Natural and Experimental Infections of Quails (Couturnix ... · PDF fileNATURAL AND...

SCVMJ, IVX (2) 2009 67

NATURAL AND EXPERIMENTAL INFECTIONS OF

QUAILS (COUTURNIX COUTURNIX JAPONICA) WITH

NEWCASTLE DISEASE VIRUS

El-Tarabili M. M.*, El-Shahiedy M. S.*, Hammouda M. S.**, Fetaih H.

A.***, Abdel-Wahab Shahira A.* and Ramzy Neven M. ****

* Dept. of Virol., Fac. of Vet. Med., SCU. ** Animal Health Research

Institute, Dokki. *** Dept. of Pathol.. Fac. of Vet. Med., SCU

**** Lab. of Anim. Health Res. Inst., Ismailia.

ABSTRACT

This study was carried out to clarify the susceptibility of quails to

the infection with Newcastle disease (ND) virus and its possible role in the

epidemiology of the disease. Also to locate the virus in tissues and organs

of naturally and experimentally infected quails. Isolation and characteri-

zation of the ND virus quail strain from naturally infected quails was done.

Twenty diseased quails aged 3 weeks-old, showing mild respiratory and

nervous manifestations were obtained from the farm of the Faculty of

Agriculture, Suez Canal University that was suffering 10% morbidity and

1.6% mortalities, were investigated. NDV was isolated from 3 birds out of

them. The isolated strain was mesogenic and used for experimental study.

The experimental infection caused deaths in 25% of the experimented

quails after one week. The serological tests including HI, HA, AGPT and

inoculation in specific pathogen free (SPF) embryonated chicken eggs

(ECE) were used for diagnosis and virus isolation along this study. In

addition, gross and histopathological investigations of different organs were

carried out. All changes in the HI titres, and changes in the body tissues

were recorded.

INTRODUCTION

Newcastle disease (ND) is a

major disease problem of poultry in

many countries of the world, espec-

ially in Africa and Asia (Spradbrow

1992, Awan et al. 1994 and Oladele

et al 2005). Over 200 species of

birds have been also reported to be

susceptible to natural and/or exper-

imental infection with ND virus.

Birds other than domestic chickens

have been known to be sources of

the spread of ND virus (Lancaster,

1963, Roy et al 1998). ND is comp-

licated so that different isolates and

strains of the virus may induce eno-

rmous variations in the severity of

68 El-Tarabili, et al.,

disease even in a given host such as

the chickens (Beard and Hanson 1984).

Concerning quails, Lima et al (2004)

considered them as important carr-

iers for ND virus. On the other ha-

nd, Higgins and Wong (1968) and

Higgins (1971) stated that quails are

rather resistant to NDV infection;

but they may become infected under

stress conditions. In other studies,

quails were found to acquire the nat-

ural infection with a velogenic strain

of ND virus (CzirJac et al 2007,

Lima et al 2004 and Sa'idu 2004).

In Egypt, (Assiut province) El-

Zanty and Abd-El-Motelb (1993)

recorded a viscerotropic velogenic

ND in quails (Coturnix coturnix jap-

onica). A natural infection occurred

in young and adult quails. The clini-

cal, postmortem changes and chara-

cterization of the virus were descr-

ibed. Oladele et al (2008) recorded

the histopathological and HI anti-

body titer in Japanese quails experi-

mentally infected with NDV. The

infected quails developed ND with

classical clinical signs and lesions

which included focal necrosis in

most of the organs, mononuclear ce-

lls infiltration and depletion of lym-

phoid tissues. There was a rise in HI

titer from zero to maximum mean

antibody titer of 10 log2. Sa'idu

(2004) studied the serological evid-

ence of ND in quails in Nigeria and

detected infection in 12% on exam-

ined birds with low mean HI titre

(0.4 log2). Czirjak et al. (2007)

recorded 100% morbidity and

mortality in an outbreak of ND in

quails with severe clinical sympt-

oms and pathological lesions in both

digestive and nervous systems. Ucan

and Catatoluk (2002) concluded that

the breeding of quails and chickens

together in the same house could be

a way of exposing chickens to the

threat of ND virus outbreaks poss-

essing more virulent character.

