Review. White striping and woody breast myopathies in the modern poultry industry: a review. V. A. Kuttappan, B. M. Hargis, and C. M.

Transcription

1 Review White striping and woody breast myopathies in the modern poultry industry: a review V. A. Kuttappan, B. M. Hargis, and C. M. Owens 1 Department of Poultry Science, University of Arkansas, Fayetteville, AR ABSTRACT Myopathies are gaining the attention of poultry meat producers globally. White Striping (WS) is a condition characterized by the occurrence of white striations parallel to muscle fibers on breast, thigh, and tender muscles of broilers, while Woody Breast (WB) imparts tougher consistency to raw breast fillets. Histologically, both conditions have been characterized with myodegeneration and necrosis, fibrosis, lipidosis, and regenerative changes. The occurrence of these modern myopathies has been associated with increased growth rate in birds. The severity of the myopathies can adversely affect consumer acceptance of raw cut up parts and/or quality of further processed poultry meat products, resulting in huge economic loss to the industry. Even though gross and/or histologic characteristics of modern myopathies are similar to some of the known conditions, such as hereditary muscular dystrophy, nutritional myopathy, toxic myopathies, and marbling, WS and WB could have a different etiology. As a result, there is a need for future studies to identify markers for WS and WB in live birds and genetic, nutritional, and/or management strategies to alleviate the condition. Key words: white striping, woody breast, myopathy, broiler, muscular dystrophy 2016 Poultry Science 95: INTRODUCTION Global attention has been drawn to the increasing incidence of myopathies in modern broiler chickens. The two main myopathies, White Striping (WS) and Woody Breast (WB), are of increasing concerns as the affected fillets have unappealing appearance of the breast fillets at the meat counter (Kuttappan et al., 2012c) and reduced protein functionality in further processed products (Mudalal et al., 2014, 2015; Tijare et al., 2016). Incidence of these conditions have already being reported in different countries such as Brazil, Italy, Finland, the United States, and the United Kingdom (Kuttappan et al., 2012c; Petracci et al., 2013b; Ferreira et al., 2014; Sihvo et al., 2014; debrotetal., 2016). Among the two myopathies, WS was studied extensively since 2009 (Bauermister et al., 2009; Kuttappan et al., 2009), while reports about WB are comparatively recent (Bilgili et al., 2014). WS is visually characterized by the white lines of intramuscular deposits in raw meat seen parallel to muscle fibers mainly in breasts (Figure 1), tenders, and certain thigh muscles (Kuttappan et al., 2013b). On the other hand, WB affects the tactile characteristics of broiler raw breast fillet making it firmer upon palpation with higher compression C 2016 Poultry Science Association Inc. Received December 17, Accepted May 22, Corresponding author: cmowens@uark.edu force compared to normal breast fillets (Sihvo et al., 2014; Mudalal et al., 2015; Figure 2). Both these conditions occur in varying degrees, often together on the same fillet. In severe cases of WB, a prominent ridgelike bulge on caudal area of fillet is present (Figure 2), and in some cases, a clear viscous fluid cover and/or petechial multifocal lesions on the fillet surface is observed (Sihvo et al., 2014). Both WS and WB had been reported to have overlapping histological lesions mainly myodegeneration and necrosis, lymphocyte and macrophage infiltration, fibrosis, lipidosis, and regenerative changes (Kuttappan et al., 2013b; Sihvo et al., 2014; Trocino et al., 2015; de Brot et al., 2016), However, the highest level of fibrosis was observed in WB (Trocino et al., 2015) and chronic lipidosis and fibrosis in fillets with both WS and WB (Soglia et al., 2015). Velleman and Clark (2015) reported that the reason for the fibrotic changes in WB could even vary between different broiler lines. It is also not clear whether WB and WS share a common etiology (Velleman, 2015). Even though the exact reason behind the occurrence of these myopathies is still unknown, there are a number of speculations about the plausible etiology. A recent study with RNA-seq analysis suggested that localized hypoxia, oxidative stress, higher levels of intracellular calcium, and muscle fiber type switching (Mutryn et al., 2015) associated with modern fast growing broilers could be associated with occurrence of these myopathies. Various studies reported that fillets with 2724

2 POULTRY MYOPATHIES 2725 Figure 1. Modified visual scoring scale (modified from Kuttappan et al., 2012c) for WS in broiler breast fillets where 0 = normal, 1 = moderate, 2 = severe, and 3 = extreme. Normal No distinct white lines. Moderate Small white lines, generally < 1 mm thick, but apparently visible on the fillet surface. Severe Large white lines (1-2 mm thick) very visible on the fillet surface. Extreme Thick white bands (> 2mm thickness) covering almost entire surface of fillet. Figure 2. Comparison of severe woody breast (WB) and normal fillets (A and B, respectively). Each fillet has a 200 g weight resting on the cranial portion of the fillet. The severe WB shows no visual signs of compression while the weight on the normal fillet compresses the surface of the fillet. higher degrees of WS were heavier (Kuttappan et al., 2013c; 2012b) and thicker (Kuttappan et al., 2013c) than normal fillets. Moreover, feeding birds with high energy and protein diets (Kuttappan et al., 2012b), age (Bauermeister et al., 2009; Kuttappan et al., 2015), gender (Kuttappan et al., 2013c; Trocino et al., 2015), feed restriction (Trocino et al., 2015), and genetics (Kuttappan et al., 2013c; Petracci et al., 2013a; Lorenzi et al., 2014) had been associated with increased severity of WS. However, many of these factors could have slaughter body weight as a lurking factor. The present review aims at discussing the comprehensive findings from various studies conducted on myopathies and their impact on the poultry meat industry. Furthermore, this review will compare and contrast characteristics of WS with known muscle conditions in animals, which could provide valuable insights for researches in this area. MYOPATHIES AND THE MODERN POULTRY INDUSTRY Poultry meat has been highly preferred among the meat consumers mainly due to its health benefits, convenience in cooking, and reasonable cost (Haley, 2001; Davis and Stewart, 2002). According to the estimates from the USDA, the per capita consumption of poultry meat in 2015 is more than double that of 1965 (National Chicken Council, 2016a).Theincreaseinconsumer demand has put pressure on producers to increase production while reducing the cost and time of production. As a result, broilers are continuously selected to attain greater body weight at younger ages. In 1925, the average market live weight of a 112 d broiler was 1.1 kg while in 2015, a market weight of 2.8 kg was achieved at 48 d (National Chicken Council, 2015). Petracci et al. (2015) reported that, over the last 10 years, the continuous selection for broilers has results in almost a 5% increase in breast meat yield, contributing to greater than one-fifth of bird weight. This increase in live weight has been driven by the shift in consumers purchasing a whole bird carcass to cut up parts with the processing sector favoring larger birds (up to approximately 4.5 kg in some markets). Furthermore, the increase in bird size has increased metabolic demands associated with rapid growth of poultry leading to an increased risk of disease

