SUSCEPTIBILITY OF RODENTS TO INFECTION
WITH SCHISTOSOMA MANSONI IN RICHARD-TOLL (SENEGAL)
S È N E M.*,**, D U P L A N T I E R J.M.*,***, M A R C H A N D B.**** & H E R V É J.P.* *****
Summary :
The susceptibility of Arvicanthis niloticus, Mastomys huberli, Mastomys erythroleucus and Mus musculus was studied to assess the capacity of these rodents to transmit Schistosoma mansoni. The susceptibility was determined by the percentage of adult
schistosomes recovered, the number of eggs per gramme of faeces, the viability of these eggs and the capacity of the rodents to maintain the life cycle of Schistosoma mansoni. The
percentages of adult worms recovered were respectively 1 8 %, 11.5 %, 8.4 % and 20.5 % in A. niloticus, M. huberti,
M. erythroleucus and M. musculus. After infection, they liberate in the environment viable eggs whose miracidia are infectious for the intermediate host (Biomphalaria pfeifferi). The mean egg load was 300 ± 327.8 in A. niloticus ; 6 6 4 ± 673.5 in M. huberti;
240 ± 304.8 in M. erythroleucus ; 4 0 0 ± 361.5 in M. musculus.
KEY WORDS : Arvicanthis niloticus, Mastomys huberti, Mastomys erythroleucus, Mus musculus, Richard-Toll, rodents, Senegal, Schistosoma mansoni.
Résumé :
SUSCEPTIBILITÉ DES RONGEURS À L'INFESTATION PAR SCHISTOSOMA MANSONI À RICHARD-TOLL (SÉNÉGAL) La susceptibilité de Arvicanthis niloticus, Mastomys huberti, Mastomys erythroleucus et Mus musculus à l'infestation par Schistosoma mansoni a été étudiée pour évaluer la capacité des Rongeurs à jouer un rôle dans la transmission de la schistosomiase intestinale à Richard-Toll. La susceptibilité de ces rongeurs a été déterminée par le pourcentage de vers adultes récupérés après infestation, le nombre d'oeufs par gramme de fèces, la viabilité de ces œufs et la capacité des rongeurs à maintenir le cycle de développement de Schistosoma mansoni. Les pourcentages d'adultes récupérés sont, respectivement, 18 %, 1 1,5 %, 8,4 % et 20,5 % chez A. niloticus, M. huberti, M. erythroleucus etM. musculus. Après infestation, les Rongeurs libèrent, dans le milieu extérieur, des œufs viables dont les miracidia sont infestants pour l'hôte intermédiaire (Biomphalaria pfeifferi). Le nombre moyen d'œufs libérés est de 300 ± 327,8 chez A. niloticus,
664 ± 673,5 criez M. huberti, 240 ± 304,8 chez M. erythroleucus et 400 ± 361,5 chez M. musculus.
MOTS CLES : Arvicanthis niloticus, Mastomys huberti, Mastomys erythroleucus, Mus musculus, Richard-Toll, Rongeurs, Sénégal, Schistosoma mansoni
INTRODUCTION
I
n Richard-Toll, North Senegal, the p r e s e n c e o f Schistosoma mansoni among rodents was reported for the first time in 1990, two years after the emer- g e n c e o f a n e w focus o f intestinal schistosomiasis.Duplantier et al. ( 1 9 9 2 ) had s h o w n that two s p e c i e s o f Muridae, Arvicanthis niloticus and Mastomys huberti.
w e r e naturally infected.
T h e present work was undertaken to study the sus- ceptibility o f A. niloticus and M. huberti to infection
* Programme « Eau & Santé -. ORSTOM, BP 1386, Dakar, Sénégal.
** Département de Biologie Animale, Faculté des Sciences, Univer- sité Cheikh Anta Diop de Dakar, Sénégal.
*** Institut des Sciences de l'Évolution, CNRS URA 327, c.c. 064, Uni- versité Montpellier II, 34095 Montpellier Cedex 05, France.
