20,924
Views
67
CrossRef citations to date
0
Altmetric
Review Article

Genetic selection of broilers and welfare consequences: a review

&

SUMMARY

The genetic selection of broilers over the past 60 years has focused narrowly and intensely on production traits, namely growth rate and feed efficiency. This has led to significant welfare problems in birds grown for meat, including leg disorders, cardiovascular diseases, and resulting high mortality rates, while the breeder birds are subjected to severe feed restriction. Bone problems such as bacterial chondronecrosis and tibia dyschondroplasia are prevalent, and recent studies have reported the prevalence of birds with moderate to severe gait impairment to be between 5.5 and 48.8%. Worldwide, over 66 billion broilers are slaughtered annually. This huge scale of meat chicken production means that welfare problems are widespread and are likely to increase in severity due to the increasing global human population, increasing demand for meat, and a continued focus on efficiency of production in the agricultural sector. The commercial broiler industry therefore represents some of the most serious animal welfare issues in agriculture. There is an urgent need to address these problems by making welfare traits high priorities in breeding programmes and integrating these with other breeding goals. Many studies recommend the use of slower-growing breeds that do not have the same welfare problems. Addressing these welfare issues is essential to improve bird welfare and for social acceptability and sustainability of the broiler industry worldwide.

Introduction

Genetic selection programmes over the past 60 years have led to rapid growth rates and increased meat yield in broilers (meat chickens), dramatically decreasing slaughter age and the amount of feed and energy required to raise these birds to market weight (Bradshaw, Kirkden, and Broom Citation2002; Tallentire, Leinonen, and Kyriazakis Citation2016). Growth rates have increased by over 400% between 1957 and 2005 (Zuidhof et al. Citation2014), with 85–90% of this increase being attributed to genetic selection and the remainder attributed to diet (Havenstein, Ferket, and Qureshi Citation2003).

Selection programmes with a narrow focus and selection for a small number of traits risk negative consequences for traits that are not selected, and there have been widespread concerns about the welfare of broilers for decades (Julian Citation1998). Problems which are directly linked to their fast growth rate include: cardiovascular diseases causing mortality by sudden death syndrome and ascites; leg disorders and bone deformations causing leg weakness, lameness, low locomotor activity and extended periods spent sitting or lying, which can produce skin lesions due to contact with moist litter (Bradshaw, Kirkden, and Broom Citation2002; Bessei Citation2006; Knowles et al. Citation2008). These issues cause significant economic losses in the broiler industry due to culling, late mortality, poor performance and carcass condemnation (Bradshaw, Kirkden, and Broom Citation2002; Hashimoto et al. Citation2013). In addition to the birds reared for meat, the breeder birds experience welfare issues due to their fast-genotypic growth rate (De Jong and Guemene Citation2011; Dawkins and Layton Citation2012). Broiler breeders are predisposed to high mortality, walking problems, and high levels of aggression, which are addressed by severe feed restriction.

Intensification of production in the poultry sector has been more dramatic than in other livestock species (Bessei Citation2018). Worldwide, over 66 billion broilers are slaughtered annually (FAO Citation2017), with the United States, China, the European Union and Brazil being the biggest producers (Mottet and Temptio Citation2017). With a growing human population, there will be a corresponding increase in the demand for meat, and greater pressure on agricultural industries to be more efficient. With the continued focus on growth rate, feed efficiency and meat yield, the genetic predisposition for compromised welfare in broilers can be expected to increase in severity (Decuypere et al. Citation2010; Dawkins and Layton Citation2012). Until recently, the discussion of poultry welfare was mostly limited to Europe. However, it is now recognised as a global issue, in part due to the international trade of poultry products (Bessei Citation2018). Due to the scale of production and the intensity and predicted increase in welfare problems, the commercial broiler industry represents some of the most serious animal welfare issues in the global agricultural sector (Morris Citation2009; Dawkins and Layton Citation2012).

While there have been some improvements in management such as health management, environmental control and the emergence of several welfare accreditation schemes in a number of countries around the world, severe welfare issues still exist in broilers which cannot be mitigated solely by a focus on environmental factors.

There have been a number of papers investigating various aspects of broiler genetics, but few recent reviews. Since existing reviews on the topic were published several years ago, this review discusses recent findings on the main welfare problems of broilers in relation to their genetic predisposition.

Cardiovascular disease

Two decades ago, Julian (Citation1998) noted that in the previous 40 years, genetic selection for rapid growth and feed efficiency resulted in a two-fold increase in the growth rate of broilers; the subsequent high muscle to bone ratio and high caloric intake caused significant mortality rates due to cardiovascular disease, primarily through sudden death syndrome and ascites. Twenty years later, Zhang, Schmidt, and Lamont (Citation2018) stated that sudden death and ascites syndromes are still major diseases in broilers. In fact, faster growth rate has resulted in a significant increase in associated mortality, which has increased in tandem with growth rate (Kalmar, Vanrompay, and Janssens Citation2013).

It can be difficult to accurately estimate the prevalence of certain conditions due to variation between farms and confidential breeder data, and there is little published information on ascites. However, some data have been reported from studies which investigated certain conditions under experimental settings. The European Food Safety Authority (Citation2010) reported that ascites and sudden death syndrome were linked to growth rate and while the prevalence of ascites was thought to have decreased in the preceding 10 years due to selective breeding, it should be given a high weighting in selection indices.

Cardiovascular diseases are still a problem in commercial meat chicken production, and cardiac arrhythmia is especially prevalent, with an incidence of 27% in fast-growing broilers and only 1% in slow-growing broilers. Cardiac insufficiency can deteriorate into ascites and sudden death syndrome. Therefore, genetic improvement is needed to optimise cardiac function while maintaining efficient growth in broilers (Zhang, Schmidt, and Lamont Citation2018).

