Accessibility / Report Error

Lipid Assessment, Cholesterol and Fatty Acid Profile of meat from broilers raised in four different rearing systems

Abstract

Evaluated lipid and cholesterol concentration and fatty acid profile of raw breast, thigh and drumstick meat from broilers raised in different rearing systems. Were used 200 male broiler carcasses from four different rearing systems (n=50 from conventional intensive; n=50 from organic; n=50 from free-range; and n=50 from antibiotic-free) distributed in a completely randomized design with four rearing systems and 50 replications (carcasses). Breast meat from conventional broilers showed higher lipid (1.47) and cholesterol (34.13) concentration. Thigh and drumstick meat from free-range broilers had higher lipid (7.53/4.73) and cholesterol (45.55/53.65) concentration. Fat contained in breast, thigh and drumstick meat from free-range broilers showed higher levels of polyunsaturated fatty acids. Fat from breast and thigh meat from free-range broilers showed higher total concentration of ω3 and ω6 fatty acids. Fat from thigh meat from organic broilers showed higher levels of EPA (C20:5n3) and DHA (C22:6n3). Fat from drumstick meat from free-range broilers showed higher total concentration of ω3 and ω6 fatty acids. Meat from chickens raised in alternative rearing systems offers less risk to cardiovascular health because it presents lower concentrations of lipids and cholesterol, greater amounts of polyunsaturated fatty acids, which are beneficial for human health.

Key words
breast; drumstick; free-range; organic; thigh

INTRODUCTION

Brazil currently ranks second in the ranking of production and the first place among the world exporters of chicken meat (ABPA 2016ABPA - BRAZILIAN ASSOCIATION OF ANIMAL PROTEIN. 2016. Annual report 2016. Accessed May. 2017. http://abpabr.com.br/setores/avicultura/publicacoes/relatorios-anuais.
http://abpabr.com.br/setores/avicultura/...
) and one of the reasons for the success of the Brazilian poultry industry is the consumer’s search for healthier meat products than the traditional red meat. Chicken breast meat can be considered important in diets because it contains a higher proportion of polyunsaturated fatty acids, when compared to meat of other species (Berzaghi et al. 2005BERZAGHI P, DALLE ZOTTE A, JANSSON LM & ANDRIGHETTO I. 2005. Near-infrared reflectance spectroscopy as a method to predict chemical composition of breast meat and discriminate between different n-3 feeding sources. Poult Sci 84: 128-136., Riovanto et al. 2012RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.).

The strategies used in aviculture, related to the animal breeding, cause the meat produced satisfy desirable nutritional characteristics, such as low fat content and relatively high concentrations of polyunsaturated fatty acids (Nkukwana et al. 2014NKUKWANA TT, MUCHENJE V, MASIKA PJ, HOFFMAN LC, DZAMA K & DESCALZO AM. 2014. Fatty acid composition and oxidative stability of breast meat from broiler chickens supplemented with Moringa oleifera leaf meal over a period of refrigeration. Food Chem 142: 255-261.) which have a known beneficial action in reducing the risk of cardiovascular diseases, hypertension, diabetes, inflammatory and immunological disorders (Zhou et al. 2012ZHOU LJ, WU H, LI JT, WANG ZY & ZHANG LY. 2012. Determination of fatty acids in broiler breast meat by near-infrared reflectance spectroscopy. Meat Sci 90: 658-664.). Thus, fat intake through food became a risk factor due to the possible consequences (Leosdottir et al. 2005LEOSDOTTIR M, NILSSON PM, NILSSON J-Å, MÅNSSON H & BERGLUND G. 2005. Dietary fat intake and early mortality patterns – data from The Malmӧ diet and cancer study. J Intern Med 258: 153-165.). The American Heart Association (2004) recommends that daily fat intake does not exceed 30% of total calories and that saturated fat intake is not more than 10%.

Lipids are essential fats for normal growth and development of all animals. The functions of these fats range from source of energy, transport and absorption of vitamins, protection of organs, physical and thermal insulation, hormone precursors in the organism and they are extremely important in texture, flavor, palatability, color and preservation of food. Meat is an important source of lipids in the human diet and its consumers are increasingly interested in fat composition, since nutritional guidelines recommend reducing total fat intake, especially saturated fat, and increasing polyunsaturated fat (Sierra et al. 2008SIERRA V, ALDAI N, CASTRO P, OSORO K, COTO-MONTES A & OLIVA M. 2008. Prediction of the fatty acid composition of beef by near infrared transmittance spectroscopy. Meat Sci 78: 249-255., De Marchi et al. 2012DE MARCHI M, RIOVANTO R, PENASA M & CASSANDRO M. 2012. At-line prediction of fatty acid profile in chicken breast using near infrared reflectance spectroscopy. Meat Sci 90: 653-657).

Although the genetic (Zanetti et al. 2010ZANETTI E, DE MARCHI M, DALVIT C, MOLETTEC, REMIGNON H & CASSANDRO M. 2010. Carcass characteristics and qualitative meat traits of three Italian local chicken breeds. British Poult Sci 6: 629-634., Riovanto et al. 2012RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.) influences the functional and nutritional meat properties (Sirri et al. 2011SIRRI F, CASTELLINI C, BIANCHI M, PETRACCI M, MELUZZI A & FRANCHINI A. 2011. Effect of fast-, medium- and slow-growing strains on meat quality of chickens reared under the organic farming method. Animal 5: 312-319.), the feed (Rymer & Givens 2005RYMER C & GIVENS DI. 2005. N-3 fatty acid enrichment of edible tissue of poultry: A review. Lipids 40: 121-130., Riovanto et al. 2012RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.) and the rearing conditions may also influence fatty acid composition and, consequently, the meat oxidative stability (Jung et al. 2010JUNG S, CHOE JH, KIM B, YUN H, KRUK ZA & JO B. 2010. Effect of dietary mixture of gallic acid and linoleic acid on antioxidative potential and quality of breast meat from broilers. Meat Sci 86: 520-526., Nkukwana et al. 2014NKUKWANA TT, MUCHENJE V, MASIKA PJ, HOFFMAN LC, DZAMA K & DESCALZO AM. 2014. Fatty acid composition and oxidative stability of breast meat from broiler chickens supplemented with Moringa oleifera leaf meal over a period of refrigeration. Food Chem 142: 255-261.). And the fatty acid profile of broiler fat can be directly influenced by the lipid source used in animal diet rations (Husak et al. 2008HUSAK RL, SEBRANEK JG & BREGENDAHL K. 2008. A survey of commercially available broilers marketed as organic, free-range, and conventional broilers for cooked meat yields, meat composition, and relative value. Poult Sci 87: 2367-2376.).

