How to exploit the potential of different compounds from chicken by-productsABSTRACT:
Adding value to daily by-products is a challenge in the chicken meat industry, since most are used to produce flour and animal feed. These by-products are rich in proteins, prompting research on the potential of feathers, feet, fat, bones, liver, intestines, and heads in creating new ingredients for food products. Additionally, clean technologies have been used to obtain compounds with functional and nutritional properties from chicken by-products. Reusing these wastes to obtain higher value-added compounds can contribute to the sustainability and financial success of the poultry industry. This review investigated the production of higher value-added compounds from chicken by-products.
Key words:
animal protein; by-products; feathers; feet; fat; bones; liver; intestine
RESUMO:
As indústrias de carne de frango enfrentam o desafio de agregar valor aos subprodutos gerados diariamente, uma vez que a maioria deles é destinada à produção de farinhas e rações para animais. Esses subprodutos são ricos em proteínas, o que tem motivado a realização de estudos que exploram o potencial de penas, pés, gorduras, ossos, fígados, intestinos e cabeças na criação de novos ingredientes para produtos alimentícios. Além disso, as tecnologias limpas têm sido empregadas para obter compostos com propriedades funcionais e nutricionais a partir desses subprodutos de frango. A reutilização desses resíduos na obtenção de compostos de maior valor agregado pode contribuir para a sustentabilidade e o sucesso financeiro das indústrias avícolas. Esta revisão tem como objetivo abordar a obtenção de compostos com maior valor agregado provenientes dos subprodutos de frango.
Palavras-chave:
proteína animal; subprodutos; penas; pés; gordura; ossos; fígado; intestino
INTRODUCTION
The sustainable use of protein-rich by-products has been gaining ground worldwide, given their considerable potential as sources of bioactive compounds and the fact that they can be used to develop new food products for human or animal consumption (LINDBERG et al., 2021). Research has shown that meat by-products contain a significant amount of functional compounds and nutrients (LAVRANOU et al., 2023). In the meat production process, animals are slaughtered, eviscerated and their heads removed, along with other parts depending on the particularities of each animal species. Then, the resulting carcass also contains edible parts of the animal with greater value. In accordance with Brazilian legislation, parts not used for human consumption are considered slaughterhouse waste, process that transforms animal waste into by-products and consist primarily of blood, the head, viscera, feathers, hooves, fat trimmings, and industrial waste. In addition to providing economic gains, this activity provides environmental benefits, as it prevents waste from animal slaughter from being incorrectly disposed (ABRA, 2023).
Animal by-products are parts not intended for human consumption due to the dietary and cultural habits of a given population or classified as unfit for human consumption by the official meat inspection system. Since the main raw material used to manufacture ingredients of animal origin comes from slaughter, the larger the number of animals slaughtered, the greater the growth of the animal recycling industry. By collecting and correctly and rationally disposing of industrial waste, the recycling industry stands out in the production of ingredients that are used by various sectors: animal feed, pet food, agriculture, petrochemical sector, hygiene and beauty industry (ABRA, 2023).
In 2023, Brazil exported 574,000 tons of flour and fats of animal origin, which is equivalent to 9.65% of total production for that year. In this respect, several studies have been conducted in different fields to search for novel products obtained from recycled slaughterhouse waste and new uses for existing products, consequently increase the volume of exported products with greater added value, contributing to agribusiness, the environment and global sustainability (ABRA, 2023).
It is estimated that global meat and dairy consumption will increase by 173 and 158%, respectively, between 2010 and 2050 (KHAN et al., 2021) and per capita consumption could double by 2050 (ALEXANDRATOS & BRUINSMA, 2012). This continuous demand for animal protein and the expansion of food production may pose enormous risks and cause potentially irreversible ecological damage. As such, there is a need to incorporate emerging technologies for high-protein food production to promote the sustainability of food systems and biodiversity (KHAN et al., 2021). According to the Organization for Economic Co-operation and Development (OECD) and the Food and Agriculture Organization (FAO), global per capita chicken meat consumption has increased by 15% in the last decade, surpassing the recorded consumption for beef and pork (PEÑA-SALDARRIAGA, 2020). This high demand for animal protein for human consumption has prompted a rapid increase in global chicken production (ILIAS et al., 2023).
