Introduction
The use of nutritional strategies to improve the quality of meat is a relatively new approach that has emerged at the interface of animal and food science. Nutritional approaches are often more effective than direct addition of the additive to meat since the compound is preferably deposited where it is most needed (Govaris et al., Reference GOVARIS, BOTSOGLOU, PAPAGEORGIOU, BOTSOGLOU and AMBROSIADIS2004; Dhama et al., Reference DHAMA, SHYMA, SAMINATHAN, ABDUL SAMAD, KARTHIK, TIWARI, KHAN, ALAGAWANY, FARAG, ALAM, LAUDADIO and TUFARELLI2015). As in other animal species, the physical quality of broiler meat is of major importance, since broiler chicken meat is usually consumed as cut up pieces or processed products rather than as whole carcasses. Physical quality refers to several meat properties, including pH and colour. Meat quality is closely related to the decrease in muscle pH post mortem. Rapid post mortem decline in pH results in pale, soft and exudative (PSE) meat with reduced water-holding capacity (Owens et al., Reference OWENS, HIRSCHLER, MCKEE, MARTINEZ-DAWSON and SAMS2000; Džinić et al., Reference DŽINIĆ, TOMOVIĆ, PETROVIĆ, STANAĆEV, TASIĆ, IKONIĆ and FILIPOVIĆ2008; Puvača and Stanaćev, Reference PUVAČA and STANAĆEV2011). The variations in colour of broiler breast meat fillets are significantly correlated with muscle pH and extremes in colour variations (Džinić et al., Reference DŽINIĆ, PETROVIĆ, TOMOVIĆ, A TASIĆ, FILIPOVIĆ and STANAĆEV2007a; Khalafalla et al., Reference KHALAFALLA, FATMA, DALIA, ZAHRAN and MOSA2011). Low ultimate pH results in ‘acidic meat’ with similar defects to those of PSE meat (Barbut, Reference BARBUT1997), while high ultimate pH leads to dark, firm and dry (DFD) meat with dark colour and poor storage quality (Allen et al., Reference ALLEN, RUSSELL and FLETCHER1997; Laudadio and Tufarelli, Reference LAUDADIO and TUFARELLI2011). Beside physical meat quality, economic importance is related to sensory and chemical characteristics of meat which should not be forgotten.
Three sensory quality characteristics colour, texture, and flavour are the main attributes affecting meat consumer acceptance, and lipid peroxidation is the primary cause of these quality deteriorations in meat and meat products (Kostadinović et al., Reference KOSTADINOVIĆ, LEVIĆ, POPOVIĆ, ČABARKAPA, PUVAČA, ĐURAGIĆ and KORMANJOŠ.2015). Antioxidants are natural or synthetic substances used to prevent lipid oxidation, and are typically present in many plant extracts. The aim of this review is to present main parameters of poultry meat quality influenced by medicinal herbs.
Sensory characteristic of poultry meat quality
Sensory analysis is one of the oldest means of meat quality control which allows producers to identify, understand and respond to consumer preferences more effectively (Saha et al., Reference SAHA, PERUMALLA, LEE, MEULLENET and OWENS2009; Matitaputty et al., Reference MATITAPUTTY, WIJAYA, BANSI, LAUDADIO and TUFARELLI2015), and increasing choice in the marketplace (Ponte et al., Reference PONTE, MENDES, QUARESMA, AGUIAR, LEMOS, FERREIRA, SOARES, ALFAIA, PRATES and FONTES2004). In the consumer research published by Puvača et al. (Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a), sensory quality of meat has high scores for smell, juiciness and overall impression, demonstrating that the addition of spices including garlic, black pepper and hot red pepper in the diet did not have an adverse effect on meat quality. Conversely, when Džinić et al. (Reference DŽINIĆ, OKANOVIĆ, JOKANOVIĆ, TOMOVIĆ and PALIĆ2013) evaluated the sensory quality of breast chicken meat with the addition of 2% of garlic powder in feed, they saw a characteristic taste and pungent smell of garlic transferred to meat. This characteristic flavour can be both non-beneficial and beneficial, depending of consumer's affinities and demands. In the same investigation, the addition of garlic led to excellent meat quality regarding the juiciness and tenderness of breast meat. Similar results were obtained by Pavelková et al. (Reference PAVELKOVÁ, KAČÁNIOVÁ, HLEBA, PETROVÁ, POCHOP and ČUBOŇ2013) using oregano essential oil in broiler diets, which resulted in improved sensory meat quality, which negated previously published influences of this phytobiotic in altering of taste, juiciness and tenderness of chicken meat. The addition of 30 mg/kg of Macleaya cordata plant extracts (Zdunczyk et al., Reference ZDUNCZYK, GRUZAUSKAS, JUSKIEWICZ, SEMASKAITE, JANKOWSKI, GODYCKA-KLOS, JARULE, MIEŽELIENE and ALENCIKIENE2010), which is from same alkaloid family as black pepper, resulted in an intense smell for breast meat without any atypical smell. The study of Waskar et al. (Reference WASKAR, RAVIKANTH and MAINI2011) reported that supplementation with polyherbal products in poultry diets was effective in improving overall meat quality attributes such as fillet and tender yield, sensory characteristics, organoleptic cooking parameters, overall palatability and consumer acceptability of meat. Plant products, such as garlic, black pepper and hot red pepper, did not have any residual or adverse effects on eating and cooking quality of meat, and can be regarded as safe for usage (Džinić et al., Reference DŽINIĆ, PETROVIĆ, JOKANOVIĆ, TOMOVIĆ and STANAĆEV2009; Puvača et al., Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a).
