World Applied Sciences Journal 16 (8): 1123-1130, 2012

ISSN 1818-4952
© IDOSI Publications, 2012

Hemorrhagic and Clotting Abnormalities in

Infectious Bursal Disease in Specific-Pathogen-Free Chicks
1
Tesfaheywet Zeryehun, 2M. Hair-Bejo and 2A. Rasedee

1
College of Veterinary Medicine, Haramaya University, P.O. Box: 301, Dire Dawa, Ethiopia
2
Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400, Serdang Selangor, Malaysia

Abstract: Investigation to know the hemorrhagic and clotting mechanisms in very virulent (vv) infectious
bursal disease virus (IBDV) infection of Malaysian isolate was carried out in chicks. One-hundred-ten, 32-day-
old Specific-pathogen-free chicks were divided into IBD and control groups, each consisting 55 chicks.
The IBD group was inoculated orally with 0.1 mL/chick of inoculums containing vvIBDV isolate with a titre of
106.8 EID50/mL, while the other group served as controls. Four chicks each in IBD and control groups were
sacrificed at 1, 3, 6 and 12 hours and days 1, 2, 3 and 4 post-infection (pi). Blood sample were collected for
thrombocyte count and coagulation tests prior to necropsy. On necropsy gross lesions were recorded.
The IBDV infected chicks showed clinical signs of acute disease starting day 2 pi. At days 3 and 4 pi significant
(p<0.05) thrombocytopenia and prolonged activated partial thromboplastin time (APTT), prothrombin time (PT)
and whole blood recalcification time (WBRT) were recorded corresponding to the occurrence of higher
frequency of hemorrhage in the bursa of Fabricus, thigh muscle and mucosal junction between proventriculus
and gizzard, which indicate the presence of clotting deficiency. Hence, it was concluded that the vvIBDV of
Malaysia isolates caused clotting abnormality that are consistent with the pathogenesis of the disease and it
appears that this abnormality in vvIBDV infection could be due to thrombocytopenia and/or coagulation factors
deficiencies, or both.

Key words: SPF Chicks VvIBDV Hemorrhage Clotting Abnormalities Coagulation Deficiencies

INTRODUCTION were reported in the country [7-8]. Exhaustion,

Infectious bursal disease (IBD) is a highly
contagious, globally occurring acute viral disease in
susceptible chicks. The causative agent is a bisegmented,
double stranded RNA virus that belongs to the genus
Avibirinavirus family Birnaviridae. The disease is
economically significant to the commercial poultry
industry through the mortality, reduced weight gain and
condemnation carcass due to marked hemorrhage in the
skeletal muscle as well as due to secondary losses
resulting from immunosuppression [1-3]. Two distinct
serotypes of IBDV namely, serotypes 1 and 2 are
identified. The serotype 1 is pathogenic to chick and
classified as classical (c), variant (va) and very
virulent (vv) IBD virus (IBDV) [4]. Clinical IBD typically
occurs in 3 to 6-week-old chick that can result in
significant mortality and transient immunosuppression
[5] is caused by either vvIBDV or caIBDV of serotype 1
[6]. In Malaysia, till to date, only vvIBDV and caIBDV
prostration, dehydration, diarrhoea, pasty vent and
even death are among the clinical signs in the clinical
form of the disease [9]. A variable degree of petecchial
and ecchymotic hemorrhage in the bursa of Fabricus,
at the thigh and pectoral muscle and at the mucosa
junction between proventriculus and gizzard are typical
gross lesions in acute IBD [8-10]. However, few studies
have tried to demonstrate the actual causes of
hemorrhage. Thus, this study seeks to determine
hemorrhage and clotting abnormalities in specific-
pathogen-free (SPF) chicks infected with vvIBDV isolate
of Malaysia.
MATERIALS AND METHODS
Study Chicks: A total of one-hundred-ten 32-day-old
(SPF) chicks were divided into two groups, namely the
IBD (55 chicks) and control (55 chicks) groups, were used
in the study.