As a result, the poultry industry has become one of the largest sectors in the global food industry, encompassing everything from animal rearing to slaughter and generating a significant number of by-products (MACGAURAN et al., 2021). In the broiler industry, by-products account for about 37% of a chicken’s total live weight during slaughter (PEÑA-SALDARRIAGA, 2020) and include meat trimmings, bones, skins, viscera, the head, cartilage, blood, abdominal fat, feet, and feathers, which are discarded or used as low-value restructured products (ANANEY-OBIRI et al., 2020).
A by-product with considerable potential for value-added human consumption is the meat that remains on the bones after mechanical deboning of poultry carcasses. This highly nutritious meat contains a significant amount of connective tissue (collagen) and protein. Consequently, collagen peptides and proteins from these by-products have attracted considerable attention due to their emulsifying and stabilizing properties and antioxidant and antimicrobial activity (LINDBERG et al., 2021).
The bones generated during chicken processing and consumption account for about 15% of carcass weight. These bones are rich in nutrients such as calcium, fatty acids, and collagen. However, only a small portion of these nutrients is used as raw material for seasoning and animal feed production. Most of these by-products are still discarded, resulting in environmental pollution or the production of low-value industrial products (ZHANG et al., 2022). Chicken feet are an abundant source of collagen, with annual global production of 3.9 million tons, making them an excellent source of collagen and gelatin, and can be used in food and pharmaceutical products (FATIMA et al., 2022). Feathers, corresponding to about 7% of the bird´s body weight, are another by-product produced in large quantities by the poultry industry. They are primarily transformed into hydrolyzed feather meal, which contains approximately 85% crude protein on a dry matter basis, with keratin as the main component (MACHADO et al., 2021).
Fat from the abdominal region and gizzard accounts for approximately 2-2.5% of the total chicken weight and is considered a by-product. The unsaturated fatty acid content of this fat means it could potentially be used in sausages and other meat products, but is nevertheless often discarded along with viscera, feathers, and blood, especially by small agro-industries. In large-scale industries, only a small portion of this by-product is used in animal feed production (PEÑA-SALDARRIAGA et al., 2020). The skin, representing about 7-10% of total chicken weight, is used to produce gelatin and meat products (GÁL et al., 2020).
In adult birds, blood makes up about 7.5% of total weight and is composed of 85% water, with the remainder consisting of proteins, lipids, and minerals with high nutritional value (GÁL et al., 2020). However, it is underused.
Given the large number of by-products generated daily by the poultry industry, this review presented recent studies that explore strategies to add value to these by-products and discuss the prospects of this market in obtaining bioactive and nutritional compounds.
Importance and impact of using poultry industry by-products
The increase in poultry production combined with the growing amount of waste from poultry slaughter is a topic of concern for the industry (Figure 1), which generates considerable volumes of waste that can seriously affect the environment when improperly disposed of (FIORESE et al., 2019).
In some industries, previously accredited companies are responsible for final waste disposal. However, in some cases, costs such as those involved in transporting this material may compromise the productivity and profitability of the enterprise, making it unfeasible. In this respect, reusing this waste is essential for both the poultry industry and local economy, in addition to benefitting the environment by reducing the consumption of natural resources and improving soil and water quality (FIORESE et al., 2019).
The increase in chicken meat production has been accompanied by a greater impact of poultry waste on the environment, generating large amounts of greenhouse gases and by-products. As such, reuse strategies aimed at adding value to these materials have been developed and encouraged, with several countries offering financial incentives to producers and industries that implement sustainable activities (IBARS-BLACH et al., 2023).
Modern lifestyles have contributed to the significant increase in the global incidence of chronic diseases. As a result, a considerable amount of research has been conducted to identify new agents with biological activities. Chicken industry by-products are rich in proteins, which can be used to obtain bioactive peptides, and also contain collagen and keratin. The generation of value-added products benefits the population and the circular economy (IBARS-BLACH et al., 2023).
Several researchers have sought to develop innovative and efficient technologies to obtain value-added products (Table 1), mainly using recently improved enzyme-based technologies.Thus, enzymatic technologis are promising strategies in waste reuse, since they address the issue of environmental pollution and provide economic benefits (ZININA et al., 2022).
