serum lipid concentrations according to the genotype of apo E, which were similar to those of the two genotypes analysed, also did not agree with the results of other authors^35,36, who found that the reduction in lipids was greater with E4 allele. However, this result has mainly been found in hyperlipaemic subjects³⁷ rather than in normolipaemic subjects such as those in our study.

Our study has important practical considerations, especially if we bear in mind that pork is recognised as an important part of the European diet. So, Spain is one of the countries with the highest meat consumption across Europe, achieving a 15% of daily energy intake³⁸. In recent years, however, consumers' perceptions of pork have not been so good because they believe it contains a high amount of visible fat with a high content of saturated fatty acids. Modern techniques of pig breeding and feeding are producing a leaner meat whose lipids contain a greater proportion of unsaturated fatty acids. Actually, fatty acid composition mainly depends on genetic origin, age, weight at slaughter, feed composition and the husbandry system.

Acknowledgements

This work was supported by grant FIS 98/0679 and the Vaquero Foundation.

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Correspondencia:
J. A Rubio
Department of Endocrinology and Nutrition.
Hospital Universitario Príncipe de Asturias. ]]> Carretera Alcalá Meco s/n. Alcalá de Henares.
Madrid 28800. Spain.
E-mail: josearubio@terra.es

Recibido: 0-IV-2005.
Aceptado: 06-VI-2005.