While sudden death syndrome and ascites are multifactorial problems and there is variation between broilers in their susceptibility, growth rate represents the main cause (Bessei Citation2006). Breeding for meat yield has resulted in a high metabolic demand for oxygen to support the fast growth rate, disproportionately small heart and lungs, diminished cardiac capacity, and a subsequent decreased ability to sufficiently oxygenate the blood, results in insufficient oxygen supply to the tissues. Ascites is primarily caused by blood oxygen deficiency, which resulting in pulmonary hypertension, heart failure, and the accumulation of large amounts of fluid in the abdominal cavity (Bessei Citation2006; Kalmar, Vanrompay, and Janssens Citation2013). Ascites is a severe welfare problem as the syndrome develops gradually and the symptoms, including breathing difficulties, are progressive and distressing to the birds (Kalmar, Vanrompay, and Janssens Citation2013).

Ascites also has a significant economic impact on the industry. Mortality due to ascites usually occurs later in life, which means that resources, such as feed, have been spent on affected birds during their lives. Therefore, even at low rates, the economic cost of ascites is considerable. However, estimates of mortality due to ascites are disturbingly high. Mortality estimates have ranged from 0 to 30% in US flocks in 2002, and more recently, mortality rates of up to 12.4% have been reported in modern strains (Arce-Menocal et al. Citation2009; Kalmar, Vanrompay, and Janssens Citation2013). Kalmar, Vanrompay, and Janssens (Citation2013) reported figures from the Canadian Food Inspection Agency which showed that 8% of condemnations at the abattoir in 2011 were due to ascites, representing over half a million birds, which does not include on-farm or transport mortalities.

Zhang, Schmidt, and Lamont (Citation2018) compared the genetic basis of cardiac development and occurrence of heart dysfunction between a modern fast-growing (Ross 708) and a heritage slower-growing broiler (Illinois broiler, unselected since 1956), and gave evidence for the genetic basis for the cardiac dysfunction in fast-growing broilers, and how cardiac health may be improved through setting targets in breeding programmes. Indeed, moderate to high heritability estimates have been found for ascites, and genetic selection for broilers which are resistant to ascites is considered the ideal permanent solution (Kalmar, Vanrompay, and Janssens Citation2013).

Musculoskeletal disorders

The main welfare issues related to musculoskeletal disorders include reduced walking ability (Sanotra et al. Citation2001; Knowles et al. Citation2008), associated pain (Danbury et al. Citation2000), increased risk of injury, reduced access to feed and water and an inability to perform natural behaviours (Weeks et al. Citation2000b; Bradshaw, Kirkden, and Broom Citation2002).

Bacterial chondronecrosis with osteomyelitis (BCO) is a condition triggered by a bacterial infection of the bone that often results in necrosis and bone fracture (Wijesurendra et al. Citation2017). It has been reported to be the most common cause of severe leg disorders in modern broilers (Bradshaw, Kirkden, and Broom Citation2002). A recent Australian study involving 20 commercial broiler farms found BCO lesions in 28% of necropsied birds (culls and mortalities) (Wijesurendra et al. Citation2017).

Although the pathogenesis is still not completely understood, Wideman et al. (Citation2014) demonstrated a significant genetic predisposition in the susceptibility of broilers to BCO. Another study by the same authors found standard broiler crosses that grew rapidly at an early age developed higher incidences of BCO compared to crosses that grew more slowly (Wideman et al. Citation2013). A more recent study by Petry et al. (Citation2018) identified 10 differentially expressed genes between normal and BCO-affected broilers and concluded that these genes are strong candidates for the development of BCO.

Similar to BCO, research has shown there is a genetic basis for the incidence of bone and leg deformities in broilers. Kestin, Su, and Sorensen (Citation1999) reported significant differences in the incidence of bone deformities including tibial dyschondroplasia (TD) and tibial curvature among four broiler crosses. Shim et al. (Citation2012) showed slower-growing birds have lower scores for TD compared to faster growing birds within the same population and suggested that growth rate was negatively associated with bone abnormality. The authors suggested that breeding strategies should aim to slow down growth for proper skeletal development before fleshing.

Heritability estimates of bone deformities including TD, valgus and varus deformities have been reported as low to moderate, and studies have reported a low negative or close to zero genetic correlation between leg health traits and body weight (Akbaş et al. Citation2009; Rekaya et al. Citation2013). However, Kapell et al. (Citation2012) demonstrated that simultaneous breeding for improved leg health and production can be achieved through a balanced breeding programme, and Rekaya et al. (Citation2013) suggested that selection for improved leg health could have minimal effects on body weight and carcase traits. Genetic selection appears to be the most effective means by which to prevent non-infectious skeletal disorders such as TD, and, has been shown to decrease the incidence of such disorders (Bradshaw, Kirkden, and Broom Citation2002; Akbaş et al. Citation2009).

Walking ability

Genetic predisposition is a major contributor to the prevalence of leg weakness, compromised walking ability and lameness (Kestin et al. Citation1992; Bizeray et al. Citation2000; Knowles et al. Citation2008; Caplen et al. Citation2012). Impaired locomotor activity, in turn, compromises the development of the skeletal system (Bizeray et al. Citation2000; Bessei Citation2006). Wilhelmsson (Citation2019) demonstrated that a fast-growing commercial Ross strain had a significantly poorer ability to walk and higher percentage of culls due to leg weakness compared to the slower-growing Rowan Range, and Bizeray et al. (Citation2000) found significant differences in locomotory behaviour and time budgets between young commercial broilers and young birds from the slower-growing Label Rouge strain.

