Are stable flies (Diptera: Stomoxyinae) vectors of Trypanosoma vivax in the Central African Republic?

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Are stable flies (Diptera: Stomoxyinae) vectors of

Trypanosoma vivax in the Central African Republic?

Frank d’Amico, Jp Gouteux, Florence Le Gall, D Cuisance

To cite this version:

Original

article

Are stable flies

_{(Diptera: Stomoxyinae)}

vectors

of

Trypanosoma

vivax

in

the

Central

African

_Republic?

F D’Amico

JP

Gouteux

F Le Gall

D

Cuisance

1 _Laboratoire

_{d’écologie}

_{moléculaire, I8EAS, université de Pau et des}

Pays

de 1 Adour, 64000 Pau;

2_{Laboratoire de}

mathématiques

appliquées,

lpra,

Orstom,

c% université de Pau et des

Pays

de l’Adour, avenue de l’Université, 64000 Pau, France;

3_{World Bank,}

_{Agricultural Technology}

_{and Services Division,}

1818 H Street, NW,

Washington,

DC 20433, USA; 4_{Cirad-EMVT, c% Orstom,}

911, avenue

_Agropolis,

BP 5045, 34032 Montpellier cedex 1, France

(Received

7 _April 1995; accepted 21 November 1995)

Summary ―

The

_epidemiology

of Trypanosoma vivax infections was studied at a riverside site in the

Ouro-Djafoun

livestock area situated in the Central African

Republic during

the _period between

_July

1991 and

July

1992. This paper examines the

_possibility

that stable flies

_{(Diptera: Stomoxyinae)}

were also vectors of this _{trypanosome species} in a

_non-cyclic

_{way. Previous} studies have revealed that the usual

cyclic

transmission

_by

the tsetse

_fly

Glossina _fuscipes

_fuscipes

was

_probably

not the

_only

trans-mission route. At the _study site, at least five

species

or

_subspecies

of stable flies were encountered: Sto-moxys nigra

nigra (approximately

60% of the

sample),

S taeniata, S sitiens, S omega omega and Haematobia spp. The

hypothesis

that stable flies could be

_good

vectors of T vivax in this country is

sup-ported

by

three main observations: _i) stable flies were _{very abundant at the cattle}

_resting

_site;

_ii)

an esti-mation of the ’contact index’ between the cattle and stable flies demonstrated close interactions between cattle and stable flies at this site,

particularly during

the

rainy

season, and

iii)

there was a

_good

correlation

_(P

_{< 0.05)} between the apparent stable fly densities at the

_resting

site and the

_frequency

of T vivax in the cattle. The relevance of this _phenomenon in terms of _epidemiology and

_combatting

T vivax-caused _{nagana is discussed.}

Trypanosoma

vivax / stable

_{fly (Diptera: Stomoxyinae)}

/

_non-cyclical

transmission / nagana

epidemiology

/ Central African

_Republic

*

Résumé &horbar; Les stomoxes

_{(Diptera : Stomoxyinae)}

sont-ils vecteurs de _Trypanosoma vivax en

République

centrafricaine ?

L’épidémiologie

des _{trypanosomoses} à T vivax a été étudiée le _long d’une

galerie

forestière dans la zone

_{d’élevage d’Ouro-Djafoun (République}

_{centrafricaine)} entre _juillet 1991 1

et juillet 1992. Des recherches antérieures indiquent que la transmission cyclique de ce _trypanosome

par la

glossine

Glossina

fuscipes fuscipes

n’est

probablement

pas la seule voie. Ainsi, le

présent

tra-vail traite de la

_{possibilité pour les}

stomoxes

(Diptera ; Stomoxyinae)

d’être des vecteurs de T vivax par voie

mécanique.

Sur les sites étudiés, au moins _cinq

_espèces

ou

_{sous-espèces}

de stomoxes ont été recensées :

Stomoxys nigra

nigra

(approximativement

60 % de _{l’échantillon),} S taeniata, S sitiens,

S omega omega et Haematobia spp.