Corresponding Author: Tesfaheywet Zeryehun, Department of Parasitology and Pathology, College of Veterinary Medicine,
P.O. Box: 301, Dire Dawa, Ethiopia.
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Virus Isolate and Inoculum: The vvIBDV isolate, namely
UPM0081 isolate in 0.1 ml phosphate buffer saline
(1:2 w/v) which was first passage once in the natural host
and twice in SPF embryonated egg was used in this study.
The inoculums was prepared from the chorioallantoic
membrane (CAM) of 9 to 10 days old SPF embryonated
egg by the method described by Senne [11] and the virus
titer of the inoculums was determined to be 106.8 EID50 by
a previously described method [12].
Experimental Design: One-hundred-ten, 32-day-old SPF
chicks used in the study, 55 of which acted as control and
the remaining 55 were inoculated orally with the 0.1 ml
(virus titre of 106.8 EID50) of inoculums containing the
vvIBDV. Sampling of chicks was scheduled at 1, 3, 6 and
12 hrs and days 1, 2, 3, 4, 5, 7, 10 post-infection (pi);
however, because of the death of most chicks in the
IBD groups beyond day 4 pi the experiment was
terminated at day 4 pi. After blood sample was collected,
four birds from both groups were sampled at 1, 3, 6 and
12 hrs and days 1, 2, 3 and 4 pi, weighed, sacrificed
humanly by cervical dislocation and necropsied. Blood
was collected from the jugular vein for the determination
of thrombocyte count and coagulation analytes prior to
necropsy. At necropsy hemorrhage in the different organs
and there frequency were recorded.
Thrombocyte Count: Two ml of blood was collected from
the jugular vein using 25G needle and was transferred to
a 4 mL tube containing 1.5 mg di-potassium
ethylenediamine tetra acetate (K2 EDTA). The blood
specimen was kept at room temperature until processing
and was immediately analyzed within 24 hours using
automatic hematologic analyzer (Cell Dyne 3700,
Abbot Diagnostics, USA) using standard reagents
(Abbot Diagnostics, USA) was used to determine the
total thrombocyte per µl of blood.
Determination of Coagulation: Another 4.5 ml of blood
was collected from the jugular vein using 25G needle and
5 ml syringe and 9 part of blood was placed in a
siliconized vacuumed tubes containing 1 part of 3.8% of
sodium citrate (0.109M). The plasma was then harvested
by spinning the blood in a centrifuge at 5000 revolution
per minute (rpm) for 5 minute. The harvested plasma was
transferred into polypropylene tubes using a plastic
pipette and stored at 4°C in a refrigerator for 3 hrs and it
was immediately used for the determination of
prothrombin time (PT), activated partial prothrombin
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time (APTT) and whole blood recalcification time
(WBRT). The APTT (STA-CK Prest®) and PT (STA®-
Neoplastine® Cl Plus) by the aid of semi-automated
analyzer (STA® analyzer) using standard reagents
(Abbot Diagnostics, USA), by the method described by
[13], while the WBRT was determined manually by the
method described previously [14].
Statistics: Mean values obtained for thrombocytes,
WBRT, PT and APTT were analyzed using SPSS v.17.01
and Duncan’s multiple range tests was used by the way
of analysis of variance (ANOVA) and values were
regarded as significant at p < 0.05.
RESULT
The IBD affected chicks showed non-specific
signs including prostration, depression, diarrhea,
anorexia and vent picking starting day 2 pi and death
characterized by a spiking mortality was observed at days
3 and 4 pi where 4 and 7 chicks died respectively, in the
IBD group.
There were no apparent gross lesions and evidence
of hemorrhage observed from 1 hr until days 2 pi in the
IBD group. Significant hemorrhagic lesions were observed
starting day 3 pi in both sacrificed and dead chicks and
the lesion characterized typically of acute hemorrhagic
bursitis. In this organ both the serosal surface and the
mucosal plica showed significant congestion and
hemorrhage. The hemorrhage was even severe at day 4 pi
in both sacrificed and dead birds. During this time,
besides the BF, hemorrhage was also witnessed at the
thigh muscle and mucosal junction between
proventriculus and gizzard (Figure 1). Furthermore, a
variable frequency of hemorrhage was observed in the
present study, the highest proportion being in dead birds
when compared with the sacrificed birds (Table 1).
Histologically, hemorrhage was clearly evident in the
bursa of two chicks at day 4 pi. These lesions were
characterized by adhesion of blood cells on the wall of
blood vessel as well as area of discontinuity of blood
vessel. Moreover, RBC’s was observed leaving the blood
vessel was also evident (Figure 2).
Although thrombocytes count remained lower than
the control group from 1 hr pi until day 1 pi; however,
there was no significant difference (p>0.05) between the
two groups during this period. Nonetheless, statistical
significance (p<0.05) in the thrombocyte count was
recorded at days 2, 3 and 4 pi.
 World Appl. Sci. J., 16 (8): 1123-1130, 2012