Moreover, the variation in fatty acid composition affects the technological, nutritional and sensory meat properties (Wood et al. 2003WOOD JD, RICHARDSON RI, NUTE GR, FISHER AV, CAMPO MM, KASAPIDOU E, SHEARD PR & ENSER M. 2003. Effects of fatty acids on meat quality: A review. Meat Sci 66: 21-32., De Marchi et al. 2012DE MARCHI M, RIOVANTO R, PENASA M & CASSANDRO M. 2012. At-line prediction of fatty acid profile in chicken breast using near infrared reflectance spectroscopy. Meat Sci 90: 653-657, Riovanto et al. 2012RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.), however, high PUFA contents, although beneficial to health, is often associated with the occurrence of oxidation and rancidity (Wood et al. 2003WOOD JD, RICHARDSON RI, NUTE GR, FISHER AV, CAMPO MM, KASAPIDOU E, SHEARD PR & ENSER M. 2003. Effects of fatty acids on meat quality: A review. Meat Sci 66: 21-32., De Marchi et al. 2012DE MARCHI M, RIOVANTO R, PENASA M & CASSANDRO M. 2012. At-line prediction of fatty acid profile in chicken breast using near infrared reflectance spectroscopy. Meat Sci 90: 653-657), which negatively affects the shelf life (Flåtten et al. 2005FLÅTTEN A, BRYHNI EA, KOHLER A, EGELANDSDAL B & ISAKSSON I. 2005. Determination of C22:5 and C22:6 marine fatty acids in pork fat with Fourier transform midinfrared spectroscopy. Meat Sci 69: 433-440., De Marchi et al. 2012DE MARCHI M, RIOVANTO R, PENASA M & CASSANDRO M. 2012. At-line prediction of fatty acid profile in chicken breast using near infrared reflectance spectroscopy. Meat Sci 90: 653-657, Zhou et al. 2012ZHOU LJ, WU H, LI JT, WANG ZY & ZHANG LY. 2012. Determination of fatty acids in broiler breast meat by near-infrared reflectance spectroscopy. Meat Sci 90: 658-664.) and makes it important the monitoring the fatty acid profile so that the industries can assign each type of meat to direct consumption or to other processes (Riovanto et al. 2012RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.).

Thus, the aim of this study was to evaluate the lipid and cholesterol concentration, as well as the fatty acid profile of raw breast, thigh and drumstick meat from broilers raised in different rearing systems.

MATERIALS AND METHODS

This research was developed at the Laboratory of Animal Products Technology of the Faculty of Agricultural and Veterinary Sciences at UNESP, Jaboticabal Campus, São Paulo, Brazil (21°08’ S, 48°11’ W, 583 m altitude).

Samples and experimental procedures

To analyze lipids, cholesterol and fatty acids, were used 200 male broiler carcasses from four different rearing systems (n=50 from conventional intensive rearing system; n=50 from organic rearing system; n=50 from free-range rearing system; and n=50 from antibiotic-free rearing system), which were acquired from commercial slaughterhouses (São Paulo, SP, Brazil) inspected by the Brazilian Federal Inspection Service.

Cobb broilers raised in conventional rearing system were confined in closed sheds at a maximum density of 40 kg/m², and slaughtered at 42 d of age. In organic system, Cobb broilers received feed containing certified organic ingredients; from 25 d of age, birds were confined in closed sheds with access to a grazing area at a maximum density of 30 kg/m², grazing area of 100 m² per m² shed and were slaughtered at 48 d of age. In free-range rearing system, ISA Label broilers were raised in closed sheds with a maximum density of 30 kg/m² and, from 28 d of age, birds had access to paddocks with density of, at least, 3 m² of area available for each bird housed. Broilers raised in free-range rearing system were slaughtered at 85 d of age. In antibiotic-free rearing system, Cobb broilers were raised in conventional closed sheds, with no access to grazing area, at a maximum density of 30 kg/m² and were slaughtered at 45 d of age. Broilers were fed a diet containing certified organic ingredients, devoid of animal ingredients and antibiotics, and were slaughtered at 48 days of age. Broilers were fed the diet shown in Table I.

Table I
Composition and calculated nutrient content of diets (as-fed basis).

In the slaughterhouse, 50 broiler carcasses, from four rearing systems studied, were collected following the flowchart of commercial slaughtering, meeting the requirements of animal welfare and regulations of the federal inspection service of the Ministry of Agriculture, Livestock and Supply. After the completion of rigor mortis (around four hours after slaughter), carcasses were divided into their main cuts(breast, n=50 for each rearing system; thigh, n=50 for each rearing system; drumstick n=50 for each rearing system).