Physical characteristic of poultry meat quality
Considering the glycolytic process, the initial pH value provides a good guideline for judging physiological meat quality. Accelerated pH decline are related to a light meat colour and poor water retention, which, in the majority of cases, is seen for pH values ranging from 5.8 to 6.0 concerning exudative meat. However many other modern sensory, instrumental and biophysical methods are involved in determination of chicken meat quality (Damez and Clerjon, Reference DAMEZ and CLERJON2008). During recent years, deviations in meat quality which did not show typical characteristics of PSE and DFD were repeatedly reported. There was acceptable colour and increased water holding capacity (WHC) as well as pale colour and good juice retention (PFN). Of especially interest is poor WHC meat, as drip-loss means a loss in weight and texture during cooking and, therefore, economic losses and poor consumer acceptability (Fischer, Reference FISCHER2001).
In the experiment of Puvača et al. (Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a), pH values ranged from 5.5 to 5.7 in breast meat and between 5.9 and 6.0 in thigh and drumsticks (P<0.05), while Qiao et al. (Reference QIAO, FLETCHER, SMITH and NORTHCUTT2001) reported pH values of lighter than-normal, normal and darker-than-normal groups of 5.81, 5.96, and 6.23, respectively, which were significantly different from each other. Puvača et al. (Reference PUVAČA, STANAĆEV, BEUKOVIĆ, LJUBOJEVIĆ, KOSTADINOVIĆ and DŽINIĆ2014) recorded pH value of 5.6 in meat from chickens fed diets containing 2% garlic powder. According to Lara et al. (Reference LARA, NEPOMUCENO, LEDUR, IDA and SHIMOKOMAKI2003), meat with a pH higher than 5.8 is classified as ‘normal’ for quality purposes. Several researchers have demonstrated a significant relationship between raw meat colour and its pH (Allen et al., Reference ALLEN, RUSSELL and FLETCHER1997; Reference ALLEN, FLETCHER, NORTHCUTT and RUSSELL1998; Fletcher, Reference FLETCHER1999). Barbut (Reference BARBUT1993) reported that lightness (L*) had the highest correlation of the L*, a*, b* colour values with PSE conditions, and dietary addition of garlic, black pepper and hot red pepper had an influence on broiler chicken meat colour. The relationship between muscle pH, colour, and meat quality in red meat species is well established (Dutson, Reference DUTSON1983). In poultry, however, the relative influence of pH on meat quality is not as well established as in the extremes of PSE and DFD conditions in pork and beef (Qiao et al., Reference QIAO, FLETCHER, SMITH and NORTHCUTT2001). Positive influences of plants and their extracts in chicken diets on meat quality has been observed by Savković et al. (Reference SAVKOVIĆ, DŽINIĆ and TOJAGIĆ2008) using a mixture of different supplements. Feeding hot red pepper showed the highest positive influence with the lowest drip-loss of breast meat after heat treatment (20.5%), while higher supplementation for thigh with drumstick quality had the most positive influence and lowest drip-loss of 27.3% (Puvača et al., Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a). Allen et al. (Reference ALLEN, FLETCHER, NORTHCUTT and RUSSELL1998) reported that initial and accumulated L* values were correlated positively with drip-loss and cooking-losses in chicken meat. Their results were in agreement with the previous findings of Barbut (Reference BARBUT1993), who observed a high correlation between L* and cooking loss, whereas Allen et al. (Reference ALLEN, FLETCHER, NORTHCUTT and RUSSELL1998) found no correlation between raw meat pH and drip-loss or cooking-losses.
