COCCIDIA PARASITISM INCREASES RESISTANCE OF MICE TO SUBCUTANEOUS INOCULATION WITH SALMONELLA ABORTUS OVIS

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COCCIDIA PARASITISM INCREASES RESISTANCE OF MICE TO SUBCUTANEOUS INOCULATION

WITH SALMONELLA ABORTUS OVIS

F. Lantier, P. Yvoré, J. Marly, P. Pardon, Dominique Kerboeuf

To cite this version:

F. Lantier, P. Yvoré, J. Marly, P. Pardon, Dominique Kerboeuf. COCCIDIA PARASITISM IN-

CREASES RESISTANCE OF MICE TO SUBCUTANEOUS INOCULATION WITH SALMONELLA

ABORTUS OVIS. Annales de Recherches Vétérinaires, INRA Editions, 1981, 12 (2), pp.169-172. �hal-

00901321�

COCCIDIA PARASITISM INCREASES RESISTANCE OF MICE TO SUBCUTANEOUS INOCULATION

WITH SALMONELLA ABORTUS OVIS

F.

LANTIER P. YVORÉ 2 J. MARLY P. PARDON Dominique ^{KERBOEUF 2}

1 Station de

Pathologie

^{de la}

Reproduction,

^{2 Station de}

Parasitologie

lnstitut National de la Recherche

Agronomique,

^{Centre de} Tours, 37380

Nouzilly,

^France

Résumé

RÉSISTANCE

DE LA SOURIS

PARASITÉE

PAR DES COCCIDIES

À

UNE INOCULATION AVEC SALMONELLA ABORTUS OVlS. - La résistance de la souris à une

épreuve

sous-cutanée par S. abortus ovis est

augmentée lorsque

les animaux ont été

préalablement

^ou simultanément

parasités

^{avec Eimeria} falciformis. Ceci a été mis en évidence par

comparaison

^{des taux de morta-} lité et des niveaux d’infection

spléniques provoqués

par l’inoculation de Salmonella chez des sou-

ris NMRI et CD-1

(ICR) parasitées

^{ou non. Un} tel effet du

parasitisme

^n’a pu être observé

lorsque

E. falciformis était administré

après

^{S. abortus ovis.}

Interactions between

parasites

and bacteria have

already

^been

reported,

but little informa- tion is available on the modifications that para- sitism _may induce in the

pathogenesis

^of

systemic

diseases caused

by

^Salmonella

(Aitken

et

al., 1978).

A murine model was

developed

^to

investigate

effects of

previous

administration of

digestive

^{Helminths on sen-}

sitivity

^{of mice to a}

challenge

^with S. abortus ovis

(Lantier

et

al., 1979).

^{In this}

model,

Helminth

parasitism

^{induced two} types ^of modifications : it favoured translocation of

orally

inoculated Salmonella from the

gastro-

intestinal tract into the

host,

^{but it increased} resistance of mice to a

parenteral challenge

with S. abortus ovis. An

experiment

^{on this}

second type of interaction is

reported

^{here. It}

concerns S. abortus ovis and E.

falciformis,

^a

common mouse coccidia

(Owen, 1975).

Materials and Methods

Experimental

^mice

Groups

^{of ten male mice from two outbred}

strains were used . NMRI

(lffa Credo,

St Ger- main sur

I’Arbresle,

France) ^and CD-1

(ICR)

(Charles

River, Elbeuf, France). They weighed

20-25 g ^at the

beginning

^{of the}

experiments.

lnoculation with E. falciformis

The E. falciformis strain was maintained

by

frequent

passages

through

coccidia-free

mice,

sporulated

^{in 2%}

potassium

dichromate and stored at 4° C. The inoculum was

prepared by appropriate

dilutions in water from a

suspension

^{counted with a Thomas chamber.}

An infectious dose of 1 x 10’ oocysts ^{in 0.1 ml} of water was administered

by

^a stomach tube to each mouse.

Inoculation with S. abortus ovis

A

Streptomycin

resistant strain derived from S. abortus ovis 15/5 was cultivated on

trypticase

soy agar

(TSA, Biomérieux, Lyon, France)

with added

Streptomycin ⁽⁵⁰⁰ ¡.tglml, Specia, Paris, France),

^then

suspended

ⁱⁿ

phosphate

buffered saline as

previously

described

(Pardon

and

Marly,

^{19791. A dose of}

5

x 10 5

bacteria was

subcutaneously

^inoculat- ed in the left hind

footpad

^{of each mouse}

(SC/P inoculation).

This dose

represents

100 LD 50 for NMRI mice and 1/100 LD 50 for CD-1 mice when inoculated

by

^the SC/P route.

Bacterial enumeration in

spleens

All mice were killed

by

cervical dislocation six

days

after inoculation with S. abortus

ovis,

the time of maximal

splenic

^infection (Pardon and

Marly,

1979). Their

spleens

^were asep-

tically

removed and

homogenized.