Methods

Fat was performed in triplicate and analyzed according to the procedure 991.36 recommended by AOAC (2005)AOAC. ‘OFFICIAL METHODS OF ANALYSIS. 2005. 18th ed., Association of Analytical Chemists, Washington, DC.. The total cholesterol was determined according to the methodology described by Bohac et al. (1988)BOHAC CE, RHEE KS, CROSS HR & ONO K. 1988. Assessment of methodologies for colorimetric cholesterol assay of meats. J. of Food Sci 53: 1642-1693., adapted by Bragagnolo & Rodriguez-Amaya (1992)BRAGAGNOLO N & RODRIGUEZ-AMAYA DB. 1992. Cholesterol content of chicken meat. Rev Farm Bioquim Univ São Paulo 28: 122-131., in which 10 g of ground raw sample was submitted to the extraction of lipids with chloroform and methanol (2:1). Thereafter, a 10 mL aliquot of the chloroform extract was evaporated with gaseous nitrogen and submitted to saponification with KOH 12% alcoholic solution. The unsaponifiable fraction (cholesterol) was extracted with n-hexane, purified and submitted to color reaction with acetic acid and sulfuric acid, using ferrous sulfate as catalyst. Absorbance was read on a spectrophotometer at 490 nm.

Fatty acids were isolated from samples according to the method proposed by Bligh & Dyer (1959)BLIGH GE & DYER JW. 1959. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917., which extracts the lipid phase from the sample. The fatty acid esterification was carried out according to the method proposed by Maia & Rodriguez-Amaya (1993)MAIA EL & RODRIGUEZ-AMAYA DB. 1993. Avaliação de um método simples e econômico para metilação de ácidos graxos de lipídeos de diversas espécies de peixes. Rev Inst Adolfo Lutz 53: 27-35. using a gas chromatograph (Shimadzu 14B, Shimadzu Corporation, Kyoto, Japan) equipped with a flame ionization detector and a fused silica capillary column (Omegawax 250); H2 was used as the carrier gas. The identification of peaks was made by comparison with the retention times of standards with known composition.

Statistical analysis

Data were analyzed using a completely randomized design with four rearing systems (conventional, organic, antibiotic free and free-range rearing systems) and 50 replications (carcasses). Results of the breast, thigh and drumstick meat from each carcass were analyzed. Data were analyzed by One-way ANOVA using SAS (SAS Institute Inc 2002, 2003SAS. 2002, 2003. Institute Inc. ‘SAS Version 9.1.’ (SAS Institute Inc.: Cary, NC).). All data were tested by analysis of variance and compared by Tukey’s test with a significance level of P < 0.05.

RESULTS

Lipid profile of breast meat

Breast meat from broilers raised in conventional rearing system showed higher lipid concentration than meat from broilers raised in antibiotic-free rearing system (Table II). Breast meat from broilers raised in organic and free-range rearing systems showed the same amount of lipid as meat from broilers raised in conventional and antibiotic-free rearing systems. Breast meat from broilers raised in conventional and antibiotic-free rearing systems had higher cholesterol levels than breast meat from broilers raised in organic and free-range rearing systems.

Table II
Lipids (%) and cholesterol (mg/100g) of breast meat and fatty acid composition (% of total fatty acids) of fat from breast meat from broilers raised in different rearing systems.

The fat contained in breast meat from broilers raised in conventional system had the highest (P<0.001) levels of saturated fatty acids (SFA) and monounsaturated fatty acids (MUFA) and the lowest (P<0.001) levels of polyunsaturated fatty acids (PUFA). Meat from broilers raised in free-range and antibiotic-free rearing systems showed higher (P<0.001) levels of PUFA (36.38%) than meat from broilers raised in conventional (18.33%) and organic (29.88%) rearing systems. In the same way, breast meat from free-range and antibiotic-free broilers showed higher PUFA/SFA ratio than the breast meat from broilers raised in conventional and organic rearing systems.

There were no differences (P>0.05) regarding to C10:0 and C20:0 fatty acids concentration in fat from breast meat from broilers raised in different rearing systems. Fat contained in breast meat from broilers raised in conventional rearing system showed higher values for almost all fatty acids, with exception for C24:1n9. Among PUFA, fat from conventional broilers had lower concentration than the others, mainly EPA (C20:5n3) and DHA (C22:6n3). Higher levels of PUFA were verified in fat from breast meat from broilers raised in alternative systems. There were no differences (P>0.05) between analyzed groups regarding to C18:2c9,t11 concentration. Breast meat from organic broilers showed higher levels of C18:3n6, C20:2, C20:3n6, C20:4n6, C20:5n3, C22:4n6 and C22:6n3 fatty acids, highlighting organic system among all studied rearing systems, with respect to the concentration of polyunsaturated fatty acids.

The fat contained in breast meat from broilers raised in free-range and antibiotic-free rearing systems showed higher total concentration of ω3 (2.59%) and ω6 (33.48%) fatty acids than the others. Fat from breast meat from conventional broilers showed higher ω6/ω3 ratio (~36:1) than fat from breast meat from broilers raised in alternative rearing systems (~14:1, on average).

Lipid profile of thigh meat

Thigh meat from broilers raised in organic and free-range rearing systems showed higher (P<0.0001) lipid concentration (7.05%, on average) than meat from broilers raised in conventional (4.82%) and antibiotic-free (3.30%) rearing systems (Table III). Thigh meat from broilers raised in free-range rearing system had higher (P<0.0001) cholesterol levels (45.55 mg/100g) than thigh meat from broilers raised in conventional (35.33 mg/100g), organic (39.58 mg/100g) and antibiotic-free (33.59 mg/100g) rearing systems.

Table III
Lipids (%) and cholesterol (mg/100g) of thigh meat and fatty acid composition (% of total fatty acids) of fat from thigh meat from broilers raised in different rearing systems.