Poultry meat proximate characteristics and caloric value
Gardzielewska et al. (Reference GARDZIELEWSKA, PUDYSZAK, MAJEWSKA, JAKUBOWSKA and POMIANOWSKI2003) reported that broiler chicken feed supplemented with echinacea (Echinacea purpurea), garlic (Allium sativum) and ginger (Zingiber officinale) had no effect on meat moisture content. In trials by Puvača et al. (Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a), the highest protein content of breast (24.0 g/100 g) and thigh with drumstick (20.6 g/100 g) was observed in diets supplemented with black and hot red pepper. From this, it can be postulated that the dietary addition of black and hot red pepper led to a significant improvement in meat quality. In earlier research by Puvača et al. (Reference PUVAČA, STANAĆEV, BEUKOVIĆ, LJUBOJEVIĆ, KOSTADINOVIĆ and DŽINIĆ2014), garlic powder addition to chicken diets at 2.0 g/100 g, gave significant increases in protein content (22.9 g/100 g) in breast meat compared to the control diet (21.8 g/100 g). Souza et al. (Reference SOUZA, FARIA and BRESSAN2011) reported that typical protein content of chicken breast meat ranged from 22.48 to 22.61 g/100 g. The content of protein in chicken breast meat ranges from 20.7 to 32.1%, as reported by Mohammed (Reference MOHAMMED2013), with energy values between 160.0 and 212.0 kcal. Puvača et al. (Reference PUVAČA, KOSTADINOVIĆ, POPOVIĆ, LEVIĆ, LJUBOJEVIĆ, TUFARELLI, JOVANOVIĆ, TASIĆ, IKONIĆ and LUKAČ2015a) showed that the energetic value of breast meat was increased by dietary spice supplementation in feed, and ranged from 92.5 kcal to 97.5 kcal. Onibi et al. (Reference ONIBI, ADEBISI, FAJEMISIN and ADETUNJI2009) reported a significant influence of plant extract addition on fat content, whereby the thigh had the highest fat content (82.9 g/kg), followed by drumstick (66.9 g/kg) and the lowest was seen in breast meat (49.1 g/kg). This is akin to research that has shown fat deposition to be higher in red (leg) meat than in breast meat (Onibi, Reference ONIBI2006; Džinić et al., Reference DŽINIĆ, TOMOVIĆ, PETROVIĆ, STANAĆEV, TASIĆ, IKONIĆ and FILIPOVIĆ2008). Breast meat fat content was affected by the interaction between sex and genetic strain, with males presenting the highest values (Souza et al., Reference SOUZA, FARIA and BRESSAN2011). On the other hand, Lonergan et al. (Reference LONERGAN, DEEB, FEDLER and LAMONT2003) reported higher fat content values in females as influenced by the interaction between sex and genetic group fed with the same plant extracts in the diet. Significantly higher ash content of chicken meat was reported by Mohammed (Reference MOHAMMED2013). Regarding the energy value of chicken meat, it can be observed that the addition of plant extracts to chicken feed had a significant influence on altering the caloric value of meat.
Cholesterol in poultry meat
The available literature is limited regarding changes in muscle cholesterol due to the effect of cholesterol-reducing agents such as medicinal plants, especially in poultry. Konjufca et al. (Reference KONJUFCA, PESTI and BAKALLI1997) reported that cholesterol concentrations were higher in thigh than breast meat when chickens were fed diets supplemented with garlic powder. A possible explanation for this could be that cholesterol is usually associated with adipose tissue, which is more abundant in the thigh than in the breast meat. Moreover, thigh meat has a greater content of slow-twitch fibres than breast meat which has many more large mitochondria, hence the metabolic rate is much faster in comparison to fast-twitch fibres.