Peroulis and O'Riley (2004) isola-

ted and characterized avian paramy-

xoviruses in quails based on their

haemagglutination and –haemagglu-

tination-inhibition activity using a panel

of antisera. PMV-1 was isolated fr-

om examined quails.

There is a contradiction in the res-

ults of previous studies and still sca-

rce information present about the

disease in quails. Therefore, the pre-

sent work was designed to deter-

mine the clinical picture and tissue

changes due to ND virus infection

in quails, changes in the HI antibody

titre in the natural and experimental

infections as well as isolation and

characterization of the virus.

MATERIAL & METHODS

1- Field study:

1- a- Quails:

A farm belonging to Faculty

of Agriculture, Suez Canal Unive-

rsity, containing about 5000 quails

(Couturnix couturnix japonica) was

kept under observation for 2 weeks.

There were 10% morbidity and

1.6% mortality, and the initial

diagnosis was directed towards the

SCVMJ, IVX (2) 2009 69

Newcastle disease. Twenty diseased

quails, 3 weeks-old, showing mild

respiratory and nervous symptoms

were submitted to the laboratory for

serum samples and tissue specimens

collection.

1- b- Serum Samples:

A total of 40 serum samples were

collected, including 20 blood sam-

ples from quails at acute stage and

20 samples of the same quails 2

weeks later. The samples were taken

for serological screening of antibod-

ies against ND virus in acute and

convalescent stages.

1- c- Serological Screening of ND

virus antibodies in serum:

Antibodies against ND virus were

screened in the collected serum sa-

mples using haemagglutination inhi-

bition test (HI).

1- d-Postmortem examination and

tissue specimens for virus isola-

tion:

After postmortem examina-

tion, pooled samples of liver, spl-

een, lung, kidneys and cecal tonsils

of each bird of the 20 quails were

finely minced, frozen and thawed 3

cycles. The inoculums were prepa-

red as usual and kept for weeks or

days at -70c until used for egg ino-

culation.

1- e- Inoculation of SPF embryonated

chicken eggs (ECE): Twenty SPF

embryonated chicken eggs were

used for each sample. The eggs

were supplied by "Abbasia Laborat-

ories for Serum and Vaccine Pro-

duction". The eggs of 3 days old

embryos were candled to exclude

the infertile eggs and dead in shell.

At 9 days old embryos, 10 eggs

were inoculated with 0.2 ml/egg by

allantoic sac route and another 10

eggs were inoculated onto chorioa-

llantoic membrane.

1- f- ND virus identification:

1- f- 1- Agar gel precipitation test:

Agar gel precipitation test was used

for identification of ND virus quail

isolates and detection of ND antibo-

dies in serum of experimentally inf-

ected quails. The test proper is done

according to Woerle (1963).

1- f- 2- Haemagglutination test :

Allantoic fluid of inoculated eggs

that suspected to contain ND virus

is subjected for detection of haema-

gglutinating property. The test was

carried out by 2 means, rapid slide

agglutination test and microtitre pla-

te method.

1- g- NDV antigen preparation:

1- g- 1- Agar gel precipitating

antigen: was prepared from harv-

ested chorioallantoic membranes th-

at showed hemorrhagic spots and

inflammation with early embryonic

death Woerle (1963).

1- g- 2- Haemagglutinating anti-

gen preparation: Allantoic fluid of

inoculated eggs were used as haem-


agglutinating antigen Allan and Go-

ugh (1974).

1- h- Titeration of NDV quail

strain and reference NDV in SPF

– ECE: ELD50 was calculated acc-

ording to formula of Reed and Mu-

nch (1938).

1- i- Strain variability and charac-

terization:

The obtained ND virus quail strains

were tested to distinguish the patho-

type of the isolates. Mean death

time of the minimum lethal dose, th-

ermo-stability of haemagglutinin and

agglutination of mammalian erythr-

ocytes were used to determine ND

virus pathotypes according to the

method of Rosenberger et al (1975)

and Islam et al (1994).

2- Experimental study: This was

performed after the isolation and ch-

aracterization the virus from the nat-

urally infected quails, to study the

pathogenicity of the isolated ND vi-

rus quail strain in quails.

