Correlations of genetic resistance of chickens to Marek's disease viruses with vaccination protection and in vivo response to phytohemaglutinin

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Correlations of genetic resistance of chickens to Marek’s

disease viruses with vaccination protection and in vivo

response to phytohemaglutinin

Js Gavora, Jl Spencer, I Okada, Aa Grunder, Ps Griffin, E. Sally

To cite this version:

Original

article

Correlations

of

_genetic

resistance

of

chickens

to

Marek’s disease

viruses

with vaccination

_protection

and in

vivo

response

to

phytohemaglutinin

JS Gavora

1

JL

_Spencer

I

Okada

3

AA Grunder

PS Griffin E.

_Sally

₂

!

Agriculture

Canada, Animal Research _{Centre, Ottaqvn, Ontario,} K1A OC6

2

Agriculture Canada, Animal Diseases Research Institute, Nepean, Ontario, Canada K2H 8P9

3

Faculty

of Applied Biological Science, Hiroshima _{University, Department of} Animal _{Science, Higashi-Hiroshima, Japan}

(Received

6 December 1989; accepted 17 September

1990)

Summary - Twenty-three genetic groups of experimental and commercial meat _{and egg}

chickens were _injected with _moderately virulent BC-1

(exp 1)

or _highly virulent RB-LB

(exp 2)

Marek’s disease

_(MD)

virus. Birds of 7 _{genetic groups} were divided into vaccinated and non-vaccinated groups and exposed by contact to the virulent RB-1B virus in exp 3.

Response to _{phytohemaglutinin}

_(PHA)

_injected in _wing webs was measured in adult birds of all 23 groups

(exp

4)

to assess its _relationship to MD resistance. There was a

_high

correlation

_(0.8)

between resistance of the _{genetic groups} to the two viruses _indicating that selection for resistance to one virus would be _expected to _improve resistance to the other virus. _Regression of MD incidence in vaccinated birds on that in non-vaccinated birds resulted in _regression coefficients of 0.41, 0.23, and 0.31% for _males, females and

combined sexes _{respectively, indicating} that MD incidence increased _linearly in vaccinated birds in relation to their _genetic

_{susceptibility}

to MD. Two

_significant

correlations in males

suggested that

_{high swelling}

response to PHA _may under some conditions be associated with MD resistance. _However, the correlation coefficients were inconsistent and it was concluded that _swelling response to PHA inoculated in the _wing web is not _predictive of MD resistance.

chicken _/ Marek’s disease _/ vaccination _{/ phytohemaglutinin}

R.ésumé - Corrélations entre la résistance _génétique de _poulets aux virus de la

maladie de Marek, la protection de la vaccination et la réaction in vivo à la

phytohémagglutinine.

Vingt-trois

types

génétiques

de _{poulets, représentant} des souches «chair» et _{«ponte» expérimentales} et _{commerciales,} ont été inoculés avec deux virus de

la Maladie de Marek: le virus _BC-1, modérément virulement

_{(expérience 1)}

et le virus

*

RB-1B, fortement virulent

_{(expérience 2).}

Les _sujets de _{sept types génétiques} ont été

repartis en _{groupes vaccinés et} non vaccinés et ont été _exposés par contact au virus virulent RB-1B dans _{l’expérience} 3. La réaction à la _{phytohémagglutinine}

_(PHA)

_injectée dans les membranes alaires a été mesurée chez des _sujets adultes des 23 _{types génétiques}

(expérience

4)

pour évaluer sa liaison avec la résistance à la maladie de Mareck. On constate une _forte corrélation

(0.8)

entre la résistance des _{types génétiques} aux deux

virus, ce _qui montre _{que la} sélection pour la résistance à un virus semble améliorer la résistance à l’autre virus. La _régression de la

_fréquence

de la maladie de Marek chez les _sujets vaccinés sur celle des _sujets non vaccinés est de 0.41; 0.23; 0.31 % pour les

mâles, les _femelles et les deux sexes combinés _{respectivement, indiquant par} là _que, chez les _{sujets vaccinés,} la

_fréquence

de la maladie de Marek _augmente de

_façon

linéaire avec les sensibilités _génétique à la maladie de Marek. Deux corrélations

_{significatives}

à _{l’injection} de PHA _peut, dans certains _conditions, être liée à la résistance à la maladie de Marek.

