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Infectious Bursal Disease: Transmission, Pathogenesis, Pathology and Control

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Infectious Bursal Disease: Transmission,

Pathogenesis, Pathology and Control - An
Overview

Ochuko Orakpoghenor, Sunday B. Oladele & Paul A. Abdu

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Bursal Disease: Transmission, Pathogenesis, Pathology and Control - An Overview, World's Poultry
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WORLD'S POULTRY SCIENCE JOURNAL
https://doi.org/10.1080/00439339.2020.1716652

Infectious Bursal Disease: Transmission, Pathogenesis,

Pathology and Control - An Overview
a
Ochuko Orakpoghenor , Sunday B. Oladelea and Paul A. Abdub
a
Department of Veterinary Pathology, Ahmadu Bello University, Zaria, Nigeria; bDepartment of Veterinary
Medicine, Ahmadu Bello University, Zaria, Nigeria

SUMMARY KEYWORDS
Infectious bursal disease (IBD) is an immunosuppressive disease of Infectious bursal disease;
poultry causing great economic losses to the poultry industry. The immunosuppression; bursa
disease is caused by infectious bursal disease virus (IBDV) and is of Fabricius; ELISA; RT-PCR
characterised by bursal lesions, atrophy and immunosuppression.
The causal virus targets B lymphocytes and is transmitted mainly by
faecal-oral routes through ingestion of contaminated feed and water.
Based on virus neutralisation, two serotypes of IBDV have been
identified (serotypes 1 and 2), with serotype 1 considered to be
virulent. Acute clinical outbreaks of classical IBDV are characterised
by sudden onset, high morbidity, spiking and mortality curves with a
rapid recovery time of about five to seven days, after clinical signs
appear. Mortality rates vary within serotype 1 IBDV strains, ranging
from no mortality by the variant strains, about 20% mortality with
classical strains and over 50% mortality by very virulent strains. Post-
mortem lesions are commonly, but not exclusively, reported in the
bursa of Fabricius (BF) observed as haemorrhages, swelling and
atrophy. The disease is diagnosed by isolation and characterisation,
serology, including agar gel precipitation test (AGPT), enzyme linked
immunosorbent assay (ELISA), and molecular techniques, such as
reverse transcription polymerase chain reaction (RT-PCR). No effec-
tive treatment has been reported for IBD; it can be prevented by
vaccination and implementation of strict biosecurity measures.

Introduction
Infectious bursal disease (IBD), alternatively called Gumboro disease (GD), is an acute,
highly contagious disease of chickens caused by the infectious bursal disease virus (IBDV;
Wahome et al., 2017; Mwenda et al., 2018). The disease is characterised by bursal lesions
and atrophy and immunosuppression in chickens between three weeks and three months
old (Mawgod, Arafa, and Hussein 2014). The virus responsible for IBD is a non-
enveloped icosahedral double stranded RNA virus with a bisegmented genome, belong-
ing to the genus Avibirnavirus and family Birnaviridae (Baxendale 2002; Jackwood et al.,
2018). The IBDV is characterised by a bipartite dsRNA genome (segments A and B)
packaged into a single-virus particle of about 70 nm in diameter (Coulibaly et al., 2005).
Five proteins have been identified in IBDV and are generally referred to as VP1 (90 Kd),

CONTACT Ochuko Orakpoghenor ochuko.orakpoghenor@gmail.com Department of Veterinary Pathology,

Ahmadu Bello University, Zaria, Nigeria
© 2020 World's Poultry Science Association.
2 O. ORAKPOGHENOR ET AL.