To reduce the risks associated with poultry waste, it is important to carry out specific life cycle assessments to identify and compare the economic potential and environmental benefits of each technology, and consider the regional opportunities and limitations to its implementation (ZININA et al., 2022).
DEVELOPMENT
Chicken feathers
The global demand for chicken meat and eggs requires the rearing of billions of chickens annually, resulting in a large amount of feathers. Composed primarily of keratin, these feathers are rich in cystine, glycine, proline, and serine. Keratinases can be used in manufacturing of cosmetics, detergents, medicines, leather, feed (QIN et al., 2023), fertilizer and biofilm (PENG et al., 2019). In a study on keratin valorization from chicken feather waste, the effect of ultrasound conditions (ultrasonic power and time) on the physical properties of keratin (feather dissolubility, keratin yield, chemical structure, thermal stability, and crystallinity) were evaluated using the cysteine reduction method. Optimal power (130W) and ultrasound time (2.7) and 15% cysteine reduction resulted in better solubility without damaging the chemical structure of keratin or compromising amino acid coposition and thermal stability. This system proved to be a promising alternative for obtaining keratin via clean low-cost techniques (QIN et al., 2023).
A study on the characterization and purification of keratinase from Bacillus licheniformis DCS 1 found that keratinase showed potential for degrading feather waste (48.5 U/mL) within 14 days due to its keratinolytic and proteolytic ability (LIAQAT et al., 2022). In another study, the keratinase-producing bacteria Bacillus licheniformis and Stenotrophomonas maltophilia were evaluated for their effectiveness in degrading chicken feathers. The keratin hydrolysis rate was 70% after 48 hours, producing bioactive peptides and amino acids. These compounds showed increased antioxidant activity as hydrolysis progressed, demonstrating the considerable potential of chicken feather hydrolysates for application in the production of food additives and amino acids (PENG et al., 2019).
Another possibility is obtaining keratinase via fungal decomposition of chicken feathers using submerged and solid-state fermentation. Aspergillus flavus was submitted to different types of fermentation and the results showed that submerged fermentation provided nine times more keratin degradation than solid-state fermentation. This is because keratinolytic activity began on the 5th day of incubation in submerged fermentation and increased over time until week four. The results demonstrated that this is an efficient method of producing keratinase, an enzyme with high industrial value (MASSOD et al., 2023).Hydrolyzed feather meal represents a new prospect for the use of chicken feather by-products. Its high protein content means it is widely used in chicken processing facilities, because using higher working pressure, desnatures proteins and resulting in loss nitrogen and consequently decresasing the protein content, thenmaking it a high added-value product. Optimizing the production conditions of hydrolyzed feather meal can result in a better-quality product and increase company profits. SINHORINI et al. (2021) assessed the influence of process parameters and raw materials on the characteristics of hydrolyzed feather meal. The effect of hydrolysis time and pressure on protein content and digestibility were evaluated using three formulations containing different types of feathers: F1 = 100% chicken feathers, F2 = 100% turkey feathers, F3 = 50% chicken feathers + 50% turkey feathers. The results showed that regardless of the pressure applied, extending the hydrolysis time to 40 minutes increased meal protein content (by 84.30% for chicken feather meal and 76.18% for turkey feather meal) and improved digestibility.
In a study, feather and blood meal were included in broiler chicken pre-starter and starter diets. In the pre-starter (1-7 days) and starter phase (8-21 days), the following pressures were applied during thermal treatment: 2.0 kgf/cm² for 40 minutes, 2.5 kgf/cm² for 30 minutes, and 3.0 kgf/cm² for 20 minutes, with hydrolysis decreasing as the internal pressure increased. The best results were achieved in the pre-starter phase at 2.5 kgf/cm² for 30 minutes, whereas optimal performance and nutrient metabolization occurred at 2.0 kgf/cm² for 40 minutes (LABOISSIÉRE et al., 2020).
Chicken feet
Chicken feet, are a by-product generated in large quantities in the poultry industry;however, due to the very low commercial price of poultry by-products and also the high demand for products with high nutritional value, this scenario has encouraged researchers to explore new food sources from these by-products (SANTANA et al., 2020).