Kestin et al. (Citation1992) developed a six-point scoring system which is commonly utilised to assess walking ability in broilers, where ‘0’ describes a bird having a normal gait, and ‘5’ a bird incapable of walking. Studies have found an average of 75–90% of broilers with a gait score greater than zero (Kestin et al. Citation1992; Sanotra et al. Citation2001), indicating an impaired ability to walk (Sanotra et al. Citation2001). Gait scores of 3 or above may indicate that welfare is compromised. The mean prevalence of broilers displaying a gait score of 3 or above has previously been reported to be between 15 and 55% (Kestin et al. Citation1992; Sanotra et al. Citation2001; Knowles et al. Citation2008). More recently, studies conducted across multiple flocks, farms and countries have reported the prevalence of birds with a moderate to severe gait impairment (gait score 3 or above) to be between 5.5 and 48.8% (Bassler et al. Citation2013; Tahamtani, Hinrichsen and Riber Citation2018; Kittelsen et al. Citation2017; Granquist et al. Citation2019).

Tahamtani, Hinrichsen and Riber, (Citation2018) showed a trend towards the reduction of lameness in Denmark, coinciding with an increase in growth rate. They suggested this may be due to improved breeding selection in parent lines or a reflection of improved production practices focused on broiler welfare in the European Union (e.g. reduced stocking density).

The prevalence of lameness and leg abnormalities may vary between individual flocks and regions (Knowles et al. Citation2008; Sanotra et al. Citation2001; Tahamtani, Hinrichsen and Riber Citation2018), and the above estimates are likely to be conservative when factoring in mortalities and culls of severely lame birds (Kestin et al. Citation1992), and age at assessment may be variable. Kestin et al. (Citation1992) found that birds of a genotype randomly bred for 11 generations, which were not subjected to selection for growth rate and feed efficiency, had significantly better gait scores compared to three commercial breeds. Similarly, a later study by the same authors found that slower-growing breeds had better gait scores than commercial broiler breeds. When the effect of live weight differences between the breeds was removed, most of the differences in gait score disappeared. This suggested that the higher gait scores observed in the commercial breeds were due to the heavier live weight (Kestin et al. Citation2001). A study by Rutten et al. (Citation2002) demonstrated that broilers were capable of enhanced locomotor activity when 50% of their body weight was alleviated using a suspended harness mechanism. The authors suggested that the increased activity was due to reduced pain in the bones and joints as a result of the reduction in weight.

Commercial broilers have unbalanced body conformation as a result of intense genetic selection for additional breast muscle and body mass (Caplen et al. Citation2012). In a kinematic analysis, Caplen et al. (Citation2012) showed that lame birds walked slower and took shorter, quicker strides than non-lame broilers, which the authors suggest may be an attempt to minimise discomfort and stress on the bones. Tallentire, Leinonen, and Kyriazakis (Citation2016) attributed body conformation of the modern broiler to genetic selection for improved feed efficiency, reduced fatness and other desirable production characteristics.

Although factors such as disease, nutrition and environmental influences play a role in the development of leg weakness, past reviews have concluded that 1) the fast growth rate and development of modern broilers should be considered the main influencer; 2) genetic selection is the most effective means of preventing non-infectious skeletal disorders, and 3) breeding programs which incorporate multi-trait selection goals to improve health and welfare should be prioritised in future (Bradshaw, Kirkden, and Broom Citation2002; Bessei Citation2006; Dawkins and Layton Citation2012).

Contact dermatitis

Contact dermatitis is an inflammation or ulcerative condition of the skin. In broilers, it is most common on the feet (foot pad dermatitis; FPD), the hock (hock burn; HB) and breast (breast burn). Depending on the severity, these lesions can cause pain, increase the susceptibility to secondary infection, and exacerbate leg and joint problems (Bessei Citation2006). The prevalence can be high, with variable estimates. A UK study by Haslam et al. (Citation2007) recorded contact dermatitis lesions at the abattoir on birds from 149 farms and reported that the mean percentage of birds in each flock with moderate to severe foot pad lesions ranged from 0 to 71.5%, with a mean of 11.1%.

More recently, using data from 138 farms, De Jong et al. (Citation2012) reported an average of 54.5% of birds with mild or severe lesions observed at slaughter, and large-scale farm surveys have reported the prevalence of birds with moderate to severe lesions to be between 9.7 and 37.3% (Bassler et al. Citation2013; Tahamtani, Hinrichsen and Riber Citation2018). Genotype and poor locomotion as a result of fast growth have been linked to the prevalence of contact dermatitis in broilers (Kjaer et al. Citation2006; Haslam et al. Citation2007; Allain et al. Citation2009; Ask Citation2010).

Heritability estimates of FPD have been reported as low to moderate, and low, or not significantly different from zero, for HB (Kjaer et al. Citation2006; Akbaş et al. Citation2009; Ask Citation2010; Kapell et al. Citation2012). Ask (Citation2010) reported varying genetic correlations of both traits with body weight between the two strains studied.

An early study by Kestin, Su, and Sorensen (Citation1999) reported differences in the prevalence of foot pad and hock burns between four broiler crosses and found that some crosses are more susceptible to these conditions. Recent work has shown significant differences in the incidence of foot pad lesions between commonly-used genotypes including the Ross 308, Cobb 500 and Hubbard Classic (Škrbić et al. Citation2015; Martins et al. Citation2016). These results confirmed the potential for genetic predisposition, in combination with good management practices, to reduce the prevalence of foot pad lesions (Škrbić et al. Citation2015).

Kjaer et al. (Citation2006) found no FPD lesions and few low-grade HB lesions in one slower-growing strain, while the incidence of FPD and HB lesions for a fast-growing strain at six weeks of age was 44 and 88%, respectively. Allain et al. (Citation2009) reported deeper footpad lesions in a fast-growing compared to a slower-growing genotype. Fast-growing birds spend more time sitting, less time walking and perching, and perform less locomotor activity compared to slower-growing birds (Bokkers and Koene Citation2003; Wilhelmsson et al. Citation2019), which, in turn, has been linked to the increased incidence of contact dermatitis (Bessei Citation2006).