In field experiments, supplementation with garlic powder significantly decreased cholesterol levels in breast meat (60.5 and 41.4 mg/100 g), thigh with drumstick (52.9 and 46.4 mg/100 g), skin (122.3 and 97.5 mg/100 g) and liver (502.9 and 474.0 mg/100 g). Other researchers have confirmed the positive influence of dietary garlic powder on the reduction of cholesterol levels in meat (Džinić et al., Reference DŽINIĆ, PETROVIĆ, JOKANOVIĆ, TOMOVIĆ and STANAĆEV2009; Stanaćev et al., Reference STANAĆEV, GLAMOČIĆ, MILOŠEVIĆ, PERIĆ, PUVAČA, STANAĆEV, MILIĆ and PLAVŠA2012) and blood (Shahriari et al., Reference SHAHRIARI, FATEMI TABATABAIE, JAFARI and GHORBANZADEH2009; Issa and Abo Omar, Reference ISSA and ABO OMAR2012; Puvača et al., Reference PUVAČA, TASIĆ, IKONIĆ, KOSTADINOVIĆ, GUBIĆ, OKANOVIĆ, LJUBOJEVIĆ, LUKAČ, TUFARELLI, KÖNYVES, DŽINIĆ and POPOVIĆ2015b). Under the influence of black pepper, cholesterol level in breast meat (54.3 and 40.1 mg/100 g), thigh with drumstick (37.8 and 30.7 mg/100 g), skin (122.2 and 100.6 mg/100 g) and liver (493.6 and 393.2 mg/100 g) can be significantly reduced (P<0.05) compared to control and garlic treatments, but with no significant differences compared to hot red pepper supplementation (Puvača et al., Reference PUVAČA, TASIĆ, IKONIĆ, KOSTADINOVIĆ, GUBIĆ, OKANOVIĆ, LJUBOJEVIĆ, LUKAČ, TUFARELLI, KÖNYVES, DŽINIĆ and POPOVIĆ2015b). These positive effects of black and hot red pepper can be attributed to antioxidative activity (Nabil Alloui et al., Reference NABIL ALLOUI, AGABOU and ALLOUI2014). In addition, black pepper constituents include essential oils (α- and β-pinene, limonene, and β-caryophyllene), piperine, eugenol, the enzyme lipase, and minerals (Singletary, Reference SINGLETARY2010). Puvača et al. (Reference PUVAČA, TASIĆ, IKONIĆ, KOSTADINOVIĆ, GUBIĆ, OKANOVIĆ, LJUBOJEVIĆ, LUKAČ, TUFARELLI, KÖNYVES, DŽINIĆ and POPOVIĆ2015b) confirmed that black pepper lowers cholesterol levels in tissues of chicken, while others (Shahverdi et al., Reference SHAHVERDI, KHEIRI, FAGHANI, RAHIMIAN and RAFIEE2013; Abou-Elkhair et al., Reference ABOU-ELKHAIR, AHMED and SELIM2014) have confirmed lowering effects of cholesterol in the blood and serum of chickens.
Al-Kassie et al. (Reference AL-KASSIE, AL-NASRAWI and AJEENA2011) reported that black pepper supplemented at levels of 0.50, 0.75 and 1.0% in broiler diets depressed cholesterol, Hb, RBC and H/L ratio concentration. The best effect on cholesterol when measured in the study of Puvača et al. (Reference PUVAČA, TASIĆ, IKONIĆ, KOSTADINOVIĆ, GUBIĆ, OKANOVIĆ, LJUBOJEVIĆ, LUKAČ, TUFARELLI, KÖNYVES, DŽINIĆ and POPOVIĆ2015b) was observed with dietary hot red pepper and spice mixtures. Hot red pepper in amount of 1.0 g/100 g, reduced cholesterol content in breast meat (41.2 mg/100 g), thigh with drumstick (24.7 mg/100 g), skin (87.4 mg/100 g) and liver (263.1 mg/100 g). Trials conducted by Al-Kassie et al. (Reference AL-KASSIE, BUTRIS and AJEENA2012) using hot red and black pepper separately and in combination showed similar benefits, whereby addition of these supplements led to a reduction in cholesterol, RBC, WBC and H/L blood ratio concentrations. Shahverdi et al. (Reference SHAHVERDI, KHEIRI, FAGHANI, RAHIMIAN and RAFIEE2013) revealed that the inclusion of hot red pepper in broilers diet decreased cholesterol, triglyceride, glucose concentrations and H/L ratio concentration in broiler blood plasma, what is in accordance with other findings. The advantage of hot red pepper in broiler nutrition is that the birds can consume the active component capsaicin without any adverse effects on feed intake, as birds are insensitive to the irritant effects via capsaicinon sensory neurons and lack vanilloid receptors for capsaicin.
Lipid oxidation of poultry meat
According to Kostadinović et al. (Reference KOSTADINOVIĆ, LEVIĆ, POPOVIĆ, ČABARKAPA, PUVAČA, ĐURAGIĆ and KORMANJOŠ.2015), the liver is an organ with a central metabolic role in the organism, often referred to as ‘the main laboratory’ since it performs detoxification and antioxidation tasks, and hence is the prime target for the study of the metabolism of xenobiotic and other toxic substances. Antioxidant enzymes counteract excessive formation and deleterious effects of reactive oxygen metabolites. For example, superoxide dismutase (SOD) catalyses the conversion of superoxide anion radical to H2O2, catalase reduction of H2O2 to water, while glutathione peroxidase (GSHPx) acts in conjunction with other enzymes to reduce H2O2 and to terminate lipid peroxidation (Halliwell and Chirico, Reference HALLIWELL and CHIRICO1993). This reduces the oxidative damage of fats in meat, extends shelf life and increases meat safety.
