Introduction
Broiler chickens are selected for rapid growth and efficient feed conversion. This accelerated growth is related to a number of health and welfare problems, mainly muscle and skeletal abnormalities. Clinically, these are manifested with locomotory problems (lameness and recumbency due to the inability to walk) which sometimes incur considerable losses from condemnation of birds on farm or the slaughterhouse. These clinical manifestations may be associated with both the leg and axial skeleton (Dinev, Reference DINEV2013). This paper reviews the various published reports related to axial skeleton pathology in broiler chickens, such as spondylolisthesis, spondylosis, spondylitis and scoliosis.
Spondylolisthesis
This is a developmental anomaly of the spinal column of broiler chickens, whereby vertebra T4 is deformed with downward rotation of the anterior end. Compression of the spinal cord at the junction of T4 and T5 causes posterior paralysis. Spondylolisthesis (commonly known as ‘kinky back’) was first reported in broiler chickens in the United Kingdom, but most probably was observed beforehand (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967). The condition was subsequently described in Australia by Kelly (Reference KELLY1971), in Canada by Riddell and Howell (Reference RIDDELL and HOWELL1972) and in Germany by Bergmann (Reference BERGMANN1972). Spondylolisthesis is considered a global problem for farmed broilers.
A genetic predisposition to the condition has been suggested (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967; Riddell and Howell, Reference RIDDELL and HOWELL1972; Wise, Reference WISE1973). This assumption, as well as the observation that recovery from posterior paralysis was satisfactory in some affected birds, were used for breeding purposes to create a broiler chicken hybrid with high prevalence of spondylolisthesis that was used in various studies (Riddell, Reference RIDDELL1973). It has been hypothesised that the incidence of clinical spondylolisthesis could depend on the genotype (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967; Riddell and Howell, Reference RIDDELL and HOWELL1972; Wise Reference WISE1973). The appearance of the condition in chickens from different genetic backgrounds and reared under significantly differing conditions including feeding regimes, does not categorically confirm that genotype may be more important than the environment for emergence of spondylolisthesis in commercial flocks (Riddell, Reference RIDDELL1973).
Wise (Reference WISE1973) demonstrated that the development of subclinical spondylolisthesis could be slowed down by feeding a high-fibre diet during the first week of life. The diet markedly reduced growth rate in experimental birds and therefore its practical application in commercial farms was not advised. Riddell (Reference RIDDELL1973) tried to explain the lack of clinical signs of spondylolisthesis after hatching of the first generation by a reduction in growth rate. A number of studies have investigated the importance of nutrition in the appearance of the condition, and subsequent losses in commercial poultry originating from regions where rations are mainly based on wheat (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967; Wise, Reference WISE1970; Kelly, Reference KELLY1971; Bergmann, Reference BERGMANN1972; Riddell and Howell, Reference RIDDELL and HOWELL1972). In summary, it can be assumed that a reduced growth rate inhibits the problem. The condition is characteristic for broilers and can reach 2% of the flock (Crespo and Shivaprasad, Reference CRESPO and SHIVAPRASAD2008). Wise (Reference WISE1973) provided evidence that subclinical spondylolisthesis was a developmental abnormality encountered during the first weeks of life, peaking at three to six weeks of age, whereas others reported a peak in clinical spondylolisthesis at two to four weeks old (Riddell, Reference RIDDELL1973). Riddell (Reference RIDDELL1973) further described clinical symptoms in birds with spondylolisthesis and spinal cord compression reared until sexual maturity. In a recent study, the incidence of spondylolisthesis was investigated at a commercial poultry farm rearing three commercial broiler chicken hybrids: Ross 308, Cobb 500 and Pureline (Dinev, Reference DINEV2012). Analysis of the identified spondylolisthesis cases demonstrated dislocation of T4 in all three studied breeds of birds. The condition corresponds to findings reported by some authors using the same nomenclature (McLelland, Reference MCLELLAND1990; Julian, Reference JULIAN2005; Crespo and Shivaprasad, Reference CRESPO and SHIVAPRASAD2008) but differs from reports where T6 was the affected vertebra according to a different nomenclature (Riddell and Howell, Reference RIDDELL and HOWELL1972; Baumel and Witmer, Reference BAUMEL and WITMER1993; Salomon and Krautwald-Junghans, Reference SALOMON and KRAUTWALD-JUNGHANS2008; Makrai et al., Reference MAKRAI, NEMES, SIMON, IVANICS, DUDAS and GLAVITS2011).