Table 1: The frequency of hemorrhage in the bursa of Fabricus, thigh muscle and mucosal junction between proventriculus and gizzard in the sacrificed and
dead chicks throughout the trial
Organs
---------------------------------------------------------------------------------------------------------------------------
Sampling time (pi) Chicks Bursa of Fabricius Proventriculus and gizzard junction Thigh Muscle
1 hr Sacrificed 0a/5b 0/5 0/5
Dead NA NA NA
3 hrs Sacrificed 0/5 0/5 0/5
Dead NA NA NA
6 hrs Sacrificed 0/5 0/5 0/5
Dead NA NA NA
12 hrs Sacrificed 0/5 0/5 0/5
Dead NA NA NA
Day 1 Sacrificed 0 /5 0/5 0/5
Dead NA NA NA
Day 2 Sacrificed 0/5 0/5 0/5
Dead NA NA NA
Day 3 sacrificed 2/5 1/5 2/5
Dead 5/5 2/5 3/5
Day 4 Sacrificed 3/5 2/5 2/5
Dead 7/8 6/8 5/8
Number positive for the lesion
a

Total number of chicks necropsied

b

NA: Not available. Death of chickens started 3 days pi

Fig. 1: The mucosal surface of bursa of Fabricus (A) in the control group; severe hemorrhagic bursitis showing
hemorrhagic and congested plicae of mucosa surface of bursa of Fabricius (B); Petechial to ecchymotic
haemorrhage in the thigh muscle (C) and the mucosal junction between the proventriculus and gizzard (D) in the
IBD group at days 3 pi.

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Fig. 2: The bursa in the control group: large active follicles consist of lymphoid cells with little inter-follicular tissue.
The covering epithelium is simple columnar, HE. Bar 100µm. (A). Severe hemorrhage mixed with fibrinous
exudates in the interstitial space of the bursa of Fabricus, at day 3 and 4 pi in the IBD group. HE. Bar 100µm. and
margination of the red blood cells (RBCs) in the endothelial wall. A break on the wall of the endothelium (black
arrow) and RBCs escaping through a discontinued endothelial wall (yellow arrows) of the bursa of Fabricius (C)
in the IBD group at day 4 pi, HE. Bar 20µm.

In the present study, as it is shown in the days 2 pi. However, at days 3 pi the WBRT, PT
Figures 4, 5 and 6, there was no significant and APTT were significantly longer (p<0.05) in
(p>0.05) difference between the IBD and control the IBD group compared with the control
groups in the WBRT, PT and APTT from 0 hr to group.

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Fig. 3: Thrombocyte counts in the infectious bursal disease and control groups throughout the trial.

Table 2: The WBRT, PT and APTT (mean±SD) in the control and IBD groups throughout the trial
WBRT (Min) PT (Sec) APTT (Sec)
------------------------------------ ---------------------------------------- ----------------------------------------
Sampling time Control IBD Control IBD Control IBD
1 hr 4.12±0.27 3.90±0.34 96.60±8.36 91.76±5.140 77.32±9.770 73.54±13.37
3 hrs 4.10±0.93 5.06±0.39 99.80±4.91 96.70±7.500 78.84±14.55 80.14±10.30
6 hrs 5.02±1.20 4.06±0.40 95.46±9.20 97.74±8.190 79.90±19.96 82.32±16.79
12 hrs 6.06±1.02 5.28±0.86 100.48±9.27 99.38±8.590 80.72±7.420 85.26±6.760
Day 1 4.58±0.63 3.10±1.05 102.56±6.03 100.34±4.600 81.34±10.20 83.30±8.890
Day 2 3.94±1.05 3.46±1.08 111.30±8.29 100.48±9.270 99.18±7.450 100.20±20.18
Day 3 3.96±0.63 7.90±0.61a 104.80±5.18 150.30±13.29a 99.86±5.310 198.92±13.02 a
Day 4 4.42±0.80 7.26±1.20 a
100.58±4.61 138.24±15.43 a
102.68±9.010 208.70±14.65 a
Each value represents the Mean ± SD of five chickens
: statistically significant compared with the control group (p<0.05)
a