**** Laboratoire Arago, Université P. et M. Curie (Paris 6), CNRS URA 2156, BP 44. 66651 Banyuls-sur-Mer Cedex, France.
***** ORSTOM Montpellier, BP 5045. 911. avenue Agropolis, 34032 Montpellier Cedex, France.
Correspondence : Dr. Manama Sène.
with S. mansoni. T w o other s p e c i e s o f rodents (Mas- tomys erythroleucus and Mus musculus) w e r e studied as controls. M. erythroleucus b e l o n g s to the s a m e genus and has the s a m e activity as M. huberti. M. mus- culus is c o m m o n l y used in laboratory. In order to determine the degree o f susceptibility o f these rodents to S. mansoni infection, w e have studied the percen- tage o f adult w o r m s r e c o v e r e d after perfusion, the fecundity o f the female schistosome harbored, and the capacity o f the hosts to maintain the life cycle o f S. mansoni.
T h e susceptibility o f A. niloticus to infection with S. mansoni had already b e e n s h o w n by Stirewalt et al.
(1951), Kuntz & Malakatis (1955), D u m o n & Quilici ( 1 9 7 6 ) , K a r o u m & A m i n (1985) a n d M b i e u l e u - Nkouedeu (1990).
Although the susceptibility o f Mastomys natalensis to infection with S. haematobium was studied by Pitch- ford & Visser (1962) and G e a r et al. (1966), the sus- ceptibility o f M. huberti and M. erythroleucus to infec- tion with S. mansoni o f African origin has never b e e n studied before.
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1996034321
MATERIALS AND METHODS
F
rom e a c h s p e c i e s o f rodents, twenty adults, 10 males and 10 females, w e r e experimentally infected. S o m e o f the A. niloticus used for this study w e r e trapped in the « Niayes », Dakar, w h e r e intestinal schistosomiasis has never b e e n reported as far as w e k n o w . H o w e v e r , to b e sure they did not harbor any S. mansoni infection, they w e r e isolated for four w e e k s , and tested for infection. All the M. huberti, the M. erythroleucus, and the M. musculus (Swiss m i c e ) w e r e born and bred in the laboratory.Using the paddling method, all rodents s p e c i e s w e r e e x p o s e d to cercaria s h e d by B. pfeifferi from Richard- Toll for 15 min. T h e n u m b e r o f cercaria used was 6 0 0 for A. niloticus, M. huberti and M. erythroleucus and 150 for M. musculus. T h e infected rodents w e r e kept at the animal house. Seven w e e k s later, they w e r e per
fused in a c c o r d a n c e with the Duwall and Dewitt ( 1 9 6 7 ) m e t h o d and the s c h i s t o s o m e s r e c o v e r e d c o u n t e d to assess the percentage o f adults worms. After perfusion, the liver, the mesenteric veins and the lungs w e r e r e m o v e d and e x a m i n e d under light m i c r o s c o p e to s e e w h e t h e r adult w o r m s w e r e trapped in.
T h e fecundity o f S. mansoni was randomly studied a m o n g 10 individuals in A. niloticus, M. huberti, M. musculus and M. erythroleucus without sexual dis
tinction. T h e n u m b e r o f eggs per g r a m m e o f faeces w a s c o u n t e d b y t h e m o d i f i e d K a t o - K a t z m e t h o d (Stelma el al.. 1 9 9 3 ) and their viability tested by hat
ching them. W e e k l y fecal examination w a s also car
ried out to establish the pre-patent period.
T o study the capacity o f rodents to maintain the life cycle o f S. mansoni from Richard-Toll w e just evaluate their ability to b e infected, to d e v e l o p adult parasite and then to pass, in the nature, viable eggs insuring the continuity o f the cycle. T h e S. mansoni strains used to maintain the life cycle in A. niloticus and M. huberti w e r e isolated respectively from t h e s e t w o s p e c i e s . Meanwhile, M. erythroleucus and M. musculus w e r e i n f e c t e d with c e r c a r i a s h e d by naturally i n f e c t e d B. pfeifferi. All the rodents and the snails (Biompha- laria pfeifferi) used throughout the study o f the life cycle w e r e born in the laboratory. At e a c h passage twenty snails w e r e e x p o s e d individually to three o r four miracidia overnight. Cercaria s h e d by the positive snails w e r e used to infect different s p e c i e s o f rodents.
Eight w e e k s later, perfusion was performed to recover adult w o r m s from rodents. T h e liver and the faeces w e r e analysed in search o f viable eggs. T h e s e last were used to infect other snails and so on. In order to find out whether the passage o f the parasite strain from o n e rodent s p e c i e s to a n o t h e r c o u l d influence the infecti- vity o f the miracidia, other s p e c i e s w e r e cross-infected at e a c h passage. For e x a m p l e , M. huberti, M. erythro
leucus and M. musculus w e r e e x p o s e d to cercaria o f first a n d s e c o n d g e n e r a t i o n s , s h e d by B. pfeifferi infected with miracidia o f A. niloticus origin and des
cent.