3 2726 KUTTAPPAN ET AL. incidences, economic loss, and welfare concerns (Julian, 2005). Anthony (1998) reported that high selection intensities, shorter generation intervals, and reduced environmental influences have reduced slaughter age, and increased body weight, muscle yields, and feed conversion efficiency. However, this selection pressure has had a negative influence on meat quality traits such as texture and flavor (Anthony, 1998). Mahon (1999) hypothesized that selection for enhanced growth may have lead for selection of inherent muscle fiber defects or insufficient capillary/fascial growth, or growth-induced myopathy. There are a number of studies reporting the relationship of increased growth rate in poultry to various muscular defects such as lower capillary density and greater metabolic stress (Hoving-Bolink et al., 2000; Macrae et al., 2006), aberration in muscle cell cation regulation (Sandercock et al., 2009), increased muscle damage (Velleman and Nestor, 2003), and incidence of pale, soft, exudative meat (Wang et al., 1999) and focal myopathy (Wilson et al., 1990). Mazzoni et al. (2015) observed that heavy broilers produced under intensive farming had higher incidence of myodegeneration, which was reflected in chemical composition and impaired water-holding capacity of the meat. Petracci et al. (2015) reported that the modern fast growing broiler chickens could have reduced thermoregulatory capacity, altered cation regulation in muscle cells, and reduced glycolytic potential resulting in various meat quality defects. Even though the mechanism by which increased growth rates in modern broilers initiates myopathies is not yet known, it is very clear from various studies that heavier birds have higher incidence of severe WS and WB (Kuttappan et al., 2012b; Lorenzi et al., 2014; Russo et al., 2015; Trocino et al., 2015). More importantly, the impact of these myopathies on poultry meat quality could result in serious economic loss. Poultry breast meat is a highly consumed meat product in part because it is an inexpensive source of lean meat. The severity of WS in breast fillets has negative effects on appearance and consumer purchases (Kuttappan et al., 2012c). The perception of increased fat deposits in the breast fillet is unfavorable for consumers as it gives the impression that the breast fillet is unhealthy (Kuttappan et al., 2012c). Consumers always prefer to see the color of the product, especially when they buy raw meat. WS can be a major problem especially when raw fillets are marketed as tray packs, which is the predominant packaging method used for raw fillets. Packing fillets with different degrees of WS in the same tray could result in rejection of the whole tray pack by the consumer. As expected from gross examination, WS fillets have an increase in fat content and a corresponding decrease in protein percentages (Kuttappan et al., 2012b; 2013a; 2013b; Petracci et al., 2014). Studies conducted on fillets with WB reported changes in proximate composition similar to WS (Soglia et al., 2015). Changes in the proximate composition of overall breast meat due to both WS and WB could result in changes in nutritive value of end meat products, leading to concerns among consumers and reduce value of the lean meat product. In addition, breast fillets with WS and WB have higher cook loss, lower marinade pick up, and reduced tenderness (Petracci et al., 2013b; Mudalal et al., 2015; Tijare et al., 2016) which could be due to degeneration of muscle fibers resulting in decreased myofibrillar and sarcoplasmic proteins (Mudalal et al., 2014). Various studies conducted by independent research groups from the United States and Italy reported that the incidence of severe WS has increased drastically from 1.4 to 8.7% (average 5%) in 2012 (Kuttappan et al., 2012b; Petracci et al., 2013b) to 25.7 to 32.3% (average 29%) in 2015 (Russo et al., 2015; Tijare et al., 2016), although there could be other confounding factors such as strain, age, gender, feed etc. involved in these studies. Furthermore, most of these studies were conducted in controlled environments with ideal growing conditions, which may have resulted in the high incidences. In terms of the overall incidence in industry, a recent article published in The Wall Street Journal (Gee, 2016) reported that 5 to 10% of the boneless, skinless breast meat produced in industry could have WB. Reports also indicate that the affected fillets are sold at a discounted price or used for further processed or ground products (Gee, 2016). The United States industry produces over 53 billion pounds live weight (National Chicken Council, 2016b) which equates to approximately 12 billion pounds of breast meat per year (based on 23% breast yield). Thus, the incidence of these conditions can result in an excess of $200 million per year lost (conservative estimate) due to decreased yield (e.g., trimming, drip loss, cook loss, etc.) and/or lost value if product is downgraded or even discarded. COMPARISON OF MODERN MYOPATHIES (WS AND WB) WITH CERTAIN EXISTING CONDITIONS Several myopathies exist in the poultry industry. Many of these show similar characteristics to WS and WB at gross and/or histopathology level. Among these conditions are hereditary such as muscular dystrophy (Julian and Asmundson, 1963; McMurtry et al., 1972; Julian, 1973), nutritional myopathy (Dam et al., 1952; Machlin and Shalkop, 1956; Klasing, 2008), deep pectoral myopathy (Wight and Siller, 1980), and toxic myopathy (Chalmers, 1981; Dowling, 1992; Roder, 2011). White intramuscular deposits similar to WS have also been observed in other species in the form of intramuscular fat, which is considered a superior quality trait in beef and pork (USDA-FSIS, 2008). Hereditary Muscular Dystrophy Hereditary muscular dystrophy is a condition seen in domestic fowl, and is similar to those seen in

4 POULTRY MYOPATHIES 2727 muscular dystrophies of human beings (Julian and Asmundson, 1963). Hereditary muscular dystrophy occurs due to a homozygous autosomal recessive gene (am), and the phenotypic expression varies due to the action of various modifying genes (Asmundson and Julian, 1956; Wilson et al., 1988). The affected birds have a broad shallow body and short thick limb bones that may prevent the birds from being able to right themselves when placed on their back (Wilson et al., 1979). WS birds have elevated serum creatine kinase levels (Kuttappan et al., 2013a), increased fat content in pectoral muscle (Kuttappan et al., 2012b; Petracci et al., 2014), gross white striations in the direction of muscle fiber, and hypertrophy of pectoral muscle (Kuttappan et al., 2013b) which are similar to observations in hereditary muscular dystrophy (Asmundson and Julian, 1956; Julian and Asmundson, 1963). However, birds with hereditary muscular dystrophy have elevated muscle cathepsins, mitochondrial enzyme activity, low levels of lactate dehydrogenase, and an enlarged sarcotubular system (Wilson et al., 1979), which factors have not been tested in WS. The histopathological studies of the condition revealed a wide variation in the fiber size, vacuolization and degeneration of the muscle