L’hypothèse

selon _laquelle les stomoxes _pourraient être de bons vecteurs de T vivax dans cette

région

est

_supportée

_par trois faits majeurs :

i)

les stomoxes étaient très abondants au niveau de l’aire de repos du bétail,

ii)

l’utilisation d’un <·index de contact» entre le bétail et les stomoxes a

_permis

d’établir l’existence d’interactions étroites entre ces animaux à l’aire de repos, en _particulier en saison des _pluies,

_iii)

il existait une bonne correlation

(p

< _0,05) entre les densités apparentes des stomoxes à l’aire de repos du bétail et les fréquences de T vivax chez les zébus. Les auteurs discutent finalement de

_{l’importance}

de ce

_phénomène

en termes

d’épidémiologie

et de lutte contre les _{trypanosomoses} à T vivax.

Trypanosoma

vivax / stomoxe

(Diptera: Stomoxyinae)

/ transmission

non-cyclique

/

épidé-miologie

du nagana /

République

centrafricaine

INTRODUCTION

The Central African

Republic (CAR)

is a

country

that does not have a

_breeding

tra-dition for cattle. Mbororo cattle arrived there around the 1920s

_{(Boutrais, 1988). By}

1928, the cattle number was estimated at 3 500

_(Bertucat,

1965; Crouail,

1969).

At

present,

there are two million head of cattle

(99%

of which are

_{trypano-susceptible}

Mbororo

zebu).

Due to _{the presence of} tsetse flies and

ticks,

the humid savannahs of the CAR remain somewhat unsuitable for livestock

_production.

As Mbororo zebu

cannot be

kept

without

chemoprophylaxis,

trypanosomosis

is a

_major

threat to

pro-ductivity.

We therefore undertook studies of the

epidemiology

of bovine

trypanoso-mosis in the CAR. Previous studies have

emphasized

the role of Glossina fusca

con-golensis (Yvor6

et

al, 1965a,

b)

and G

fuscipes fuscipes

(Finelle,

1957;

Cuisance

et

al,

1992).

In the centre of the

CAR,

where

G

_{f fuscipes}

is

dominant,

we found that this

species appeared

to be a _poor vector of

Trypanosoma

species

in cattle as no

rela-tionship

was observed between the Berenil index

(for

definition,

see

_Rogers,

1985,

and

Claxton et

al,

1989), trypanosome

infec-tions and

_challenges

at three

_study

sites

(D’Amico,

1993).

Moreover,

a recent sur-vey on the

_feeding

behavior of this tsetse

_fly

species

demonstrated that the number of bloodmeals from cattle was rather low

(12%

on

_{average) (Gouteux}

et

al,

1994).

Thus,

we

_postulated

that others vectors

_might

play

an

_important

role in the transmission of

trypanosomosis

to the

cattle,

in

_particular

Trypanosoma

vivax.

The purpose of the

_present

_paper was

to

_investigate

stable flies as

_potential

vectors

of these

trypanosomes.

MATERIALS AND METHODS

Area of

_study

The _{investigation} was carried out in the centre of the CAR, in the

_{Ouro-Djafoun breeding}

zone of the Ouaka district. A total of 19 Mbororo zebu cattle herds were studied

(Le

Gall et al,

1995).

One of these, because of its

epidemiological

inter-est and numerous other facilities, was

bank of the Mbonou river. In this zone, as else-where in the country, the climate is characterized

by a short dry season from December to March and a _longer

_rainy

season from

_April

to November

(Franquin

et al,

1988).

The _{average rainfall} recorded at Bambari from 1950 to 1981 was 1 500

mm _{per year. The landscape} consists of wet savannahs with a

_{large gallery}

forest network. The main tree species are Burkea africana,

Lophira

lanceolata and Daniella olivieri. The

grasslands

are characterized _by the

_development

of

_Andropogon

gayanus,

Hyparrhenia

welwitschii and H familiaris

(Boulvert, 1986).

Survey

of stable flies

The apparent densities of stable flies were deter-mined from catches in

_bipyramidal

traps

(Gou-teux,

1991)

and were

_expressed

as the number of flies

_caught

per trap per

day. Specific

identification of the flies was made

_according

to _{Zumpt (1973).} Their distribution was monitored

_along

a 500 m

transect

_using

11 traps set at

_regular

intervals. The transect followed the usual path used

_by

the herd

daily

to reach the

drinking

site and savannah

grazing

areas

_{(fig 1}

_The

flies were

_sampled

for 9-12

days

per month from

July

1991 to

_July

1992,

with the _exception of _January 1992.