VP2 (40 Kd), VP3 (35 Kd), VP4 (28 Kd) and VP5 (21 Kd) (Dobos 1979; Luque et al.,
2008). Segment A has two open reading frames (ORFs), of which the smaller of the two
encodes VP5 and the larger encodes a polyprotein that is cotranslationally processed by
the viral protease VP4, to yield VP2, VP3 and VP4 (Feldman et al., 2006). Segment B has
been reported to be monocistronic and encodes VP1 (Pan, Vakharia, and Tao 2007). The
virus shows selective tropism for lymphoid tissue and has affinity for immature B
lymphocytes in the bursa of Fabricius (BF) (Lukert and Saif 2003; Mwenda et al.,
2018). It has been reported to cause lymphoid depletion in the BF in free-living wild
birds, but infection is generally sub-clinical (AHA 2009).

Serotypes of infectious bursal disease virus

Two serotypes of IBDV (1 and 2) have been recognised as having considerable antigenic
variation within each serotype (Swai et al., 2011; Jackwood et al., 2018). Serotype 1 is
pathogenic only to chickens, and can be further divided based on antigenicity/genetic
aspects (classical and variant) and level of pathogenicity (attenuated, virulent vIBDV and
very virulent vvIBDV) (Wang et al., 2007; Jackwood et al., 2018). However, the trends of
mortality vary within serotype 1 IBDV strains ranging from no mortality by the variant
strains, about 20% mortality by the classical strains (Müller, Islam, and Raue 2003) and over
50% mortality by the vvIBDV (Mülleret al., 2003; Escaffre et al., 2013). Variant IBDV
(designated as IBDV TY2 strain) has been isolated from broilers cohabitating with sentinel
chickens immunised using the classical-type IBD vaccine (Yamazaki et al., 2017). The
emergence of new IBDV variants can threaten poultry health and production all over the
world causing significant economic losses. Serotype 2 viruses are naturally avirulent and do
not cause clinical disease in chickens and turkeys (Motohiko, Takashi, and Tsuyoshi 1998).
Serological evidence of serotype 1 IBDV infection in wild birds suggests that they may play
a role in the epidemiology of IBDV by serving as reservoirs for the virus (Motohiko et al.,
1998; Gilchrist 2005; AHA 2009). Reports have shown that serotype 2 of IBDV is more
prevalent in many species of free-living wild birds, with the natural host considered to be
turkeys (Motohiko et al., 1998).

Routes of infection
The faecal-oral route via ingestion of contaminated feed and water constitutes the natural
means by which IBDV infection occurs in chickens and turkeys (AHA 2009). However, for
experimental purposes, other mucosa routes, such as respiration, have been demonstrated
(AHA 2009). In free-living, wild birds, IBDV infection is likely to be indirect through
scavenging of dead infected chickens, ingestion of contaminated water, or exposure of
respiratory or conjunctival membranes to contaminated poultry dust (Gilchrist 2005). This
is enhanced by unrestricted interactions between free-living wild birds and poultry (AHA
2009).

Host and host reservoirs of infectious bursal disease virus

IBDV is host specific, with chickens and turkeys reported to be the natural hosts
(Jackwood and Sommer-Wagner 2007). In addition, IBDV infection has been reported
 WORLD’S POULTRY SCIENCE JOURNAL 3

in ostriches (Gouch et al., 1998), Baltic ducks, Herring gulls (Hollmen et al., 2000) and
sparrows (AHA 2009). However, IBDV antibodies have been detected in pigeons
(Columba livia; Fagbohun et al., 2000a), village weavers (Ploceus cucullatus) and pied
cordon blues (Uraeginthus bengalus; Nawathe, Okonkwo, and Smith 1978), speckled
pigeons (C. guinea), laughing doves (Streptolepia senegalensis; Adamu, Balami, and Abdu
2017), Antarctic penguins (Gardner et al., 1997), and various raptors and passerines in
Japan (Ogawa et al., 1998). The virus has been detected in lesser mealworm (Alphitobius
spp.) fed on IBDV contaminated feed (Snedeker, Wills, and Moulthrop 1967).
Experimental IBDV inoculation of pheasants, partridges, guinea fowls and quails showed
no signs of IBD (Van Den Berg et al., 2001). Furthermore, viable IBDV has been isolated
from the faeces of dogs two days after oral inoculation with the virus, suggesting that
dogs could be potential carriers of IBDV (Torrents et al., 2004).