fibers, mononuclear infiltration, fat deposition, and increase in connective tissues (Jordan et al., 1959; Holliday et al., 1968; McMurtry et al., 1972; Julian, 1973). Furthermore, Barany et al. (1966) reported that there was a decrease in the sarcoplasmic proteins, myosin and actin in breast muscles of genetically dystrophic birds when compared to the normal chickens. Besides the effect of hereditary muscular dystrophy on the appearance of meat, it was also shown to affect the tenderness (Scholtyssek et al., 1967; Peterson and Lilyblade, 1969), fat content, and fatty acid profile of the poultry meat (Jordan et al., 1959; Jordan et al., 1964; Chio et al., 1972). Hereditary muscular dystrophy and WS/WB closely share some gross and/or histological lesions. Interestingly, the hardness or stiffness aspect of WB has been previously described by Hete and Shung (1991) when they described excised muscle from dyptrophic chickens (New Hampshire Line 413). Authors stated that tissue was stiff and had a rubbery texture as opposed to their control lines (Leghorn and New Hampshire Line 412) which exhibited flaccid muscles. These are characteristics observed in today s woody and normal breast meat, respectively. Even though the majority of chicken muscular dystrophy studies were on New Hampshire strains, there are reports of similar condition in Cornish chickens (Wagner and Peterson, 1970). However, there are no reports which suggest hereditary muscular dystrophy exists in modern commercial broiler birds. Unlike hereditary muscular dystrophy, WS has higher incidence across various commercial broiler strains (Bauermeister et al., 2009, 2011; Kuttappan et al., 2013c; Petracci et al., 2013a). Some of the strains showed higher percentages of severe WS, but this may be due to the increased body weight of these strains rather than a genetic predilection. In fact, a recent study reported that there is a strong non-genetic component for all the breast muscle myopathy traits such as deep pectoral myopathy, WS, and WB (Bailey et al., 2015). Various studies reported higher incidence of WS in high yielding strains (Kuttappan et al., 2013c; Lorenzi et al., 2014), although Trocino et al., (2015) observed no genotypic influence on occurrence of myopathy. On the other hand, Velleman (2015) compared the gene expression of WB in affected meat and observed differences in cellular mechanisms with respect to various broiler lines used in the study. These reports had difficulties in linking hereditary muscle dystrophy with modern myopathies, but did not completely rule out the possibility of any underlying genetic defect associated with fast growing birds. Nutritional Myopathy Vitamin (Vitamin E) or mineral (selenium and sulfur) deficiencies in the poultry diet may result in pathological conditions such as encephalomalacia, exudative diathesis, and nutritional myopathy in chicks, ducks, and turkeys (Klasing, 2008). Vitamin E, along with the selenium dependent - glutathione peroxidase, catalase, and superoxide dismutase, is involved prevention of the propagation of free radicals (such as polyunsaturated lipid peroxyl radical) which are involved in several diseases processes (Herrera and Barbas, 2001). The deficiency of these nutrients in the diet could result in the disruption of the integrity of the cells resulting in damage leading to pathological conditions. Nutritional myopathy is grossly characterized by white striations on breast and leg muscles, and histopathology reveals degeneration of muscle fibers with fragmentation, hyalinization, loss of striation, multiplication of sarcolemmal cells, infiltration by heterophils and clumping of fibers into eosinophilic masses (Dam et al., 1952; Machlin and Shalkop, 1956) which are similar to the lesions observed in WS and WB (Kuttappan et al., 2013b; Sihvo et al., 2014). Although lesions of nutritional myopathy are similar to modern myopathies, the etiology seems different. Various studies showed that adequate levels of dl-αtocopherol acetate (0.01%), l-cystine (0.24%), and dlmethionine (0.5%) in the diet ration (Dam et al., 1952; Machlin and Shalkop, 1956) or 900 to 1025 μg/100 ml of total plasma tocopherol levels (Scott and Desai, 1964) can almost completely prevent the incidence of nutritional myopathy. No recent reports of nutritional myopathy in modern broilers have been found due to the use of adequate levels in vitamin E (>10 IU/kg of feed; NRC, 1994) and associated nutrients in the poultry diet. Guetchom et al., (2012) compared dietswithandwithoutaddedvitamineandobserved that diet with added vitamin E (50 mg/kg) increased plasma vitamin E and mildly reduced damaged muscle fibers. On the other hand, the study conducted by

5 2728 KUTTAPPAN ET AL. Kuttappan et al. (2012a) showed that even 400 IU of vitamin E/kg of feed could not completely prevent the occurrence of severe WS. In fact, the studies that reported the occurrence of WS and WB, however, used poultry rations with adequate or higher levels of vitamin E and associated nutrients (Kuttappan et al., 2013a; 2013c). Nonetheless, other vitamin E deficiencyassociated conditions such as encephalomalacia and exudative diathesis are never seen in flocks having WS and WB. These make WS and WB less likely to be a vitamin E deficiency. However, further studies are needed to evaluate whether the recommended levels of vitamin E are adequate for the fast growing modern birds and also the effect of selenium or sulfur containing amino acids and/or in combinations with dietary vitamin E on incidence of modern myopathies. Deep Pectoral Myopathy Deep pectoral myopathy (DPM), Oregon disease, or green muscle disease is a condition affecting the supracoracoideus muscle (tenders) in broilers and turkeys. The incidence of deep pectoral myopathy ranged from 0 to 1.88% (average 0.06%) in broilers (Kijowaski and Konstanczak, 2009). Contraction of the supracoracoideus muscle, located in a compartment between the keel and the tough inelastic fascia, may lead to the muscle to expand up to 20% of its weight. In some cases, there is not enough room for the muscle to expand resulting in ischemia of the muscle (Siller, 1985; Mitchell, 1999; Bilgili and Hess, 2002). According to Wight and Siller (1980), gross lesions of DPM include acute edema followed by green necrosis and replacement of the caudal region with fibro-adipose tissue. Histopathological study of the green lesions showed necrotic, anucleated muscle fibers surrounded by a fibrous capsule externally surrounded by region of normal/regenerating muscle or fibro-adipose tissue (Wight and Siller, 1980). Electron microscopic examinations showed ischemic necrotic lesions with early loss of glycogen and disintegration of sarcoplasmic reticulum, mitochondria, nuclei, and Z-lines. Besides the significant change in color (from pink to green), they also observed that the meat became more tough and fibrous towards the later stages of deep pectoral myopathy (Wight and Siller, 1980). Siller (1985) suggested that the condition could be a result of the selection for improved muscle growth, and hypothesized that selection based on the plasma creatine kinase levels could reduce the incidence. According to Petracci et al. (2015), the increased growth rate and breast yield could be the reason for increased incidence of myopathies such as deep pectoral myopathy, PSE, WS, and WB. Bailey et al. (2015) compared the incidences