2- a- Experimental design:

Thirty six healthy native quails (Co-

uturnix couturnix japonica), aged 3

weeks-old were randomly divided

into 4 groups: The first group (gp I):

12 quails received 0.2 ml of NDV

quail strain of titer 107 ELD50 /ml,

intraperitoneally. The second group

(gp II): 12 quails received the same

dose, intraocular. The third group

(gp III): 6 quails, received the same

dose but of VVND virus reference

chicken strain, intraocular for comp-

arison. The fourth group (gp IV):

contained 6 quails as non infected

control group, injected intraperiton-

ially only with sterile saline.

Quails in each group were kept in a

separate room and separate cages.

All quails were kept at restricted hy-

gienic measures and supplied water

ad libitum and non drug suppleme-

nted ration for 5 weeks. All quails

were observed daily for presence of

clinical signs or death. Serum and

tissue samples were collected wee-

kly. Serum was used for mean HI

antibody titre determination of all

birds. Part of the tissue samples was

kept frozen at -20 °C for ND virus

reisolation, while the other part was

taken for histopathological examin-

ation.

2- b- Pathological examination:

Four quails from gps (I and II) were

taken every week for pathological

investigations. The other 2 groups

were subjected to the same inves-

tigations at the end of the experi-

ment.

Specimens from lungs, heart, liver,

kidneys, spleen, brain, intestine and

proventriculus of each quails were

taken at necropsy and immediately

fixed in 10% neutral buffered form-

alin for 24 hours. The specimens

were then processed by the conven-

tional methods, embedded in para-

ffin wax, sectioned at 4-5 microns

and stained with the routine stain

SCVMJ, IVX (2) 2009 71

H&E, according to Drury and Wa-

llington (1980).

RESULTS

Clinical signs of naturally infected

quails: The affected birds showed

loss of appetite, abnormal thirst, hu-

ddling and weakness. Some birds

showed mild respiratory dyspnea

and gasping with coughing and sn-

eezing. The morbidity occured in

10% of quails. The affected quails

started to die after 1 week from on-

set of the disease. Mortality rate was

80/5000 with a percentage of 1.6%.

Postmortem lesions of naturally

infected quail: Postmortem exami-

nation of dead quails showed infla-

mmatory and focal hemorrhagic les-

ions in the respiratory system. Liver,

spleen, kidneys and heart showed

occasionally hemorrhagic spots on

the serosal surface, enlargement in

size and pale discolouration. No ob-

vious postmortem changes were ob-

served in alimentary tract.

Results of Serological screening of

naturally infected quails: Forty se-

rum samples were collected during

the acute phase of the disease and

another 40 samples were collected

during the convalescent phase 2

weeks later. As shown in table (1),

seroconversion of NDV antibodies

were observed between the two

stages.

Table (1): HI antibody titer and agar gel precipitating antibodies to

NDV in the quail's farm: Antibodies in acute stage Antibodies in convalescent

stage

Mean HI antibody titer 25 (1/32) 28 (1/256)

*AGP antibodies + +++

* AGP = agar gel precipitating antibodies.

Isolation and characterization of

NDV from the quails: After the

third passage of 20 inoculums pre-

pared from tissues of naturally infe-

cted birds, in SPF-ECE, 15 samples

gave haemagglutination results for

chicken RBCs with HA titer ranged

from 1/8 to 1/2048 dilutions and the

embryo death rate was 35/100. Six

samples were positive with the agar

gel precipitation test, but 3 only of

them were strong positive. So, ND

virus was successfully isolated from

3 quails (Srtains N0. 8, 18 & 19).

Titration of NDV quail strains

and reference NDV strains: After

three passages of the virus in SPF

embryonated chicken eggs, the obta-

ined results are shown in table (2).


Table (2): Titers of NDV quail and reference strains in embryonated

chicken eggs: ND virus strain First

Passage

Second

Passage

Third

Passage

ELD

50/ml

HA

titer

ELD

50/ml

HA

titer

ELD50/ml HA

titer

NewJersy LaSotastrain

VVND strain

NDV quail strain 18

NDV quail strain 19

NDV quail strain 8

*106

104

103

105

105

1/1024

1/2048

1/512

1/1024

1/1024

107

106

105

107

106

1/1024

1/2048

1/1024

1/1024

1/1024

108

108

107

108

107

1/2048

1/2048

1/1024

1/2048

1/2048

* Titer are expressed log10 ELD50/ml.