Cependant, les _coefficients de corrélation sont contradictoires et les auteurs concluent _que la réaction de _gonflement consécutive à l’inoculation de PHA dans la membrane alaire ne

peut servir à _prédire la résistance à la maladie de Marek.

poulet / maladie de Marek _/ vaccination _{/ phytohémagglutinine}

INTRODUCTION

Marek’s disease

_(MD)

is caused

_by

a

_herpes

virus that induces

_neoplastic

trans-formation of host

_T-cells,

_resulting

in formation of

_lymphoid

tumors. Protection

by

vaccines is not

_complete

and the combination of both vaccination and

_genetic

resistance is

_required

for

_optimum

_protection

_(Spencer

et

_al,

_1972,

Gavora and

Spencer,

1979).

Appearance

of very virulent strains of MD virus associated with

increased MD losses in vaccinated flocks

_(Witter,

₁₉₈₈₎

_emphasizes

the need to

improve

vaccines and to increase levels of

_genetic

resistance.

In this _context,

_questions

of

_practical

_importance

are

₍₁₎

whether _genotypes

resistant to

_moderately

virulent MD viruses are also resistant to

_highly

virulent

viruses,

and

₍₂₎

what is the

_degree

of

_protection

_by

vaccination

_against

the virulent

viruses in _genotypes that differ in their natural MD resistance. Genetic

improvement

of resistance can be

accomplished by

direct selection based on _response to MD virus _or, more

_desirably,

on marker traits measurable without exposure to the

pathogen.

Response

of chickens to

_{phytohemaglutinin}

_(PHA)

was considered a

potential

marker trait for this _purpose.

T-cells

_{play a}

dual role in the

_pathogenesis

of

_MD,

in that

_they

are both the

target cells for

neoplastic transformation,

and act with natural killer

_cells,

in defence

against

MD tumors

_(Sharma

et

_al,

_1977,

_Sharma,

_1981).

_{Susceptibility}

to MD

tumors may be linked to strong cell-mediated immune response and is influenced

by

both age and genotype of the bird

_{(Calneck, 1986)}

and MD resistance

_is,

at least

partly,

the _property of the _target T-cells

_(Gallatin

and

_Longenecker,

_1979).

Response

of chickens to PHA

_{injected intradermally}

is a measure of cell-mediated

immunity

involving

T-cells

_(Goto

et

_al,

_1978),

_although

the _response is

_cellularly

heterogeneous

(Edelman

et

_al,

_1986).

_Response

of chickens to PHA differs among

commercial stocks

_(Van

der

_Zijpp,

_1983),

or

_experimental

lines

_(Lamont

and

_Smyth,

1984)

and is influenced

_by

both sex and

_major

_{histocompatibility haplotype}

_(Taylor

The

_relationship

of PHA _response and MD resistance is not

_clearly

understood.

A line of chickens selected for

_high

plasma

corticosterone had an

_impaired

in vitro response of

_lymphocytes

to PHA and greater MD tumor incidence and

mortality

than a low corticosterone line

_(Thompson

et

al,

1980).

In contrast, Lee and Bacon

₍₁₉₈₃₎

_reported

_{that increased in vitro response} of

_lymphocytes

to

phytohemaglutinin

was associated with increased

_{susceptibility}

to MD.

_However,

Calnek et al

₍₁₉₈₉₎

dit not _{observe any}

_general

correlation between _{the responses}

of

_{multiple genetic}

_groups of chickens to

_mitogens

Concavalin A and PHA or mixed

lymphocyte

reaction,

and MD

_{susceptibility.}

In this

_study,

correlations between resistance of several

_genetic

groups of chickens

to two strains of MD virus that differed

_widely

in virulence were

investigated

and

the

_relationship

between

_genetic

resistance to MD and

protection by

vaccination

was assessed. The

relationship

of

_genetic

resistance to MD with

_swelling

response

induced

_by

the

_injection

of PHA into the

_wing

web is also

_reported.

MATERIALS AND METHODS

Chickens

A

_description

of the

_genetic

groups used in the

study

is

given

in table I and

intermingled

in floor pens and housed in individual cages as adults.

They

were vaccinated for

_MD,

infectious bronchitis and Newcastle

_disease,

as well as avian

encephalomyelitis,

and were fed mash rations

_throughout

their lifetime.

_They

were

given

a uniform

_light

diet in all

_generations.