The chicken feet product is commercially classified, according to the requirements of the purchasing markets, into three specifications: type A, better quality feet, which do not present any lesions; type B, second quality, which present lesions limited in their extension; type C, feet with extensive lesions; therefore, inedible and intended for the rendering industry. In recent years, with the unification of standards required by countries that purchase chicken feet, countries could export type A and B feet, as long as they were inspected. However, since these products were considered inedible, Brazilian legislation did not allow the sale of type B feet. Subsequently, circular 599/2010/CGPE/DIPOA was published, which allowed the sale of these feet, if the hygienic and sanitary conditions were met (TEIXEIRA et al., 2019).
Chicken feet are excellent sources of gelatin, can be used for a variety of purposes and contain important nutrients with essential health-benefitting properties (SANTANA et al., 2020). Gelatin has several applications in the food, packaging and pharmaceutical industries, acting as a stabilizer, thickener, texturizing agent and a key ingredient for packaging (RATHER et al., 2022).
Two drying methods for obtaining gelatin were tested, namely hot air and freeze drying. Physicochemical and functional characteristics were evaluated, with no significant differences between the methods in terms of yield. Greater gel strength was obtained with hot air drying (45 ºC). Neither method had a significant effect on the water retention capacity of gelatin; however, emulsification capacity, oil binding, and stability were more significant in gelatin obtained by hot air drying. As such, both technologies are promising and can be used in industrial-scale gelatin production (RATHER et al., 2022).
Another application explored was the use of collagen obtained from chicken feet to produce Frankfurter-type sausages from low-fat chicken meat. The aim was to replace fat and compare the collagen obtained from chicken feet with commercially sold collagen. Three sausage formulations were prepared: F1) 15% fat, F2) 7.5% fat and 7.5% commercial collagen, and F3) 7.5% fat and 7.5% chicken feet collagen. The collagen from chicken feet provided excellent emulsion stability and water retention capacity. However, texture parameters were negatively affected by chicken feet collagen, suggesting that further research with different collagen proportions is needed to evaluate the impact on texture quality (ARAÚJO et al., 2019).
In a recent study, gelatin obtained from chicken feet was used to develop active packaging aimed at extending the shelf life of fresh grapes. Chitosan and zinc oxide nanoparticles were incorporated into the packaging materials using five different formulations: F1) gelatin (control formulation), F2) chitosan, F3) gelatin + chitosan, F4) gelatin + 0.2% chitosan, zinc oxide, and nanoparticles, and F5) gelatin + 0.3% chitosan, zinc oxide, and nanoparticles. The gelatin pre-extraction parameters were optimized by varying acetic acid concentration, temperature, time, yield, and strength. The conditions used were 4.2% acetic acid at 66 ºC for 4.2 hours, resulting in a 7.5% yield and 186 g gel strength. Formulations F4 and F5 reduced browning and microbial growth; although, grape weight loss occurred during storage when compared to the control sample. The nanoparticles and zinc oxide present in these formulations improved the barrier properties and antimicrobial effect of the film. Thus, chicken by-products such as feathers and feet can be used in gelatin extraction, which can be applied in developing low-cost biodegradable packaging (FATIMA et al., 2022).
Chicken feet are also a novel alternative source of calcium-chelating peptides. The bones and meat residue from chicken feet heated with water to remove fat and fine meat after hydrolysis formed a broth containing peptides with amino acids such as aspartic and glutamic acid, glycine, leucine, and lysine, which have a high calcium-binding capacity. This demonstrated that these peptides could improve calcium levels in food formulations, benefiting consumer health (MALISON et al., 2021).
Chicken liver, intestine, and skin
Cardiorenal syndrome, caused by renal and cardiac dysfunction and other factors related to a high-fat diet, may be mitigated by ingesting peptides with a protective effect on the tissue of these organs. Peptides obtained from chicken livers through the action of the enzyme pepsin could protect against myocardial and renal damage. Liver hydrolysates were administered to rats and blood samples collected to assess the effects. The rats were submitted to the following treatments: (I) control diet, (II) high-fat diet (46.5% of calories), (III) high-fat diet and digested chicken liver hydrolysate (170 mg/kg), (IV) high-fat diet and chicken liver hydrolysate (510 mg/kg), and (V) chicken liver hydrolysate and L-carnitine (500 mg/kg). The results showed that rats supplemented with chicken liver hydrolysates exhibited a cardiorenal protective effect (WU et al., 2020).