Cattle surveys

The movements of the cattle were monitored in order to establish how their

grazing

range related to the distribution of the stable flies. This was achieved

by observing

the _daily

activity

patterns for 5-7

days

in the

dry

season

_(February),

interseason

(May)

and

rainy

season

_{(August 1992).}

The times of

departure for the

_grazing

and

_drinking

site and the times of return from the savannah were noted.

The presence of trypanosomes in the blood of the cattle was determined

_{by parasitological}

and

serological techniques.

Blood

samples

were col-lected from the cattle in October 1991 and Febru-ary, June and

_August

1992. The

_{parasitological}

techniques used were haematocrit

_{centrifugation}

and examination of the

buffy

coat or direct

micro-scopic examination of the thin and thick blood films stained with Giemsa (Molyneux, 1975; Murray et al,

1977).

The

_{serological technique}

used was

_antigen

detection _using monoclonal antibodies _(ELISA),

as described _{by Nantulya} and

_Lindqvist

₍₁₉₈₉₎ and

Nantulya

et al

(1992).

Each animal that was

found to be

positive by buffy

coat examination was

immediately treated with Berenil’A, at a dose of 3.5

mg/kg body weight.

The

_frequency

was assessed from

_{parasitological}

and

_serological

data and was

Data

_analysis

The data were

_analysed:

_i) in order to estimate the

intensity

of contact

(K)

between stable flies and cattle at the two

points

of

presumed

interaction, ie,

the

_drinking

site and the

_resting

and

_milking

site;

Kwas determined from the product of the appar-ent

_density

of flies and the time

(h)

spent

daily

by

one zebu at these two sites

_{(fig 1)}

divided

_by

the number of zebu in each group

(n);

and

ii)

to examine the

_relationship

between stable

_fly

den-sities and _{trypanosome frequency.} The latter

rela-tionship was measured after

pooling monthly

data for stable

_fly

densities at the

_resting

site; these values were then compared with the next month’s

trypanosome frequency in the cattle. Statistical

analysis was

_{performed using regression}

analy-sis

(Foucher, 1992).

RESULTS

Stable

_fly

_species

and relative densities

At the

_study

site,

at least five

_species

belonging

to two _{genera of}

_Diptera

were

encountered. Four

_{species belonged}

to the

genus

Stomoxys: Stomoxys nigra nigra

Macquart,

1851,

S taeniata

_Bigot,

1888,

S sitiens

Rondani,

1873 and S omega omega

Newstead,

1907. The individuals

that

_belonged

to the _genus Haematobia

have

_yet

not been

_accurately

identified. The

most

_{widespread species}

was S

_{nigra nigra}

(approximately

60% of the whole

_sample)

followed

_by

Haematobia sp. In the

follow-ing

discussion,

all these

_species

are

_grouped

under the name ’stable flies’. Their distri-bution and

abundance,

_along

the transect,

are shown in

_figure

2. The stable flies were

caught anywhere along

the main cattle

_paths

between the

_resting

site and the

_drinking

site as well as the

grazing

site further away.

However,

the maximum

_density

was observed at the

_resting

and

_milking

site where it reached up to ten _{flies per}

_day

at

trap

10, in June 1992.

_During

the

dry

sea-son, the number of flies

caught greatly

decreased,

to less than 0.1

_fly

_per

_trap

_per

Daily activity pattern

of cattle

Our field work showed that time

_spent

at

the

_resting

site,

as well as at

pasture,

varied

according

to the season.

_During

the

_dry

sea-son, it was shorter than in the

_rainy

season. The time

spent

at the

_drinking

site was

extremely

short,

averaging

5 to 10 _{min per}

day (see

table

_I).

Contact index between stable flies and cattle

A

simple

index of contact

_(K)

between one zebu and stable flies was calculated for

calves and adults at two

_particular

sites:

i)

the cattle

_resting

and

_milking

site;

and

ii)

the cattle

_drinking

site. K estimates for the months of

_February

_(dry

_{season), May}

(interseason)

and

_{August (rainy season)}

are shown in table I. This index is

_extremely

low or even zero at the

drinking

site. It ranges between 0.02 and 2.94 at the

rest-ing

and

_{milking place.}

K is

_{always higher}

for calves than it is for adults.