of deep pectoral myopathy, WS, and WB in two different lines of broiler birds and found that the line with higher breast yield (29% vs. 21%) showed higher incidence of all the three myopathies. Although growth performance is a common aspect connecting deep pectoral myopathy with WS and WB, immediate predisposing factor for deep pectoral myopathy is ischemia that can be induced by encouraging birds to flap (Wight and Siller, 1980; Lien et al., 2012). However, deep pectoral myopathy has some similarities in the microscopic lesions seen in the tenders/supracoracoideus muscle (Wight and Siller, 1980) with that of WS and WB, which suggests that ischemia may also be associated with these modern myopathies. Toxic Myopathies Most frequently observed toxic myopathy in poultry is from ionophore usage. Ionophores have a broad spectrum of activity but a narrow range of safety in poultry. Commonly used ionophore anticoccidial drugs in poultry industry are monensin (100 to 125 μg/kg), salinomycin (60 to 75 μg/kg), lasalocid (75 to 125 μg/kg), and narasin (60 to 80 μg/kg) and an over usage by 20 to 50% can cause toxicity (Dowling, 1992). Monensin is the most studied ionophore for toxicity due to its myopathic lesions in broilers, laying hens, growing and breeder turkeys (Mitchell, 1999). Clinical signs of ionophore toxicity are feed refusal, growth depression, incoordination, cream-colored diarrhea, dyspnea, leg weakness, muscular stiffness, and/or weakness and sternal recumbency. Post mortem examination may not show any specific gross lesions (Chalmers, 1981; VanderKop et al., 1989), but extensive microscopic myopathic lesions on major pectoral, supracoracoideus, cranial iliotibial, medial crural flexor, femoral adductor, and gastrocnemius muscles have been observed (Chalmer, 1981). The histopathological lesions associated with ionophore toxicities in skeletal muscles are variable and usually include myofiber necrosis and fragmentation, eosinophilic granular masses of disrupted sarcoplasm, intermyofibrillar fatty infiltration, mitochondrial degeneration, infiltration of heterophils and macrophages into interstitium and sarcoplasm (Dowling, 1992). Sandercock and Mitchell (1999) reported that the selection for rapid growth and higher meat yield increased the susceptible of broilers to monensininduced myopathy. It has been proposed that the toxicity of ionophores could result in sodium-potassium imbalance across the sarcolemma leading to an increased calcium influx causing cellular damage through the activation of various enzymes such as intracellular phospholipase and calcium dependent proteases, thus damaging both internal structure of the muscle fiber and also the plasma membrane (Jackson et al., 1984; Alderton and Steinhardt, 2000; Sandercock and Mitchell, 2003; Sandercock and Mitchell, 2004; Whitehead et al., 2006). The ionophore toxicity could be exacerbated due to its interaction with other drugs such as tiamulin, macrolide antibiotics, chloramphenicol, sulfonamides, etc (Dowling, 1992; Roder, 2011). Lesions similar to ionophore toxicity can be seen in different species of animals due to toxicity from

6 POULTRY MYOPATHIES 2729 gossypol present in cottonseed meal and also other plants such as Taxus spp., Nerium oleander (oleander), Cassia occidentalis (senna), Eupatorium rugosum (white snakeroot), vetch, and Karwinskiahum boldtiana (coyotillo) (Roder, 2011). High levels (> 400 mg/kg of feed) of gossypol in broiler diets can result in reduced feed intake, growth and feed efficiency, alteration in the spleen and bursa of Fabricius, liver damage, and enlarged gall bladder (Henry et al., 2001; Silva et al., 2003). Furthermore, C. occidentalis produces lesions in pectoral and leg muscles similar to those of ionophore toxicity in chicken (Mahon, 1999). Daily administration of C.occidentalis extract could result in weight loss, muscular weakness, degenerative histopathological lesions in skeletal and cardiac muscle (Graziano et al., 1983). Electron microscopy revealed enlarged mitochondria with disrupted or excessively branched cristae in skeletal muscle in affected birds, which is suggestive of mitochondrial myopathy (Cavaliere et al., 1997). Some of the gross and histological lesions of toxic myopathy have similarities to modern myopathies. However, most of the studies have reported the occurrence of severe degrees of WS used anticoccidial-ionophore drug (monensin at the level of 90 g/ton of feed) within the reported therapeutic dose of the drug. In addition, these studies did not use any of the above toxic plant contents in diet formulation (Kuttappan et al., 2012a; 2012b; 2013a; 2013b). Recently, a study conducted by Dalle Zotte et al. (2015) observed that vaccination against coccidiosis did not affect the incidence of WS although dietary inclusion of anticoccidial drugs resulted in better growth performance and higher prevalence of severe WS. Moreover, the lack of the typical clinical signs of ionophore toxicity like feed refusal, growth depression, and creamy-colored diarrhea (Wagner et al., 1983; VanderKop et al., 1989) in birds with modern myopathies implies that the chance of toxic myopathic etiology is implausible. Pale Soft and Exudative (PSE) Meat Pale, soft, exudative is a condition where the meat show pale color, soft consistency, and poor water holding capacity and the causes of the condition may be genetic and/or environmental factors related to preslaughter stress (Owens et al., 2009). The incidence of the condition is mainly attributed to the rapid decline of ph in the post mortem period, while the temperature of meat is still high (Pietrzak et al., 1997). The occurrence of the condition could be due to excess release of calcium ions stored in the sarcoplasmic reticulum of skeletal muscle because of a defect in the ryanodine receptors (Strasburg and Chiang, 2009). These calcium ions stimulate the activity of various enzymes in muscle resulting in denaturation of the protein (Jackson et al., 1984; Alderton and Steinhardt, 2000; Sandercock and Mitchell, 2003; Mitchell and Sandercock, 2004; Whitehead et al., 2006). Pale, soft, exudative meat was initially reported in pork, but there are reports of a similar condition in broiler chickens (Van Laack et al., 2000; Wilkins et al., 2000; Zhang and Barbut, 2005). Wilhelm et al. (2010) found that the broiler fillets with PSE-like condition had lower ph, water holding capacity, and shear force but higher color (L value), myofibrillar fragmentation index (MFI), and cook loss than normal fillets. The authors also reported the PSElike meat showed electron microscopic lesions such as shrinking and depolymerisation of myofilaments and Z-lines disorganization (Wilhelm et al., 2010). A consumer study conducted by Garcia et al. (2010) didnot show any significant difference between the normal and PSE chicken meat with respect to tenderness and flavor. However, the reduced water holding capacity and aesthetic defect caused by the pale color of PSE meat could cause economic loss to the producer. About 5 to 40% of the meat in the poultry industry was estimated to have PSE-type characteristics, which could result in an economic loss of $200 million per year (Owens et al., 2009). Although WS and WB do not share any direct relationship with PSE in gross changes, the studies conducted by Petracci et al., (2015) suggested that the increased accumulation of calcium ions in