As the fat contained in breast meat, the fat contained in thigh meat from broilers raised in conventional system had the highest (P<0.001) levels of saturated fatty acids (SFA) and monounsaturated fatty acids (MUFA) and the lowest (P<0.001) levels of polyunsaturated fatty acids (PUFA). Fat contained in thigh meat from broilers raised in alternative rearing systems showed lower (P=0.0003) levels of saturated fatty acids. Thigh meat from broilers raised in free-range rearing system showed higher (P<0.001) levels of PUFA (34.48%) than thigh meat from broilers raised in conventional (21.25%), organic (26.70%) and antibiotic-free (26.51%) rearing systems. Thigh meat from free-range broilers showed higher PUFA/SFA ratio (1.18) than the thigh meat from broilers raised in conventional (0.58), organic (0.83) and antibiotic-free (0.78) rearing systems. There was no difference (P>0.05) only for the C10:0 fatty acid concentration between studied groups. Fat contained in thigh meat from organic broilers showed higher (P<0.001) levels of EPA and DHA. In this study no EPA levels were detected in thigh meat from conventional broilers.

The fat contained in thigh meat from broilers raised in free-range rearing system showed higher total concentration of ω3 (2.33%) fatty acids than the others. The fat contained in thigh meat from broilers raised in free-range rearing systems showed higher total concentration of ω6 (31.90%) than conventional (19.95%), organic (25.02%) and antibiotic-free (24.80%) rearing systems. Fat from thigh meat from free-range broilers showed lower ω6/ω3 ratio (~14:1) than fat from thigh meat from broilers raised in other studied rearing systems (~17:1).

Lipid profile of drumstick meat

Drumstick meat from broilers raised in free-range rearing system showed higher (P=0.0003) lipid concentration (4.73%) than meat from broilers raised in other rearing system (3.45%, on average) (Table IV). As for thigh meat, drumstick meat from broilers raised in free-range rearing system had higher (P<0.0001) cholesterol levels (53.65 mg/100g) than drumstick meat from broilers raised in conventional (37.38 mg/100g), organic (46.89 mg/100g) and antibiotic-free (49.02 mg/100g) rearing systems.

Table IV
Lipids (%) and cholesterol (mg/100g) of drumstick meat and fatty acid composition (% of total fatty acids) of fat from drumstick meat from broilers raised in different rearing systems.

Unlike what was observed for breast and thigh meat, the highest (P<0.001) level of saturated fatty acids (39.68%) was observed in fat from drumstick meat from antibiotic-free broilers, while fat from drumstick meat from free-range broilers showed the lowest level of SFA (27.69%) between evaluated groups. The fat contained in drumstick meat from free-range broilers showed higher PUFA concentration (37.94%) than fat contained in drumstick meat from conventional (14.33%), organic (22.78%) and antibiotic-free (26.08%) broilers.

Regarding to fatty acid composition of fat from drumstick meat from broilers raised in different rearing systems, it was detected significant difference for all fatty acids tested, wherein the highest levels of EPA were verified in drumstick meat from organic and free-range broilers and, the highest level of DHA was verified in drumstick meat from free-range broilers. The fat contained in drumstick meat from broilers raised in free-range rearing system showed higher total concentration of ω3 (2.82%) and ω6 (34.75%) fatty acids than the others. Fat contained in drumstick meat from free-range and antibiotic-free broilers showed lower ω6/ω3 ratio (~12:1) than fat from drumstick meat from broilers raised in other studied rearing systems (~26:1, on average).

DISCUSSION

Lipid content

The consumer’s preference is influenced by the variation of the quality of chicken meat available in the market and may be affected by factors such as bird feeding, strain, age, gender and slaughter processing (Rodrigues et al. 2008RODRIGUES KF, RODRIGUES PB, BRESSAN MC, NAGATA AK, SILVA JHV & SILVA EL. 2008. Qualidade da carne de peito de frangos de corte recebendo rações com diferentes relações lisina digestível: proteína bruta. R Bras Zootec 37: 1023-1028.). Some studies (Castellini et al. 2006CASTELLINI C, DAL BOSCO A, MUGNAI C & PEDRAZZOLI M. 2006. Comparison of two chicken genotypes organically reared: oxidative stability and other qualitative traits of the meat. Italian J. Animal Sci 5: 355-363., Lonergan et al. 2003LONERGAN SM, DEEB N, FEDLER CA & LAMONT SJ. 2003. Breast meat quality and composition in unique chicken populations. Poult Sci 82: 1990-1994., Faria et al. 2009FARIA PB, BRESSAN MC, SOUZA XR, RODRIGUES EC, CARDOSO GP & GAMA LT. 2009. Composição proximal e qualidade da carne de frangos das linhagens Paraíso Pedrês e Pescoço Pelado. R Bras Zootec 38: 2455-2464.) have reported that broilers of fast-growing strains tend to have a higher concentration of fat in breast meat than chickens from slow-growing or crossbred strains; and Husak et al. (2008)HUSAK RL, SEBRANEK JG & BREGENDAHL K. 2008. A survey of commercially available broilers marketed as organic, free-range, and conventional broilers for cooked meat yields, meat composition, and relative value. Poult Sci 87: 2367-2376., observed a lower amount of fat in chicken meat from broilers raised in organic rearing system than in meat from conventional broilers, possibly due to the greater locomotion and other activities due to grazing access.

Animals from the same lineage may exhibit differentiated fat deposition (Faria et al. 2009FARIA PB, BRESSAN MC, SOUZA XR, RODRIGUES EC, CARDOSO GP & GAMA LT. 2009. Composição proximal e qualidade da carne de frangos das linhagens Paraíso Pedrês e Pescoço Pelado. R Bras Zootec 38: 2455-2464.), depending on the slaughter age, since increasing age results in greater fat deposition. In this study, it was observed that the breast meat from Cobb broilers raised in a conventional system and slaughtered at 42 days of age, had higher (P = 0.0400) lipid concentration (1.47) than breast meat from Cobb broilers raised in antibiotic-free (0.93) system and slaughtered at 45 days of age, suggesting that the breeding system, besides the slaughter age, influences the carcass fat deposition. The chicken meat shows variable fat concentration, depending on the evaluated cut (Givens et al. 2011GIVENS DI, GIBBS RA, RYMER C & BROWN RH. 2011. Effect of intensive vs. free range production on the fat and fatty acid composition of whole birds and edible portions of UK retail chickens. Food Chem 127: 1549-1554., Dalziel et al. 2015DALZIEL CJ, KLIEM KE & GIVENS DI. 2015. Fat and fatty acid composition of cooked meat from UK retail chickens labelled as from organic and non-organic production systems. Food Chem 179: 103-108.) and, differently that was reported in the literature, in this study was found a greater amount of fat in thigh (6.57/7.53) and drumstick (3.51/4.73) meat from broilers raised with grazing access (organic and / or free-range) than in meat from confined broilers.