Thus,

if K

actually

reflects the interactions

_existing

between the cattle and the stable

flies,

we

can assume that

only

rare interactions occur between the cattle and the stable flies at the

_drinking

site. In contrast, such

interac-tions are

_{frequent particularly during}

the

rainy

season

_(August)

at the

_resting

and

milking place

and

they

are

_higher

for calves than for adults.

Trypanosome frequency

in cattle Table II shows the four

_monthly

estimates of

trypanosome

frequency

detected in Mbororo cattle

_using

either

parasitological techniques

or a

_{serological immunodiagnostic technique}

(ELISA).

The ELISA

_technique

revealed a

high frequency

of

_{T congolense,}

the

domi-nant

_species.

T vivax

_{frequency ranged}

from

0 to 14.5%

using parasitological

methods

and from 8.2 to 19.4%

_using

ELISA.

Relationship

between stable flies densities and

_trypanosome

frequency

in cattle

No

_relationship

was found between the four

fre-quency of T congolense and T brucei using

either

_{parasitological techniques}

or the

immunodiagnostic technique. Significant

regressions

occurred between the four

monthly

estimates of T vivax

_frequency

in cattle and the stable

_fly

densities at the

rest-ing

site. This

_relationship

was

_highly

signif-icant

_(P

_{< 0.05)}

with a correlation coefficient

(r)

of 0.968 for

_{parasitological techniques}

and of 0.997 for the ELISA

_technique.

The

equations

obtained for the

_regression

anal-yses shown are _y = 0.207x - 0.062 if the

parasitological

frequency

was considered and y= 0.149x+ 0.046 if ELISA data were used

_{(fig 3).}

DISCUSSION

The

_possibility

of

_{haematophagous}

arthro-pods transferring trypanosomes

between hosts without any

biological development

of the

_agent

has been under

_study

for a

_long

time

_(Bouet

and

Roubaud, 1912; Buxton,

1955). Many species

of

_{trypanosomatids}

are known to be transmitted

_through

a

mechanical mechanism

_(Wells,

1972; Foil,

1989).

T evansi,

the first

_pathogenic

try-panosome shown to cause disease in

domestic

livestock,

is

_{usually mechanically}

transmitted

_by

tabanids and stable flies

Amer-ica,

T vivax is

_thought

to be transmitted

sim-ilarly

(Gardiner, 1989).

In these areas,

devoid of tsetse, 5 calcitrans and horse flies such as

_Cryptotylus

_{unicolor (Foil, 1989),}

Tabanus

_importunus

_{(Raymond, 1990)}

and T nebulosus

_(Otte

and

Abuabara,

1991)

are efficient transmission vectors. In

tropical

Africa,

where tsetse

flies,

tabanids and

sta-ble flies

coexist,

the

_problem

of

determin-ing

the contribution of mechanical

trans-mission is

_especially

acute. The

_persistence

of

_{trypanosomosis}

due to T vivax in endemic foci in tsetse-free areas

_emphasizes

the role of other insects such as tabanids and stable flies

(Bauer

et

al,

1988; Nawathe et

al, 1988;

Chollet, 1992;

Van der

Merwe,

1992).

In

Sudan

_{(Buxton, 1955)}

and Zimbabwe

_(Boyt

et

al,

1970),

the existence of mechanical transmission for T

_congolense

has been

suspected.

It has been

experimentally

demonstrated with the tabanid Tabanus

tho-racinus (Foil, 1989).

It has now _been

exper-imentally

proven that T brucei can be

trans-ferred

_{through non-cyclic propagation by}

tabanids

_{(Foil, 1989),}

the stable

_fly

5

calci-trans

_(Straif

et

al,

1990)

and

_by

G

morsi-tans morsitans

_(Roberts

et

al,

1989).

Recently,

Mihok et al

(1995a)

demonstrated that six taxa of African

_{stomoxyinae biting}

flies

_{(S niger niger,}

5

_niger

bilineatus,

S

varipes,

5

taeniatus,

5

pallidus

and Haema-tobosca

_squalida)

were

_capable

of

trans-mitting

T brucei,

T vivax and T evansi

mechanically

to mice in

_laboratory.