Continued selection for increased body weight and feed efficiency, while ignoring FPD, in breeding goals is likely to lead to an increased prevalence of FPD. It is important that genetic selection is performed to improve both FPD and HB (Ask Citation2010). Since estimates of genetic correlations between FPD and HB have been reported as non-significant (Kjaer et al. Citation2006), this indicates that improvement in both traits can be achievable with simultaneous genetic selection against both traits. Further, studies have suggested that it is possible to decrease the incidence of FPD and HB via genetic selection without negatively impacting body weight (Kjaer et al. Citation2006; Ask Citation2010).

Breeders

There is a strong negative relationship between body weight and reproductive efficiency in poultry. This has led to the development of two different types of chickens – layer hens to produce eggs, and broilers to produce meat (Decuypere et al. Citation2010). The intense genetic selection for increased growth rate and meat yield in broilers has focused on birds bred for consumption (De Jong and Guemene Citation2011). However, there is a whole other subset of the broiler population – breeder birds. Broiler breeders experience poor welfare as an unintended consequence of selection for fast growth (Dawkins and Layton Citation2012).

Broilers grow quickly, with high meat yields and high feed consumption. This causes the birds to become rapidly obese, which compromises reproductive function and sexual activity in the breeder birds, which are grown to a much older ages compared to their progeny. Breeders have higher rates of mortality and suffer from walking problems and increased aggression. In an attempt to curb these problems, a serious welfare issue has resulted whereby the birds are subjected to chronic, severe feed restriction (De Jong and Guemene Citation2011; Dawkins and Layton Citation2012) where feed intake is limited to approximately one-third of their ad libitum intake (De Jong et al. Citation2002). This causes poor welfare due to chronic hunger, chronic stress, frustration, boredom, aggressive and abnormal behaviours and injurious feather pecking (De Jong and Guemene Citation2011; Nicol et al. Citation2017).

Breeder birds face what is termed the ‘broiler breeder paradox’, which has come about as a direct result of genetic selection – if the birds consume feed ad libitum, they experience compromised welfare including walking problems, reduced reproductive function, and mortality. However, if their feed intake is heavily restricted, this causes other welfare problems, including chronic hunger and stress (Decuypere et al. Citation2010). This paradox has worsened due to the continued focus on increasing genetic efficiency and meat production from broilers (Dawkins and Layton Citation2012).

De Jong and Guemene (Citation2011) pointed out the impossibility of meeting both production requirements and good welfare in broiler breeders, and the inability to reconcile good performance and health of breeder birds while their offspring achieve satisfactory growth and feed efficiency. They noted that, while health criteria have been included in selection programmes and there are some alternative breeds available, welfare issues including feed restriction are still present (De Jong and Guemene Citation2011).

In 1999, Pollock predicted that the rate of improvement in growth rate is unlikely to continue, and that, if current trends continue, by 2075 a 2 kg broiler would be possible at day one, and that selection may be required to alleviate reproduction problems in the breeder population (Pollock Citation1999). Since severe feed restriction is practiced in broiler breeder populations today, genetic improvement for reproductive characteristics and growth rate is still required.

Dilution of feed, or ‘qualitative feed restriction’ for example by adding fibre, is a controversial practice (Dawkins and Layton Citation2012), and there have been conflicting findings with regards to its efficacy and humaneness. While qualitative feed restriction has been proposed as a temporary approach to reduce hunger and improve health and production outcomes, metabolic ‘hunger’ remains, and so this is not a solution to the problem (Nicol et al. Citation2017). Feeding strategies have been studied and are being developed, but more sustainable breeding goals need to be set which eliminate the need for severe feed restriction in broiler breeders (Decuypere et al. Citation2010).

Genotypes with slower growth rates offer longer-term solutions as alternatives to feed restriction and are increasing in popularity in Europe (De Jong and Guemene Citation2011). The selection of birds requiring less feed restriction as breeders should be a priority, even if this involves a compromise in growth rate (Nicol et al. Citation2017). However, Dawkins and Layton (Citation2012) explained that commercially, animal welfare is most likely to be improved if breeding programmes incorporate multiple goals which encapsulate economic productivity as well as high animal welfare traits. They asserted that progress in this area has been hampered by the assumption that fast growth rate is incompatible with good welfare. Further, studies have presented evidence that there are different genes, which control growth at different stages of the birds’ lives, which gives the potential for selection for different traits and growth rates at different ages (Ankra-Badu et al. Citation2010; Gao et al. Citation2010; Dawkins and Layton Citation2012).

Future breeding

Breeding programmes have traditionally focused on economic indices, which has caused several significant welfare problems. While welfare traits may have been included in breeding programmes which, according to the relevant companies, has improved leg health and reduced the incidence of ascites in recent years (Aviagen Group Citation2016), leg weakness, lameness and cardiovascular conditions still occur at high rates in commercial flocks. Selection goals need to counteract these negative effects and focus on production efficiency and health and welfare characteristics (Decuypere et al. Citation2010). To do this, it is important to identify means to reduce conflict between high welfare and profitability and select broilers with commercially competitive growth rates which have no requirement for feed restriction in the breeder population (Dawkins and Layton Citation2012).

Combining health and welfare traits into breeding programmes is not always easy because they are usually difficult to measure, heritability is often low, and economic values uncertain (Hocking Citation2014). However, experimentally low values of heritability or unfavourable correlations should not prevent attempts to advance broiler-breeding programmes, and individuals should be studied rather than just correlations at the population level (Dawkins and Layton Citation2012). Further, there are new technologies available for trait measurement, whole genome selection and targeted genetic modification, with considerable potential to enhance welfare traits (Hocking Citation2014).

Many studies have recommended that slower-growing strains should be used which do not have the welfare problems of the current commercial strains including leg weakness and metabolic diseases (Wilhelmsson et al. Citation2019). Slower-growing breeds have lower mortality, less incidence of leg weakness and cardiovascular diseases, and generally improved welfare (Bessei Citation2006).

