The disease

In IBV infected flocks, the morbidity rate can reach 100% but the mortality rate depends on the presence of secondary infections, flock age, immune status, management and environmental factors. In young chickens, the mortality rate is typically 25-30% but it can approach 80% depending on the virulence of the strain. Even though all age group of chicks are susceptible to IBV, baby chicks are more susceptible than older ones (Cavanagh and Gelb, Reference CAVANAGH and GELB2008).

The most notable symptoms are those which affect the respiratory tract, hence the term ‘infectious bronchitis’. The severities of the clinical signs are influenced by several factors associated with the field virus (such as strain, virulence and dosage), host (age, sex, type and immune status), environment (dust, ammonia and stress) and management and biosecurity levels (Ganapathy, Reference GANAPATHY2009). The other forms of the disease are mainly associated with the reproductive, renal and gastro-intestinal systems. It has been reported that the virus can cause infertility in male chickens (Jones, Reference JONES2010a), and the virus has been isolated from the testicles and semen of infected males birds (Gallardo et al., Reference GALLARDO, HOERR, BERRY, VAN SANTEN and TORO2011).

The typical signs of IBV in chickens of less than six weeks of age are depression, huddling under the heat source, difficulty with breathing (often more noticed at night when the birds are resting), gasping, coughing, tracheal râles, nasal discharge, lethargy, watery eyes and mildly swollen sinuses in severe conditions (Cavanagh and Gelb, Reference CAVANAGH and GELB2008; Ganapathy, Reference GANAPATHY2009). Baby chicks may die due to IBV and, in uncomplicated infections in chickens aged more than five weeks old, the disease may not be serious. In any age groups if IBV is mixed with other pathogens more severe diseases can occur (Cavanagh, Reference CAVANAGH2007).

Following infection via the respiratory route the virus spreads to other tissues including the reproductive tract. Infection at an early age may cause permanent damage to the reproductive tract leading to a decrease in quantity and quality of eggs (Raj and Jones, Reference RAJ and JONES1997; Benyeda et al., Reference BENYEDA, MATÓ, SÜVEGES, KARDI, ABONYI-TÓTH, RUSVAI and PALYA2009; Ganapathy, Reference GANAPATHY2009). Infection in laying birds results in decreases in egg production and the extent of the damage can vary depending on the time of the infection and hens health status (Cook and Mockett, Reference COOK and MOCKETT1995). Affected flocks are unlikely to return to the normal level of production (Benyeda et al., Reference BENYEDA, MATÓ, SÜVEGES, KARDI, ABONYI-TÓTH, RUSVAI and PALYA2009; Ganapathy, Reference GANAPATHY2009).

The nephritic form of IBV mostly occurs in broiler chickens but can affect young growing pullets and even layers. Litter can be very wet and may contain excessive urate. After a few days of infection, the droppings of infected birds become completely wet and birds may die suddenly within the first ten days (Meulemans and Van den Berg, Reference MEULEMANS and VAN DEN BERG1998). Infection with IBV was believed to cause deep pectoral myopathy via atypical clinical findings in chickens (Raj and Jones, Reference RAJ and JONES1996). IBV serotype 793B was isolated from a broiler breeder flock which had bilateral myopathy affecting both deep and superficial pectoral muscles. It is characterised by paleness and swelling of the deep pectoral muscles with the presence of occasional facial haemorrhages (Gough et al., Reference GOUGH, RANDALL, DAGLESS, ALEXANDER, COX and PEARSON1992; Raj and Jones, Reference RAJ and JONES1996; Reference RAJ and JONES1997).

Droual and Woolcock (Reference DROUAL and WOOLCOCK1994) reported that a commercial broiler flock in the central valley of California experienced respiratory disease and signs of swollen head syndrome (SHS). IBV M41 was isolated from the tissue samples as well as serum, and samples were positive for IBV but negative for avian metapneumovirus (aMPV). This finding suggested that SHS can be associated with IBV other than aMPV (Droual and Woolcock, Reference DROUAL and WOOLCOCK1994). In an experimental infection with IS/885/00 in commercial broilers, head swelling was found at 15 days post-infection (dpi). Following necropsy, sterile incision of skin was made, and swabs were taken from tissues underneath the skin, and this was positive for the IS/885/00 by RT-PCR and virus isolation (Awad and Ganapathy, unpublished).