WS or WB, similar to PSE lesions, could have an important role in development of associated lesions. Soglia et al., (2015) observed that increased expression of calcium ATPase in WB and WS/WB samples leading to higher calcium levels, which could play a key role in these myopathies. Intramuscular Marbling and WS Occurrence of WS could give the impression of marbling in chicken, so a comparison between WS and marbling in beef, veal, mutton, and lamb is important. Marbling refers to the white flecks of intramuscular fat deposit seen in raw meat and has been found to be influenced by many factors species, breed, gender, age, growth rate, muscle location, and level of nutrition (Hocquette et al., 2010). Occurrence of marbling could enhance the flavor and juiciness of meat, so it has been considered as a superior quality in grading of beef, veal, mutton, and lamb (USDA- FSIS, 2008). In poultry, the majority of the fat is deposited subcutaneously or abdominally with very little fat stored in the muscle (Sams and Alvarado, 2010). As a result, consumers consider poultry meat, especially breast fillets, as a lean cut (Davis and Stewart, 2002). Thus, occurrence of WS, although similar to marbling in appearance, caused reduced consumer acceptance (Kuttappan et al., 2012c) Marbling is mainly associated with increased deposition of fat near blood capillary network, in the perimysial layer of red muscle (Moody and Cassens, 1968; Judge et al., 1989; Nishimura et al., 1999; Harper and Pethick, 2004; Hocquette et al., 2010) but is not related to any disorder or disease process (Harper and Pethick, 2004). A

7 2730 KUTTAPPAN ET AL. series of events contributing to initiation and maintenance of preadipocyte proliferation and differentiation as well as maturation into adipocytes results in marbling (Smith et al., 2000; Tong et al., 2015). In WS of poultry meat, the increased fat deposit apparently replaces damaged muscle fibers, and occurs primarily in white muscle compared to red muscle (Kuttappan et al., 2013b). The occurrence of marbling is mainly associated with certain breeds (Crouse et al., 1989; Albrecht et al., 2006) and deposition of intramuscular fat in beef is inversely related to muscle mass (Albertí et al., 2008; Hocquette et al., 2010). On the other hand, WS does not show any breed or strain predilection (Kuttappan et al., 2013c; Petracci et al., 2013a), but is associated with heavier birds (Kuttappan et al., 2013c) or birds with heavier fillets (Bauermeister et al., 2011) in the same flock. From these observations, WS in broilers and marbling in red meat animals could be two different conditions. In fact, the exact mechanisms that control the occurrence of both marbling and WS are still unknown and needs further researches comparing the two. MODERN MYOPATHIES: CHALLENGES AND AREAS FOR FUTURE RESEARCH One of the major challenges in research involving WS and WB is the lack of an effective biomarker to identify the condition in live birds. Until now, it is impossible to predict the occurrence of WS, although efforts are being made to palpate and identify WB in live birds. Mutryn et al. (2015) conducted RNA-sequencing study on birds with WB and identified genes, which could be associated with the condition. Conducting similar omics studies on the modern myopathy conditions on birds at different age groups could help to differentiate causative from resultant tissue changes and thereby identify specific biomarkers for the conditions. Identification of specific biomarkers can help to accurately evaluate the effect of various feed additives, genetics, environmental, or management conditions in improving or aggravating the condition in live birds. Another challenge in comparing different studies conducted on WS and WB is lack of effective standardized scoring scale, as both WS and WB rely on subjective scoring systems. In case of WS, the scoring scale developed by Kuttappan et al. (2012c) is widely used in various studies. However, the effectiveness of this scale can depend on various factors. It is important to score fillets under similar conditions to avoid noise from various processing conditions. Temperature, humidity, light source, and light intensity in the room, post mortem age, temperature of the samples, and surface wetness or moistness should be kept identical for comparable results. Samples should be scored against a white background (preferably, use a white tray to keep fillets while scoring). It is ideal to have same person/people scoring, if possible, to get comparable results at least in the same replicates in a study. Since there are reports that the incidence of WS and WB has increased over the years, there could be chances that the degree of severity may also be increasing over the years. In this case, the scale needs to be standardized and modified with more anchor points over time (Figure 1). Use of objective techniques such as image analysis (Kuttappan et al., 2012c) for inline scoring require more research and attention. The scoring scale for WB needs more standardization compared to WS as it is difficult to define anchors on a tactile scoring scale compared to visual scoring. Tijare et al. (2016) described scoring methods for this condition with some description with regard to level of hardness and location (cranial vs. entire fillet). When scoring for WB, it may be ideal to use more than one person to score for consensus especially when first using the scoring system until scorers become experienced. Instrumental evaluation of hardness would be useful, especially if a rapid method could be developed. Mudalal et al. (2015) used texture analyzer to determine the force required to compress fillets and the values showed meaningful difference between normal and WB fillets. In addition, Lee et al. (2008) developed a novel laser air puff technique to measure tenderness in raw fillets. These techniques with modifications could be an effective tool to identify fillets with different degrees of hardness, or WB. CONCLUSION White striping and woody breast are two myopathies seen in modern broiler breast with faster growth rate. Occurrence of severe degrees of these modern myopathies in broiler breast fillets reduces the quality and acceptance of both raw as well as cooked meat and meat products. To date, the insults which initiate the myopathies are unclear. Comparison of WS and WB with various known myopathic conditions suggests that these modern myopathies may have a different etiology than any of conditions such as hereditary muscular dystrophy, nutritional myopathy, toxic myopathy, and intramuscular marbling. Similarity of gross and histological lesions of WS and WB with various myopathies and the possible difference in etiology suggest that muscle may respond to insults in a similar manner irrespective of the etiology. Various studies have shown that the incidence of these modern myopathies have been increased over the past few years. In addition, other conditions such as spaghetti meat or surface fraying of fillets, feathering of tenders etc. are also gaining attention of poultry producers, although there are few published studies on these conditions. Nonetheless, if these myopathic changes precede more severe condition in the future, especially with increasing growth rate and feed conversion rates in birds, it could lead to serious economic loss and also result in welfare issue in live birds.