According to our data (Dinev, Reference DINEV2012) regarding the incidence of spondylolisthesis in modern broiler hybrids and in strains used in the period when the problem was discovered, no relationship to genotype could be found, as others have hypothesised (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967; Riddell and Howell, Reference RIDDELL and HOWELL1972; Wise, Reference WISE1973). It was also not possible to estimate differences in the prevalence of the condition, despite the extensive selection work performed with regard to the fast growth of broiler chicken hybrids (Dinev, Reference DINEV2012).
No substantial differences were observed between the prevalence of spondylolisthesis among the studied broilers strains. Statistically, the highest incidence of lower limb paralysis was observed in Cobb 500 broilers (0.24%), followed by Ross 308 with (0.14%) and Pureline (0.12%). In addition, there was no correlation between the frequency of observed problems and the age of the respective broiler breeder flocks.
In general, the observed prevalence of spondylolisthesis corresponded to the lower range of other researchers reports, whereby an incidence of 1% was considered high, although a frequency of up to 2% was reported (Wise, Reference WISE1975; Crespo and Shivaprasad, Reference CRESPO and SHIVAPRASAD2008). It should be however remembered that the cited studies were based on clinical manifestations of spondylolisthesis. It may be speculated that the observed lower prevalence of clinical spondylolisthesis in contemporary broiler strains is due to the shorter finisher period and hence, the impossibility for clinical manifestation of subclinical cases, in which the abnormality was proved to be present as early as the first couple of weeks of age (Wise, Reference WISE1973).
A specific finding in the studies of Dinev (Reference DINEV2012) in broiler chickens with clinical spondylolisthesis is the lack of deaths due to dehydration, as reported by others. Probably, this was due to moving the birds in isolation facilities, where the access to food and water was readily available and where they could not be crushed by healthy chicks (Crespo and Shivaprasad, Reference CRESPO and SHIVAPRASAD2008).
According to Dinev (Reference DINEV2012) the peak of clinical spondylolisthesis occurred in broiler chickens at three to four weeks of age, in agreement with other published data (Wise, Reference WISE1970; Riddell, Reference RIDDELL1973). Therefore, despite the enormous selection work throughout the years, mainly directed to shorten the fattening period, no differences in the age-related onset of spondylolisthesis can be established. In previous studies, nutritional and environmental factors were not always taken into account, as all broilers were housed under equal conditions (Kelly, Reference KELLY1971; Bergmann, Reference BERGMANN1972; Riddell and Howell, Reference RIDDELL and HOWELL1972; Wise, Reference WISE1973).
A further, large-scale survey among broiler chickens with clinical signs of posterior paralysis attempted to determine the prevalence of axial skeletal pathological conditions (Dinev, Reference DINEV2013). In 36 broiler flocks, clinical signs of posterior paralysis were observed in 1480 (0.21%) chickens from 23 flocks. They were shown to be mainly due to cases of spondylolisthesis in nearly half of affected birds (42.3%), followed by spondylosis (35.8%) and spondylitis (12.6%). Scoliosis was demonstrated in 9.3% of birds.
The occurrence of spondylolisthesis may be explained by the anatomical structure of the chicken vertebral column. It is acknowledged that most thoracic and lumbosacral vertebrae fuse to form two immobile units; the notarium and synsacrum (Baumel and Witmer, Reference BAUMEL and WITMER1993; Salomon and Krautwald-Junghans, Reference SALOMON and KRAUTWALD-JUNGHANS2008), a process which is normally completed at the beginning of the sexual maturity (Riggins et al., Reference RIGGINS, ABBOT, ASHMORE, RUCKER and MCCARREY1977). That is why there is the assumption that the remaining freely mobile Т4 and the adjacent vertebrae are most prone to development of abnormalities during the period of skeletal immaturity (Osbaldiston and Wise, Reference OSBALDISTON and WISE1967; McCaskey et al., Reference MCCASKEY, ROWLAND, PAGE and MINEAR1982; Riddell et al., Reference RIDDELL, KING and GUNASEKERA1983; Kelly, Reference KELLY1971; Riddell and Howell, Reference RIDDELL and HOWELL1972).