Similarly, in another study with diets, the effects on palatability and digestibility were evaluated in dog diets where hydrolyzed chicken liver powder was included as the sole source of nutrients. Two diets were administered to the dogs, the first consisting of chicken meat by-products and bovine bones, and the second only hydrolyzed chicken liver powder. The animals fed the hydrolyzed chicken liver powder diet showed good acceptance, digestibility (protein hydrolysates are generally more digestible than intact protein), and high levels of essential nutrients (protein, amino acids and fatty acids). Due to the high levels of essential amino acids and fatty acids, stool quality had no adverse effect (PINTO et al., 2021).
As an alternative application, chicken intestine by-products, in the form of protein hydrolysates, were provided as feed for fish, whose growth performance was assessed. The physicochemical properties of chicken hydrolysate were evaluated using four different formulations: F1) autolysis of chicken intestine hydrolysate at pH 3, F2) hydrolysate autolysis by enzyme addition (Multifect PR 6 L enzyme), and F3) a combination of enzyme addition and autolysis at pH 3, and the control formulation F4) tuna hydrolysate. Adding the enzyme (F2) provided more significant proteolytic activity than autolysis at pH 3 (F1). The results showed that all three formulations (F1, F2 and F3), particularly F2, could be used as a new feed for freshwater fish. When administered to the fish, the chicken intestine hydrolysate obtained by enzymatic action (F2) promoted better growth performance, improved hematological parameters, and resulted in higher body protein content (LIMPISOPHON et al., 2023).
In addition to the chicken by-products already mentioned, chicken skin is the most abundantly generated in the poultry industry. With a view to using this by-product, the fat and gelatin extracted from chicken skin were studied for applications in food technology. The skin was moistened and submitted to different gelatin and fat extraction times and temperatures. Gelatin yield ranged from 0.74 to 2.03%, and fat yield from 24.01 to 27.91%. These extraction conditions influenced gelatin yield and caused variations in protein, hydroxyproline content, free fatty acids, peroxide value, and the oxidation induction period. The gelatin obtained showed higher viscosity and greater foam-forming and gelling ability with different extraction times and temperatures than the commercial bovine gelatin. These results indicate that gelatin and fat from chicken skin could add value to the meat industry (MOHAMMADNEZHAD & FARMANI, 2022).
Abdominal fat and chicken skin were incorporated into chicken sausages that were frozen for 135 days and evaluated every 45 days for lipid and protein oxidation. Three formulations were used: (1) chicken meat and abdominal fat, (2) chicken meat and skin, and (3) chicken meat, abdominal fat, and skin. The sausages made using the second formulation exhibited lower lipid and protein oxidation values throughout storage, while those obtained with the third formulation obtained higher consumer preference and purchase intention in sensory analysis and intermediate oxidation values. The authors concluded that including chicken skin and abdominal fat could enable industrial-scale chicken sausage production (LIMA et al., 2020).
The remaining abdominal and gizzard fat inside a chicken carcass could be used as a fat source in the production of sausages and other meat products, mainly due to the presence of unsaturated fatty acids. The resulting chicken fat by-products (abdominal and gizzard fat) showed color parameters consistent with values into the range for chicken skin reported in the literature. The predominant fatty acids in the by-products were oleic, palmitic, and linoleic, with higher amounts than those observed in traditionally used fats. The by-products analyzed in this study have a higher proportion of polyunsaturated fatty acids (approx. 40%) than pork and beef (less than 20%). Unsaturated fatty acids include essential fatty acids that play beneficial roles in human health. Oleic acid may help to lower circulating concentrations of low-density lipoprotein (LDL) cholesterol and in humans is considered a “healthy” fat and protects against coronary heart disease. Essential fatty acids are not biologically synthesized by humans, but are required for biological processes and should therefore be included in the human diet. The authors concluded that chicken abdominal and gizzard fat can be used in meat product formulations, thereby adding value to these by-products (PEÑA-SALDARRIAGA et al., 2020a).