Cholesterol content

In contrast to that observed for breast meat, wherein was found higher (P<0.0001) cholesterol concentration in breast meat from confined broilers, thigh and drumstick meat from free-range broilers showed higher (P <0.0001) cholesterol concentration than thigh and drumstick meat from conventional, organic and antibiotic-free broilers.

Cholesterol is an important molecule of the membranes structure and is a precursor of steroid hormones, vitamin D and bile acids; it can be obtained directly from the diet or synthesized by biosynthesis de novo, allowing cholesterol production required to meet the needs of the large variety of biological processes which is involved (Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.). The total cholesterol levels in meat plays an important biological role because they are closely related to cardiac diseases (Salma et al. 2007SALMA U, MIAH AG, MAKI T, NISHIMURA M & TSUJII H. 2007. Effect of dietary rhodobactercapsulatus on cholesterol concentration and fatty acid composition in broiler meat. Poult Sci 86: 1920-1926.), such as obstruction of the coronary veins caused by the fatty material accumulation (cholesterol, calcium, blood cells, and the cells from the arterial wall), and may evolve over time, reducing the blood flow and also making the individual more susceptible to thrombus or clots (Chou & Friedman 2016CHOU CS & FRIEDMAN A. 2016. Atherosclerosis: The Risk of High Cholesterol. In: Introduction to Mathematical Biology. Available at <http://link.springer.com/chapter/10.1007/978-3-319-29638-8_12>[Verified 06 July 2016].
http://link.springer.com/chapter/10.1007...
). The compromising of normal heart functioning can affect consumer acceptance of some kinds of meat and, therefore, there has been increasing interest in recent years in modulating of the cholesterol concentration and fatty acid composition in chicken meat products (Sacks 2002SACKS FM. 2002. The role of high-density lipoprotein (HDL) cholesterol in the prevention and treatment of coronary heart disease. Am J Cardiol 15: 139-143., Salma et al. 2007SALMA U, MIAH AG, MAKI T, NISHIMURA M & TSUJII H. 2007. Effect of dietary rhodobactercapsulatus on cholesterol concentration and fatty acid composition in broiler meat. Poult Sci 86: 1920-1926.).

Ponte et al. (2008)PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88. obtained results of cholesterol levels in breast meat from free-range chickens equal to 48 mg/100g, a lower concentration than that found in meat from conventional chickens (56 mg/100g). The results obtained in the present study are below than results published in the literature (47.11 mg/100g, Ponte et al. 2004PONTE PIP, MENDES I, QUARESMA M, AGUIAR MNM, LEMOS JPC, FERREIRA LMA, SOARES MAC, ALFAIA CM, PRATES JAM & FONTES CMGA. 2004. Cholesterol levels and sensory characteristics of meat from broilers consuming moderate to high levels of alfalfa. Poul Sci 83: 810-814., 66.79 mg/100g, Rosa et al. 2006ROSA FC, BRESSAN MC, BERTECHINI AG, FASSANI EJ, VIEIRA JO, FARIA PB & SAVIAN TV. 2006. Effect of cooking methods on carcass chemical composition and cholesterol of poultry breast and thigh meat. Ciênc Agrotec 30: 707-714., 45.96 mg/100g, Oliveira e Vieira et al. 2007OLIVEIRA e VIEIRA J, BRESSAN MC, FARIA PB, FERREIRA MW, FERRÃO SPB & SOUZA XR. 2007. Effect of cooking methods on the chemical composition and cholesterol of the breast in different chicken strains. Ciênc Agrotec 31: 164-170., 93.6 mg/100g, Salma et al. 2007SALMA U, MIAH AG, MAKI T, NISHIMURA M & TSUJII H. 2007. Effect of dietary rhodobactercapsulatus on cholesterol concentration and fatty acid composition in broiler meat. Poult Sci 86: 1920-1926.) for cholesterol levels in chicken breast meat; also are below the range of variation described by Bragagnolo & Rodriguez-Amaya (1992)BRAGAGNOLO N & RODRIGUEZ-AMAYA DB. 1992. Cholesterol content of chicken meat. Rev Farm Bioquim Univ São Paulo 28: 122-131. (between 48 and 79 mg/100g), and below the average total cholesterol content considered by Ponte et al. (2008)PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88. (50 mg/100 g); the reasons for such low results are still unknown.

The cholesterol concentration in chicken meat may be influenced by the diet composition, by the bird’s age and by the gender (Wang et al. 2005WANG JJ, PAN TM & SHIEH MJ. 2005. Effect of red mold rice supplements on serum and meat cholesterol levels of broiler chicken. Appl Microbiol Biotechnol 71: 812-818.). Pastures consumed by broilers raised in some alternative rearing systems, such as organic and free-range, are a good source of tocopherols and tocotrienols, the latter being known to contribute to the reduction of cholesterol levels in blood plasma; however, the effects of pasture intake on cholesterol levels in free-range chicken meat is still unknown (Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.).