The clinical occurrence of spondylolisthesis and the reported incidence of subclinical signs confirm the reported predisposition of broiler chickens to this problem (Howlett and Wood, Reference HOWLETT and WOOD1984). In their survey, Dinev (Reference DINEV2013) established a moderate extent of vertebral dislocation (spondylolisthesis), causing vertebral canal stenosis and always (in 100% of cases) affecting the T4 articulation inconsistent with a similar study investigating the subclinical disease in adult male broiler breeders (60-61 weeks of age) where the condition was present in only 11% of birds (Duff, Reference DUFF1988). This may support the findings of researchers who have proposed a considerable predisposition to spondylolisthesis at the age of skeletal immaturity (McCaskey et al., Reference MCCASKEY, ROWLAND, PAGE and MINEAR1982; Riddell et al., Reference RIDDELL, KING and GUNASEKERA1983).
Spondylosis
Spondylosis, together with ankylosis and osteosclerosis with fractures (35.8%), is the second most prevalent disorder in broiler chickens with clinical posterior paralysis (Dinev, Reference DINEV2013). Lesions were observed on the same vertebrae (Т4 and Т5), affected by the dominating spondylolisthesis, leading to the assumption that this condition could be secondary to spondylolisthesis. It may be that the dislocation of the respective thoracic vertebra forms a precondition for the occurrence of degenerative necrobiotic lesions in vertebral bodies, and this process could be provoked by impaired vertebral body articulation and resulting vertebral column deformation. Spondylosis is well described in other instances, as well as simultaneously with spondylolisthesis (Riddell, Reference RIDDELL1973). Episodes of enzootic spondylosis have been observed in turkeys (Friedman et al., Reference FRIEDMAN, DISON, PERL and WEISMAN1988); and a single case of cervical spondylosis has been reported in a single black swan (Hultgren et al., Reference HULTGREN, WALNER-PENDLETON, WATROUS and BLYTHE1987).
Spondylitis
Spondylitis is an inflammation of the vertebra. In many cases spondylitis involves one or more vertebral joints as well, which itself is called spondylarthritis. Spondylitis in broiler chickens has been associated with different infectious agents, including Staphylococcus aureus (Carnaghan, Reference CARNAGHAN1966), Enterococcus cecorum (Aziz and Barnes, Reference AZIZ and BARNES2007; Stalker et al., Reference STALKER, BRASH, WEISZ, OUSKAMA and DURDA2010) and Aspergillus fumigatus (Van Veen et al., Reference VAN VEEN and DWARS1999). Enterococcal spondylitis has been experimentally reproduced in male broiler breeders (Martin et al., Reference MARTIN, MARTIN and BARNES2011).
In the survey by Dinev (Reference DINEV2013) on clinical posterior paralysis manifestations in broiler chickens, spondylitis cases were etiologically related to E. coli infection. At the same time in these flocks, there were cases of femoral head necrosis (FHN), arthritis and osteomyelitis. The localisation of gross lesions was comparable to spondylitis caused by E. cecorum (Stalker et al., Reference STALKER, BRASH, WEISZ, OUSKAMA and DURDA2010), but differed from that seen in A. fumigatus spondylitis (vanVeen et al., 1999) where both cervical and thoracic vertebrae were affected. The effect of pressure exerted by the histologically demonstrated epidural pseudocysts, compressing the spinal cord between T2 and T5, was outlined as a direct cause for the appearance of posterior paralysis in reported cases of spondylitis.
Scoliosis
Duff (Reference DUFF1988) investigated the prevalence of vertebral column abnormalities in adult (> 60 weeks of age) male broiler breeders without associated clinical signs. The data showed scoliosis at various extents, angular deformity of the vertebral canal and articular osteochondrosis in about 60% of examined birds. Comparing this percentage with the occurrence of scoliosis (9.3%) confirmed by radiography in broiler chickens with various axial skeleton pathologies, this difference may be attributed to the stage of skeletal maturity.
Conclusions
The available literature suggests that the most prevalent axial skeletal pathology in commercial broiler chickens is spondylolisthesis, followed by spondylosis, spondylitis and scoliosis. Studies suggest that broilers with a lower degree of skeletal maturity are more prone to dislocations (spondylolisthesis), while in those with a mature skeleton have more permanent abnormalities, which are related to deformations (scoliosis). No association between the prevalence of spondylolisthesis and the genotype of the bird could be detected.
Most probably, considering their site and clinical manifestation, the cases of spondylosis are secondary to existing spondylolisthesis. The episodes of spondylitis in commercial broiler chickens are spontaneous, and their etiology are bacterial (Staphylococcus aureus, Enterococcus cecorum, E. coli) or mycotic (Aspergillus fumigatus).