RESULTS
PERCENTAGE O F ADULT W O R M S R E C O V E R E D
^ he n u m b e r o f adult S. mansoni recovered from rodents varied greatly b e t w e e n different spe- _1_ cies, and b e t w e e n individuals within s p e c i e s ( T a b l e I ) .
T h e 2 0 A. niloticus e x p o s e d h a r b o r e d a total o f 2,159 schistosomes, 1,506 males and 6 5 3 females, with a m e a n w o r m load o f 108 ± 130.5 and a w o r m return o f 18 %. T h e sex-ratio o f male to female is 2.3. No sub
stantial differences were observed b e t w e e n the n u m b e r o f s c h i s t o s o m e s r e c o v e r e d from m a l e a n d f e m a l e rodents (X2 = 2 . 8 9 , P > 0 . 0 5 ) . Considering the m e a n w o r m load, the results b e t w e e n males and females w e r e c o m p a r a b l e ( T a b l e II).
In total, the M. huberti harbored 1,380 S. mansoni a m o n g w h i c h 8 3 4 males and 5 4 6 females, represen
ting a w o r m return o f 11.5 % and a mean parasite load o f 6 9 ± 4 7 . 2 . T h e sex-ratio o f m a l e to female w a s 1.5.
T h e difference o b s e r v e d b e t w e e n male and female rodents was barely significant (%2 = 4 . 4 0 8 , P = 0 . 0 5 ) . H o w e v e r , the mean w o r m load did not vary signifi
cantly b e t w e e n male and female M. huberti ( T a b l e II).
T h e 2 0 M. erythroleucus harbored 1,013 s c h i s t o s o m e s , 7 1 2 males and 301 females. T h e worm return was 8.4 % with a m e a n parasite load o f 5 0 . 5 ± 4 1 . 7 . T h e sex-ratio o f male to female was 2.4. T h e n u m b e r o f adult S. mansoni r e c o v e r e d from M. erythroleucus males was significantly higher than that r e c o v e r e d from females (%2 = 2 3 . 3 , P < 0 . 0 0 1 ) . O n the contrary, the m e a n worm load w a s not different b e t w e e n male and female rodents ( T a b l e II).
T h e 2 0 M. musculus h a r b o r e d 6 1 6 s c h i s t o s o m e s , 3 9 4 males and 2 2 2 females. T h e w o r m return was 20.5 % with a m e a n parasite load o f 3 0 . 8 ± 3 0 . 4 . T h e sex-ratio o f male to female is 1.8. T h e n u m b e r o f adult schistosomes recovered was significantly higher among male than female rodents (j2 = 4 8 . 0 2 , P < 0 . 0 0 1 ) . T h e m e a n load worm was higher in male than female M. musculus ( T a b l e II).
No worm was found in the lungs od A. niloticus, M. huberti, M. erythroleuceus and M. musculus.
F E C U N D I T Y O F S. MANSONI FEMALE
14.3 % o f the A. niloticus b e g a n to e x c r e t e eggs six w e e k s post infection. All o f the M. huberti, M. ery-
322 Mémoire Parasite, 1996, 4, 321-326
RODENTS AND SCHISTOSOMA MANSONI IN SENEGAL
N u m b e r o f w o r m s r e c o v e r e d
R o d e n t s A. niloticus M. huberti M. etythroleucus M. musculus
S m M S m F Total S m M S m F T o t a l S m M S m F T o t a l SmM S m F T o t a l
8 3 11 4 5 9 3 3 6 1 3 3 16
1 11 12 11 0 I 1 4 4 8 13 6 19
11 7 18 17 o 17 1 i 4 18 13 8 21
11 3 2 5 21 9 3 0 2 3 11 3 4 19 3 2 2
M a l e s 9 2 4 3 3 3 3 8 il 3 5 2 0 5 5 19 6 2^
(n = 1 0 ) 19 1 8 3 7 7 0 0 7 0 3 2 3 1 6 3 13 18 31
4 5 36 81 5 8 4 6 1 0 4 4 3 3 0 7 3 3 6 8 4 4
7 4 5 8 1 3 2 5 7 51 1 0 8 i3 2 8 " 1 3 9 2 4 6 3
2 0 7 1 0 7 3 1 4 5 8 6 7 1 2 5 5 3 3 5 8 8 6 2 31 9 3
2 6 4 1 1 3 3 7 7 1 0 3 3 3 1 3 6 157 15 1 7 2 7 5 5 2 127
10 8 18 1 4 9 7 11 18 4 4 8