Fatty acids profile

It is observed that, in general, the fat present in meat from broilers raised in alternative systems (mainly organic and free-range) had lower (P<0.05) saturated (SFA) and monounsaturated (MUFA) fatty acid concentration, and higher concentration of polyunsaturated fatty acids (PUFA). Meat from alternative broilers presented higher PUFA/SFA ratio. Lower PUFA in relation to SFA levels may be risk factors for cardiovascular diseases, which are among the main causes of mortality in some countries (Hu et al. 2001HU FB, MANSON JE & WILLETT WC. 2001. Types of dietary fat and risk of coronary heart disease: A critical review. J Am Coll Nutr 20: 5-19., Ganji et al. 2003GANJI SH, KAMANNA AM & KASHYAP ML. 2003. Niacin and cholesterol: Role in cardiovascular disease (review). J Nutr Biochem 14: 298-305., Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.). Saturated fatty acids would be related to increased levels of total cholesterol, LDL and triglycerides, whereas monounsaturated fatty acids would be related to their reduction, and may promote the increase of blood levels of HDL (Hautrive et al. 2012HAUTRIVE TP, MARQUES AC & KUBOTA EH. 2012. Avaliação da composição centesimal, colesterol e perfil de ácidos graxos de cortes cárneos comerciais de avestruz, suíno, bovino e frango. Aliment Nutr Araraquara 23: 327-334.) and benefit the body together with the polyunsaturated fats (Cuppari 2005CUPPARI L. 2005. Nutrição: nutrição clínica no adulto. Barueri: Manole 145: 29 p., Mahan & Escott-Stump 2005MAHAN LK & ESCOTT-STUMP S. 2005. Alimentos, nutrição & dietoterapia. 11. ed., São Paulo: Roca, 1242 p., Hautrive et al. 2012HAUTRIVE TP, MARQUES AC & KUBOTA EH. 2012. Avaliação da composição centesimal, colesterol e perfil de ácidos graxos de cortes cárneos comerciais de avestruz, suíno, bovino e frango. Aliment Nutr Araraquara 23: 327-334.). Data from the literature indicate that the PUFA/SFA ratio below 0.45, quite close to that found in this study for conventional chicken meat, may be considered unhealthy (Wood & Enser 1997WOOD JD & ENSER M. 1997. Factors influencing fatty acids in meat and the role of antioxidants in improving meat quality. Br J Nutr 78: 49-60., Hautrive et al. 2012HAUTRIVE TP, MARQUES AC & KUBOTA EH. 2012. Avaliação da composição centesimal, colesterol e perfil de ácidos graxos de cortes cárneos comerciais de avestruz, suíno, bovino e frango. Aliment Nutr Araraquara 23: 327-334.). Based on this, it is suggested that meat from alternative chickens offers less risk to cardiovascular health because it presents a greater quantity of PUFA in relation to the amount of SFA.

Alternative rearing systems, in general, provided higher omega-3 and omega-6 concentrations to chicken meat. Conventional chicken meat showed higher n-6/n-3 ratio in breast and drumstick meat; such imbalance in the n-6/n-3 ratio may be responsible for the occurrence of cardiovascular, inflammatory and autoimmune diseases (Simopoulos 2004SIMOPOULOS AP. 2004. Omega-6 / omega-3 essential fatty acid ratio and chronic diseases. Food Res Int 20: 77-90., Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.). Data from the literature indicate that the proportion of n-6/n-3 fatty acids should be 5:1 to 10:1 (Hautrive et al. 2012HAUTRIVE TP, MARQUES AC & KUBOTA EH. 2012. Avaliação da composição centesimal, colesterol e perfil de ácidos graxos de cortes cárneos comerciais de avestruz, suíno, bovino e frango. Aliment Nutr Araraquara 23: 327-334.), values ​​quite different to those found in this study for chickens from all rearing systems studied. Some authors suggest that organically grown birds could use n-3 fatty acids as an essential nutrient for their own immune system’s action against external agents rather than depositing it in the meat (Küçükyilmaz et al. 2012KÜÇÜKYILMAZ K, BOZKURT M, CATLI AU, HERKEN EN, CINAR M & BINTAŞ E. 2012. Chemical composition, fatty acid profile and colour of broiler meat as affected by organic and conventional rearing systems. South Afri J. of Animal Sci 42: 360-368., Sales 2014SALES J. 2014. Effects of access to pasture on performance, carcass composition, and meat quality in broilers: A meta-analysis. Poult Sci 93: 1523-1533.) which could justify the results found in this research.

The chicken meat is considered one of the main sources of omega-3 fatty acids (Howe et al. 2006HOWE P, MEYER B, RECORD S & BAGHURST K. 2006. Dietary intake of long-chain w-3 polyunsaturated fatty acids: Contribution of meat sources. Nutrition 22: 47-53., Sioen et al. 2006SIOEN IA, PYNAERT I, MATTHYS C, BACKER GD, CAMP JV & HENAUW SD. 2006. Dietary intakes and food sources of fatty acids for Belgian women, focused on n-6 and n-3 polyunsaturated fatty acids. Lipids 41: 415-422., Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.). In general, broiler meat raised in alternative rearing systems showed the highest levels of EPA and DHA, which are important for the health of the retina, for phospholipids of the membranes of the brain and also help in reducing the risks of heart disease (Rymer & Givens 2005RYMER C & GIVENS DI. 2005. N-3 fatty acid enrichment of edible tissue of poultry: A review. Lipids 40: 121-130., Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.). However, because the pasture is a poor source of EPA and DHA, it is still unknown whether broilers are able to utilize α-linoleic acid (18:3n-3) from the pasture as a precursor to the synthesis and deposition of these fatty acid in the meat (Ponte et al. 2008PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.), and it is unknown if the higher levels of EPA and DHA present in meat from alternative chickens are influenced by the pasture.

CONCLUSION

Meat from chickens raised in alternative rearing systems offers less risk to cardiovascular health because it presents lower concentrations of lipids and cholesterol, and greater amounts of polyunsaturated fatty acids, which are beneficial for human health, once they have anti-inflammatory action, promotes heart health, blood circulation and improves cognitive processes.

