Spotlight on avian pathology: current growth-related breast meat abnormalities in broilers

ABSTRACT

Selection for fast-growing and high-breast-yield hybrids has enormously increased the pressure on muscle development rate and mass, indirectly promoting the development of muscular abnormalities affecting the pectoral muscles such as White Striping, Wooden Breast and Spaghetti Meat. Macroscopically, the muscles affected by these defects exhibit distinctive traits, whereas the microscopic examinations evidenced similar histological alterations. Therefore, a common causative mechanism (involving genes related to several metabolic pathways and functional categories) underpinning the occurrence of these abnormalities may be hypothesized and directly associated with muscle hypertrophy induced by selection. Within this context, as the occurrence of growth-related abnormalities may negatively affect consumer attitude and certainly leads to considerable economic losses, resulting from meat downgrading, it clearly emphasizes the need to consider those issues related to muscle growth and meat quality when selecting meat-type genotypes.

KEYWORDS:

• Broiler
• muscle abnormalities
• White Striping
• Wooden Breast
• Spaghetti Meat

Evolution of poultry market and emergence of the problem

Nowadays, most of the chicken meat production in the world is merely based on intensive farming of a few types of fast-growing hybrids reaching the slaughter weight in a very short time (i.e. 4–5 wks for producing rotisserie-type carcasses) and exhibiting high feed-efficiency (Petracci et al., 2015; Tallentire et al., 2018). Selection programmes of broiler chickens have also been adapted through the last decades according to the evolution of the market demand for chicken meat. In detail, because of the market shift from the whole carcass to ready-to-cook and ready-to-eat products, the selection criteria have been addressed to increase cut-up (i.e. breast, leg) and meat yields. In this context, the poultry industry has also been pushed to produce heavier birds for further processing (Petracci et al., 2017; Kuttappan et al., 2016). However, during the past 30 years, this market evolution has led to an increased pressure on muscle development rate and mass and indirectly favoured the progressive incidence of muscles exhibiting abnormal pale colour (Pale Soft and Exudative-like condition) and myopathies (i.e. Deep pectoral myopathy) (Petracci et al., 2015). More recently, growth-related abnormalities, such as White Striping (WS), Wooden Breast (WB) and Spaghetti Meat (SM), have been observed to affect (alone or in combination) the Pectoralis major muscle of fast-growing chickens (Kuttappan et al., 2009; Sihvo et al., 2014; Baldi et al., 2018). WS has been observed for several years in heavy male turkeys and limited implications on meat quality were recently found (Soglia et al., 2018). Muscles affected by growth-related abnormalities macroscopically exhibit distinctive traits such as the presence of white striations parallel to the direction of muscle fibres (WS), the out-bulging and pale areas of hardened consistency (WB) and the tendency towards separation of fibre bundles composing the muscle tissue (SM) that primarily affect the superficial portion of the cranial part of the P. major muscle. On the other hand, microscopic observations have evidenced both similar and distinctive histological features among these conditions (Kuttappan et al., 2013; Sihvo et al., 2014; Velleman, 2015; Papah et al., 2017; Baldi et al., 2018) (Table 1). Intriguingly, the histological features attributed to WS, WB and SM abnormalities have been observed even on some grossly normal muscles that, exhibiting focally diffused mild myodegeneration, might be presenting an early phase of these conditions (Kuttappan et al., 2013; Mazzoni et al., 2015; Sihvo et al., 2018).

Table 1. Main common and distinctive traits of growth-related breast meat abnormalities in broilers.

Growth-related breast meat abnormalities
	White striping (WS)	Wooden breast (WB)	Spaghetti meat (SM)
Main macroscopical traits (gross lesion)	White striations parallel to the muscle fibre direction	Out-bulging and pale areas of hardened consistency as well as superficial petechiae and exudate	Tendency towards separation of the fibre bundles composing the muscle tissue itself
Common histological features	Loss of normal muscle architecture. Abnormal fibres exhibiting rounded profile, nuclear internalization, degeneration, necrosis up to lysis and concurrent regenerative processes (small-calibre regenerative fibres intermingled to abnormal ones having large calibre). Compromised perimysial and endomysial connective tissue, fat and inflammatory cell infiltration
Assigned score (overall impact/alteration level)	Moderate	Severe	Severe
Distinctive microscopic features	Abnormal deposition of adipose tissue at perymysial level (lipidosis)	Proliferation and thickening of the perimysial network (fibrosis)	Progressive rarefaction of the endomysial and perimysial connective tissue