1 " 1 I 31 1 4 5 12 8 2 0 8 2 lu
17 2 0 3 7 1 5 1 8 3 3 1 1 11 2 2 6 5 11
2 7 11 3 8 4 7 2 2 6 9 21 8 2 9 9 1 11
F e m a l e s 3 8 1 9 5 7 29 |2 " 1 1" 13 3 0 8 6 14
(n = 1 0 ) 2 6 4 1 6 7 6 1 2 9 9 0 11 8 3 0 7 8 15
3 5 IS 8 0 4 1 5 3 9 4 2 8 5 3 3 9 9 1 8
112 ¡9 161 7 3 32 1 0 5 2 8 5 3 3 12 8 2 0
112 5 2 K . I 3 9 6 7 1 0 6 8 4 1 8 L02 9 12 21
4 5 2 14 4 6 6 9 5 5 6 L51 7 5 3 3 108 2 0 7 r
T a b i c I. — N u m b e r o f w o r m s r e c o v e r e d from 1 0 m a l e s a n d 1 0 f e m a l e s o f t h e r o d e n t s Art'icantbis niloticus, Mastomys huberti, Mastomys erythroleucus and Mus musculus, s e v e n w e e k s after e x p o s u r e t o Schistosoma mansoni f u r c o c e r c a r i a ; S m M = S. mansoni m a l e , S m F = S. man- soni f e m a l e .
MAINTENANCE O F LIFE CYCLE
S. mansoni w a s maintained for at least three genera- tions in M. musculus (Swiss m i c e ) , t w o generations in A. niloticus a n d M. erythroleucus and only o n e g e n e - ration in M. huberti.
Snails e x p o s e d to miracidia o f first generation isolated from e g g s e x c r e t e d b y o n e A. niloticus naturally infected, b e g a n to p r o d u c e cercaria four w e e k s later.
A. niloticus, M. huberti, M. erythroleucus e x p o s e d to these cercaria o f first generation d e v e l o p adult worms.
Miracidia o f s e c o n d generation isolated from their liver and faeces w e r e used to infect other snails which give birth to infective cercaria o f s e c o n d generation. As far as S. mansoni o f A. niloticus origin a n d descent are c o n c e r n e d , only S. mansoni males w e r e r e c o v e r e d from A. niloticus and M. huberti at the e n d o f the s e c o n d passage. T h e cercaria o f A. niloticus origin and M. huberti o r M. erythroleucus d e s c e n t w e r e infective.
T h e y d e v e l o p into adult w o r m s a n d pass viable eggs in nature.
T h e miracidia isolated from viable eggs e x c r e t e d b y o n e M. huberti trapped in Richard-Toll w e r e used to infect B. pfeifferi. Four w e e k s post-infection, the snails shed cercaria which w e r e used to infect o n e A. nilo- ticus, o n e M. huberti a n d o n e M. erythroleucus. Eight w e e k s later, all S. mansoni adult recovered w e r e long, thin a n d tangled o f shape. It was difficult to distinguish the male a n d the female schistosomes.
R o d e n t s s p e c i e s S e x Schistosoma mansoni m e a n ± s.d.
T e s t t d e S t u d e n t
d.f. = 1 8
A. niloticus M a l e F e m a l e
1 0 4 ± 1 3 3 . 4 1 1 1 . 9 ± 1 3 . 6
0 . 1 3 2 NS
M. huberti Male F e m a l e
6 5 . 1 ± 4 . 7 7 9 . 9 ± 4 6 . 9
0 . 3 6 1 NS
M. erythroleucus Male F e m a l e
5 8 . 8 ± 4 9 . 1 4 2 . 5 ± 3 3 . 4
0 . 8 6 8 NS
M. musculus Male F e m a l e
4 6 . 1 ± 3 7 . 4 1 5 . 5 ± 5 . 9
2 . 5 5 8 *
Table II. — Mean number of S. mansoni adult recovered from male and female rodents; d.f. = degree of freedom, NS = not significa- tive. * = significative.
throleucus, M. musculus a n d 7 1 % o f the A. niloticus b e g a n to e x c r e t e eggs in their faeces seven w e e k s after infection. T h e number o f eggs per g r a m m e o f faeces and o f miracidia h a t c h e d p e r 24 h varied considerably in different individuals. T h e m e a n e g g load a n d the mean miracidia hatched per 24 h are shown in Table II.