Cells attacked by infectious bursal disease virus

The macrophages and lymphoid cells of the gut mucosa are the targets for IBDV
infection and replication (Müller et al., 1979), while the B lymphocytes in the BF are
the targets for extensive replication of IBDV (Kaufer and Weiss 1980). Classical and
variant IBDV primarily attack immature B lymphocytes, while both immature and
mature B lymphocytes are targets for vvIBDV (Williams and Davison 2005).

Pathogenesis of infectious bursal disease

Following infection, IBDV is transported by infected macrophages to the BF where the
virus undergoes intracytoplasmic replication in IgM+ B lymphocytes (Hiraga et al.,
1994). In the BF, there is production of interferon-γ (IFN-γ) enhanced by the activation
of macrophages (Eldaghayes et al., 2006). This is accompanied by the release of proin-
flammatory cytokines such as interleukin-6 (IL-6) and nitric oxide (NO) (Eldaghayes et
al., 2006; Rauw, Lambrecht, and Van den Berg 2007). These cytokines may then exacer-
bate the bursal lesions (Kim et al., 1998). In addition, the IFN-γ produced during IBDV
infection may induce apoptosis of infected and surrounding healthy B-cells (Lam 1997;
Tanimura and Sharma 1998).
However, following infection of susceptible chickens by vvIBDV, dissemination of the
virus to other lymphoid organs, such as bone marrow, thymus, spleen, Peyer’s patches,
caecal tonsils and Harderian glands, has been reported (Eterradossi and Saif 2008). The
replication of IBDV at a later time may be supported by the caecal tonsils and bone
marrow (Elankumaran, Heckert, and Moura 2002). At 48 h post infection (pi), inflam-
mation of the BF occurs and at days three–four pi and cytolytic changes becomes
prominent in all infected bursal IgM+ B cells (Cheville 1967). At days 7–21 pi, there is
a significant reduction in the IgM+ B-cell population relative to IgA and IgG B cells, as
determined by flow cytometric analysis (Petkov et al., 2009). However, the mesenchy-
mally derived reticular cells residing in the bursal cortex, and periarteriolar lymphoid
sheaths, germinal centre (GC) and red pulp of the spleen have been reported to be
relatively resistant to IBDV (Biro et al., 2011). The disappearance of bursal follicular
dendritic cells in IBDV infection is thought to result from the absence of B-cell prolif-
erative environment (Jeurissen et al., 1998; Kabell et al., 2006).
4 O. ORAKPOGHENOR ET AL.

Clinical disease due to infectious bursal disease virus

The age and immune status of infected chickens (Iván et al., 2005), route of infection and
nature of the infecting viruses (Skeeles et al., 1979; Elankumaranet al., 2002) influence the
development of clinical signs of IBD and virus shedding. The incubation period of IBD
ranges from 2 to 4 days (Cosgrove 1962) and the most severe clinical signs are seen in
chickens infected between 3 and 6 weeks of age (Eterradossi and Saif 2008). However,
clinical signs are rare in chickens younger than 2 weeks and older than 6 weeks of age
(Vervelde and Davison 1997). In susceptible chicken flocks (3–6-week-old broilers and
replacement pullet flocks), acute clinical outbreaks of classical IBDV are characterised by
sudden onset, high morbidity, spiking mortality curves and a rapid recovery time of
about 5–7 days post clinical signs (Van Den Berg et al., 2000; Lukert and Saif 2003).
Within 2–3 days post-exposure of susceptible chickens to vvIBDV and classical
virulent strains, the sudden onset of depression with disinclination to move (Cosgrove
1962) and ruffled feathers have been reported (Van Den Berg et al., 2004). Reports of vent
pecking and staining of pericloacal feathers with urates have been documented
(Landgraf, Vielitz, and Kirsch 1967). There is an absence of clinical signs and mortality
in broilers with high maternal antibodies (MAB) levels following exposure to vvIBDV, as
reported by Van Den Berg et al. (2000). Furthermore, IBDV shedding in faeces for up to 2
weeks by naturally infected chickens and those birds vaccinated with live IBDV vaccine
have been reported (Kabell et al., 2005). The detection of faecal IBDV using RT-PCR for
up to 4 weeks have been documented (Kabell et al., 2005).