Possible causative mechanisms

The existence of a common causative mechanism resulting in myodegenerative processes and leading to the occurrence of these muscle abnormalities may be hypothesized. In this regard, by using a quanQTL mapping approach, it has been recently demonstrated that there is not a major causative gene responsible for the occurrence of the WS condition, but rather a polygenic inheritance exists (Pampouille et al., 2018). Similarly, previous studies evidenced differentially expressed genes related to several functional categories (i.e. muscle development, polysaccharide and glucose metabolism metabolic processes, proteoglycan synthesis, inflammation and calcium signalling pathway) (Abasht et al., 2016; Zambonelli et al., 2016). In this context, the profound alteration in gene expression might be considered as a direct consequence of muscle hypertrophy induced by selection (Zambonelli et al., 2016). Indeed, as hypertrophic pectoral muscles exhibit a reduced capillary density, such inadequate blood vessel development results in an impaired oxygen supply and metabolic waste product displacement from breast myofibres (Sihvo et al., 2018). This condition, likely exacerbated by phlebitis, is currently considered as the major causative mechanism underlying the occurrence of these muscular abnormalities (Papah et al., 2017; Boerboom et al., 2018). In addition, an overall reduction in satellite cell number, and the concurrent loss of their ability to proliferate and differentiate, were observed within the pectoral muscle of the hypertrophic fast-growing and high-breast-yield hybrids (Daughtry et al., 2017).

Impact and costs associated with the problem

Nowadays, the occurrence of growth-related abnormalities affecting the pectoral muscles, the most valuable part of the broiler carcass, results in considerably increased meat downgrading because of the altered visual appearance, sensory and technological properties (especially when used for high-quality processed products) (Petracci et al., 2015; Kuttappan et al., 2016; Baldi et al., 2018). Indeed, the major contribution to economic loss is the increased labour cost for the identification and grading especially of WB and SM abnormalities which have unacceptable properties for fresh consumption. Overall, the incidence rates of these abnormalities are alarming and seem no longer sustainable for the poultry industry. It was recently roughly estimated that the incidence of these conditions can entail an excess of $200 million lost per year (conservative estimate) in the US due to yield reduction (e.g. trimming, drip loss, cook loss) and/or loss of value in case of meat downgrading or discarding (Kuttappan et al., 2016).

Current approaches for mitigation

As these abnormalities affect only fast-growing hybrids, direct and indirect mechanisms underlying their occurrence can be found in broiler pectoral muscle hypertrophy and growth rate. Several studies have been conducted to identify the possible causative processes involved in the occurrence of WS and WB. In detail, the incidence is higher in flocks belonging to high-breast-yield hybrids and augments at increasing growth rate and weight at slaughter (Lorenzi et al., 2014; Griffin et al., 2018; Kuttappan et al., 2017). On the other hand, males seem more prone to develop WB abnormality (Trocino et al., 2015), while females exhibit a higher prevalence of SM condition (personal communication). Otherwise, since an overall reduction in the occurrence of muscle abnormalities has been observed only as an indirect consequence of a reduced growth rate and/or slaughter weight (Lorenzi et al., 2014; Kuttappan et al., 2017), dietary and prophylactic treatments seem not to be directly associated with the incidence of these abnormalities (Petracci et al., 2016). Therefore, there is a low margin to find effective management and dietary solutions able to mitigate the occurrence of these muscular defects without negatively affecting the live bird performance. Otherwise, the most effective post mortem solution is to incorporate downgraded meat into processed products.

Current risks and outstanding questions

The emergence of growth-related meat abnormalities not only increases downgrading percentages but may also negatively affect consumer attitude because of perceived bird welfare concerns and decreased eating quality. In addition, it has been recently estimated that the possibilities to further improve feed-efficiency and growth performances through selection are minimal and strictly subordinated to the biology of the birds (Tallentire et al., 2018). Thus, it seems that the poultry industry can no longer postpone considering the issues related to muscle growth and to the quality of the resulting meat when selecting meat-type genotypes.

Disclosure statement

No potential conflict of interest was reported by the authors.

ORCID

Francesca Soglia http://orcid.org/0000-0003-3920-3879

Maurizio Mazzoni http://orcid.org/0000-0002-7384-5990

Massimiliano Petracci http://orcid.org/0000-0002-5671-5676