In all rodents s p e c i e s the n u m b e r o f e g g s p e r g r a m m e correlated significantly with t h e n u m b e r o f female w o r m s recovered, apart from A. niloticus.
T h e eggs r e c o v e r e d from the liver a n d t h e faeces w e r e viable a n d infective.
R o d e n t s N u m b e r S e x - N u m b e r o f e g g s N u m b e r o f m i r a c i d i a
o f 5 . mansoni r a t i o e p g e p g / S m f / 2 4 h / 2 4 h / S m f
f e m a l e
A. nilolicus
M B A 6 4 8 3 7 . 3 0 о 0 0
M B A 6 7 0 3 2.7 6 0 2 0 0 0
M B A 5 5 8 14 3 2 . 3 0 0 0 0
M B A 6 7 1 il 0 . 6 8 0 1.9 0 0
M B A 6 6 7 5 8 1.3 180 3 1 0 0
M B A 6 6 9 52 2 . 1 2 8 0 0 0 0
R E T 8 7 4 9 2 . 3 9 8 0 2 0 4 0 0 . 8
R E T 1 0 8 1 0 7 1.9 3.7 12 0 . 1
R E T 1 0 4 1 13 2 . 3 7 4 0 6 . 5 1 3 4 1.2
E 1 9 9 / 1 14 1.2 2 8 0 2 0 6 0 . 4
M e a n ± s.d. 4 5 . 4 ± 3 9. 7 3 0 0 ± 3 2 7 . 8 192 ± 4 2 . 2
Mastotnys huberti
E 81/11 9 2 . 3 5 6 0 6 2 . 2 5 0 5.5
E 81/11 6 7 0 . 9 6 4 0 9 . 6 2 7 0 4
E 81/11 8 4 2 6 0 3 2 . 5 0 0
E 106/11 2 2 2.1 8 8 0 4 0 0 0
E 97/11 0 0 0 0 о
E 9 7 / I I 0 0 0 (1 0
E 97/11 0 0 0 о 0
E 78/11 6 7 0 . 6 1.780 2 6 . 6 1 3 0.2
E 97/11 5 3 0 . 8 7 2 0 1 3 . 6 1 6 2 3.1
E 1 9 4 / 1 4 2 0 . 7 1,800 4 2 . 9 111 2 . 6
M e a n ± s.d. 2 6 . 8 ± 2 7 . 9 6 6 4 ± 6 7 3 . 5 6 0 . 6 ± 9 2 . 7
Mastomys erythroleucus
E 94/11 15 10.5 7 0 0 4 6 . 7 3 9 1 2 6 . 1
E У 1 II 2 0 1.75 10 2 9 0. 4 5
M B A 5 8 9 1 3 1.3 8 0 6.2 1 4 1.1
E 1 0 5 / Ш 3 5 1.5 8 8 0 2 5 . 1 0 0
M B O 2 0 9 1 1 1 0 о 0 0
E 1 0 5 / I I I 5 5 . 6 0 0 0 0
M B A 6 3 3 8 2 . 6 8 0 in 0 0
i: 9 0 in s 1.5 2 0 0 2 5 2 8 3 . 5
E 96/111 8 1 1 160 8 0 0 0
E 96/11 18 4 . 7 2 6 0 5.7 2 3 1.3
M e a n ± s.cl. 14.1 ± 8 . 8 2 4 0 ± 3 0 4 . 8 4 6 . 5 ± 1 2 1 . 5
M. musculus
S 1 5 2 1.4 1 , 2 6 0 2 4 . 2 о 0
S 2 31 2 2 6 0 8.4 0 0
S 6 8 1.5 2 0 0 2 5 1 5 3 19.1
S 2 3 6 L.3 8 0 1 3 . 3 7 1.2
S 2 5 2 4 . 5 2 0 0 1 0 0 о 0
S 2 3 8 1.5 6 4 0 8 0 о 0
S 2 9 4 1 3 0 0 7 5 0 0
S 3 0 12 0 . 8 6 8 0 5 6 . 7 1 3 1 1
S 2 6 1 8 1 1 8 0 2 0 i 0.1
S 3 2 8 0 . 9 2 0 0 2 5 16 2
M e a n ± s.d. 1 4 . 9 ± 15.5 4 0 0 ± 3 6 1 . 5 1 9 ± 4 7 . 5
Table III. — Number of Schistosoma monsoni female (Smf), number of egg per gramme of faeces (epg) and number of miracidia hatched per 24 h, s.d. = standard deviation.