Virus replication and spread

IBV has an incubation period of 24 to 48 hours and viral spread occurs rapidly among chickens in a flock by aerosol and mechanical means. The initial replication of IBV occurs in the upper respiratory tract, causing loss of ciliated epithelial cells in the sinuses and trachea. In addition, some IBV strains replicate in tissues along the alimentary tract (oesophagus, proventriculus, duodenum, jejunum, bursa of Fabricius, caecal tonsils, rectum, and cloaca) without significant pathological effects (Raj and Jones, Reference RAJ and JONES1997; Boltz et al., Reference BOLTZ, NAKAI and BAHR2004; Villarreal et al., Reference VILLARREAL, SANDRI, SOUZA, RICHTZENHAIN, DE WIT and BRANDAO2010).

Renal damage associated with different IBV strains is an increasingly important feature of the infection, especially in broilers, as nephropathogenic strains produce less respiratory signs (Ziegler et al., Reference ZIEGLER, LADMAN, DUNN, SCHNEIDER, DAVISON, MILLER, LU, WEINSTOCK, SALEM, ECKROADE and GELB2002) and lesions (Glahn et al., Reference GLAHN, WIDEMAN and COWEN1989), but can induce high mortality (De Wit et al., Reference DE WIT, NIEUWENHUISEN-VAN WILGEN, HOOGKAMER, VAN DE SANDE, ZUIDAM and FABRI2011b). Nephropathogenic IBV outbreaks can be complicated and/or exacerbated by management problems such as high dietary calcium (Glahn et al., Reference GLAHN, WIDEMAN and COWEN1989). Infection of enteric tissues does usually not manifest itself clinically, but persists for long periods and results in faecal virus excretion. It has also been reported that the virus replicates in the gut for longer periods than in the respiratory tract (Jones, Reference JONES2010b).

In recent years some strains of IBV have caused proventriculitis (Yu et al., Reference YU, JIANG, LOW, WANG, NAM, LIU and KWANG2001; Gough et al., Reference GOUGH, COX, WELCHMAN, WORTHINGTON and JONES2008; Benyeda et al., Reference BENYEDA, SZEREDI, MATÓ, SÜVEGES, BALKA, ABONYI-TÓTH, RUSVAI and PALYA2010; De Wit et al., Reference DE WIT, COOK and VAN DER HEIJDEN2011a; Sun et al., Reference SUN, HAN, MA, ZHANG, YAN, SHAO, XU, KONG and LIU2011) and enteritis (Jones, Reference JONES2010a). Field infection with 793B has been associated with enteritis (Jones, Reference JONES2010a). Apart from this, IBV replicates in the oviduct and testes of infected chickens, leading to decreases in egg production and fertility (Boltz et al., Reference BOLTZ, NAKAI and BAHR2004; Villarreal et al., Reference VILLARREAL, BRANDAO, CHACON, ASSAYAG, MAIORKA, RAFFI, SAIDENBERG, JONES and FERREIRA2007; Grgic et al., Reference GRGIC, HUNTER, HUNTON and NAGY2008). In breeder and laying hens the arrival of IBV QX has reinforced the ability of some IBV strains in causing substantial pathological damage to female chicken's reproductive tracts. This in turn causes delayed onset of production, poor peak in egg production, high percentage of false-layers and poor quality of eggs (Ganapathy, Reference GANAPATHY2009; De Wit et al., Reference DE WIT, NIEUWENHUISEN-VAN WILGEN, HOOGKAMER, VAN DE SANDE, ZUIDAM and FABRI2011b;).

Infectious bronchitis virus and strain variations

IBV is caused by a coronavirus, of the family Coronaviridae with over twenty five known genotypes worldwide (Snyder, Reference SNYDER2002). It is a single stranded RNA, envelope virus. Three virus-specific proteins have been recognised: (i) the spike (S) glycoprotein; (ii) the membrane or matrix (M) glycoprotein; and (iii) the nucleocapsid (N) protein (Lai and Cavanagh, Reference LAI and CAVANAGH1997). Being a single stranded RNA virus, IBV has an enormous capacity to change by both spontaneous mutation and by genetic recombination (Cavanagh and Gelb, Reference CAVANAGH and GELB2008) . When these events occur in IBV, both are most likely to result in the emergence of new variants if they occur in the hypervariable regions of the S gene.

Most countries are now known to have their own indigenous IBV variants which are characterised and are frequently named after the laboratory or researcher in which or by whom they were first isolated for instance Massachusetts, Connecticut, Arkansas, D274 and QX. It is very well understood that, whilst many new variants are unable to replicate or survive for long time, a few manage to emerge and become of economic importance either worldwide or in restricted geographic areas.

Host range

It is accepted that chickens are the most significant natural hosts of IBV, however, farmed pheasants have also been found to be natural hosts (Ignjatovic and Sapats, Reference IGNJATOVIC and SAPATS2000). With a history of clinical respiratory disease and reduced egg production, this suggests that pheasants could be secondary natural hosts for IBV (Cook and Mockett, Reference COOK and MOCKETT1995). However, it appears that some species of pheasant are not susceptible to the virus or possibly only certain strains of IBV may infect pheasants (Ignjatovic and Sapats, Reference IGNJATOVIC and SAPATS2000). Recently, there has been more evidence which suggests that IBV has a wider host range than was previously thought and is not only limited to galliforms (chicken-like) birds (Cavanagh, Reference CAVANAGH2007; Cavanagh and Gelb, Reference CAVANAGH and GELB2008), but other species such as geese, ducks, and pigeons might also play a role in the spread of IBV strains over the world (Felippe et al., Reference FELIPPE, DA SILVA, SANTOS, SPILKI and ARNS2010; De Wit et al., Reference DE WIT, COOK and VAN DER HEIJDEN2011a) . Interestingly the role of the wild birds in IBV spread is largely unknown and speculative but it is certainly a critical area that deserves more attention and research in near future.

Incidence and geographical distribution

In 1931 Schalk and Hawn reported the first occurrence of IBV in the United State, as a new respiratory disease of baby chicks (Schalk and Hawin, Reference SCHALK and HAWIN1937). The first isolate of IBV was the Beaudette strain (Beaudette and Hudson., Reference BEAUDETTE and HUDSON1937). Later, the M4 1 strain was isolated in the North Dakota and found to be serologically related to the Beaudette strain (Bracewell, Reference BRACEWELL1975). Strains of this serotype were among the first to be made into live vaccines, e.g. H 120 derived from a Dutch isolate of 1955 (Bijlenga et al., Reference BIJLENGA, COOK, GELB and WIT2004).

The 'T' strain was the first IBV strain isolated in Australia in 1962 (Cumming, Reference CUMMING1963; Ignjatovic et al., Reference IGNJATOVIC, SAPATS and ASHTON1997). Many different IBV variants have been isolated and characterised since then and IBV has always evolved independently in this country from the rest of the world due to its geographical isolation (Ignjatovic et al., Reference IGNJATOVIC, GOULD and SAPATS2006).

In Europe, only 30% of the isolates were serologically related to known North American serotypes in the 1970s. The majority of the remainder strains were found to be related to four Dutch strains; D207, D212, D3128 and D3896 (Davelaar et al., Reference DAVELAAR, KOUWENHOVEN and BURGER1984), by VN test. Many of the British IBV strains isolated between 1981 to 1983 were closely related to the Dutch strains; D207, 03128 and D3896 (Cook, Reference COOK1984). Although these viruses caused respiratory disease and aberrant drop in egg production in layer flocks, they were not associated with poor egg quality (Cook, Reference COOK1984; Cook and Huggins, Reference COOK and HUGGINS1986). Thereafter, many IBV variants were isolated from the UK (Gough et al., Reference GOUGH, COX, GUTIERREZ, MACKENZIE, WOOD and DAGLESS1996) and in other European countries including France (Picault et al., Reference PICAULT, DROUIN, GUITTET, BENNEJEAN, PROTAIS, L'HOSPITALIER, GILLET, LAMANDE and BACHELIER1986) Belgium (Meulemans et al., Reference MEULEMANS, CARLIER, GONZE, PETIT and VANDENBROECK1987), Italy (Capua et al., Reference CAPUA, GOUGH, MANCINI, CASACCIA and WEISS1994; Zanella et al., Reference ZANELLA, COARO, MARCHI, FABRIS and LAVAZZA2000; Reference ZANELLA, LAVAZZA, MARCHI, MARTIN and PAGANELLI2003), Poland (Minta et al., Reference MINTA, BUGAJEK, KARPINSKA, GOUGH, CAVANAGH, MAWDITT, COX, BARTNICKA and WIERCINSKI1998) and Spain (Dolz et al., Reference DOLZ, PUJOLS, ORDÓÑEZ, PORTA and MAJÓ2006; Reference DOLZ, PUJOLS, ORDÓÑEZ, PORTA and MAJÓ2008). Among these, of major importance internationally was the variant called 793B that emerged in the1990s and quickly spread to many parts of the world (Gough et al., Reference GOUGH, RANDALL, DAGLESS, ALEXANDER, COX and PEARSON1992; Parsons et al., Reference PARSONS, ELLIS, CAVANAGH and COOK1992). In Brazil, in addition to the local strains, viruses similar to the European 793B type, Mass-type and Arkansas viruses have been reported (Villarreal et al., Reference VILLARREAL, SANDRI, SOUZA, RICHTZENHAIN, DE WIT and BRANDAO2010).

In 2002 sequencing of a new IBV genotype, named Italy 02 which had economical importance, was submitted to the GenBank nucleotide database. By using virus neutralisation assays it was demonstrated that little antigenic relatedness exists between Italy 02 and some of the reference IBV serotypes, which indicated that Italy 02 was likely to be a new serotype (Dolz et al., Reference DOLZ, PUJOLS, ORDÓÑEZ, PORTA and MAJÓ2006). Later on, Italy 02 was described to be the third most frequently detected IBV strain and is probably the dominant wild type in Western Europe. The origin of Italy 02 is unknown, but it has been spreading predominantly throughout Europe (Worthington et al., Reference WORTHINGTON, CURRIE and JONES2008).

By the mid-1990s many published reports revealed the diversity of IBVs causing disease in different part of China. But, possibly the most significant IBV variant that has emerged from China is the QX variant reported in association with proventriculitis (Wang et al., Reference WANG, WANG, ZHANG, FAN, JIANG, LIU XIANG, DING and WANG1998). IBV QX later appears to have spread to Russia and then on to Europe (Bochkov et al., Reference BOCHKOV, BATCHENKO, SHCHERBAKOVA, BORISOV and DRYGIN2006; Worthington et al., Reference WORTHINGTON, CURRIE and JONES2008). This genotype of IBV mainly affects the respiratory and reproductive systems (Terregino et al., Reference TERREGINO, TOFFAN, SERENA BEATO, DE NARDI, VASCELLARI, MEINI, ORTALI, MANCIN and CAPUA2008; Ducatez et al., Reference DUCATEZ, MARTIN, OWOADE, OLATOYE, ALKALI, MAIKANO, SNOECK, SAUSY, CORDIOLI and MULLER2009). IBV QX isolated in Netherlands causes renal disease and false lay (Terregino et al., Reference TERREGINO, TOFFAN, SERENA BEATO, DE NARDI, VASCELLARI, MEINI, ORTALI, MANCIN and CAPUA2008; Irvine et al., Reference IRVINE, COX, CEERAZ, REID, ELLIS, JONES, ERRINGTON, WOOD, MCVICAR and CLARK2010). In the UK, IBV QX-like was isolated from proventriculus of broilers with poor feed conversion ratio (FCR) and body weight gain which were also showing respiratory symptoms (Ganapathy et al., Reference GANAPATHY, WILKINS, FORRESTER, LEMIERE, CSEREP, MCMULLIN and JONES2012).

Another IBV genotype, the Q1, which was genetically and serologically distinct from IBV classical strains, was reported in China during 1996 to 1998 (Yu et al., Reference YU, JIANG, LOW, WANG, NAM, LIU and KWANG2001). Recently, Q1 IBV strain has been identified in Europe (Toffan et al., Reference TOFFAN, TERREGINO, MAZZACAN, CASTALDELLO, CAPUA and BONCI2011), South America (Jackwood, Reference JACKWOOD2012), Middle East and the Indian subcontinent (Ganapathy, unpublished)

Of late, IBV genotypes with certain regional importance, such as IBV IS/855/00 (Meir et al., Reference MEIR, ROSENBLUT, PERL, KASS, AYALI, PERK and HEMSANI2004), and IS/1494/06, were isolated in Israel (Meir, Personal communication). Later on these strains were found in Turkey (Kahya et al., Reference KAHYA, COVEN, TEMELLI, EYIGOR and CARLI2013), Egypt (Abdel-Moneim et al., Reference ABDEL-MONEIM, AFIFI and EL-KADY2012), Iraq (Mahmood et al., Reference MAHMOOD, SLEMAN and UTHMAN2011) and Libya (Awad and Ganapathy, unpublished).

To sum up, important global variants of IBV, such as 793B or QX have spread over Asia, Europe and Africa in a short period, but have not been reported in the USA or Australia. On the other hand, the major Arkansas strain has hardly been reported outside the USA. A pathogenic strain like D1466 that has been endemic in some countries in Western Europe for three decades, but has hardly been reported outside Western Europe. This is despite it being very difficult to achieve a sufficient level of protection against this strain (Cook et al., Reference COOK, ORBELL, WOODS and HUGGINS1999), which would make it easier for it to spread to other areas. It seems likely that geographical isolation and control measures employed in countries play a part in preventing entry of new IBV variants (De Wit et al., Reference DE WIT, COOK and VAN DER HEIJDEN2011a).

Prevention and control

Since the discovery of the disease, past and present control strategies have struggled to control it, due to the existence of numerous IBV strains, more of which continue to emerge. With such diversity, it is becoming increasingly difficult to control infection using the currently available live and inactivated vaccines. Alongside biosecurity and management improvements, these vaccines are in use worldwide. There is a continuous emergence of variants through natural recombination. Even though most of these variants disappear, a few tend to linger and continue to cause disease resulting in production loss (De Wit et al., Reference DE WIT, COOK and VAN DER HEIJDEN2011a). This appears to be due to an inability of currently available vaccines or vaccination programmes in tendering full protection against emerging strains. In recent years, IBV QX has become a major threat to the poultry industry, despite high and proper use of IBV vaccination programs in the Western Europe. It appears that current vaccination strategies have managed to reduce the impact of these newly emerged IBVs, in terms of the occurrence of disease and production losses, but has allowed the continuous spread of the viruses.

The appropriate strategy for control of IBV is to use vaccine strains that are similar to those found in a particular farm or area. In areas where this is not possible or where there were no vaccines available for the prevalent strains, vaccination programmes consisting of different strains tend to induce a higher and broader protection against challenges with several heterologous strains (Cook et al., Reference COOK, ORBELL, WOODS and HUGGINS1999; Reference COOK, CHESTER, BAXENDALE, GREENWOOD, HUGGINS and ORBELL2001; Terregino et al., Reference TERREGINO, TOFFAN, SERENA BEATO, DE NARDI, VASCELLARI, MEINI, ORTALI, MANCIN and CAPUA2008). Generally, the success rate depends on the genetic differences between the vaccine viruses and the field viruses.

Live vaccines are mostly administered by spray or drinking water (Cavanagh and Gelb, Reference CAVANAGH and GELB2008), but for better vaccine-take take it is preferable to vaccinate intraocularly or intranasally. In long-lived birds, for example breeders and layers, IBV inactivated vaccines are used. This vaccine is given by intra-muscular or subcutaneous injections for induction of high levels of humoral antibodies, which protect the birds against invading IBVs and avoids problems in egg production or quality. Such vaccination in breeder birds helps in ensuring transfer of high and uniform levels of maternal antibodies to hatching chicks. Maternal antibodies are important in conferring some protection against of virulent IBVs (Davelaar and Kouwenhoven, Reference DAVELAAR and KOUWENHOVEN1977; Mondal and Naqi, Reference MONDAL and NAQI2001; De Wit et al., Reference DE WIT, NIEUWENHUISEN-VAN WILGEN, HOOGKAMER, VAN DE SANDE, ZUIDAM and FABRI2011b).