Consumers

The ethical and social acceptability of animal breeding practices need to be considered (Decuypere et al. Citation2010). Consumers in many countries around the world are becoming increasingly aware of farm animal welfare, and more discerning about the quality of life that the animals experience (Animal Welfare Institute Citation2019). Broiler welfare, including the genetic predisposition for poor welfare traits, is gaining awareness worldwide, with several food companies committing to using higher welfare breeds (Compassion in World Farming Citation2019). A Dutch study found that the majority of consumers (87.5% of respondents) are willing to pay more for products from higher welfare broilers (Mulder and Zomer Citation2017), and in China, where the modern concept of animal welfare is still in the early stages of development, one study reported that, while more than one third of survey respondents had never previously heard of ‘animal welfare’, more than half of respondents were willing to pay more for higher welfare pig and poultry products, which may be related to an assumption of improved meat quality with increasing animal welfare (You et al. Citation2014).

Aside from government regulation, retailers and animal welfare organisations have become a driving force for improvements in farm animal welfare (Bessei Citation2018), and breeding companies argue that improvements in welfare traits are driven by market requirement (Hiemstra and Napel Citation2013), thereby assigning responsibility to consumers to drive change.

Social Licence to Operate is generally thought of as the acceptance of a company or industry’s practices by the general public (Futureye Citation2018; Hampton and Teh-White Citation2019). This concept is applicable to animal industries, where animal housing and husbandry practices are subject to public scrutiny. Current breeding practices may be considered a violation of ethical responsibility (Decuypere et al. Citation2010).

Community expectations dictate that practices must be ethically justifiable, and consideration is needed to minimise suffering and to allow animals opportunities to experience positive emotions and have a life worth living (Vaarst, Steenfeldt, and Horsted Citation2015). The results of a recent Brazilian study showed people had mostly negative perceptions of animal welfare in the poultry supply chain, and those with some background or knowledge about the industry were more likely to have this negative perception (De Queiroz et al. Citation2018). Reflecting on the ethical significance and broader acceptability of breeding goals may assist in assessing the limits of acceptability (Decuypere et al. Citation2010). Transparency in the supply chain is required in order for consumers to make informed decisions. However, the poultry industries have been described as complex and non-transparent (Vaarst, Steenfeldt, and Horsted Citation2015).

Sustainability

Breeding goals must be regularly reviewed in light of ethical acceptability, as well as economic and welfare outcomes, in order to establish and maintain a sustainable industry (Decuypere et al. Citation2010). Recently, Vaarst, Steenfeldt, and Horsted (Citation2015) used four core principles of sustainability – environmental, institutional, social and economic – to assess the sustainability of the global poultry sector. They concluded that poultry production may only be deemed ‘sustainable’ if the challenges across all four areas can be managed; economic development must not undermine initiatives to support social development (Vaarst, Steenfeldt, and Horsted Citation2015). From an animal welfare perspective, the ‘social’ (promotion of a life worth living; Social Licence to Operate) and ‘institutional’ (transparency; industry-led initiative and coordination) sustainability aspects of broiler production are in need of most attention. Additionally, although higher welfare production systems can be less efficient, mainly in terms of feed input, opportunities for improvement in this area exist and should be explored (Vaarst, Steenfeldt, and Horsted Citation2015). Future investment and research in this area is needed, as well as meaningful progress towards long-term sustainability, encompassing all four principles. Substituting commercial fast-growing breeds for slower-growing strains, in combination with improved husbandry practices, should be a priority for any industry or regulatory body that is seriously committed to improving animal welfare (Morris Citation2009).

Conclusions

Breeding goals in the broiler industry over the past 60 years have generally narrowly focused on production traits, leading to several welfare problems. Due to the projected increase in the global human population, there will be greater pressure on agricultural industries to be more efficient, thereby putting poultry welfare under more strain. This is not a sustainable trajectory and is ethically questionable.

Two of the most serious welfare problems in the broiler industry – feed restriction in breeders and health issues in broilers grown for meat – are directly linked to genetic selection. With pressure on the broiler industry to increase efficiency and production, these problems will only increase in severity unless there is an urgent focus on not only including welfare traits in broiler breeding goals but prioritising them.

Slower-growing genetic strains of broilers have been found to have improved cardiac health, lower mortality and less incidence of musculoskeletal disorders, bone deformities, and contact dermatitis. Many studies recommended the use of slower-growing strains, which do not exhibit the same welfare problems as current fast-growing commercial breeds. Further, there are new genetic technologies available which aid in genetic modification, with considerable potential to improve welfare traits.

While the broiler industry is competitive and goals have been economically driven, food industries, including the broiler industry are subject to public scrutiny and approval. Addressing welfare problems is a key consideration in ensuring the broiler industry’s sustainability and ongoing Social Licence to Operate. For a sustainable livestock sector, animal welfare must be at the forefront of discussions. Increases in productivity must take into account the effects on the welfare of the animals, and to be truly sustainable, the societal implications of farming must be considered.

Disclosure statement

No potential conflict of interest was reported by the authors. The cost of publishing in open access was funded by RSPCA Australia.

Additional information

Notes on contributors

K.M. Hartcher

K.M. Hartcher was employed by RSPCA Australia in the role of Scientific Officer (Farm Animals) at the time of writing this review.

H.K. Lum

H.K. Lum is employed by RSPCA Australia in the role of Scientific Officer (Special Projects).

