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In our study we have applied RT-PCR method at first for the detection and identification of NDV in allantoic fluids of infected embryonated eggs and then in tissues of experimentally [r]

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DETECTION OF NEWCASTLE DISEASE VIRUS

IN INFECTED CHICKEN EMBRYOS AND CHICKEN TISSUES BY RT-PCR

Department of Poultry Diseases, National Veterinary Research Institute, 24-100 Pulawy, Poland

e-mail: ksmiet@piwet.pulawy.pl

Received for publication November 30, 2005

Abstract

RT-PCR for the detection of Newcastle disease

virus (NDV) in allantoic fluids of SPF embryonated eggs as

well as in tissues of SPF chickens infected experimentally is

described The method proved to be specific as all tested

NDVs were detected and no cross reaction with other RNA

viruses was observed Sensitivity of the method was

established at 10 5 ELD50/0.1 ml To detect NDV in chicken

tissues, SPF chickens were inoculated with 10 6 EID 50 of 3

NDV reference strains: La Sota (lentogenic), Roakin

(mesogenic) and Italy (velogenic pigeon variant) and 5 d p.i

various tissue samples were aseptically collected followed by

RT-PCR and virus isolation on SPF embryos The results

showed high concordance: 93% (La Sota and Italy) to 100%

(Roakin) between both methods

Key words: chicken embryos, chickens,

Newcastle disease virus, RT-PCR

Newcastle disease (ND) is a highly contagious

infection of poultry caused by avian paramyxovirus

serotype 1 (Newcastle disease virus, NDV) The disease

is spread worldwide affecting various species of poultry

and other birds (2, 3, 14) However, chickens appear to

be the most susceptible to the disease whereas aquatic

birds, including geese and ducks, are relatively resistant

NDV differs in virulence and has been grouped into 5

pathotypes: velogenic viscerotropic, velogenic

neurotropic, mesogenic, lentogenic and asymptomatic It

was shown that NDV virulence is dependent on the

amino acid sequence at the cleavage site of F0 gene The

presence of multiple basic amino acids at the cleavage

site indicates that the virus isolate is pathogenic (2) In

diagnosis of Newcastle disease, methods recommended

by OIE Manual (16) and EU Council Directive (5)

comprise isolation on SPF embryonated eggs and

identification in the haemagglutination inhibition test

Recently, as an alternative, OIE regulations have

proposed methods based on molecular biology (16)

Reverse transcription and polymerase chain reaction

(RT-PCR) methods are applied in many laboratories of

the world for the detection and identification of NDV (1)

The aim of the present study was to apply RT-PCR for rapid detection of Newcastle disease virus in experimentally infected chicken embryos and tissues of chickens

Material and Methods

Embryonated eggs Specific pathogen free

(SPF) eggs were imported from Valo-Lohmann (Germany)

Viruses In the study 17 NDV strains were

used: 3 reference strains representing different pathotypes: La Sota (lentogenic), Roakin (mesogenic) and Italy (velogenic, pigeon variant) and 14 field strains isolated in Poland from: chickens - Radom strain isolated at the beginning of the 70-ties and 3 strains isolated in 1990-2004, turkeys - 1 strain isolated in

2004, racing pigeons - 7 strains isolated at the late 80-ties and beginning of the 90-80-ties, kindly provided by the Department of Microbiology, Agricultural University in Lublin, and feral pigeons - 2 strains recovered in 2002 Prior to testing in RT-PCR, all the strains were propagated on SPF embryonated eggs and allantoic fluid was used for further studies

Virus isolation assay Virus isolation was

performed on 9-11 SPF embryonated eggs according to the Annex III of the Council Directive 92/66/EEC (5)

Experimantel design Three groups of four

4-week-old SPF chickens kept in isolation were inoculated intraocularly and intranasally with 106 EID50 of the following strains of NDV: La Sota, Roakin and Italy

Five days post inoculation (p.i.) tracheal and cloacal

swabs as well as samples from the trachea, lungs, liver, spleen, heart, brain, kidneys, bursa of Fabricius, duodenum, caecal tonsils, and rectum were aseptically collected Supernatants of the organs (used for viral isolation as well as for RT-PCR) were prepared according to the Annex III of the Council Directive