Determination of NDV virulence

quail strains: The mean death

times of minimal lethal dose of the 3

strains were 70, 80, and 75 hours,

the haemaglutinin was not stable at

56 oC for 5 minutes and haemagglu-

tination of mammalian erythrocytes

(equine and bovine RBCs) was neg-

ative. Therefore, the isolated NDV

quail strains were found to be meso-

genic strains, according to the kno-

wn parameters used for determin-

ation of NDV virulence.

Pathogenicity of NDV quail strain

in experimentally infected quails:

Clinical signs and mortalities:

Clinical signs were observed only in

quails inoculated intraperitoneally

(gp I). The signs included: general

weakness, loss of appetite, unthri-

ftness, dropped wings (Fig.1) and

mild respiratory manifestations as

coughing and gasping with respi-

ratory rales. There were no obvious

digestive symptoms. The morbidity

rate was the same like the mortality

rate. Mortalities occurred only in the

same group, 3 quails in the 1st week

PI (25%) and one quail in the 2nd

week PI (8.3%). In gp (II) that was

inoculated intraocular, no deaths

occurred. Five days post infection of

gp (III) with VVND virus chicken

stain, only one bird died.

Mean HI antibody titer and virus

reisolation: Mean HI antibody titer

and virus reisolation from tissues

and organs of quails experimentally

infected with ND virus quail strain

in gp (I) and VVND virus reference

virus in gp (III) were shown in table

(3). Results of the gp (II) inoculated

intraocular, were negative.

SCVMJ, IVX (2) 2009 73

Table (3): mean HI titre and virus isolation of intraperitonially infected

group with NDV quail strain and infected group with VVNDV

chicken strain: Times

postinfection & post

Challenge

Intraperitoneal infection group (gp I)

Group infected with VVND chicken strain

(gp III) Mean

HI Titer Log2

Virus Isolation

Mean HI Titer

Log2

Virus Isolation

1st week PI

2nd

week PI 3

rd week PI

0 1/128 1/128

+ + -

1/64 1/1280

+ +

Pathological changes: Postmortem

examination of all groups revealed

pathological lesions only in quails

of groups I & II (gp I & gp II) and

only in the first two weeks PI. After

the 3rd

week PI the remaining quails

appeared normal on gross examina-

tion. The detected pathological lesi-

ons were severe to moderate in dead

or moribund quails of the group ino-

culated intraperitoneally (gpI), whi-

le they were mild to non significant

in gp (II) inoculated intraocular. Gr-

ossly, there were generalized conge-

stion of the internal organs, petec-

heal hemorrhages on the serosal

surface of digestive tract, particula-

rly proventriculus, also on pancreas

and on trachea. Dark red pneumonic

areas (Fig. 2) and occasionally nod-

ular lesions were seen in the lung.

Enlargement of liver, spleen, kidn-

eys with pale discoloration were

also observed. Heart was, some-

times, suffering from enlargement

and exhibiting a wrinkled surface.

Histopathological examination of

the lung revealed severe to moderate

pneumonia in the affected lungs wh-

ere the bronchioles and parabronchi

were filled with inflammatory exud-

ate, mostly lymphocytes and macro-

phages (Fig. 3), with necrosis of the

lining epithelium and underlying smo-

oth muscles. In the nodular pneum-

onic lesions there was heavy infiltr-

ation of the lung tissue and all air

spaces with the same types of cells

(Fig. 4), beside presence of some

necrotic areas. Large blood vessels

exhibited severe congestion, vascu-

litis and perivascular edema. The

digestive tract showed only mild

catarrhal inflammation with necrosis

of lymphoid aggregations.

Proventriculus showed necrosis and

loss of surface epithelium, slough-

ing of the glandular epithelium in

the glandular lumens that mixed wi-

th inflammatory cells and aggrega-

tions of lymphocytes in the subepit-

helial and interglandular connective

tissue septa. Liver and kidneys sho-

wed degenerative changes with foc-

al necrosis and infiltration with mo-

nonuclear cells. In some cases, glo-

merulonephritis was diagnosed. The

heart muscles suffered from dege-


neration and focal necrotic areas

that was infiltrated with mononuc-

lear cells (Fig. 5). Marked depletion

of lymphocytes was observed in the

spleen (Fig. 6). Brain of most cases

showed neuronal degeneration and

perivascular and pericellualar ede-

ma. Pathological examination of gr-

oups (III) & (IV) did not show

significant changes.