References

  • Akbaş, Y., S. Yalçin, S. Özkan, F. Kirkpinar, Ç. Dem Takma, Y. Gevrekçi, H. C. Güler, and L. Türkmut. 2009. “Heritability Estimates of Tibial Dyschondroplasia, Valgus-varus, Foot-pad Dermatitis and Hock Burn in Broiler.” Arch.Geflügelk 73: 1–6.
  • Allain, V., L. Mirabito, C. Arnould, M. Colas, S. Le Bouquin, C. Lupo, and V. Michel. 2009. “Skin Lesions in Broiler Chickens Measured at the Slaughterhouse: Relationships between Lesions and between Their Prevalence and Rearing Factors.” British Poultry Science 50: 407–417. doi:10.1080/00071660903110901.
  • Animal Welfare Institute. 2019. “Consumer Perceptions of Farm Animal Welfare.” Accessed 27 March 2019. https://awionline.org.
  • Ankra-Badu, G. A., E. LE Bihan-Duval, S. Mignon-Grasteau, F. Pitel, C. Beaumont, M. J. Duclos, J. Simon, et al. 2010. “Mapping QTL for Growth and Shank Traits in Chickens Divergently Selected for High or Low Body Weight.” Animal Genetics 41: 400–405. doi:10.1111/j.1365-2052.2009.02017.x.
  • Arce-Menocal, J., E. Avila-Gonzalez, C. Lopez-Coello, L. Garibay-Torres, and L. A. Martinez-Lemus. 2009. “Body Weight, Feed-particle Size, and Ascites Incidence Revisited.” Journal of Applied Poultry Research 18: 465–471. doi:10.3382/japr.2008-00095.
  • Ask, B. 2010. “Genetic Variation of Contact Dermatitis in Broilers.” Poultry Science 89: 866–875. doi:10.3382/ps.2009-00496.
  • Aviagen Group. 2016. “Decades of Welfare and Sustainability Selection at Aviagen Chickens and Turkeys.” accessed 18 July 2019. http://en.aviagen.com/about-us/sustainability/.
  • Bassler, A. W., C. Arnould, A. Butterworth, L. Colin, I. C. Jong, V. De Ferrante, P. Ferrari, S. Haslam, F. Wemelsfelder, and H. J. Blokhuis. 2013. “Potential Risk Factors Associated with Contact Dermatitis, Lameness, Negative Emotional State, and Fear of Humans in Broiler Chicken Flocks.” Poultry Science 92: 2811–2826. doi:10.3382/ps.2013-03208.
  • Bessei, W. 2006. “Welfare of Broilers: A Review.” World’s Poultry Science Journal 62: 455–466. doi:10.1079/WPS2005108.
  • Bessei, W. 2018. “Impact of Animal Welfare on Worldwide Poultry Production.” World’s Poultry Science Journal 74: 211–224. doi:10.1017/S0043933918000028.
  • Bizeray, D., C. Leterrier, P. Constantin, M. Picard, and J. M. Faure. 2000. “Early Locomotor Behaviour in Genetic Stocks of Chickens with Different Growth Rates.” Applied Animal Behaviour Science 68: 231–242.
  • Bokkers, E. A. M., and P. Koene. 2003. “Behaviour of Fast- and Slow Growing Broilers to 12 Weeks of Age and the Physical Consequences.” Applied Animal Behaviour Science 81: 59–72. doi:10.1016/S0168-1591(02)00251-4.
  • Bradshaw, R. H., R. D. Kirkden, and D. M. Broom. 2002. “A Review of the Aetiology and Pathology of Leg Weakness in Broilers in Relation to Welfare.” Avian and Poultry Biology Reviews 13: 45–103. doi:10.3184/147020602783698421.
  • Caplen, G., B. Hothersall, J. C. Murrell, C. J. Nicol, A. E. Waterman-Pearson, C. A. Weeks, and G. R. Colborne. 2012. “Kinematic Analysis Quantifies Gait Abnormalities Associated with Lameness in Broiler Chickens and Identifies Evolutionary Gait Differences.” PloS One 7: e40800. doi:10.1371/journal.pone.0040800.
  • Compassion in World Farming. 2019. “Join The Better Chicken Initiative.” Accessed 27 March 2019. www.ciwf.com.
  • Danbury, T. C., C. A. Weeks, J. P. Chambers, A. E. Waterman-Pearson, and S. C. Kestin. 2000. “Self-selection of the Analgesic Drug Carprofen by Lame Broiler Chickens.” Veterinary Record 146: 307–311. doi:10.1136/vr.146.11.307.
  • Dawkins, M. S., and R. Layton. 2012. “Breeding for Better Welfare: Genetic Goals for Broiler Chickens and Their Parents.” Animal Welfare 21: 147–155. doi:10.7120/09627286.21.2.147.
  • De Jong, I. C., and E. Guemene. 2011. “Major Welfare Issues in Broiler Breeders.” World’s Poultry Science Journal 67: 73–82. doi:10.1017/S0043933911000067.
  • De Jong, I. C., J. Van Harn, H. Gunnink, V. A. Hindle, and A. Lourens. 2012. “Footpad Dermatitis in Dutch Broiler Flocks: Prevalence and Factors of Influence.” Poultry Science 91: 1569–1574. doi:10.3382/ps.2012-02156.
  • De Jong, I. C., S. Van Voorst, D. A. Ehlhardt, and H. J. Blokhuis. 2002. “Effects of Restricted Feeding on Physiological Stress Parameters in Growing Broiler Breeders.” British Poultry Science 43 (2): 157–168. doi:10.1080/00071660120121355.
  • De Queiroz, R. G., C. H. De Faria Domingues, M. E. A. Canozzi, R. G. Garcia, C. F. Ruviaro, J. O. J. Barcellos, and J. A. R. Borges. 2018. “How Do Brazilian Citizens Perceive Animal Welfare Conditions in Poultry, Beef, and Dairy Supply Chains?” PloS One 13: 1–10. doi:10.1371/journal.pone.0202062.
  • Decuypere, E., V. Bruggeman, N. Everaert, Y. LI, R. Boonen, J. De Tavernier, S. Janssens, and N. Buys. 2010. “The Broiler Breeder Paradox: Ethical, Genetic and Physiological Perspectives, and Suggestions for Solutions.” British Poultry Science 51: 569–579. doi:10.1080/00071668.2010.519121.