Lipids are an important component of meat and contribute to desirable sensory characteristics of meat. Lipids enhance the flavour and aroma profile of meat and increase tenderness and juiciness (Gorelik et al., Reference GORELIK, LIGUMSKY, KOHEN and KANNER2008). However, it is generally accepted that lipid oxidation is the primary process responsible for quality deterioration of meat during storage. Many investigations have shown that plant flavinoids have the capacity for powerful antioxidant activity by scavenging free radicals and terminating oxidative reactions. Kostadinović et al. (Reference KOSTADINOVIĆ, LEVIĆ, POPOVIĆ, ČABARKAPA, PUVAČA, ĐURAGIĆ and KORMANJOŠ.2015) reported that concentrations of the oxidative indicator malondialdehyde (MDA) were significantly lower and GSHPx activity was higher in the group supplemented with Artemisia absinthium than in the unsupplemented group, and found less lipid peroxidation in the blood and plasma of broiler chickens fed the supplemented diet.
All meat and fish products are prone to oxidation. Amongst meat products, poultry meat is considered to be more prone to the development of oxidative rancidity compared to red meat, due to the higher content of phospholipids in poultry meat. It has been demonstrated that meat oxidation starts by a peroxidation of the phospholipid fraction. The lowest level of MDA in breast meat (0.05 mg/kg), thigh with drumstick (0.12 mg/kg) and liver (0.13 mg/kg) was observed in treatment with addition of 1.0 g/100 g of black pepper, while the highest was observed in the control group (Puvača et al., Reference PUVAČA, TASIĆ, IKONIĆ, KOSTADINOVIĆ, GUBIĆ, OKANOVIĆ, LJUBOJEVIĆ, LUKAČ, TUFARELLI, KÖNYVES, DŽINIĆ and POPOVIĆ2015b). Lipid oxidation reduces meat quality by a number of ways, including off-flavours, higher drip loss and colour changes. During lipid oxidation, poly-unsaturated fatty acids are degraded to volatile short-chain oxidation products, which cause bad odours (Jensen et al., Reference JENSEN, SKIBSTED and BERTELSEN1998), and affect the ability of the membranes to hold water, contributing to drip loss (Weber and Antipatis, Reference WEBER and ANTIPATIS2001).
Results of thiobarbituric value (TBARS) methods showed that supplementation with lemon balm and the combination of hawthorn and yarrow in broiler diets caused a reduction in lipid oxidation in the thigh muscle (Marcinčáková et al., Reference MARCINČÁKOVÁ, ČERTÍK, MARCINČÁK, POPELKA, ŠIMKOVÁ, KLEMPOVÁ, PETROVIČ, TUČKOVÁ and BAČA2011). Luna et al. (Reference LUNA, LÁBAQUE, ZYGADLO and MARIN2010) added thymol and carvacrol to broiler diets at levels of 150 mg/kg for 42 days and reported positive effects on the oxidative stability during the storage of red meat. Similar positive effects of medicinal plants and aromatic herbs on shelf life were observed by Šperňáková et al. (Reference ŠPERŇÁKOVÁ, MÁTÉ, RÓZAŇSKA and KOVÁČ2007) using rosemary powder and by Govaris et al. (Reference GOVARIS, BOTSOGLOU, PAPAGEORGIOU, BOTSOGLOU and AMBROSIADIS2004) with oregano powder.
Conclusions
It can be concluded that the dietary addition of plants and their extracts to broiler diets can have significant influence in improvement of sensory, physical and proximate composition of meat. Meat from chickens fed with such supplementary compounds has higher energetic values which are of practical importance for human nutrition. Many plant extracts act as powerful antioxidants in the alteration of chicken meat quality and safety; lowering cholesterol and decreasing lipid-oxidation processes. Spices, herbs and aromatic plants can be used as very effective natural supplements, and there is evidence that, apart from improving meat quality, they can provide an alternative to antibiotic growth promoters. Moreover, the technological as well as nutritional and sensory quality of chicken meat can be reached with proven feed supplements, because not all plant-derived additives may have beneficial effects on meat quality.
Acknowledgments
This paper is a part of the project III 46012 which is financed by Ministry of Education, Science and Technological development of the Republic of Serbia.