8 POULTRY MYOPATHIES 2731 ACKNOWLEDGMENTS The authors thank the photographers, Fred Miller, Sara Landis, and Luke Gramlich (University of Arkansas Division of Agriculture), for providing photography services for images used in this review. REFERENCES Albertí,P.,B.Panea,C.Sañudo, J. L. Olleta, G. Ripoll, P. Ertbjerg, M. Christensen, S. Gigli, S. Failla, and S. Concetti Live weight, body size and carcass characteristics of young bulls of fifteen European breeds. Livest. Sci. 114: Albrecht, E., F. Teuscher, K. Ender, and J. Wegner Growthand breed-related changes of marbling characteristics in cattle. J. Anim. Sci. 84: Alderton, J. M., and R. A. Steinhardt Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J. Biol. Chem. 275: Anthony, N. B A review of genetic practices in poultry: Efforts to improve meat quality J. Muscle Foods. 9: Asmundson, V. S., and L. M. Julian Inherited muscle abnormality in the domestic fowl. J. Hered. 47: Bailey, R. A., K. A. Watson, S. F. Bilgili, and S. Avendano The genetic basis of pectoralis major myopathies in modern broiler chicken lines. Poult. Sci. 94: Barany, M., E. Gaetjens, and K. Barany Myosin in hereditary muscular dystrophy of chicken. Ann. N. Y. Acad. Sci. 138: Bauermeister, L. J., A. Morey, C. M. Owens, E. T. Moran, and S. R. McKee Occurrence of WS in two different fast growing strains of broilers. Poult. Sci. SPSS Meeting Abstr. 51. Bauermeister, L. J., A. U. Morey, E. T. Moran, M. Singh, C. M. Owens, and S. R. McKee Occurrence of WS in chicken breast fillets in relation to broiler size. Poult. Sci. 88:104. (Abstr.). Bilgili, S. F., and J. B. Hess Green Muscle Disease in broilers increasing. World Poult. 18: Bilgili, S. F., K. J. Meloche, A. Campasino, and W. A. Dozier The influence of carnitine and guanidinoacetic acid supplementation of low and high amino acid density diets on Pectoralis major myopathies in broiler chickens. Poult. Sci. 93:M56. (Abstr.). Cavaliere, M. J., E. E. Calore, M. Haraguchi, S. L. Górniak, M. L. Z. Dagli, P. C. Raspantini, N. M. P. Calore, and R. Weg Mitochondrial myopathy in Senna occidentalis-seed-fed chicken. Ecotoxicol. Environ. Saf. 37: Chalmers, G. A Monensin toxicity in broiler chickens. Can. Vet. J. 22: Chio, L. F., D. W. Peterson, and F. H. Kratzer Lipid composition and synthesis in the muscles of normal and dystrophic chickens. Can. J. Biochem. 50: Crouse, J. D., L. V. Cundiff, R. M. Koch, M. Koohmaraie, and S. C. Seideman Comparisons of Bos indicus and Bos taurus inheritance for carcass beef characteristics and meat palatability. J. Anim. Sci. 67: Dam, H., I. Phange, and E. Sondergaard Muscular degeneration (white striation of muscles) in chicks reared on vitamin E deficient, low fat diets. Acta. Pathol. Microbiol. Scand. 31: Dalle Zotte, A, G Tasoniero, E Russo, C Longoni, and M Cecchinato Impact of coccidiosis control program and feeding plan on white striping prevalence and severity degree on broiler breast fillets evaluated at three growing ages. Poult. Sci. 94: Davis, D. E., and H. Stewart Changing consumer demands create opportunities for US food system. Food Rev. 25: de Brot, S., S. Perez, H. L. Shivaprasad, K. Baiker, L. Polledo, M. Clark, and L. Grau-Roma Wooden breast lesions in broiler chickens in the UK. Vet Rec. 11. pii: vetrec doi: /vr Dowling, L Ionophore toxicity in chickens: a review of pathology and diagnosis. Avian Pathol. 21: Ferreira, T. Z., R. A. Casagrande, S. L. Vieira, D. Driemeier, and L. Kindlein An investigation of a reported case of white striping in broilers. J. Appl. Poult. Res. 23: Garcia, R. G., L. W. Freitas, A. W. Schwingel, R. M. Farias, F. R. Caldara, A. M. A. Gabriel, J. D. Graciano, C. M. Komiyama, and I. C. L. Almeida Paz Incidence and physical properties of PSE chicken meat in a commercial processing plant. Revista Brasileira de Ciência Avícola. 12: Gee, K Poultry s tough new problem: Woody Breast. Wall Street Journal. Sect. Business and Tech, Mar 29. CCLXVII: B1. Graziano, M. J., W. Flory, C. L. Seger, and C. D. Hebert Effects of a Cassia occidentalis extract in the domestic chicken (Gallus domesticus). Am. J. Vet. Res. 44: Guetchom, B., D. Venne, S. Chénier, and Y. Chorfi Effect of extra dietary vitamin E on preventing nutritional myopathy in broiler chickens. J. Appl. Poult. Res. 21: Haley, M. M Changing consumer demand for meat: The US example, Pages in Changing Structure of Global Food Consumption and Trade. A. Regmi, ed. US Department of Agriculture, Economic Research Service, Agriculture and Trade Report, ERS WRS No May 2001, Washington, DC. Harper, G. S., and D. W. Pethick How might marbling begin? Aust. J. Exp. Agric. 44: Henry, M. H., G. M. Pesti, and T. P. Brown Pathology and histopathology of gossypol toxicity in broiler chicks. Avian Dis. 45: Herrera, E., and C. Barbas Vitamin E: action, metabolism and perspectives. J. Physiol. Biochem. 