  • European Food Safety Authority. 2010. “Scientific Opinion on the influence of genetic parameters on the welfare and the resistance to stress of commercial broilers.” EFSA Journal 8 (7:1666): 1–82. doi:10.2903/j.efsa.2010.1666.
  • Food and Agriculture Organization of the United Nations (FAO). 2017. Accessed 8 May 2019. http://www.fao.org.
  • Futureye. 2018. “Public Relations and Enterprise Risk Management. Australia’s Shifting Mindset on Farm Animal Welfare.” accessed 27 March 2019. http://www.agriculture.gov.au.
  • Gao, Y., Z. Q. Du, C. G. Feng, X. M. Deng, N. Li, Y. Da, and X. X. Hu. 2010. “Identification of Quantitative Trait Loci for Shank Length and Growth at Different Development Stages in Chicken.” Animal Genetics 41: 101–104. doi:10.1111/j.1365-2052.2009.01962.x.
  • Granquist, E. G., G. Vasdal, I. C. De Jong, and R. O. Moe. 2019. “Lameness and Its Relationship with Health and Production Measures in Broiler Chickens.” Animal 21: 1–8.
  • Hampton, J. O., and K. Teh-White. 2019. “Animal Welfare, Social License, and Wildlife Use Industries.” The Journal of Wildlife Management 83 (1): 12–21. doi:10.1002/jwmg.v83.1.
  • Hashimoto, S., K. Yamazaki, T. Obi, and K. Takase. 2013. “Relationship between Severity of Footpad Dermatitis and Carcass Performance in Broiler Chickens.” Avian Pathology 75 (11): 1547–1549.
  • Haslam, S. M., T. G. Knowles, S. N. Brown, L. J. Wilkins, S. C. Kestin, P. D. Warriss, and C. J. Nicol. 2007. “Factors Affecting the Prevalence of Foot Pad Dermatitis, Hock Burn and Breast Burn in Broiler Chicken.” British Poultry Science 48 (3): 264–275. doi:10.1080/00071660701371341.
  • Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003. “Growth, Livability, and Feed Conversion of 1957 versus 2001 Broilers When Fed Representative 1957 and 2001 Broiler Diets.” Poultry Science 85: 1500–1508. doi:10.1093/ps/82.10.1500.
  • Hiemstra, S. J., and J. T. Napel. 2013. “Study of the Impact of Genetic Selection on the Welfare of Chickens Bred and Kept for Meat Production.” IBF International Consulting. Accessed 8 August 2019. https://ec.europa.eu/food/sites/food/files/animals/docs/aw_practice_farm_broilers_653020_final-report_en.pdf
  • Hocking, P. M. 2014. “Unexpected Consequences of Genetic Selection in Broilers and Turkeys: Problems and Solutions.” British Poultry Science 55: 1–12. doi:10.1080/00071668.2014.877692.
  • Julian, R. J. 1998. “Rapid Growth Problems: Ascites and Skeletal Deformities in Broilers.” Poultry Science 77: 1773–1780. doi:10.1093/ps/77.12.1773.
  • Kalmar, I. D., D. Vanrompay, and G. P. J. Janssens. 2013. “Broiler Ascites Syndrome: Collateral Damage from Efficient Feed to Meat Conversion.” Veterinary Journal 197: 169–174. doi:10.1016/j.tvjl.2013.03.011.
  • Kapell, D. N., W. G. Hill, A. M. Neeteson, J. Mcadam, A. N. Koerhuis, and S. Avendano. 2012. “Genetic Parameters of Foot-pad Dermatitis and Body Weight in Purebred Broiler Lines in 2 Contrasting Environments.” Poultry Science 91: 565–574. doi:10.3382/ps.2011-01934.
  • Kestin, S. C., G. Su, and P. Sorensen. 1999. “Different Commercial Broiler Crosses Have Different Susceptibilities to Leg Weakness.” Poultry Science 78: 1085–1090. doi:10.1093/ps/78.8.1085.
  • Kestin, S. C., S. Gordon, G. Su, and P. Sorensen. 2001. “Relationships in Broiler Chickens between Lameness, Liveweight, Growth Rate and Age.” Veterinary Record 148: 195–197. doi:10.1136/vr.148.7.195.
  • Kestin, S. C., T. G. Knowles, A. E. Tinch, and N. G. Gregory. 1992. “Prevalence of Leg Weakness in Broiler Chickens and Its Relationship with Genotype.” Veterinary Record 131: 190–194. doi:10.1136/vr.131.9.190.
  • Kittelsen, K. E., B. David, R. O. Moe, H. D. Poulsen, J. F. Young, and E. G. Granquist. 2017. “Associations among Gait Score, Production Data, Abattoir Registrations, and Postmortem Tibia Measurements in Broiler Chickens.” Poultry Science 96: 1033–1040. doi:10.3382/ps/pew433.
  • Kjaer, J. B., G. Su, B. L. Nielsen, and P. Sorensen. 2006. “Foot Pad Dermatitis and Hock Burn in Broiler Chickens and Degree of Inheritance.” Poultry Science 85: 1342–1348. doi:10.1093/ps/85.8.1342.
  • Knowles, T. G., S. C. Kestin, S. M. Haslam, S. N. Brown, L. E. Green, A. Butterworth, S. J. Pope, D. Pfeiffer, and C. J. Nicol. 2008. “Leg Disorders in Broiler Chickens: Prevalance, Risk Factors and Prevention.” PLoSone 3 (2): e1545. doi:10.1371/journal.pone.0001545.
  • Martins, B., M. Martins, A. Mendes, B. Fernandes, and E. Aguiar. 2016. “Footpad Dermatitis in Broilers: Differences between Strains and Gender.” Revista Brasileira De Ciência Avícola 18: 461–466. doi:10.1590/1806-9061-2015-0105.