WBRT = whole blood recalcification time

PT = prothrombin time
APTT = activated partial thromboplastin time

DISCUSSION and eccymotic hemorrhage in the BF, at the musculature,

The vvIBDV isolate of Malaysia namely, UPM04190
and UPM0081 have successfully infected the SPF
chickens and revealed typical clinical signs characterized
by diarrhea, dehydration, anorexia, depressions as well as
death at days 3 and 4 pi, which was consistent with acute
IBDV infection [15] and this finding is consistent with
field IBD outbreaks [16].
Among the gross changes in the necropsied chicks,
hemorrhage and congestion in the BF was presented
among the most important lesions in the present study.
Though the frequency of hemorrhage was shown to be
higher in the BF, similarly a good number of the thigh
muscle and mucosal junction between proventriculus and
gizzard in the infected chicks also revealed variable
hemorrhage and congestion at days 3 and 4 pi. Petecchial
especially at the thigh muscle and the mucosa at the
junction of proventriculus and gizzard [2, 10, 17-18] has
been reported. The frequency of hemorrhage in the BF,
thigh muscle and mucosal junction between
proventriculus and gizzard was higher in the dead chicks
than that of sacrificed ones. This might suggest that
hemorrhage could be a most important risk factor to
mortality.
Histology of the BF at days 4 pi revealed congested
blood vessels and hemorrhagic bursa with some activity
of RBCs escaping through damaged blood vessel wall.
These strongly suggested damage to the blood vessel
and a possible disseminated intravascular coagulation
(DIC). A histologic evidence of DIC is common to see in
diseases of chicks characterized by hemorrhage, among
others highly pathogenic influenza, bacterial infection

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such as Erysipelothrix rshusiopathie and bacterial
vasculitis [19-21]. Dos-Santos et al. [22] suggested an
immune mediated damage to the blood vessel in IBDV
infection which is mainly due to the effect of macrophage
derived tumor necrosis factor (TNF) and interleukins.
Shibatani et al. [20] has also suggested possibility of DIC
to be cause of hemorrhage in IBDV infection.
The present study revealed a significant
thrombocytopenia in the chicks suffering from IBDV at
days 3 and 4 pi. This finding agreed with previous report
elsewhere [23]. In contrast, Lima et al. [24] observed
normal thromboctye count and this discrepancy could be
due to the strain variation used in the study.
Thrombocytopenia in birds is an indicator of haemostatic
disorder which usually follows excessive peripheral
demands for thrombocytes [21]. Hence, these results
suggested that the thrombocytopenia might be due to
damage to the blood vessels, whereby thrombocytes are
being mobilized for the reparative process.
Thrombocytopenia in chicks has been reported in
diseases like classical swine fever [25], Newcastle disease
[26] and avian influenza [19] which are characterized by
severe hemorrhage.
The delayed WBRT, PT and APTT at days 3 and 4 pi,
in the present study could be due to a coagulopathy
affecting all three (intrinsic, extrinsic and common)
clotting pathways [27-28]. Similarly, Skeeles et al. [29]
documented clotting deficiency characterized by
prolonged WBRT, PT and APTT in IBDV infection
elsewhere. The PT and APTT are useful for preliminary
but holistic assessment of the status of the coagulation
cascade [30]. The WRCT is a measures the intrinsic
pathway [29]. While PT is the measure of the extrinsic and
common coagulation pathway, APTT is a measure of the
intrinsic and common coagulation pathways [31]. Thus
the prolonged WBRT, PT and APTT indicate coagulation
deficiencies. These analytes singly or together with other
factors have been an indicator of coagulation deficiencies
of various natures in mammals and birds. Coagulation
characterized by prolonged WBRT and/or PT and APTT
in DIC, diseases like Erysipelothrix rshusiopathie [20],
infection with avian influenza [19], fowl cholera in turkeys
[32] and in conditions like hepatocellular inflammation and
inflammation [33]. Hemorrhagic diathesis and mortality
which invariably occurs in infection of chickens with
vvIBDV was postulated to have been resulted from
clotting abnormality [14, 29]. Thus the presence of
hemorrhage in the face of the gross and histopathology
in the bursa of Fabricius, at the mucosal junction between
proventriculus and gizzard and muscle visa vi significant
elevation of WBRT, PT and APTT in the present study
1128
strongly suggest that hemorrhage in IBDV is the result of
combination of factors particularly thrombocytopenia
and/or coagulation factors deficiency.
Hence it was concluded that vvIBDV of the
Malaysian isolate (UPM0081) causes hemorrhage in SPF
chicks and the cause of hemorrhage could be due to
clotting deficiency following either thrombocytopenia
related to DIC or injury to blood vessel or secondary
coagulation defect characterized by prolonged WBRT,
APTT and PT, or the combined effects of all these factors.
Further, the present study suggests that hemorrhage is an
important risk for mortality and this strongly upholds the
contribution of blood coagulation disorders in the
pathogenesis of the disease.
ACKNOWLEDGEMENT
This project was supported by Research
University Grant Scheme (RUGS), Universiti Putra
Malaysia, Malaysia.
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