^Individual

homogenates

^were diluted and cultivated on

TSA

plates

^with

Streptomycin ⁽⁵⁰⁰ N g/ml)

^as

previously

^described

^(Pardon

^and

Marly, 1979).

Viable counts of S. abortus ovis _per

spleen

^were

expressed

^as

log,, ^units,

^{the mean}

and standard deviation of the mean were cal- culated from the

logarithmic

^values.

XZ ^test (qualitative results),

^{t and F tests}

(quantitative results)

were used for statistical

analysis

^of results.

Experimental protocol

In a first

experiment,

groups of NMRI and CD-1 mice were inoculated at time of clinic

coccidiosis, eight days

after oral adminis- tration of E. falciformis. Controls received

only

^one of the

pathogens

^or

nothing (table 1 ).

In a second

experiment,

CD-1 mice were

inoculated with S. abortus ovis at various times before

(Exp. ^A)

^{or after}

(Exp. ^B)

^admi-

nistration of coccidia

(fig. ^{11. ).}

Results

Challenge

^{with S. abortus ovis at time of clinic}

coccidiosis

(table 1)

The

mortality

^{rate of}

parasitized

^{NMRI mice}

challenged

^with Salmonella was

significantly

reduced with

regard

^to the coccidia free controls (P <

0.05).

At the same

time, splenic

infection observed in CD-1 mice

previously

infected with E. falciformis was lower than that of controls (P < 0.01). Both Salmo- nella and Coccidia infections induced an

enlargment

^of

spleen.

Challenge

^{with S.} abortus ovis at various times before or after E. falciformis inoculation

(fig.

^{1A and}

^1B).

No difference

appeared

ⁱⁿ

splenic

^infections of CD-1 mice inoculated with bacteria one or

three

days

^{before coccidia}

administration,

when

compared

^to the coccidia-free controls.

In contrast, ^a

significant

^reduction

^(P

^<

^0.01)

of the number of bacteria in

spleens

^of

parasi-

tized mice was

regularly

observed when Sal- monella were inoculated at the same time or

after E. falciformis.

Discussion

Prior or simultaneous administration of a

high single

^{dose of} Coccidia resulted ^{in a} reduced

sensitivity

^{of CD-1 and NMRI mice to}

a subcutaneous

challenge

with S. abortus ovis. The

enlargment

^of

spleen

^{that was} induced

by

coccidia infection is indicative of

an activation of the reticulo-endothelial system

by

these

parasites.

The

pathological

process and

parts

^{of the}

immunological

process

associated

with cocci- dia infection in mice have been described

(Mesfin

and

Bellamy, 1978, 1979). They

include a local and

systemic inflammatory

^res-

ponse, that is concomittant to the destruction of intestinal

epithelial

^cells. As evidenced

by

Fauve and Hevin

(1975)

and Giroud et al.

(1979) artificially

^induced

inflammatory

^reac-

tions determine an

early

increase of resistance of mice to Salmonella

typhimurium

^{and Liste-}

ria

monocytogenes

infections.

Inflammatory

reactions may be

partly responsible

^{for the}

increase of resistance to S. abortus ovis of coccidia infected mice.

However,

^the pro- tective effect of the

parasite

^infection per- sisted at least two weeks and it

might

^be

mediated

by

^{other non}

specific

processes.

While similar types ^of

protection against

^bac-

teria have been described in other murine models with different

species

^of

parasites,

^the

mechanisms involved remain unknown

( Cypess et al., 1974a, b ; Katz, ^1980).

At least three types ^of modifications

by parasites

of host response

against

^bacteria

have been described in

litterature, depending

on the

parameters

^{that were} measured and times and routes of

antigen

administrations.

They

^{concern :}

- non

specific

enhancement of resistance as

described ⁱⁿ this paper,

-

contrasting

alteration of immune response

(Capron

^et

a/., 1977 ; Ogilvie

^and

Wilson, 1976),

- increase dissemination of bacteria from

gastro-intestinal

^{tract into the host.}

Accepted

^for

publication,

^June

l8th,

1981.

Summary

Resistance of outbred mice to subcutaneous

challenge

^with S. abortus ovis was increased when

previously

^or

simultaneously parasitized

with Eimeria falciformis. This was measured

by mortality

rates and levels of

splenic

^{infection induced}

by

Salmonella in

parasitized

and control NMRI or

CD-1

(ICR)

mice. No effect was observed when E. falciformis was inoculated

after

S. abortus o vis.

References

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P.W.,

^HALL

G.A.,

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CAPRON A., CAMUS D., DESSAINT J.P., LE BOUBENNEC-FISCHER E., 1977. Alterations de la reponse immune au cours des infections

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