No

_major

disease outbreak was

experienced

in _any of the

_parental

flocks or the 1983 flock used for the PHA test.

In all these

_{flocks, rearing mortality}

was less than 8% and

_laying

house

_mortality

less than 10%. In addition to the above _parents,

_{parallel specific}

_{pathogen-free}

(SPF)

parent

populations

for

_genetic

groups

CS,

CK,

and NH were maintained on a

filtered-air,

_{positive-pressure}

building

where

they

received no vaccines and were

free of Marek’s disease virus and other avian

_pathogens.

Marek’s disease

_challenge

tests

_(exp

_1,

2 and

₃₎

For the MD

_challenge

tests the birds were in floor pens in an isolation

_facility

(Grunder

et

al,

1972).

At 3 weeks of age, each bird was inoculated

_{intraperitoneally}

with the

_respective

MD virus isolant. In exp

1,

the inoculum contained the BC-1

virus

_(Spencer

et

_al,

₁₉₇₂₎

and the birds

_produced

from both

_{conventionally}

housed and SPF _parents were observed for 63 d after inoculation. _{In exp 2} the inoculum was the RB-1B virus

_(Schat

et

_al,

₁₉₈₁₎

and the duration was 56 d after inoculation. The inocula for both

_experiments

were from lots of cell-associated virus stored in

liquid nitrogen

that had

_previously

been tested for

_{pathogenicity.}

were

_kept

in isolation until 14 d of _age and were then

_exposed

to seeder birds

previously

infected with the RB-1B virus. The birds were killed at 53 d after the

exposure.

All birds that died or were killed because of

_illness,

and survivors that were

killed at termination of the tests, were

necropsied.

MD incidence was based on

gross lesions.

Phytohemaglutinin

(PHA)

response test

(Exp 4)

The dose and inoculation site for this

_experiment

was determined on the basis of a

preliminary

test

_using

30 adult White

_Leghorn

females and 12 adult White

_Leghorn

males inoculated with

75,

500 and 1250 mg of PHA per bird in the wattle or

wing-web.

_Wing

webs were found easier to measure as wattles tended to be soft and

pliable.

Of the doses

_tested,

500 _{and 1250 mg gave similar}

_swelling

_{responses in} the

wing

web.

The

_procedure

used in _exp 4 was similar to that of Van der

Zijpp

(1983).

Adult

birds

₍₄₈₂

d of age at PHA

_inoculation)

were each inoculated

_{intradermally}

with 0.125 ml of

_phosphate

buffered saline

_(PBS)

in the left

_wing

web. The same volume

of PBS

_containing

_{500 mg PHA}* was inoculated in the

_{right wing}

web. Prior to the inoculation the

_wing

webs were

_plucked

free of feathers and the inoculation _sites, close to but not on the

_edge

of the web were marked with a felt _pen.

Thickness of the

_wing

web was measured before

_inoculation,

as well as 24 and

48 h after

_{inoculation, using Miluyo}

electronic

micrometer,

model No 293-701 that

applied

constant _pressure on all

_{wing webs,}

_independent

of the _operator. The

swelling

index

_(I)

was calculated as

where &dquo;T&dquo; is the thickness and

_subscripts

&dquo;R&dquo; and &dquo;L&dquo; indicate the

_right

and left

_wing

web and &dquo;1&dquo; and &dquo;2&dquo; indicate thickness before and after

_inoculation,

respectively.

Statistical

_analyses

Spearman’s

rank and Pearson’s

_{product-moment}

correlation between resistance to

the BC-1 and RB-1B viruses and PHA response were calculated on the basis of

genetic

group means. The

_dependence

of MD incidence in vaccinated birds on MD incidence in non-vaccinated birds was assessed

_by

linear

_regression

_{using genetic}

group means. MD incidence _among

_genetic

_groups and vaccination treatments was

compared by homogeneity

X

2

tests

and differences between

_grouping

of

_genetic

groups

by

the student’s t-test. Individual bird

_swelling

index data after PHA

challenge

were

subjected

to

_analysis

of variance

_using

a model

_containing

the effects of

_genetic

_group, sex and their interaction.

*

RESULTS

Resistance to the BC and RB-LB isolants of MD virus

MD incidence after

_challenge

with the BC-1 and the RB-1B isolants of MD virus

differed

_widely

in _exp 1 and 2

_(table

_II).