How-ever, until now, little data was available to

address the

_question

of the relative

impor-tance of

_non-cyclic

transmission of

try-panosomes under natural conditions when the

major

route of transmission of these par-asites is due to tsetse flies

_(Wells,

1972;

D’Amico, 1993; D’Amico et al,

1992).

Since the

_beginning

_{of studies of nagana}

in

_Africa,

_{the group of}

_Stomoxyinae

flies has been the _{least studied among all proven} or

suspected

vectors.

Nevertheless,

it is a well-distributed group in several countries and the recent

study

of Mihok

₍₁₉₉₃₎

in

Kenya

demonstrated 11

_species

and

_subspecies.

In

the

CAR,

our

_{preliminary investigations}

reveal the occurrence of at least five

species.

Further

studies,

together

with a

systematic

revision of the stable

_fly

group, will

_probably

lead to an increase in this num-ber.

Independent

of the abundance and

ecology

of each

species,

our work

sug-gested

that these

_arthropods

were

_good

candidates as vectors of T vivax

try-panosomosis

in this

country.

This

hypoth-esis,

initially proposed

to

explain

the

appar-ent seasonal and uncertain

aspects

of

_cyclic

trypanosome

transmission due to

G

_{f fuscipes (D’Amico, 1993),}

was

_supported

by

the data

_presented

above. The first observation was the abundance of stable flies at the cattle

_resting

site. The second was the

_high

value for the contact index between cattle and

_Stomoxys

_spp at this

resting

site. The

_concept

of contact

index,

although

imperfect

and

_simply

calculated,

is of interest and deserves a more refined mathematical

_approach.

The third correlation was the one

_existing

between the

_apparent

densities of the

_Stomoxys

spp at the

_resting

site and the T vivax

_frequency

in cattle.

Although

it was based on a small

_sample,

limited in _space and

time,

and the ELISA

immunodiagnostic technique

needs further

confirmation,

the

_general

association seemed valid.

Moreover,

this

_hypothesis

was also

_{supported by}

the fact that a control

strategy

using

bipyramidal

traps

set at

cat-tle

_{drinking points}

had no _{effect upon the}

Tvivaxfrequency

in cattle

_{(D’Amico, 1993).}

This observation

_suggested

that this

_parasite

species

was

_probably

not transmitted at this

site

_{by only}

the tsetse

_fly

G

_{f fuscipes,}

as

populations

of this tsetse

_species

are

seri-ously

affected

_by

this mode of control

(Gou-teux and Le Gall,

1992; Le Gall et al,

1995).

However,

to confirm the

_proposed

hypothesis

that stable flies were efficient

vectors of T vivax we must

_initially

extend our observations to

_larger

_{epidemiological}

foci in the CAR and

_secondly

we need to

acquire

direct evidence. The presence of

should be

_conclusively

_proven

_by

PCR

tech-niques

(Masiga

et

al, 1992;

Bromidge

et

al,

1993).

However,

the detection of the

para-site does not

_{unequivocally}

_{prove its}

trans-mission to cattle.

_Similarly,

the existence of the

_pathology

in the cattle is not

_proof

of

transmission. This

_knowledge

is,

neverthe-less,

essential as it

_permits

the estimation of the

_proportion

of stable flies

_bearing

try-panosomes in natural

populations

and is of

particular

value for

_quantifying

the

impor-tance of mechanical transmission under

nat-ural conditions. The actual demonstration of the mechanical transmission of T vivax

by Stomoxys

spp

requires

in situ

experi-mental transmission trials.

_Eventually,

the information obtained from control

_campaigns

against haematophagous

insects

_using

cat-tle

’pour-on’

insecticides will be

_important

in

_{demonstrating}

the existence of mechan-ical transmission. At the moment, we are

testing

the effects of pour-on

impregnations

(Deltamethrin

Spot-on

*

and Flumethrin

Bayticol°)

on natural

_populations

of stable flies and tsetse flies in the

_Ouro-Djafoun

livestock area of the CAR.