With a view to using these by-products, meat products were developed to replace conventional fats with those obtained from abdominal and gizzard fat, in a complementary study, the same researchers (PEÑA-SALDARRIAGA et al., 2020b). Added abdominal and gizzard fat to chicken sausages, but at fat replacement rates of 40 and 50%. Sensory analysis of the 50% fat-replaced sausages indicated differences in color, aroma, and flavor compared to controls. However, these sensory differences in relation to controls were not observed in sausages with 40% fat replacement. Thus, the authors concluded that the sausages with 40% fat replacement showed market potential.
Chicken bones and heads
A significant amount of chicken bones are generated by the poultry industry, accounting for 15% of the carcass. However, only a small portion of bones are used in condiments and animal feed, while the remainder are incorrectly disposed of in the environment. These by-products are rich in nutrients such as collagen, calcium, fatty acids, and amino acids. The effects of micro (particle size 1-300 μm) and nano (particle size 30-1000 nm) scale in different concentrations (0; 0.25; 0.50; 0.75 and 1.0 g/100g) of chicken bones on the heat-induced gelation properties of low-salt pork batter were evaluated to identify an industrial application for these by-products. Adding micro- (0.75 g/100 g) and nano-scale (0.5 g/100 g) chicken bones promoted ordered protein aggregation, forming a denser and more uniform gel network with smaller pore diameters. This improved gel and increased water retention capacity and distribution. These modifications reduced cooking time and the amount of water released during cooking (ZHANG et al., 2022).
Given the substantial amount of chicken bones generated as by-products, a study using green technology assessed the effect of ultrasonic pretreatment on the structure and functionality of chicken bone protein was analyzed using an enzymatic method. Ultrasound modified secondary and tertiary protein structures, increasing their hydrophobicity, and improved functional properties such as solubility, emulsification, foam formation, and oil retention. These functionalities are crucial in food formulation, allowing the industry to use proteins from these by-products (DONG et al., 2019).
Another by-product studied for direct human consumption is chicken heads, which represent 2% of the total weight and are generally used in animal feed or meal production. This by-product can also be used to obtain gelatin, favoring its use within the poultry industry. The technological processing conditions to extract gelatin from chicken heads were evaluated using different amounts of the Polarzyme 6.0 T enzyme (0.4-1.6%) with varying enzymatic action (18-48 h) and extraction times (1-4 h) over two processing stages. In the first stage, 0.8% enzyme was used for 24 hours with 45 minutes of extraction. The same enzyme and action time were applied in the second stage, but extraction time was increased to 120 minutes. Gelatin yield was 22.6% in the first stage and 29.9% in the second. These results were considered promising for gelatin production. The solid residues remaining after gelatin extraction could be used in fertilizer production (GÁL et al., 2020).
The research presented in this review highlighted the potential use of chicken by-products in different applications (Table 1), adding value to the product and consequently contributing to reduced environmental impact.
CONCLUSION
The by-products generated during chicken processing, such as feathers, feet, liver, intestines, skin, bones, and head, have significant potential for transformation into products with functional and bioactive properties. These by-products can be incorporated into different sectors of the food and pharmaceutical industries. Clean technologies are a promising strategy in converting these by-products, adding value to the resulting compounds. Thus, collaboration between universities, research centers, and industries is vital to apply new technologies and develop products with different biological properties from the by-products. This partnership enables economic and environmental gains, since the industry typically discards many of these by-products.
ACKNOWLEDGMENTS
This study was partially financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001.
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CR-2024-0552.R2
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DATA AVAILABILITY STATEMENT
We declare that all data obtained and analyzed in this study are available and can be provided upon request to the authors.
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DECLARATION OF USE OF ARTIFICIAL INTELLIGENCE
We declare that no artificial intelligence tools were used in the writing, preparation, or development of this manuscript, and that all contents is the exclusive result of the authors’ intellectual work.
Edited by
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ASSOCIATE EDITOR:
Rudi Weiblen (0000-0002-1737-9817)
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SCIENTIFIC EDITOR:
Gabriel Augusto Marques Rossi (0000-0001-7967-7628)
We declare that all data obtained and analyzed in this study are available and can be provided upon request to the authors.