O n e M. erythroleucus was e x p o s e d to cercaria shed by B. pfeifferi recolted in Richard-Toll. Eight w e e k s later, the rodents was perfused and snails were infected with miracidia isolated from the liver and f a e c e s . O n e M. erythroleucus, o n e M. huberti, o n e M. musculus and o n e A. niloticus w e r e e x p o s e d to cercaria from these snails. S. mansoni male and female w e r e r e c o v e r e d
324 Mémoire Parasite, 1996, 4, 321-326
from M. erythroleucus and A. niloticus after the s e c o n d passage. V i a b l e e g g s w e r e found in the liver and faeces o f these rodents. O n l y S. mansoni males w e r e r e c o v e r e d from M. huberti and M. musculus.
In M. musculus, the strain o f S. mansoni was main
tained for three generations. M. musculus was infected with cercaria from B. pfeifferi naturally infected. Eight
RODENTS AND SCHISTOSOMA MANSONI IN SENEGAL
w e e k s later, M. musculus was e x a m i n e d , adult w o r m s r e c o v e r e d and then snails b r e d in the laboratory w e r e e x p o s e d to miracidia from the liver and the faeces.
After five w e e k s , o n e M. erythroleucus, o n e M. huberti, o n e At. musculus and o n e A. niloticus w e r e infected with cercaria s h e d b y t h e s e snails. T h e s e rodents d e v e l o p S. mansoni adults and eliminate viable eggs with faeces.
DISCUSSION
A
ll four rodent species studied w e r e susceptible to infection with S. mansoni and are thus potential hosts. T h e parameters w h i c h determine the susceptibility o f rodents to infection with S.
mansoni vary considerably b e t w e e n s p e c i e s and bet
w e e n individuals o f a s a m e species.
Differences in the n u m b e r o f adult w o r m s r e c o v e r e d may result from variation occurred either w h e n the cer- cariae penetrated the host skin or w h e n the schisto- somula migrated and b e c a m e mature. Warren and Peters ( 1 9 6 7 ) s h o w e d that the cercarial penetration was not directly responsible for the variation in the n u m b e r o f adult s c h i s t o s o m e s r e c o v e r e d from hamster, m o u s e , guinea pig, rabbit and rat. Earlier results suggest that the n u m b e r o f S. mansoni r e c o v e r e d is related to the capacity o f migration and maturation o f the schisto- somula rather than the capacity o f penetration o f cer- cariae. H o w e v e r , as far as A. niloticus, M. huberti, and M. erythroleucus are c o n c e r n e d the question o f w h e ther the variation in w o r m return is related to diffe
r e n c e s in cercariae penetration or migration o f the schistosomula remains o p e n .
It has b e e n s h o w n that the p e r c e n t a g e o f w o r m s r e c o vered may b e influenced b y production o f host anti
b o d i e s (Auriault et al., 1 9 8 4 ; Capron, 1 9 8 9 ) . S o m e authors like Stirewalt et al. ( 1 9 5 1 ) , Kuntz and Malakatis ( 1 9 5 5 ) , Smithers and Terry ( 1 9 6 5 ) , Imbert-Establet ( 1 9 8 6 ) observed a mortality o f adult schistosmes related to duration o f infection.
In the w o r k presented here, M. huberti had the grea
test n u m b e r o f e g g s per g r a m m e o f faeces, w h e r e a s h e did not h a v e the highest w o r m load. T h e heavily infected rodents did not necessarily passed the grea
test n u m b e r o f eggs. According to Kuntz ( 1 9 6 1 ) the relationship « hosts with the greater n u m b e r o f para
sites p a s s e d larger quantities o f eggs » is not always valid and o n several o c c a s i o n s g o o d hosts with only a few s c h i s t o s o m e s p a s s e d n u m e r o u s eggs.