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202 bp

92/66/EEC (5) Tracheal and cloacal swabs were

suspended in PBS with antibiotics (1 ml/swab) and after

1 h incubation at room temperature and centrifugation,

supernatants were harvested All the supernatants were

pooled in batches of four Additionally, pooled

supernatants of the trachea, lungs, liver, spleen, kidneys,

heart, and brain (pooled sample No 1) and duodenum,

caecal tonsils, and rectum (pooled sample No 2) were

also used as separate samples

RNA isolation RNA was isolated from

allantoic fluids using commercial RNeasy Mini Kit

(Qiagen, USA) as recommended by the supplier

Reverse transcription (RT) cDNA was

synthesized using 5 µl of the total RNA, 4 µl of 5x first

strand buffer, 2 µl of 0.1 M DTT, 1 µl of ribonuclease

inhibitor (20 U/µl), 1 µl of 10mM dNTP, 1 µl (200 U)

of Super-Script II reverse transcriptase (Invitrogen,

USA), 0.5 µl of random hexamers (Promega, USA) in a

total volume of 20 µl for 50 min at 42°C

Primers A set of primers according to Creelan

et al (6): NDV/F (5’ - GGT GAG TCT ATC CGG ARG

ATA CAA G – 3’) and NDV/R (5’ - TCA TTG GTT

GCR GCA ATG CTC T– 3’) that flanks the region

encompassing the cleavage site of the fusion protein

gene (F) was used in the study The expected size of

PCR product was 202 bp Oligonucleotides were

prepared in the Institute of Biochemistry and Biophysics

in Warsaw

Polymerase chain reaction (PCR) PCR was

carried out in a total volume of 20 µl containing 2 µl of

cDNA, 2 µl of 10x PCR buffer, 0.5 µl of dNTP, 1.4 µl

of MgCl2 (25 mM), 0.5 µl of Taq polymerase

(Fermentas, Lithuania) and 1 µl of each primer The

thermocycler conditions were as follows: 2 min at 94ºC

(initial denaturation), followed by 40 cycles of 15 s at

94ºC (denaturation), 30 s at 48ºC (annealing), 30 s at

72ºC (elongation) The PCR ended with a final

elongation for 7 min at 72ºC

Detection of PCR products PCR products

were separated in 1.5% agarose gel in 1 x TAE buffer

stained with ethidium bromide, compared with

molecular mass marker and visualized by ultraviolet

(UV) transillumination

Sensitivity of RT-PCR The sensitivity of the

RT-PCR was established by the ten-fold diluting of the

allantoic fluid containing lentogenic La Sota strain (108 ELD50/0.1 ml) Subsequently, RNA was isolated and RT-PCR was performed according to the procedure described above The highest dilution with positive RT-PCR signal was determined

Specificity of RT-PCR To evaluate specificity

of the method, cDNA of the following RNA viruses was used: paramyxovirus serotype 3, avian influenza virus (H5N2 and H7N1), infectious bursal disease virus (vaccinal 228E strain and very virulent 99/150 Polish field strain), and avian infectious bronchitis virus (strains M-41 and 4/91) PCR was performed according

to the protocol described above

Results

All strains previously identified serologically as NDV also tested positive in RT-PCR test with NDV specific primers (Fig 1) No cross reaction was found with other RNA viruses used in the study (data not shown) Sensitivity of the RT-PCR has been established

at 105ELD50/0.1 ml (Fig 2)

Table 1 shows the results of RT-PCR and virus isolation performed on tissue samples collected from

SPF chickens 5 days p.i By RT-PCR method the

positive results were obtained in all 13 tested samples

(13/13) p.i with mesogenic Roakin strain, 11 samples p.i with velogenic Italy strain and 8 samples p.i with

lentogenic LaSota strain Positive result of virological examination was noted in all samples (Roakin strain), 12 samples (Italy strain) and 10 samples (La Sota strain) Both pooled samples (number 1 and 2) were positive in RT-PCR and virus isolation (La Sota, Roakin and Italy strains) Italy strain was isolated from all samples after the first embryo passage Isolation of Roakin strain required one passage from all samples except for cloacal and tracheal swabs La Sota strain was isolated during the first embryo passage only from the samples collected from the respiratory tract, brain, bursa of Fabricius and pooled sample 1 Concordance between RT-PCR and virus isolation was: 93% (La Sota and Italy strains) and 100% (Roakin strain)