Gross pathological changes due to infectious bursal disease

The extent of tissue distribution and severity of lesions resulting from IBD has been
determined by the strains and pathogenicity of the infecting IBDV (Regenmortel 2003).
In chickens that died of acute IBD, dehydration of subcutaneous fascia and pectoral
muscles were observed (Cosgrove 1962). Haemorrhages in the thigh and pectoral mus-
cles, mucosa at the proventriculus-ventriculus junction and on the serosal surface and
plica of the BF have been reported (Hanson 1962; Oluwayelu et al., 2002).
The BF is the principal diagnostic organ in which gross pathological changes occur
during the course of an IBDV infection (Regenmortel 2003). There is rapid bursal
atrophy with or without inflammation following variant IBDV infection, while haemor-
rhagic inflammation of the BF occurs following vvIBDV infection (Lam 1997; Tanimura
and Sharma 1998). The bursal atrophy resulted from lymphoid cell depletion induced by
IBDV and is evident as early as 7–8 days pi (Cheville 1967). An increase in bursa to body
weight ratio usually due to bursal oedema has been reported (Lukert and Saif 2003). A
yellowish colouration of the serosal surface of the BF usually occurs due to the accumula-
tion of serous transudate resulting from marked inflammation of the bursal mucosa in
severe cases (Lukert and Saif 2003).
The kidneys, tubules and ureters may appear distended with deposition of urates
(Confer and MacWilliams, 1982). Increased mucus in the intestine in diseased birds and
renal changes probably result from dehydration, but these findings are not consistent
(Baxendale 2002; Etteradossi; Saif 2008). The spleen becomes enlarged with uniformly
dispersed small grey foci (Morales and Boclair 1993).
 WORLD’S POULTRY SCIENCE JOURNAL 5

Histopathological changes due to infectious bursal disease

The lymphoid structures primarily affected by IBDV are BF, spleen, thymus, Harderian
glands, caecal tonsils, gut-associated lymphoid tissue (GALT) and head-associated lym-
phoid tissues (HALT). Lymphocytic degeneration and necrosis in the medullary region of
the BF at 1 day pi are the first signs (Regenmortel 2003). This is followed by replacement of
depleted lymphocytes with heterophils, pyknotic debris and hyperplastic reticulo-endothe-
lial cells (Oluwayelu et al., 2002). The bursal follicles are later replaced by cysts lined by
columnar epithelium with fibroblastic interfollicular stroma (Okoye and Uzoukwu 1990).
The cystic cavities contain globules of mucin, which indicate regression of the inflamma-
tory reaction (Eterradossi and Saif 2008). There is appearance of scattered foci of lympho-
cytes in the bursal follicles during the recovery period (Eterradossi and Saif 2008).
The GCs of the spleen have been reported to show hyperplastic perivascular reticulo-
endothelial cells and lymphoid necrosis at 3 days pi (Helmboldt and Garner 1964). At 5
days pi, there is lymphocytic repopulation (Okoye and Uzoukwu 1990) with negligible
damage to germinal follicles (Cheville 1967).
A reduction in the number of plasma cells in the Harderian glands has been reported
following serotype 1 IBDV infection in broilers without maternal IBD antibodies
(Dohms, Lee, and Rosenberger 1981). Severe lymphoid depletion has been demonstrated
in the caecal tonsils, thymus, spleen and bone marrow and these depletions resulted from
vvIBDV infection (Eterradossi and Saif 2008). In addition, slight pervascular monocytic
infiltration may be seen in the liver (Peters 1967).