  • Morris, M. C. 2009. “The Ethics and Politics of Animal Welfare in New Zealand: Broiler Chicken Production as a Case Study.” Journal of Agricultural and Environmental Ethics 22: 15–30. doi:10.1007/s10806-008-9128-3.
  • Mottet, A., and G. Temptio. 2017. “Global Poultry Production: Current State and Future Outlook and Challenges.” World’s Poultry Science Journal 73: 245–256. doi:10.1017/S0043933917000071.
  • Mulder, M., and S. Zomer. 2017. “Dutch Consumers’ Willingness to Pay for Broiler Welfare.” Journal of Applied Animal Welfare Science 20 (2): 137–154. doi:10.1080/10888705.2017.1281134.
  • Nicol, C. J., J. Bouwsema, G. Caplen, A. C. Davies, J. Hockenhull, S. L. Lambton, J. A. Lines, S. Mullan, and C. A. Weeks. 2017. “Farmed Bird Welfare Science Review.” Accessed 8 March 2019. www.agriculture.vic.gov.au.
  • Petry, B., I. R. Savoldi, A. M. G. Ibelli, E. Paludo, J. De Oliveira Peixoto, F. R. F. Jaenisch, D. De Córdova Cucco, and M. C. Ledur. 2018. “New Genes Involved in the Bacterial Chondronecrosis with Osteomyelitis in Commercial Broilers.” Livestock Science 208: 33–39. doi:10.1016/j.livsci.2017.12.003.
  • Pollock, D. L. 1999. “A Geneticist’s Perspective from within A Broiler Primary Breeder Company.” Poultry Science 78: 414–418. doi:10.1093/ps/78.3.414.
  • Rekaya, R., R. L. Sapp, T. Wing, and S. E. Aggrey. 2013. “Genetic Evaluation for Growth, Body Composition, Feed Efficiency, and Leg Soundness.” Poultry Science 92: 923–929. doi:10.3382/ps.2012-02649.
  • Rutten, M., C. Leterrier, P. Constantin, K. Reiter, and W. Bessei. 2002. “Bone Development and Activity in Chickens in Response to Reduced Weight-load on Legs.” Animal Research 51: 327–336. doi:10.1051/animres:2002027.
  • Sanotra, G. S., J. D. Lund, A. K. Ersboll, J. S. Petersen, and K. S. Vestergaard. 2001. “Monitoring Leg Problems in Broilers: A Survey of Commercial Broiler Production in Denmark.” Worlds Poultry Science Journal 57: 344–354. doi:10.1079/WPS20010006.
  • Shim, M. Y., A. B. Karnuah, N. B. Anthony, G. M. Pesti, and S. E. Aggrey. 2012. “The Effects of Broiler Chicken Growth Rate on Valgus, Varus, and Tibial Dyschondroplasia.” Poultry Science 91: 62–65. doi:10.3382/ps.2011-01599.
  • Škrbić, Z., Z. Pavlovski, M. Lukić, and V. Petričević. 2015. “Incidence of Footpad Dermatitis and Hock Burns in Broilers as Affected by Genotype, Lighting Program and Litter Type.” Annals of Animal Science 15: 433–445.
  • Tahamtani, F. M., L. K. Hinrichsen, and A. B. Riber. 2018. “Welfare assessment of conventional and organic broilers in Denmark, with emphasis on leg health.” Veterinary Record 183 (6): 192. doi:10.1136/vr.104817.
  • Tallentire, C. W., I. Leinonen, and I. Kyriazakis. 2016. “Breeding for Efficiency in the Broiler Chicken: A Review.” Agronomy for Sustainable Development 36: 66.
  • Vaarst, M., S. Steenfeldt, and K. Horsted. 2015. “Sustainable Development Perspectives of Poultry Production.” World’s Poultry Science Journal 71: 609–620.
  • Weeks C. A., Danbury T. D. Davies, H. C. Hunt, P., and S. C. Kestin. 2000b. “The Behaviour of Broiler Chickens and Its Modification by Lameness.” Applied Animal Behaviour Science 67: 111–125.
  • Wideman, R. F., A. Al-Rubaye, A. Gilley, D. Reynolds, H. Lester, D. Yoho, J. M. Hughes, and I. Pevzner. 2013. “Susceptibility of 4 Commercial Broiler Crosses to Lameness Attributable to Bacterial Chondronecrosis with Osteomyelitis.” Poultry Science 92: 2311–2325.
  • Wideman JR., R. F., Al-Rubaye, A., Reynolds, D., Yoho, D., Lester, H., Spencer, C., Hughes JR., J. D. and Pevzner, I. Y. 2014. “Bacterial Chondronecrosis with Osteomyelitis in Broilers: Influence of Sires and Straight-run versus Sex-separate Rearing.” Poultry Science 93: 1675–1687.
  • Wijesurendra, D. S., A. N. Chamings, R. N. Bushell, D. O. Rourke, M. Stevenson, M. S. Marenda, H. Amir, and A. Stent. 2017. “Pathological and Microbiological Investigations into Cases of Bacterial Chondronecrosis and Osteomyelitis in Broiler Poultry.” Avian Pathology 46 (6): 683–694.
  • Wilhelmsson, S., J. Yngvesson, L. Jönsson, S. Gunnarsson, and A. Wallenbeck. 2019. “Welfare Quality® Assessment of a Fast-growing and a Slower-growing Broiler Hybrid, Reared until 10 Weeks and Fed a Low-protein, High-protein or Mussel-meal Diet.” Livestock Science 219: 71–79.
  • You, X., Y. Li, M. Zhang, H. Yan, and R. Zhao. 2014. “A Survey of Chinese Citizens’ Perceptions on Farm Animal Welfare.” PloS One 9: 1–10.
  • Zhang, J., C. J. Schmidt, and S. J. Lamont. 2018. “Distinct Genes and Pathways Associated with Transcriptome Differences in Early Cardiac Development between Fast- and Slow-growing Broilers.” PloS One 13 (12): e0207715.
  • Zuidhof, M. J., B. L. Schneider, V. L. Carney, D. R. Korver, and F. E. Robinson. 2014. “Growth, Efficiency, and Yield of Commercial Broilers from 1957, 1978, and 2005.” Poultry Science 93: 2970–2982.