In

conclusion,

in tsetse-infested areas,

the

_possible

occurrence of mechanical

trans-mission of T vivax to cattle

_by

haematophagous

insects continues to be

an unresolved

_{problem. Although}

mechan-ical transmission

_by

stable flies and

partic-ularly by

horse flies has

_already

been

exper-imentally

proven, the

_{epidemiological}

importance

of this

_phenomenon

in the field is still

poorly

understood. In the

CAR,

our initial

_{investigations suggest}

that

mechani-cal transmission does take

_place

and we have

presented

evidence that stable flies were

_significant

vectors _{of T vivax and}

per-haps T congolense or

T brucei. This

_study

provides

new data

_concerning

the modes of transmission of bovine

_{trypanosomosis}

in the CAR. Until now, in most

epidemio-logical

foci,

the transmission of nagana was

chiefly

ascribed to G

_{f fuscipes}

and the

cat-tle

_{drinking point}

was considered to be the

privileged

site of transmission. In

_future,

it

must be considered that modes of

try-panosomosis

transmission are more

com-plex

than

_{previously thought.}

G

_{f fuscipes}

is the main vector of T

con-golense,

T vivax and T

brucei,

because it transmits these

_{parasites cyclically}

and

per-haps mechanically

and also because it con-stitutes an

_important

reservoir for these

try-panosomes

(D’Amico

et

al,

1992). Although

intervention

_by

stable flies is

_{highly probable,}

the

possible

role of other

_{haematophagous}

diptera

such as horse flies and G fusca must

be

_kept

in mind

_(Finelle,

_1957;

Finelle et

al,

1963). Finally,

it is _very

_likely

that this

epi-demiological

system

is based on a mixed

transmission,

_combining

mechanical and

cyclical

methods,

and

involving

at least two

groups of vectors.

_According

to this

_theory,

cattle

_resting

and

_milking

sites are at risk from

trypanosome

challenge

as well as

drinking points.

The

_{epidemiological}

impli-cations of movement

_patterns

of cattle are detailed elsewhere

_(D’Amico

et

al,

1995).

These facts are

_important

_{for nagana} control. At

present,

the

_{campaign against}

this

_pest

in CAR is based on a combina-tion of

_{chemoprophylaxis}

and

_trapping

against

G

_{f fuscipes using bipyramidal}

_traps

(Gouteux, 1991)

set at

_{drinking points}

(Cui-sance et

al,

1992; Gouteux and Le

Gall,

1992). Strategies

should now include

tech-niques

for

_reducing

the number of stable flies which are, in _any case, serious live-stock

pests,

causing

irritation to the cattle which results in

_weight

loss and reduction in

milk

_{yield. Following}

the

_strategy

chosen

in this

_country,

we advocate the use of

bipyramidal

traps

at both the

_drinking

_points

and the

_resting

sites. The

traps

designed

for

_collecting

tsetse flies have also

_proved

effective

_against

_Stomoxys

_(Rugg,

1982;

Mihok et

al,

1995b).

There is also scope for

_improving

the

_traps

and

_controlling

sta-ble flies

_{populations by using}

colour blue

(Holloway

and

_{Phelps, 1991}

_{). In}

the

future,

efficacy

of

_bipyramidal

traps

in

_catching

sta-ble flies in the CAR. We also look forward to

the results _{of the programme}

_presently

being

initiated in the same areas to

_attempt

to control the

_populations

of tsetse flies and stable flies

_{using ’pour-on’}

and

_{’spot-on’}

formulations of insecticides

placed directly

on the cattle.

ACKNOWLEDGMENTS

This _study received financial support from the Government of the CAR, the World Bank, the

European Development

Fund and the govern-ment of France

(Fonds

d’aide et de

cooperation).

F D’Amico was _financially

_{sponsored by}

the gov-ernment of France

(Ministere

de la Recherche et de

_I’Espace).

We thank the director of CIRAD-EMVT

_(France),

the director of the

_D6partement

Sant6 of ORSTOM

_(France),

the director and the staff of the

Agence

nationale pour le

d6veloppe-ment de

[’61evage (CAR),

VM

Nantulya

and PAO

Majiwa

of ILRAD

(Kenya),

JL Frezil and C Bel-lec of ORSTOM

_(France),

C Mouches of Univer-site de Pau et des

_Pays

de I’Adour

_(France),

M Bouchier of INRA

_(France),

C Foucher of CIRAD

(France)

and

especially

P Gardiner of ILRAD

(Kenya)

and G

Uilenberg

of CIRAD-EMVT

(France)

for their

help

and valuable comments

on the _manuscript.

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