57: Hete, B., and K. K. Shung Using RF ultrasound to monitor the progression of muscular dystrophy through passive stretching.. Ultrasonics Symposium, Proceedings. Institute of Electrical and Electronics Engineers. 2: Hocquette, J. F., F. Gondret, E. Baéza, F. Médale, C. Jurie, and D. W. Pethick Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, identification of putative markers. Animal. 4: Holliday, T. A., L. M. Julian, and V. S. Asmundson Muscle growth in selected lines of muscular dystrophic chickens. Ana. Rec. 160: Hoving-Bolink, A. H., R. W. Kranen, R. E. Klont, C. L. M. Gerritsen, and K. H. de Greef Fibre area and capillary supply in broiler breast muscle in relation to productivity and ascites. Meat Sci. 56: Jackson, M. J., D. A. Jones, and R. H. T. Edwards Experimental skeletal muscle damage: the nature of the calcium activated degenerative processes. Eur. J. Clin. Invest. 14: Jordan, J. P., F. H. Kratzer, A. M. Johnson, and R. L. Freeman Fat deposition in musculature of the genetically dystrophic chicken. Exp. Biol. Med. 101: Jordan, J. P., F. H. Kratzer, and N. S. Zarghami Lipid composition of the Pectoral muscles of chickens with inherited muscular dystrophy. Proc. Soc. Exp. Biol. Med. 116: Judge, M. D., E. D. Aberle, J. C. Forrest, H. B. Hedrick, and R. A. Merkel Principles of meat science. 2nd ed. Kendall/Hunt, Dubuque, Iowa. Julian, L. M Animal model: Hereditary muscular dystrophy of chickens. Am. J. Pathol. 70: Julian, L., and V. Asmundson Muscular dystrophy of the chicken. Muscular Dystrophy in Man and Animals Julian, R. J Production and growth related disorders and other metabolic diseases of poultry-a review. Vet. J. 169: Kijowaski, J., and M. Konstanczak Deep pectoral myopathy in broiler chickens. Bull. Vet. Inst. Pulawy. 53: Klasing, K. C Nutritional diseases. Pages in Diseases of Poultry. 12th ed. Y. M. Saif, A. M. Fadley, J. R. Glisson, L. R. McDougald, L. K. Nolan, and D. E. Swayne, eds. Blackwell Publishing Professional, Ames, IA. Kuttappan, V. A., G. R. Huff, W. E. Huff, B. M. Hargis, J. K. Apple, C. Coon, and C. M. Owens. 2013a. Comparison of hematologic and serologic profiles of broiler birds with normal (NORM) and severe (SEV) degrees of WS in breast fillets. Poult. Sci. 92:

9 2732 KUTTAPPAN ET AL. Kuttappan, V. A., H. L. Shivaprasad, D. P. Shaw, B. A. Valentine, B.M.Hargis,F.D.Clark,S.R.McKee,andC.M.Owens.2013b. Pathological changes associated with WS in broiler breast muscles. Poult. Sci. 92: Kuttappan, V. A., J. Caldas, F. L. Yang, V. Tijare, B. H. Hargis, C. N. Coon, J. Escobar, M. Vazquez-Anon, and C. M. Owens White striping and woody breast: Effect on raw broiler breast fillet quality. Poult. Sci. 94:521P. (Abstr.). Kuttappan, V. A., S. D. Goodgame, C. D. Bradley, A. Mauromoustakos, B. M. Hargis, P. W. Waldroup, and C. M. Owens. 2012a. Effect of different levels of dietary vitamin E (DL-α-tocopherol acetate) on the occurrence of different degrees of WS on broiler breast fillets. Poult. Sci. 91: Kuttappan, V. A., V. B. Brewer, A. Mauromoustakos, S. R. Mc- Kee, J. L. Emmert, J. F. Meullenet, and C. M. Owens. 2013c. Estimation of factors associated with the occurrence of WS in broiler breast fillets. Poult. Sci. 92: Kuttappan, V. A., V. B. Brewer, F. D. Clark, S. R. McKee, J. F. Meullenet, J. L. Emmert, and C. M. Owens Effect of white striping on the histological and meat quality characteristics of broiler fillets. Poult. Sci. 88: (Abstr.) Kuttappan, V. A., V. B. Brewer, P. W. Waldroup, and C. M. Owens. 2012b. Influence of growth rate on the occurrence of WS in broiler breast fillets. Poult. Sci. 91: Kuttappan, V. A., Y. S. Lee, G. F. Erf, J.-F. C. Meullenet, S. R. McKee, and C. M. Owens. 2012c. Consumer acceptance of visual appearance of broiler breast meat with varying degrees of WS. Poult. Sci. 91: Lee, Y. S., C. M. Owens, and J. F. Meullenet A novel laser air puff and shape profile method for predicting tenderness of broiler breast meat. Poult. Sci. 87: Lien, R. J., S. F. Bilgili, J. B. Hess, and K. S. Joiner Induction of deep pectoral myopathy in broiler chickens via encouraged wing flapping. J. Appl. Poult. Res. 21: Lorenzi, M., S. Mudalal, C. Cavani, and M. Petracci Incidence of white striping under commercial conditions in medium and heavy broiler chickens in Italy. J. Appl. Poult. Res. 23: Machlin, L. J., and W. T. Shalkop Muscular degeneration in chickens fed diets low in vitamin E and sulfur. J. Nutr. 60: Macrae, V. E., M. Mahon, S. Gilpin, D. A. Sandercock, and M. A. Mitchell Skeletal muscle fibre growth and growth associated myopathy in the domestic chicken (Gallus domesticus). Br. Poult. Sci. 47: Mahon, M Muscle abnormalities: morphological aspects. Pages in Poultry Meat Science - Poultry Science Symposium Series Volume Twenty-Five. R. I. Richardson, and G. C. Mead, eds. CABI Publishing, Wallingford, UK. Mazzoni, M., M. Petracci, A. Meluzzi, C. Cavani, P. Clavenzani, and F. Sirri Relationship between pectoralis major muscle histology and quality traits of chicken meat. Poult. Sci. 94: McMurtry, S. L., L. M. Julian, and V. S. Asmundson Hereditary muscular dystrophy of the chicken. Quantitative histopathological findings of the Pectoralis at 6 weeks of age. Arch. Pathol. 