ACKNOWLEGMENTS

The authors thank the São Paulo Research Foundation Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil (FAPESP, 2012/10276-0) for financing this study.

REFERENCES

  • ABPA - BRAZILIAN ASSOCIATION OF ANIMAL PROTEIN. 2016. Annual report 2016. Accessed May. 2017. http://abpabr.com.br/setores/avicultura/publicacoes/relatorios-anuais
    » http://abpabr.com.br/setores/avicultura/publicacoes/relatorios-anuais
  • AHA - AMERICAN HEART ASSOCIATION. 2004. Heart and stroke encyclopedia. Dietary guidelines for healthy American adults. Cholesterol. Fat. Available at: <http://www.americanheart.org> [Verified 20 February 2019].
    » http://www.americanheart.org
  • AOAC. ‘OFFICIAL METHODS OF ANALYSIS. 2005. 18th ed., Association of Analytical Chemists, Washington, DC.
  • BERZAGHI P, DALLE ZOTTE A, JANSSON LM & ANDRIGHETTO I. 2005. Near-infrared reflectance spectroscopy as a method to predict chemical composition of breast meat and discriminate between different n-3 feeding sources. Poult Sci 84: 128-136.
  • BLIGH GE & DYER JW. 1959. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
  • BOHAC CE, RHEE KS, CROSS HR & ONO K. 1988. Assessment of methodologies for colorimetric cholesterol assay of meats. J. of Food Sci 53: 1642-1693.
  • BRAGAGNOLO N & RODRIGUEZ-AMAYA DB. 1992. Cholesterol content of chicken meat. Rev Farm Bioquim Univ São Paulo 28: 122-131.
  • CASTELLINI C, DAL BOSCO A, MUGNAI C & PEDRAZZOLI M. 2006. Comparison of two chicken genotypes organically reared: oxidative stability and other qualitative traits of the meat. Italian J. Animal Sci 5: 355-363.
  • CASTELLINI C, MUGNAI C & DAL BOSCO A. 2002. Meat quality of three chicken genotypes reared according to the organic system. Italian J. of Food Sci 14: 401-424.
  • CHOU CS & FRIEDMAN A. 2016. Atherosclerosis: The Risk of High Cholesterol. In: Introduction to Mathematical Biology. Available at <http://link.springer.com/chapter/10.1007/978-3-319-29638-8_12>[Verified 06 July 2016].
    » http://link.springer.com/chapter/10.1007/978-3-319-29638-8_12
  • CUPPARI L. 2005. Nutrição: nutrição clínica no adulto. Barueri: Manole 145: 29 p.
  • DALZIEL CJ, KLIEM KE & GIVENS DI. 2015. Fat and fatty acid composition of cooked meat from UK retail chickens labelled as from organic and non-organic production systems. Food Chem 179: 103-108.
  • DE MARCHI M, RIOVANTO R, PENASA M & CASSANDRO M. 2012. At-line prediction of fatty acid profile in chicken breast using near infrared reflectance spectroscopy. Meat Sci 90: 653-657
  • FARIA PB, BRESSAN MC, SOUZA XR, RODRIGUES EC, CARDOSO GP & GAMA LT. 2009. Composição proximal e qualidade da carne de frangos das linhagens Paraíso Pedrês e Pescoço Pelado. R Bras Zootec 38: 2455-2464.
  • FLÅTTEN A, BRYHNI EA, KOHLER A, EGELANDSDAL B & ISAKSSON I. 2005. Determination of C22:5 and C22:6 marine fatty acids in pork fat with Fourier transform midinfrared spectroscopy. Meat Sci 69: 433-440.
  • GANJI SH, KAMANNA AM & KASHYAP ML. 2003. Niacin and cholesterol: Role in cardiovascular disease (review). J Nutr Biochem 14: 298-305.
  • GIVENS DI, GIBBS RA, RYMER C & BROWN RH. 2011. Effect of intensive vs. free range production on the fat and fatty acid composition of whole birds and edible portions of UK retail chickens. Food Chem 127: 1549-1554.
  • HAUTRIVE TP, MARQUES AC & KUBOTA EH. 2012. Avaliação da composição centesimal, colesterol e perfil de ácidos graxos de cortes cárneos comerciais de avestruz, suíno, bovino e frango. Aliment Nutr Araraquara 23: 327-334.
  • HOWE P, MEYER B, RECORD S & BAGHURST K. 2006. Dietary intake of long-chain w-3 polyunsaturated fatty acids: Contribution of meat sources. Nutrition 22: 47-53.
  • HU FB, MANSON JE & WILLETT WC. 2001. Types of dietary fat and risk of coronary heart disease: A critical review. J Am Coll Nutr 20: 5-19.
  • HUSAK RL, SEBRANEK JG & BREGENDAHL K. 2008. A survey of commercially available broilers marketed as organic, free-range, and conventional broilers for cooked meat yields, meat composition, and relative value. Poult Sci 87: 2367-2376.
  • JUNG S, CHOE JH, KIM B, YUN H, KRUK ZA & JO B. 2010. Effect of dietary mixture of gallic acid and linoleic acid on antioxidative potential and quality of breast meat from broilers. Meat Sci 86: 520-526.
  • KÜÇÜKYILMAZ K, BOZKURT M, CATLI AU, HERKEN EN, CINAR M & BINTAŞ E. 2012. Chemical composition, fatty acid profile and colour of broiler meat as affected by organic and conventional rearing systems. South Afri J. of Animal Sci 42: 360-368.
  • LEOSDOTTIR M, NILSSON PM, NILSSON J-Å, MÅNSSON H & BERGLUND G. 2005. Dietary fat intake and early mortality patterns – data from The Malmӧ diet and cancer study. J Intern Med 258: 153-165.
  • LONERGAN SM, DEEB N, FEDLER CA & LAMONT SJ. 2003. Breast meat quality and composition in unique chicken populations. Poult Sci 82: 1990-1994.
  • MAHAN LK & ESCOTT-STUMP S. 2005. Alimentos, nutrição & dietoterapia. 11. ed., São Paulo: Roca, 1242 p.
  • MAIA EL & RODRIGUEZ-AMAYA DB. 1993. Avaliação de um método simples e econômico para metilação de ácidos graxos de lipídeos de diversas espécies de peixes. Rev Inst Adolfo Lutz 53: 27-35.
  • NKUKWANA TT, MUCHENJE V, MASIKA PJ, HOFFMAN LC, DZAMA K & DESCALZO AM. 2014. Fatty acid composition and oxidative stability of breast meat from broiler chickens supplemented with Moringa oleifera leaf meal over a period of refrigeration. Food Chem 142: 255-261.
  • OLIVEIRA e VIEIRA J, BRESSAN MC, FARIA PB, FERREIRA MW, FERRÃO SPB & SOUZA XR. 2007. Effect of cooking methods on the chemical composition and cholesterol of the breast in different chicken strains. Ciênc Agrotec 31: 164-170.
  • PONTE PIP, ALVES SP, BESSA RJB, FERREIRA LMA, GAMA LT, BRÁS JLA, FONTES CMGA & PRATES JAM. 2008. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poult Sci 87: 80-88.
  • PONTE PIP, MENDES I, QUARESMA M, AGUIAR MNM, LEMOS JPC, FERREIRA LMA, SOARES MAC, ALFAIA CM, PRATES JAM & FONTES CMGA. 2004. Cholesterol levels and sensory characteristics of meat from broilers consuming moderate to high levels of alfalfa. Poul Sci 83: 810-814.
  • RIOVANTO R, DE MARCHI M, CASSANDRO M & PENASA M. 2012. Use of near infrared transmittance spectroscopy to predict fatty acid composition of chicken meat. Food Chem 134: 2459-2464.
  • RODRIGUES KF, RODRIGUES PB, BRESSAN MC, NAGATA AK, SILVA JHV & SILVA EL. 2008. Qualidade da carne de peito de frangos de corte recebendo rações com diferentes relações lisina digestível: proteína bruta. R Bras Zootec 37: 1023-1028.
  • ROSA FC, BRESSAN MC, BERTECHINI AG, FASSANI EJ, VIEIRA JO, FARIA PB & SAVIAN TV. 2006. Effect of cooking methods on carcass chemical composition and cholesterol of poultry breast and thigh meat. Ciênc Agrotec 30: 707-714.
  • RYMER C & GIVENS DI. 2005. N-3 fatty acid enrichment of edible tissue of poultry: A review. Lipids 40: 121-130.
  • SACKS FM. 2002. The role of high-density lipoprotein (HDL) cholesterol in the prevention and treatment of coronary heart disease. Am J Cardiol 15: 139-143.
  • SALES J. 2014. Effects of access to pasture on performance, carcass composition, and meat quality in broilers: A meta-analysis. Poult Sci 93: 1523-1533.
  • SALMA U, MIAH AG, MAKI T, NISHIMURA M & TSUJII H. 2007. Effect of dietary rhodobactercapsulatus on cholesterol concentration and fatty acid composition in broiler meat. Poult Sci 86: 1920-1926.
  • SAS. 2002, 2003. Institute Inc. ‘SAS Version 9.1.’ (SAS Institute Inc.: Cary, NC).
  • SIERRA V, ALDAI N, CASTRO P, OSORO K, COTO-MONTES A & OLIVA M. 2008. Prediction of the fatty acid composition of beef by near infrared transmittance spectroscopy. Meat Sci 78: 249-255.
  • SIMOPOULOS AP. 2004. Omega-6 / omega-3 essential fatty acid ratio and chronic diseases. Food Res Int 20: 77-90.
  • SIOEN IA, PYNAERT I, MATTHYS C, BACKER GD, CAMP JV & HENAUW SD. 2006. Dietary intakes and food sources of fatty acids for Belgian women, focused on n-6 and n-3 polyunsaturated fatty acids. Lipids 41: 415-422.
  • SIRRI F, CASTELLINI C, BIANCHI M, PETRACCI M, MELUZZI A & FRANCHINI A. 2011. Effect of fast-, medium- and slow-growing strains on meat quality of chickens reared under the organic farming method. Animal 5: 312-319.
  • WANG JJ, PAN TM & SHIEH MJ. 2005. Effect of red mold rice supplements on serum and meat cholesterol levels of broiler chicken. Appl Microbiol Biotechnol 71: 812-818.
  • WOOD JD & ENSER M. 1997. Factors influencing fatty acids in meat and the role of antioxidants in improving meat quality. Br J Nutr 78: 49-60.
  • WOOD JD, RICHARDSON RI, NUTE GR, FISHER AV, CAMPO MM, KASAPIDOU E, SHEARD PR & ENSER M. 2003. Effects of fatty acids on meat quality: A review. Meat Sci 66: 21-32.
  • ZANETTI E, DE MARCHI M, DALVIT C, MOLETTEC, REMIGNON H & CASSANDRO M. 2010. Carcass characteristics and qualitative meat traits of three Italian local chicken breeds. British Poult Sci 6: 629-634.
  • ZHOU LJ, WU H, LI JT, WANG ZY & ZHANG LY. 2012. Determination of fatty acids in broiler breast meat by near-infrared reflectance spectroscopy. Meat Sci 90: 658-664.

Publication Dates

  • Publication in this collection
    31 July 2020
  • Date of issue
    2020

History

  • Received
    10 June 2019
  • Accepted
    9 Dec 2019
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100, CLOCKSS system has permission to ingest, preserve, and serve this Archival Unit - Rio de Janeiro - RJ - Brazil
E-mail: aabc@abc.org.br