M 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Fig 1 Electrophoresis of RT-PCR products: M: marker Gene Ruler 100 bp DNA Ladder (Fermentas, Lithuania), Lane 1:

NDV/Radom/chicken/70; Lane 2: NDV/chicken/89/90; Lane 3: NDV/chicken/18/91; Lane 4: NDV/chicken/548/04; Lane 5: NDV/pigeon/AR1; Lane 6: NDV/pigeon/AR2; Lane 7: NDV/pigeon/AR3; Lane 8: NDV/pigeon/AR4; Lane 9: NDV/pigeon/AR5; Lane 10: NDV/pigeon/AR6; Lane 11: NDV/pigeon/AR7; Lane 12: NDV/pigeon/PW/46/02; Lane 13:NDV/pigeon/PW/166/02; Lane 14: NDV/turkey/549/04; Lane 15: NDV/LaSota; Lane 16: NDV/Roakin; Lane 17: NDV/Italy; Lane 18: negative control

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M 1 2 3 4 5 6 7

Fig.2 Sensitivity of RT-PCR: M: marker Gene Ruler 100 bp DNA Ladder (Fermentas, Lithuania); Lane 1: positive control; Lane 2:

10 7 ELD 50 ; Lane 3: 10 6 ELD 50 ; Lane 4: 10 5 ELD 50 ; Lane 5: 10 4 ELD 50 ; Lane 6: 10 3 ELD 50 ; Lane 7: 10 2 ELD 50

Table 1

Comparison of RT-PCR and virus isolation for the detection of NDV in tissues of infected chickens

Virus

Samples

Virus isolation Passage PCRRT- isolationVirus Passage PCR RT- isolation Virus

Passage

RT-PCR Cloacal

swabs

Tracheal

Bursa of

Caecal

Pooled

Pooled

202 bp

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Discussion

As Newcastle disease is one of the most

important infectious diseases of poultry, rapid detection

and identification of the virus is crucial for the effective

control of the disease Conventional diagnostic methods

such as virus isolation on SPF embryonated eggs

followed by serological identification in

haemagglutination-inhibition test is laborious and

time-consuming The speed of the diagnosis can be

considerably increased by using methods based on

molecular biology e.g reverse transcription –

polymerase chain reaction (1, 6, 7, 10- 13)

RT-PCR for the detection of NDV was first

described by Jestin & Jestin in 1991 (10) and to date it

has been successfully developed in different

modifications (1) e.g using universal primers to detect

all NDVs (6, 7), pathotype specific primers that enable

rapid differentiation of the pathotype (12) or nested PCR

(11, 13) In our study we have applied RT-PCR method

at first for the detection and identification of NDV in

allantoic fluids of infected embryonated eggs and then in

tissues of experimentally infected chickens with NDV

strains of different virulence: lento-, meso- and

velogenic

Our study on the sensitivity of the test indicates

that at least 105ELD50 should be present in 0.1 ml of the

allantoic fluid to obtain a positive result The sensitivity

can be improved by the development of a modification

of RT-PCR e.g “nested” RT-PCR (11, 13) On the

other hand, during infection with NDV strains, even

with lentogenic ones, the ELD50 value of the virus in

infected tissues is usually higher that the sensitivity

threshold established in our studies (8, 9, 15) Indeed,

applied RT-PCR method proved to be useful for the

detection of NDV directly in chicken tissues and a high

degree of correlation with virus isolation test was

observed Collection of samples was carried out 5 d

post infection because the high amount of the virus was

expected to be found in a variety of organs at that very

time Velogenic and to some extent mesogenic NDV

strains are pantropic and can be found in many organs,

what was confirmed by our studies (Roakin: 13/13

samples by RT-PCR and virus isolation, Italy: 11/13

samples by RT-PCR and 12/13 by virus isolation)