In _{exp 1,} the overall MD incidence induced

by

BC-1 was close to 15% and this was

_{significantly}

lower

_(P

<

0.01)

than the 47%

MD incidence induced

_by

RB-1B in _exp 2.

The ranges of MD incidence _among the

_genetic

groups tested were from 0 to

46.4% in males and 0 to

89.7%

in females _{in exp}

_1,

and from 5.7 to 93.7% in males and from 4.1 to 97.2% in females _{in exp 2. In}

_genetic

groups

8R,

XP02,

and XP21 there was no incidence of MD after BC-1

challenge

while MD was observed in all

genetic

groups after

challenge

with RB-LB

_{(table II).}

_Among

the birds

_challenged

with BC-1 there was a

significant

sex difference

(P

<

_0.05),

the incidence

_being

11.5%

higher

in females than in males. The

_{corresponding}

sex difference of 4.2% in birds

_challenged

with RB-1B was not

_{statistically significant.}

With the

_exception

of strain NH

_females,

MD incidence in strains

_{CS, CK,}

and NH in exp 1 was not

significantly

different between birds

_produced

from

_{conventionally}

and SPF housed

dams.

The

_relationship

between resistance of the

_genetic

_groups to the BC-1 and

RB-1B

_challenge

was

_expressed

in terms of

_Spearman’s

rank and Pearson’s

product-moment correlations

_{(table III).}

the correlations for males and females

_separately,

as well as for sexes combined were all

_high

and

_significant,

_although

correlations tended to be

_higher

in females.

Relationship

of

_genetic

resistance to MD and vaccination

_protection

Incidence of Marek’s disease in the non-vaccinated birds

_{exposed by}

contact to

RB-LB in exp 3 at 2 weeks of _age

_(fig

₂₎

was in

good

_agreement

with that in the

same

_genetic

groups

challenged

by injection

at 3 weeks of _{age in exp 2}

_{(table II),}

although

the _average MD incidence in contact

_challenge

was 6.6% lower. Vaccination

conferred

_significant

_protection

_(P

<

_0.05)

to both males and females and there were

_high

and

_significant

correlations between MD incidence in the vaccinated and

non vaccinated birds

(table

III).

Linear

_regressions

were fitted for the

_relationship

between MD incidence in

non-vaccinated birds. The

_regression

accounted for

_92,

68 and 95% of total variation

_(R

₂

₎

for

_males,

females and sexes combined. The

_respective

_regression

coefficients were

0.41, 0.23,

and 0.31 for

_males,

females and sexes combined.

_Thus,

in this

_experiment,

MD incidence in vaccinated birds increased

_linearly

with their

_{genetic susceptibility}

(fig 2)

and a combination of

_genetic

resistance with vaccination resulted in the best

protection.

Marek’s disease resistance _{and response} to

_{phytohemaglutinin}

The means of the

_swelling

index measured at 24 h after

_injection

with PHA are

was, as a

_rule,

_greater

than that of 48 h. There were

_highly

significant

differences

among the

genetic

groups and sexes and

_genetic

_group

_by

sex interaction was also

significant

for the 24 h index

_{(table IV).}

The mean

_swelling

at 24 h was

_larger

comparisons

between sexes, the greater

swelling

was in males in 11

_genetic

_groups

and in females in 12

_genetic

_groups. The

_tendency

was for

_swelling

to

_develop

more

slowly

and to

_peak

later in females than in males.

Rank-order and

_{product-moment}

correlations of MD incidence and

_wing

web

swelling

after PHA inoculation are shown in table V.

_Only

the

_negative

correla-tions of the 48 h

_swelling

index of males with MD resistance reached statistical

significance.

The

_remaining

correlations of 24 h and 48 h

_swelling

indices for males

were also

_negative,

while those for females were inconsistent in both

_sign

and

mag-nitude.

DISCUSSION

Incidence of Marek’s disease _among the

_genetic

_{groups in both exp} 1 and 2 varied

showing

that the

_predominant

lesion in BC-1 inoculated females was in the _ovary and in males in nerves. The RB-1B virus induced a

_high

_proportion

of visceral

lesions in both males and females. As observed

_previously

_(Grunder

et

_al,

_1972),

BC-1 induced a

_higher

incidence of MD in females than males. No

_significant

sex difference was observed in MD incidence after RB-1B

_{challenge. This, together}

with the

_large

difference between the overall MD incidences after BC-1 and

RB-1B

_{challenge, emphazises}

the

_genetic

_divergence

between the two virus strains. The correlations between resistance to the MD viruses

_{(table III),}

as well as that between this resistance and PHA

_{(table V),}

express

genetic relationships

because

the correlations are based on means of the

_genetic

groups, which are themselves

genetic

characteristics.