Outcomes of infectious bursal disease virus infection

The severity of clinical signs, lesions in organs and immunosuppression constitute the
outcomes of IBDV infection (Eterradossi and Saif 2008). The determinants of the nature
of these outcomes are immune status, age and genetic make-up of affected chickens and
virulence of the infecting IBDV strain (Van Den Berg 2000). In vvIBDV infected specific
pathogen-free (SPF) chickens, there have been reports of earlier onset of mortality and
more severe bursal lesions when compared to broiler chickens with maternal antibodies
or vaccinated chickens (Hassan, Afify, and Aly 2002; Aricibasi et al., 2010).
The aggravation of bursal lesions resulting from massive infiltration of mast cells has been
demonstrated in SPF chickens infected with vvIBDV, which suggested an acute hypersensi-
tivity response (Wang et al., 2008, 2012). The early onset of severe humoral immunosuppres-
sion due to B-cell depletion in younger chickens is induced by cytokine-mediated bursal
lesions (Rautenschlein, von Samson-himmelstjerna, and Haase 2007). However, predomi-
nant lesions have been reported in 3-week-old SPF layer type chickens compared to broiler
type chickens of the same age (Aricibasi et al., 2010). Permanent damage to immunologic
responses has been reported in IBDV infected susceptible neonatal chickens younger than 2
weeks of age, due to entire B-cells destruction (Withers, Young, and Davison 2005).

Convalescence from IBD infection

The functional restoration mechanisms of B cells have been described during convales-
cence from IBDV infection (Sharma et al., 2000). However, the restoration mechanisms
6 O. ORAKPOGHENOR ET AL.

of the T-cell immunological functions remain unclear (Williams and Davison 2005). The
bursal stem cells that survive depletion undergo proliferation to form new and larger
bursal follicles. These follicles become repopulated with IgM+ B cells, Bu-1+ cells
expressing IgM or IgY (Williams and Davison 2005) and dendritic-like cells (Withers
et al., 2005). The recovering follicles later express Lex and chB1 genes (Ivan et al., 2001).
This indicates conversion of the immunoglobulin (Ig) gene by B-cells to enhance Ig
diversity and immunological function specificity (Withers et al., 2005; Withers, Davison,
and Young 2006). In contrast, the lack of Ig gene conversion due to small follicles
formation from surviving medullary B cells leads to a lack of antibodies production,
thus suggesting a permanent immunosuppressive state (Withers et al., 2006).

Diagnosis of infectious bursal disease

Gross and histopathological examinations of the bursa are used to diagnose IBD in
young chickens or in those having maternal antibodies (Lukert and Saif 2003).
However, other methods used in diagnosis include isolation and detection of IBDV
using embryonated chicken eggs, cell culture, enzyme linked immunosorbent assay
(ELISA), reverse transcription polymerase chain reaction (RT-PCR; Abdel-Alim and
Saif 2001) and serology, such as virus neutralisation, indirect ELISA and agar gel
precipitation test (AHA 2009). Molecular detection and characterisation, involving
sequencing, and phenotypic and genotypic analyses have been utilised in the diagnosis
of IBD (Mawgod et al., 2014; Msomi et al., 2018). Restriction fragment length
polymorphism (RFLP) profiles and nucleotide sequence could be used to predict
relative differences between IBD strains, but in vivo testing is essential for the detec-
tion of the actual antigenic differences (Jackwood and Sommer-Wagner 2002).
Furthermore, there a multiplex RT-PCR test capable of differentiating between
IBDV virus serotypes (Lin et al., 1994), a multiplex real time quantitative RT-PCR
for detection of RNA levels in blood from infected chickens using Taq-Man® technol-
ogy (Moody, Sellers, and Bumstead 2000), and a quantitative competitive PCR (QC-
PCR; Wu, Lin, and Akin 1997) test for estimating viral genomic copy number.