Lentogenic strains are generally less invasive and can be

found usually in the respiratory and digestive tracts (2,

4, 14, 17) but some of them spread to internal organs,

especially during early phase of infection (7-9, 15) It is

presumed that their multiplication rate in

parenchymatous organs is lower than for meso- or

velogenic strains (9) In our study La Sota strain was

detected in 8/13 and 9/13 samples by RT-PCR and virus

isolation, respectively The need to perform 2 passages

to obtain a positive result in case of samples collected

from the liver, spleen, kidneys and duodenum suggests

the LaSota strain multiplies in lower titres in these

organs

Regardless of the virulence of the strains,

pooled samples of different organs were always positive

in either test Due to the fact that NDV strains of

different virulence show diversity in tissue predilection

in different time post infection, it is recommended to pool samples of various organs rather than examine selected tissues It should also be taken into account that the viral titres decline relatively quickly in certain organs

A significant reduction of time required to complete the RT-PCR test (8-12 h) in comparison with the standard virus isolation (up to 2 weeks) seems to be the greatest advantage of the RT-PCR method Moreover, the use of primers encompassing cleavage site of F0 gene enables to establish virulence of an isolate, either by direct sequencing or by restriction

enzyme analysis and can be used alternatively to in vivo

method (1 day-old chicks inoculation) of the virulence assessment

References

1 Aldous E.W., Alexander D.J.: Detection and differentiation of Newcastle disease virus (avian

paramyxovirus type 1) Avian Pathol 2001, 30, 117-128

2 Alexander D.J.: Newcastle disease, other avian paramyxoviruses, and pneumovirus infections In:

Diseases of Poultry, Iowa State Press,11th edition 2003,

pp 63-99

3 Alexander D J.: The epidemiology and control of avian influenza and Newcastle disease J Comp Pathol 1995,

112, 105-126

4 Brown C., King D.J., Seal B S.: Pathogenesis of Newcastle disease in chickens experimentally infected

with viruses of different virulence Vet Pathol 1999, 36,

125-132

5 Council Directive 92/66/EEC of 14 July 1992 introducing Community measures for the control of Newcastle disease Official J Europ Commun, L260, pp 1-20

6 Creelan J.L., Graham D.A., McCullough S.J.: Detection and differentiation of pathogenicity of avian paramyxovirus serotype 1 from field cases using one-step reverse transcriptase-polymerase chain reaction Avian

Pathol 2002, 31, 493-499

7 Gohm D.S., Thur B., Hofmann M.A.: Detection of Newcastle diseases virus in organs and faeces of experimentally infected chickens using RT-PCR Avian

Pathol 2000, 29, 143-152

8 Gough R.E., Allan W.H.: The potential as an aerosol vaccine of Ulster 2 C strain, Newcastle disease virus Vet

Rec 1974, 95, 263-265

9 Hofstad M.S.: A quantitative study of Newcastle disease virus in tissues of infected chickens Am J Vet Res 1951,

12, 334-339

10 Jestin V., Jestin A.: Detection of Newcastle disease virus

RNA in infected allantoic fluid by in vitro enzymatic

amplification (PCR) Arch Virol 1991, 118, 151-161

11 Jestin V., Cherbonnel M., Arnauld C.: Direct identification and characterization of A-PMV-1 from suspicious organs by nested PCR and automated sequencing Proceedings of the Joint First Annual Meetings of the National Newcastle Disease and Avian Influenza Laboratories of the European Communities, Brussels, 1993, pp 89-97

12 Kant A., Koch G., Van Roozelaar D., Balk F., Ter Huurne A.: Differentiation of virulent and non-virulent

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polymerase chain reaction Avian Pathol 1997, 26,

837-849

13 Kho C.L., Mohd Azmi M.L., Arshad S.S., Yusoff K.:

Performance of an RT-nested PCR ELISA for detection

of Newcastle disease virus J Virol Methods 2000, 86,

71-83

14 Kouvenhoven B.: Newcastle disease In: Virus Infection

of Birds, Elsevier Science Publishers B.V.1993, pp

341-361

15 Minta Z.: Uodparnianie kurcząt rzeźnych przeciwko rzekomemu pomorowi drobiu (ND) przez rozpylanie szczepionki „L” PhD dissertation, Puławy 1980

16 OIE Manual of Standards for Diagnostic Tests and Vaccines for Terrestrial Animals, 5 th edition, 2004 Chapter 2.1.15 Newcastle disease, pp 270-282

17 Singh K.V., El-Zein A.: Viral proliferation patterns of a velogenic (VLT), a mesogenic (Komarov), and a lentogenic (F) strain of Newcastle disease virus Poult Sci

1978, 57, 1563–1566

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