Since there were

high

correlations between resistance to BC-1 and

RB-1B,

selection for resistance to one of the viruses would also be

_expected

to

improve

resistance to the other. This conclusion was

_supported

_by

_comparisons of related

genetic

groups that have

undergone

various

degrees

of selection. There were 3

such sets of

_genetics

_{groups of}

_Leghorns,

each

_originating

from a different

_genetic

base

_population

_{(table I).}

The sets consisted each of a strain selected for

_high

egg

production,

egg

weight

and related

economically

important

traits

including viability

(P-strains),

and of strains selected for resistance to the BC-1 virus in addition to the above traits

_(R-strains).

Selection for resistance to the BC-1

_{significantly (P <_ 0.01)}

improved

resistance of the R-strains 3R and the 8R to the RB-1B virus

_compared

with their

respective

P-strain _counterpart strains 1 and 8

_{(table II).}

In the third

set, there was no

_significant

difference between the P-strain 2 and R-strain 2R in

RB-1B resistance.

Our results from lines XP02 and XP21 confirm the resistance of the

B2i

haplotype

(XP21)

and

B

2

_haplotype

_(XP02)

_against

_multiple

MD viral strains

(Gavora

et

al, 1986;

Bacon

_1987).

The commercial stocks differed

_widely

in MD resistance:

_Leghorn

stock A was among the most _{resistant group,}

however,

stocks

B and C were far more

_susceptible

(table II).

The linear

_relationship

between

_genetic

resistance to MD and

_protection

_by

vaccination

_{(fig 2)}

was based on

_only

7

_genetic

_groups but should have a broad

validity

for the virus strain and vaccine _type

_tested,

as the resistance of the non-vaccinated groups

practically spanned

0 to 100%. The

_positive

correlation between resistance to the RB-LB and BC-1 isolants of MD virus _suggest that the

_relationship

of MD resistance and

protection

by

vaccination may also be valid for other MD

viruses.

In the determination of the PHA

_{swelling index, possible}

differences in

_wing

web thickness of the

_right

and left

_wing

or the variation in the _{response to} PBS

were not considered as it was shown that

_they

are

_{negligible (Van}

der

_Zijpp,

_1983).

Overall,

the levels of response to PHA in this

_study

were lower than those observed

by

Van der

_Zijpp

₍₁₉₈₃₎

and Lamont and

_Smyth

_(1984).

This

_discrepancy

may be

due to the lower dose of PHA _{and older age} of the birds in this

_study,

as well as the

_genotypes

of birds tested. Similar to the _present

_study,

Van der

_Zijpp

_(1983),

Lamont and

Smyth

(1984),

as well as Goto et al

₍₁₉₇₈₎

used

_{conventionally}

housed

birds

for the PHA inoculation

_experiments.

zero, as well as the

_sign

of 7 out of the 8 correlations for sexes combined in the

table, suggested

a

_tendency

for the

_high

PHA _response to be associated with MD resistance. Consistent with the observations of

_Thompson

et al

_(1980),

this

would indicate that the bird’s

_ability

to mount a cell-mediated immune _response is

important

for MD resistance.

Of the three sets of R- and

_{P-strains, described,}

for combined _sexes, the R-strains 2R and 3R had _greater PHA _response than the

_{corresponding}

P-strains 2

and 1

_{(table II).}

The reverse was observed for the third set of R-strains 8R and

P-strains 8. In addition most of the correlations between PHA _response and MD resistance were non

_{significant (table V).}

_Therefore,

in _agreement with Calnek et al

(1989),

who studied in vitro PHA _response of

_lymphocytes

from strains of

_varying

resistance to

MD,

we conclude that

_swelling

response to PHA inoculation in the

wing

web is not

_{sufficiently predictive}

of MD resistance to

_justify

its use in

_genetic

selection.

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Influence of the

_{major histocompatibility complex}

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Calnek,

BW

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Marek’s disease: A model for

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Adene

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