(1) (2)

(3) (4)

(5) (6)

SCVMJ, IVX (2) 2009 75

Legend:

Pathological figures of quails intraperitoneally infected with NDV quail strain, 1

week PI showing: 1) Ruffled feathers, dropped wings, unthriftness and opened

mouth. 2) Severe congestion and dark pneumonic areas in the lung. 3) Pneumonia

with severe congestion and inflammatory exudate filling the parabronchi and other

air spaces, in addition to vasculitis and perivascular edema. H&E. X60. 4) Severe

pneumonia due to heavy infiltration of the lung tissue with mononuclear cells.

H&E. X180. 5) Focal area of cardiac necrosis and infiltration with mononuclear

cells. H&E. X180. 6) Severe depletion of the lymphoid tissue with necrotic changes

in the white pulp of spleen. H&E. X60.

DISCUSSION

Newcastle disease is defined as a

"list A" disease by OIE (1996), as it

is highly contagious causes severe

economic losses in domestic and

wild bird species specially chickens

(Kaleta, 1992 and Alexander and

Jones, 2001). The virus is capable

to infect all bird species and some

other vertebrates (Leighton and

Heckert, 2007). Concerning quails,

Silva Lima et al (2004) considered

quails as important carrier for ND

virus. In this study it was proved

that quails can be infected either

naturally or experimentally but with

low mortality and morbidity rates.

This is in agreement with the

findings of Sa'idu et al. (2004) and

Tawfik Hoda et al (2004) but they

recorded higher rates of mortality

and morbidity. This also was in

partial agreement with the findings

of Islam et al (1994) who consi-

dered stress is an important factor

for getting the infection. The iso-

lated quail strain in this work was

mesogenic and the infection resu-

lted in signs, mainly of respiratory

and nervous illness, as recorded

previously by Czerjak et al. (2007).

In this aspect, Calnek et al (1997)

mentioned that the clinical signs,

gross lesions and the organs affe-

cted are dependent on the strain and

the pathotype of ND virus, in

addition to the host and other fact-

ors like the rout of infection.

The main diagnostic tests used in

this study were HI, HA and AGPT.

These techniques are applied for

many virus infections in chickens

(Calnek et al 1997). For confir-

mation of ND, the OIE standards

commission prescribes ND virus

isolation in embryonated chicken

eggs and identification using HA

and HI test with a NDV monos-

pecific antiserum (OIE, 1996). The

HI test had proved the seroconve-

rsion in the natural infection study

and clarified the immune status in

experimental infection. In this as-

pect, it is worth of mentioning that

the low HI antibody titer of natu-

rally infected quails recorded in our

study is below the protective level,

as said by Lancaster (1963).

Accordingly, Czirjak et al (2007)

stated that any outbreak of ND in


quails may attain very significant

economic importance. So that, there

is a great need to routine vaccina-

tion against ND. The other tests, in

addition to RT-PCR, were used for

isolation and characterization of the

ND virus quail strain. Increase in

HA titres after 3rd

passage of inoc-

ulums from natural cases in SPF is

in accordance with the explanation

of Ismail et al (1979) and Sa'idu et

al (2004). Concerning the mean HI

titers and virus isolation of NDV

from experimentally infected and

challenged quail with VVND virus

are indicating that the mean HI titer

appear to begin in the 2nd

weeks

post infection and 2 weeks post

challenge, in other hand ND virus

strains could be isolated only 1

week and 2 weeks post infection

and post challenge. The same

results obtained by Czirjak et al

(2007) and Oladele et al (2008).

Quails experimentally infected by

intraperitoneal route showed signs

and gross lesions one and two wee-

ks post infection. These results are

mostly in agreement with those

reported in quails and other avian

species by Cross (1991), Emmer-

son (1994), Lam (1996) and Ola-

dele et al (2008). In this study, the

infection with ND virus quail strain

intraperitoneally induced 25% mor-

talities in the first week post infec-

tion, and no deaths occurred after

challenge with VVND virus chick-

en strain. This may be due to that

the quails evoked anti NDV imm-

une response that protected them. In

this point, these results disagree

with that of Usman et al (2008)

who recorded high mortalities

(100%) in a challenged group.