E x c e p t for A. niloticus, the two s p e c i e s o f Mastomys and M. musculus s h o w e d a significant correlation bet
w e e n the n u m b e r o f female S. mansoni and the eggs r e c o v e r e d in faeces. This indicates that the n u m b e r o f eggs e x c r e t e d with f a e c e s d o e s not d e p e n d only o n
the n u m b e r o f females recovered; other factors may influence the excretion o f eggs with faeces. T h e s e w o u l d include intrinsic or extrinsic factors to the para
sites. In fact, schistosomes have to migrate through the blood-stream to the liver, then pair before maturing and continue their migration to the mesenteric veins w h e r e the oviposition takes place. T h e host species could influence the development, the evolution and the fecundity o f S. mansoni female. As s h o w n by B a s c h ( 1 9 8 1 a , b) and B a s c h and Humbert ( 1 9 8 1 ) the s p e c i e s o f host is relevant with regard to d e v e l o p m e n t o f female S. mansoni. T h e y believe that« a specific deve
lopmental stimulus, present in permissive animal host, is necessary for proper maturation o f schistosomes o f both s e x e s ». Imbert-Establet ( 1 9 8 6 ) highlighted a low w o r m return, high adult w o r m mortality, low fecun
dity and total a b s e n c e o f S. mansoni eggs in faeces a m o n g Rattus norvegicus.
According to Imbert-Establet (1986) the pulmonary localisation o f growing s c h i s t o s o m e s could prevent the spreading o f eggs. After staying in the mesenteric veins the schistosomes are able to migrate towards the lungs; this capacity o f migration may play an impor
tant role in the elimination o f eggs with faeces as eggs deposited in pulmonary tissue will not b e e x c r e t e d . Eggs associated with an inflammatory reaction and bil- harzial tubercles developed in relation to ova w e r e res
pectively observed in the lungs o f A. niloticus and Mas
tomys natalensis by G e a r et al. (1966). T h e s e rodents w e r e experimentally infected with Schistosoma hae
matobium for o n e year. In the present work, n o bil- harzial lesions o f the lungs w e r e found in A. niloticus, M. huberti, M. erythroleucus and M. musculus.
T h e physiological state o f the intestinal mucus can also c a u s e the differences o b s e r v e d a m o n g A. niloticus, M. huberti, M. erythroleucus and M. musculus. Eggs p o n d e d in mesenteric veins must migrate through the intestinal wall before b e i n g e x c r e t e d b y the faeces.
W h e n eggs are numerous, they may c a u s e lesions and form intestinal nodules which m a k e migration difficult.
This p h e n o m e n o n was o b s e r v e d in A. niloticus natu
rally infected at Richard-Toll ( S e n e , 1 9 9 4 ) .
W e s u c c e e d e d in maintaining the S. mansoni strain in e a c h s p e c i e s o f rodents for at least o n e generation.
H o w e v e r after a certain n u m b e r o f successive passages a cessation o f life cycle was observed. This sudden stop, w h e n related to a degradation or a sterilization o f the parasite strain, m a y b e explained by an altera
tion o f the cercariae infectivity. Even if they mature the cercariae only d e v e l o p into male parasites. This phe
n o m e n o n o f sterilisation has already b e e n o b s e r v e d a m o n g Rattus rattus b y J o u r d a n e and Imbert-Establet
(1980).
In short, A. niloticus, M. huberti, M. erythroleucus and M. musculus are susceptible to infection with s e n e g a -
lese S. mansoni. T h e y are c a p a b l e o f b e i n g infected and o f passing viable a n d infective eggs. Consequently, the s p e c i e s (A. niloticus a n d M. huberti) found natu- rally infected are potential natural reservoirs.
ACKNOWLEDGEMENTS
W
e a r e g r a t e f u l t o D r . V . R . S o u t h g a t e ( D e p a r t m e n t o f Z o o l o g y , T h e B r i t i s h N a t u r a l H i s t o r y M u s e u m ) a n d Dr. F.F. Stelma ( D e p a r t m e n t o f Parasitology, Univer- sity o f Leiden) for reviewing the manuscript.T h i s w o r k r e c e i v e d f i n a n c i a l s u p p o r t from t h e U N D P / W o r l d B a n k / W H O S p e c i a l P r o g r a m m e for Research a n d Training in Tropical Diseases a n d from O R S T O M ( H e a l t h D e p a r t m e n t , W a t e r , H e a l t h a n d D e v e l o p m e n t P r o g r a m m e ) .
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Reçu le 18 décembre 1995 Accepté le 16 septembre 1996
.326 Parasite, 1996, 4. 321-326
Mémoire