Control and prevention of infectious bursal disease

The IBDV is contagious and contact with infected birds and contaminated fomites
could result in the spread of infection (AHA 2009). The virus is environmentally
stable and resistant to many chemical and physical agents (Eterradossi and Saif
2008). Its spread between flocks can be restricted through implementation of strict
biosecurity measures (Lukert and Saif 2003; Saif 2008). However, with the integrated
nature of commercial poultry operations, litter reuse and the possibility of interac-
tion with free-living wild birds, the control of IBD faces difficulties (AHA 2009).
The use of therapeutic treatment has been reported to have no effect on the course
of infection (Cosgrove 1962; Lukert and Saif 2003).
The prevention of IBD outbreaks in the field has been achieved globally through
vaccination (Yamaguchi et al., 1996). Commercially available vaccines against IBDV are
live attenuated and inactivated vaccines, whereas, in some countries, the use of recombi-
nant and subunit vaccines has been licenced (Jackwood and Sommer-Wagner 2002).
 WORLD’S POULTRY SCIENCE JOURNAL 7

Based on the level of attenuation and residual virulence for SPF chickens, live vaccines
have been classified into mild, intermediate or intermediate-plus vaccines (Van Den Berg
et al., 2000). The intermediate-plus vaccines are regularly applied to protect chickens
against vvIBDV challenges. The Deventer formula may help to determine the optimal
time for IBDV vaccination to circumvent the neutralising activity of MAB (de Wit 1998).
Live vaccines induce strong humoral and cellular immunity and are favourable when
mass application is used in drinking water (Mülleret al., 2003; 2012). However, there is
a possible reversion to virulence and residual immunosuppressive effects
(Rautenschlein et al., 2005; 2007) in extensive field applications. The priming of
breeders using live vaccines, which is boosted with inactivated oil-emulsion vaccines
prior to laying, ensures transfer of higher levels of MAB to the progeny (Maas et al.,
2001; Müller et al., 2012) and this has been applied in some countries. In addition,
commercially available IBD immune complex (IBD-ICX) vaccines have been found to
be safe and efficacious for in ovo and post-hatch vaccination of broilers (Giambrone,
Dormitorio, and Brown 2001; Iván et al., 2005). These IBD-ICX vaccines are prepared
by combining an IBDV-hyperimmune serum with live intermediate-plus IBDV
(Whitfill et al., 1995; Johnston et al., 1997). The immune enhancing mechanism of
the IBD-ICX vaccines may be due to the entrapment and retention of ICX on bursal
follicular dendritic cells (FDCs) and on splenic FDCs in the GC (Jeurissen et al., 1998).

Conclusions
IBD is important to the poultry industry, as it causes welfare problems and great
economic losses. The disease is characterised by bursal lesions and atrophy and the
resulting immunosuppression predisposes birds to secondary opportunistic infections.
IBDV is ubiquitous and effective vaccinations and strict biosecurity measures are
required for its control. The roles of wild birds in the epidemiology of the disease need
to be elucidated due to their direct and indirect interactions with commercial poultry.

Disclosure statement
No potential conflict of interest was reported by the authors.

Notes on contributors
Ochuko Orakpoghenor is a researcher at Veterinary Pathology, Ahmadu Bello University, Zaria,
Nigeria.
Sunday B. Oladele is a professor of Veterinary Pathology, Ahmadu Bello University, Zaria,
Nigeria.
Paul A. Abdu is a professor of Avian Medicine, Ahmadu Bello University, Zaria, Nigeria.

ORCID
Ochuko Orakpoghenor http://orcid.org/0000-0003-0833-1640
8 O. ORAKPOGHENOR ET AL.

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