The pathological changes seen in

this study indicated the pantropism

of the virus. Most of the body

organs were involved. The detected

histopathological changes were in

accordance with that of Usman et al

(2008) and that of Oladel et al.

(2008) in two studies on quails in

Nigeria. In chickens nearly similar

changes were found in studies done

by Alexander (1991), Okoye et al.

(2000) and Oladel et al. (2005).

Some differences with that of the

other birds were recorded. The lun-

gs in some quails showed a nodular

form of pneumonia. The route of

infection might play a role in the

lesion distribution and form. The

blood vessels exhibited necrotizing

vasculitis and perivascular edema.

Changes in the proventriculus were

detected mainly on microscopical

examination, and changes in the

intestinal tract seemed to be of low

significance in this type of birds.

Concerning the involvement the

heart, Brown et al. (1999) sugge-

sted that the compromise of the

myocardium may predispose meso-

gen and lentogen infected birds to

secondary infection.

In a conclusion this study has de-

monstrated that ND virus quail str-

ain of intermediate virulence can

infect quails, naturally or experime-

SCVMJ, IVX (2) 2009 77

ntally and can cause changes in

body parameters as HI titres and

injury in different organs. The virus

causes the disease with low morb-

idity and mortality rates. The pict-

ure of the disease in quails is slig-

htly different from that in chickens.

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الملخص العربى

العدوى الطبيعية والتجريبية فى السمان بفيروس مرض النيوكاسل

حمدى فتيح،*** متولى حمودة، ** محمد الشهيدى، * مختار الطرابيلى،*

نيفين رمزى**** شهيرة عبد الوهاب، *

جامعة قناة السويس –كلية الطب البيطرى –قسم الفيرولوجيا *

بالدقىمعهد بحوث صحة الحيوان **

جامعة قناة السويس –كلية الطب البيطرى –قسم الباثولوجيا ***

.معمل االسماعيلية –معهد بحوث صحة الحيوان ****

اجريت هذه الدراسذة اليحذاد مذدى امكانيذة حذدوث مذرك النيوكاسذل بالعذدوى الطبيعيذة

راسذذة االعذذراك والتجريبيذذة ذذى طذذامر السذذمان والذذدور المحتمذذل لذذم ذذى وباميذذة المذذرك وكذذهل د

والتغيرات المرحذية ذى اعحذا و انسذجة الطذامر ذى حالذة العذدوى ولهذها الغذرك تمذت محاولذة

من طيور السمان كانت قد اظهذرت اعذراك تنفسذية وعصذبية ذى 02عزل يروس النيوكاسل من

وو يذات % 02مزرعة كلية الزراعة بجامعة قناة السويس والتى ظهر بها اعذراك مرحذية بنسذبة

حذذاالت واسذذتادم الفيذذروس المعذذزول بعذذد هلذذ 3ولقذذد امكذذن عذذزل الفيذذروس مذذن %. 1 0بة بنسذذ

مذذن الطيذور التذى اسذتادمت ذذى % 02الحذداث عذدوى تجريبيذة للمذرك حيذذث احذدثت و يذات ذى

ولعذذزل الفيذروس واجذذرا التوذذايص والفحذص للطيذذور ذذى هذذه . التجربذة بعذذد اسذذبوا مذن العذذدوى

لمناعية الماتلفة وذاملة ااتبذار التلذزن الذدموى وااتبذار منذز التلذزن الدراسة استادمت االاتبارات ا

الدموى وااتبار الترسيب ى االجار وكذهل الحقذن ذى البذيك الماصذب الاذالى مذن الميكروبذات

باالحذا ة الذى الفحذص بالتوذريم المرحذى والنسذجوباثولوجى هذها وقذد سذجلت كذل التغيذرات التذى

ولقذد تذم توصذيت عتذرة يذروس النيوكاسذل المعزولذة . ى الدراسذةحدثت ى السمان الهى استادم

.من السمان وتحديد حراوتها من الدرجة المتوسطة

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