94: Mitchell, M. A Muscle abnormalities: pathophysiological mechanisms. Pages in Poultry Meat Science - Poultry Science Symposium Series Volume Twenty-Five. R. I. Richardson, and G. C. Mead, eds. CABI Publishing, Wallingford, UK. Moody, W. G., and R. G. Cassens A quantitative and morphological study of bovine longissimus fat cells. J. Food Sci. 33: Mudalal, S., E. Babini, C. Cavani, and M. Petracci Quantity and functionality of protein fractions in chicken breast fillets affected by WS. Poult. Sci. 93:1 9. Mudalal, S., M. Lorenzi, F. Soglia, C. Cavani, and M. Petracci Implications of white striping and wooden breast abnormalities on quality traits of raw and marinated chicken meat. Animal. 9: Mutryn, M. F., E. M. Brannick, W. Fu, W. R. Lee, and B. Abasht Characterization of novel chicken muscle disorder through differential gene expression and pathway analysis using RNAsequencing. BMC Genomics. 16:399. doi: /s National Chicken Council. 2016a. Statistics and research: Per capita consumption of poultry and livestock, 1965 to Estimated 2016, in Pounds. about-the-industry/statistics/per-capita-consumption-of-poultry -and-livestock-1965-to-estimated-2012-in-pounds/, Accessed March, 19, National Chicken Council. 2016b. Statistics and research: Broiler Chicken Industry Key Facts chickencouncil.org/about-the-industry/statistics/broiler-chicken -industry-key-facts/, Accessed April 4, National Chicken Council Statistics and research: U.S. Broiler Performance. Accessed March 19, National Research Council Nutrient requirements of poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC. Nishimura, T., A. Hattori, and K. Takahashi Structural changes in intramuscular connective tissue during the fattening of Japanese Black cattle: effect of marbling on beef tenderization. J. Anim. Sci. 77: Peterson, D. W., and A. L. Lilyblade Relative differences in tenderness of breast muscle in normal and two dystrophic mutant strains of chickens. J. Food Sci. 34: Petracci, M., F. Sirri, M. Mazzoni, and A. Meluzzi. 2013a. Comparison of breast muscle traits and meat quality characteristics in 2 commercial chicken hybrids. Poult. Sci. 92: Petracci, M., S. Mudalal, A. Bonfiglio, and C. Cavani. 2013b. Occurrence of WS under commercial conditions and its impact on breast meat quality in broiler chickens. Poult. Sci. 92: Petracci, M., S. Mudalal, E. Babini, and C. Cavani Effect of WS on chemical composition and nutritional value of chicken breast meat. Italian J. Anim. Sci. 13: Petracci, M., S. Mudalal, F. Soglia, and C. Cavani Meat quality in fast-growing broiler chickens. World s Poult. Science. Journal. 71: Pietrzak, M., M. L. Greaser, and A. A. Sosnicki Effect of rapid rigor mortis processes on protein functionally in pectoralis major muscle of domestic turkeys. J. Anim. Sci. 75: Roder, J. D Ionophore toxicity and tolerance. Vet. Clin.North Am. Food Anim. Pract. 27: Russo, E., M. Drigo, C. Longoni, R. Pezzotti, P. Fasoli, and C. Recordati Evaluation of white striping prevalence and predisposing factors in broilers at slaughter. Poult Sci. 94: Sams, A. R., and C. Z. Alvarado Introduction to poultry meat processing. Pages 1 3 in Poultry Meat Processing. 2nd ed. C. M. Owens, C. Z. Alvarado, and A. R. Sams, eds. CRC Press, Boca Raton, FL. Sandercock, D. A., and M. A. Mitchell Differential sensitivity to monensin-induced myopathy in fast and slow growing lines of broiler chicken? Br. Poult. Sci. 40:S55 S56. Sandercock, D. A., and M. A. Mitchell Myopathy in broiler chickens: a role for Ca (2+)-activated phospholipase A2? Poult. Sci. 82: Sandercock, D. A., and M. A. Mitchell The role of sodium ions in the pathogenesis of skeletal muscle damage in broiler chickens. Poult. Sci. 83: Sandercock, D. A., Z. E. Barker, M. A. Mitchell, and P. M. Hocking Changes in muscle cell cation regulation and meat quality traits are associated with genetic selection for high body weight and meat yield in broiler chickens. Genet. Sel. Evol. 41:1 8. Scholtyssek, S., L. M. Bele, R. N. Sayre, A. A. Klose, and D. W. Peterson Tenderness of dystrophic chicken meat. Poult. Sci. 46: Scott, M. L., and I. D. Desai The relative anti-muscular dystrophy activity of the d- and l- epimers of α-tocopherol and of other tocopherols in the chick. J. Nutr. 83: Sihvo, H. K., K. Immonen, and E. Puolanne Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol. 51: Siller, W. G Deep pectoral myopathy: A penalty of successful selection for muscle growth. Poult. Sci. 64: Silva, T. C., S. L. Gorniak, S. C. S. Oloris, P. C. Raspantini, M. Haraguchi, and M. L. Z. Dagli Effects of Senna occidentalis on chick bursa of Fabricius. Avian Pathol. 32: