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1 December 2012 Review of Infectious Bronchitis Virus Around the World
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Abstract

Infectious bronchitis virus (IBV) is a gamma coronavirus that causes a highly contagious disease in chickens. The virus can affect the upper respiratory tract and the reproductive tract, and some strains can cause a nephritis. Different serotypes and genetic types of the virus have been identified worldwide and for the most part do not cross-protect. In addition, new types of the virus continue to arise due to mutations and recombination events in the viral genome, making this virus difficult to identify and extremely difficult to control. Surveillance and identification of IBV types is extremely important for control of the disease and the advancement of molecular methods have aided in this pursuit. Genetic typing of IBV, which involves reverse transcription–PCR amplification and sequence analysis of the S1 glycoprotein gene, has revolutionized diagnosis and identification of this virus by making it possible to type and compare the relatedness of a large number of virus isolates in a short period of time. The purpose of this review is to give an update on the strains of IBV currently circulating in commercial chickens worldwide and hopefully to present a clear picture of the relationship between many of these viruses. The information on IBV types presented herein is from published manuscripts, submissions to GenBank, our own unpublished data, and personal communications with scientists and diagnosticians working with IBV worldwide.

For the most part, coronaviruses that affect mammals occur as only one or a few different serotypes within a species, but there are many different serotypes of avian coronavirus infectious bronchitis virus (IBV), making it unique among all other coronaviruses. The first isolation of IBV was in Massachusetts in the 1930s, and for many years the Mass serotype of IBV was the only recognized serotype until Jungherr et al. reported a different IBV type in 1956 using the virus neutralization test 35. He found that the different IBV serotypes did not cross-protect. Since that initial discovery many different serotypes, defined by neutralizing antibodies, and genetic types, based on the deduced amino acid sequence (from the nucleic acid sequence) of the spike gene, have been described worldwide. Although there are some exceptions 14,43, the genetic relationship between viruses in the S1 amino acid sequences can be used to predict the level of cross-protection between different IBV types, with type referring generically to both serotype and genetic type 15,37,39. This review presents an overview of IBV and the disease it causes then focuses on the different IBV types found around the world and their relationship to each other.

Infectious bronchitis is a highly contagious upper respiratory tract disease of chickens 16. Morbidity is typically 100% and mortality is low but can be >50% with some strains that cause nephritis or when opportunistic pathogens such as Escherichia coli complicate the disease. In addition, the reproductive tract of layer and breeder birds can be affected, causing decreased egg quality and production. When young pullets are affected, damage to the reproductive tract can result in layers and breeders failing to come into production.

IBV is a gamma coronavirus with single-stranded positive-sense RNA genome surrounded by a lipid envelope 51. Proteins encoded by the viral genome are the viral RNA-dependent RNA polymerase (RdRp), and structural proteins spike, envelope, membrane, and nucleocapsid. In addition, there are numerous accessory and regulatory proteins encoded by the genome. The spike glycoprotein, which forms club-shaped projections on the surface of the virus, is the most significant protein for identification of virus type because it contains epitopes for neutralizing and serotype-specific antibodies. 16,51. Spike is made up of two subunits: S1, which forms the outer portion of the protein, and S2, which anchors the protein to the viral envelope. Spike mediates cell attachment and virus-cell membrane fusion, and plays an important role in host cell specificity.

Because IBV exists as multiple different types that do not cross-protect, it is very difficult to control. Attenuated live vaccines are used in broilers and pullets and killed vaccines are typically used in layers and breeders. Effective control involves identification of the virus type causing disease followed by vaccination with an appropriate vaccine against that type 16. However, there are only a few different types of IBV vaccines available for use, whereas countless different types and variants of the virus capable of causing disease can be found throughout the world. In addition, some countries only allow vaccination with one or a few vaccine types, making control even more challenging.

Rapid replication, a high mutation rate, and genome recombination results in extensive genetic diversity and translates into many different types of the virus. The mechanism behind the emergence of new types and variants of the virus is largely unknown. What we do know is that the viral RdRp has low fidelity and limited ability to correct mistakes when replicating the viral genome. However, all coronaviruses, including IBV, have an exoribonuclease (ExoN) protein associated with the RdRp, which was shown to provide some proofreading capabilities 22,56, and most coronaviruses other than IBV exist as only one of a few different types. It follows that either ExoN is involved in limited variability of other coronaviruses and IBV has some other as yet unidentified factor(s) that contribute to its variability, or ExoN is not involved in limited variability.

Many different virus types that do not cross-protect make constant worldwide surveillance and identification of IBV types extremely important. Currently this is done by reverse transcriptase–PCR amplification of the S1 glycoprotein gene or the hypervariable 5′ end of the S1 gene followed by nucleic acid sequencing and analysis with other similar S1 sequences. Initial sequence analysis typically uses the Basic Local Alignment Search Tool on the database of sequences found in GenBank ( www.ncbi.nih.gov) to identify viruses in the database with similar sequences. Further analysis can be done using an alignment program to compare the sequence relatedness of unknown viruses with specific strains in the database. Genetic typing of IBV has revolutionized diagnosis and identification of this virus by making it possible to type a large number of virus isolates in a short period of time and to compare the relatedness of those types to each other as well as to other IBV types from other laboratories.

The purpose of this review is to give a brief history and an update on the strains of IBV currently circulating in commercial chickens worldwide. This review builds on the excellent review previously published by de Wit et al. 20, which describes the history and gives an overview of IBV variant viruses and their control. The IBV types presented and discussed below are from published manuscripts, sequence submissions to GenBank, our own unpublished data and personal communications with other laboratories around the world. The country of origin, strain name, GenBank accession number, and reference citation of representative strains are shown in Table 1. Fig. 1 shows the phylogenetic relationship between the strains in Table 1, which was constructed using the amino acid sequence of the S1 protein, where sequences were available. This phylogenetic reconstruction only contains representative strains from around the world and is not intended to show groupings of viruses into clades, which usually requires a number of similar viruses for each group.

Fig. 1. 

Phylogenetic tree showing amino acid sequence relatedness of the S1 protein for IBV strains computed using neighbor-joining and the Nei-Gojobori method with 1000 bootstrap replicates. The amino acid sequence were aligned with ClustalW (DNASTAR, Madison, WI), and the amino acid substitutions (×100) are shown taking into account increased gap extension penalties for different length sequences. GenBank accession numbers are shown in Table 1.

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Table 1. 

Infectious bronchitis virus types reported worldwide.

i0005-2086-56-4-634-t01.tif

Table 1. 

Continued.

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For many years there was a lack of standardization of IBV strain nomenclature. Recently, most scientists working with IBV have tried to adapt strain designations according to Cavanagh 12, which is similar to avian influenza viruses. Following this style, it is suggested that IBV strains be identified by the following scheme: IBV/bird type/country of origin/genotype or serotype/strain designation/year of isolation. In this scheme, IBV and bird type (assuming it is a chicken) could be dropped from the name of the isolate. If, however, the type of bird was not a chicken or the type of chicken (broiler, layer, breeder) is important, it should be included. Hopefully the coronavirus group of the International Committee on Taxonomy of Viruses will address this important issue, not only for IBV, but also for all coronaviruses.

IBV TYPES IN THE UNITED STATES

The most commonly isolated type of IBV in the United State is Arkansas and the presence of Ark-like isolates indicates that this virus continues to change 31. Ark-like viruses are defined as viruses within the Arkansas genetic clade but different enough to bring into question whether Ark vaccines will protect against them. Arkansas viruses have been shown to persist in commercial broiler flocks 31, which likely contributes to the genetic differences observed among the group 52. Other commonly detected viruses in the United States are Delaware, Conn, and Mass types 25,31. It is probably not a coincidence that the commonly isolated types are the same as the routinely used IBV vaccines.

California-type viruses were first isolated in the 1990s and were designated California variant 59. In 1999, another related but unique virus designated CAL99 was reported 57,63. Since those reports several other unique California viruses including CA/557/03 and CA/1737/04 33 have been reported, indicating that the California-type viruses continue to evolve. Also in the late 1990s, PA/Wolgemuth/98 and PA/171/99 nephropathogenic strains were identified in Pennsylvania 71.

In 2007 and 2008, two new IBV variants were detected Georgia and South Carolina broilers with respiratory disease. The viruses were distinct from each other and designated GA07 and GA08. Sequence analysis showed the GA07/GA07/07 virus to be similar to CA1737/04 and the GA08/GA08/08 virus to be somewhat similar to CA/557/03, suggesting possible origins. The GA08 type virus became the predominant virus at that time and commercially available live IBV vaccines, either alone or in combination, did not provide protection. A vaccine using the GA08/GA08/08 strain was developed 32 but not used commercially; however, an autogenous modified live vaccine was produced by one company and successfully used.

IBV TYPES IN MEXICO AND SOUTH AMERICA

Early reports found several variant viruses circulating in Mexico including MX/BL56-19/UNAM/96 (MX/5697/99), MX/UNAM-97/97, MX/07484/98, and MX/7277/99 (MX/1765/99) (10,24,26). All of those viruses were unique and not similar to vaccine strains in the United States. More recent reports of IBV in Central America include Conn (EU526403), Mass (EU526411), and MX/47/UNAM/01 (EU526405). Arkansas-type virus has been reported in Mexico 62, and there are unpublished reports that the Arkansas virus has recently been identified in Mexico (Jackwood, unpubl. data). A new publication characterized three IBV isolates from Cuba 3, and found that Cuba/La Habana/CB13/09 virus was similar to Mass-type viruses, Cuba/La Habana/CB19/09 was related to Belgium/B1648/95, and Cuba/La Habana/CB6/09 was similar to CA/1737/04.

In South America the most recent work has been conducted in Chile (Chile/12103b/09, HM446012) and Colombia (Colombia/Q1/92079/12) with both countries reporting a Q1-type virus. The Q1 type of IBV was originally isolated in China and a brief history is given below. In Brazil three unique types have been reported: BR1 (Brazil/BR1/USP-28/07), BR2 (Brazil/BR2/USP-21/07), and BR3 (Brazil/BR3/USP-16/07) 67. In addition, a variant virus isolated in 2005 (Brazil/USP-01/05), viruses similar to the European 793B type (Brazil/4/91/USP-31/07), and Mass-type viruses have been reported 67. There are also unpublished reports of Arkansas isolations in South America.

IBV TYPES IN EUROPE

Early reports of IBV types in Europe included Mass-type viruses as well as B/D274/84 and E/D3896/84 in England, Netherlands/D207/79, and Netherlands/D1466/79 13. In 1991 a unique virus type designated 793B (793B/4/91/91) emerged 18 and since that time it has spread to many parts of the world including Eastern Europe, Russia, Turkey, the Middle East, China, Japan, Morocco, and South America (see above). A 4/9 vaccine strain was developed and is commercially available in many countries.

In Italy, an early variant designated Italy/624I/94 was reported 11 as well as a more recent type designated Italy-02 (Italy/Italy-02/497/02). Italy-02 was found in almost all European countries but in 2004 it was reported to be declining in prevalence in all countries except Spain 69. Because of its pathogenicity, the most significant IBV type to become widespread in Europe in recent years is the QX IBV type and so called QX-like types 2,6,21,27,58,66,69.

A 2001 report on IBV isolates identified in Belgium between 1986 and 1995 found that half of the viruses were Mass-type, 38% were B/D274/84-type, 11% were Belgium/B1648/96, and 1% was 793B-type 55. It is not clear if these viruses are still circulating in Belgium.

IBV TYPES IN RUSSIA, UKRAINE, KAZAKHSTAN, AND SLOVENIA

Early isolations from this region of the world were closely related to the Mass type, whereas isolates from the late 1990s up to 2002 resembled the Mass type as well as European types 793B, D274, B1648, 624I, and Italy-02 9. In addition, numerous novel types were detected as well as QX. Between 2007 and 2010, a number of IBV isolates were characterized and it was reported that the most common serotype was Mass, followed by 793B, then D274, and finally QX 60. Isolations of 793B and QX increased in more recent years. In addition, it was reported that about 12% of isolates belonged to Arkansas, B1648, or Italy-02 types. Up until 2005, in Slovenia, Mass-, 624/I-, and B1648-type viruses were detected 36. The QX IBV type was first detected in Slovenia in 2005. Recently, a number of isolates similar to the Italy-02–type and LX4-type (QX IBV) viruses were identified in broilers, broiler breeders, and layers in Slovenia 36.

IBV TYPES IN AFRICA, THE MIDDLE EAST, EGYPT, AND INDIA

In Israel, Mass was the only type detected for many years until the 793B type of IBV (Israel/793B/variant 1/96) was identified in 1996 53. Two years later a new virus Israel/variant 2/98 was characterized 10. Other variant viruses have also been characterized in Israel, including Israel/IS720/720/99 and Israel/IS720/885/00, both belonging to the IS720 type 54. The IS720-type virus was also identified in Iraq (Iraq/IS720/Sul/01/09) and Egypt (Egypt/IS720/Beni-Seuf/01) 1. Other viruses in Egypt include Mass (Egypt/Mass/F/03) and D274 (Egypt/D274/D/89) and a recent report found QX-like IBV in Zimbabwe 65.

In Iran and Iraq, the 793B type was reported 47,64. In addition, Mass was reported in Iran 17, and in Iraq, the Iraq/Sul/01/09 strain belonging to the IS720 type was characterized 47.

The Mass (GenBank accession number HM179146) and 793B types were the most common IBV types reported in India since 1991 23. Around the year 2000, visceral gout and nephritis was observed in birds less than 2 wk of age and several nephropathogenic strains of IBV were identified 5, including India/PDRC/Pune/9/99. Since that time, many nephropathogenic strains of IBV associated with gout in chicks have been isolated and genetically characterized.

IBV TYPES IN CHINA AND THE FAR EAST

A number of publications on IBV types in China have been published but unfortunately they have not always agreed on type designations for the viruses detected 28,34,42,43,45,46. Herein we will refer to the different IBV types as reported by a recent publication by Han et al. 28. Currently, nine different genetic groups have been recognized in China: LX4, LDT3, LHLJ, BJ, LDL, N1/62, and LSC 28, as well as Mass- and 793B-type viruses. Two of the most significant IBV types in China and elsewhere are QX IBV in the LX4 group and Q1 IBV in the LDL group; they are significant because of their pathogenicity and widespread distribution.

QX IBV . 

Around 1996, a new virus was identified and described as belonging to the LX4 type of viruses was reported in China 68. That virus, designated here as QX IBV, was associated with tracheitis, severe nephritis, egg production losses, false layer syndrome, and proventriculitis. Morbidity was 100% and mortality was high due to the nephropathogenic nature of the virus. In 2001 similar viruses were reported in Eastern Europe 9 and in the Netherlands in 2003 38 and other western European countries including the United Kingdom 7,8,66.

Q1 IBV . 

Between 1996 and 1998, three IBV isolates associated with respiratory disease and proventriculitis in 25- to 70-day-old layer chickens were characterized and designated J2, T3, and Q1 70. All three viruses were >98.9% similar in the S1 gene and formed a distinct genetic group that was only 82.3% (Israel/Variant2/96) and 80.3% (D207) similar to the next closest groups. In pathogenicity studies, respiratory signs were observed and the challenge virus was detected in trachea, proventriculus, duodenum, and cecal tonsil of specific-pathogen-free layer-type chickens challenged with the virus 70. Since that initial characterization, Q1-like viruses have been reported in Taiwan (ABD64050, 2005), Italy (AFD09483, 2011), Chile (HM446012, 2009) and Colombia (Jackwood, unpubl. data).

In the early 1990s in Korea, a nephropathogenic strain designated KM91 was identified and became widespread in that country 41. Ten years later, a number of IBV strains similar to strains circulating in China were identified, including QX 45. Detection of IBV isolates between 2003 and 2006 identified three genetic groups, designated Korea (K)-I, K-II (LX4-type), and K-III (LDL-type) 40. More recently, strains that appear to be recombinants of KM91 and QX were detected 44.

Since 1995 in Japan, four different genetic groups have been identified: Japan (JP)-I, JP-II, JP-III (LX4), and JP-IV 4,49. The JP-III group falls into the China LX4 group (QX IBV), whereas JP-I, JP-II, and JP-IV appear to be unique variants. The 793B type, as well as Mass and, interestingly, Gray types have also been reported 4,50.

In Malaysia two variant viruses were reported in 2009 72. The Malaysia/MH5356/95 isolate appears to be QX-like and the Malaysia/V9/04 virus is a unique variant. Between 2008 and 2009 in Thailand, Mass and QX-like (group 2) viruses were reported as well as a unique group 1 IBV type 61.

IBV TYPES IN AUSTRALIA

In Australia, IBV isolates have been separated into subgroup 1 (classical strains), and subgroups 2 and 3 (novel strains) based on genetic analysis of S1, the 3′ ends of the genome, and serologic cross-reaction. Examining the 3′ end of the genome may correlate with some biologic characteristic of the virus (e.g., growth rate or pathogenicity) but would not affect classification of the virus type, which is based on spike. Subgroup 1 viruses include, among others, the nephropathogenic Australia/N1/62 strain, the first isolate of IBV in Australia, and the vaccine strain Australia/VicS/62 19. The subgroup 2 viruses were identified in 1988 and include Australia/subgroup 2/N1/88, Australia/subgroup 2/Q3/88, and Australia/subgroup 2/V18/91 30. The subgroup 3 strains were first identified around 2002 29 and appear to be chimeras resulting from recombination between subgroup 1 and 2 viruses 48. Examples of subgroup 3 viruses include Australia/subgroup 3/N1/03 and Australia/subgroup 3/N2/04. Both subgroup 2 and 3 viruses are respiratory pathogens, and to date, none have been found to be nephropathogenic like the classical strains in subgroup 1.

CONTROL STRATEGY

Identifying new variant IBVs associated with disease in vaccinated birds is only the first step in control of this economically important upper respiratory disease in chickens. The pathogenicity of new variant IBV isolates needs to be characterized and current vaccines or combinations of commercial vaccines ought to be tested for efficacy. When a variant virus becomes widespread and commercial vaccines do not provide adequate protection, it is sometimes necessary to develop specific vaccines to control the disease. Killed vaccines or attenuated live vaccines using the new variant IBV are typically produced. But that can take months or over a year to accomplish when typically there is a sense of urgency to control the new virus. However, it should be recognized that using attenuated live vaccines for an IBV type not previously identified in an area is not recommended because of the ability of the virus to rapidly mutate and recombine with other IBVs, which may lead to the emergence of new strains capable of causing disease. Although our ability to quickly and accurately identify new IBV variants has improved tremendously, we clearly need new vaccine development methodologies to safely and rapidly respond to outbreaks of the disease.

ACKNOWLEDGMENTS

I would like to thank all the scientists typing IBV isolates around the world.

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Abbreviations

ExoN

exoribonuclease

IBV

infectious bronchitis virus

RdRp

RNA-dependent RNA polymerase

American Association of Avian Pathologists
Mark W. Jackwood "Review of Infectious Bronchitis Virus Around the World," Avian Diseases 56(4), 634-641, (1 December 2012). https://doi.org/10.1637/10227-043012-Review.1
Received: 2 May 2012; Accepted: 1 June 2012; Published: 1 December 2012
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