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Abstract Planorbarius metidjensis measuring 2 or 3 mm in diameter and originating from three populations in the Agadir province (Ida Ou Gnidif, Imouzzer, and ...
Parasitol Res (1999) 85: 239 ± 242

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B. Yacoubi á A. Zekhnini á A. Moukrim á D. Rondelaud

Schistosoma haematobium : comparative studies on the characteristics of infection in three populations of Planorbarius metidjensis from the Agadir province in South Morocco Received: 2 July 1998 / Accepted: 21 July 1998

Abstract Planorbarius metidjensis measuring 2 or 3 mm in diameter and originating from three populations in the Agadir province (Ida Ou Gnidif, Imouzzer, and Sidi Belkacem) were experimentally infected with Schistosoma haematobium to determine if the complete larval development of the parasite might be ensured by any snail population of the Agadir province and to compare the general characteristics of infection. No signi®cant di€erence between the three populations was noted in the survival rates of snails when the ®rst shedding occurred or in the prevalence of infection. The mean duration of the shedding period was signi®cantly higher in the Imouzzer population (111 days versus 53±58 days). The total number of cercariae shed per mollusc was signi®cantly lower in the Ida Ou Gnidif planorbids (1,398/snail versus 3,346 and 3,343/snail in the other 2 groups). The same rhythm in daily cercarial production was noted in the three snail groups, with the periodicity being 18±20 days. Despite some di€erences in parasite development between the three snail populations, the di€erent populations of P. metidjensis can ensure the complete development of S. haematobium and maintain local transmission in the South of Morocco.

Schistosomosis haematobium again prevails in several provinces of Morocco (Ministry of Public Health 1996). Two snails are considered intermediate hosts in this B. Yacoubi á A. Zekhnini (&) á A. Moukrim Laboratoire Eaux et Environnement, DeÂpartement de Biologie, Faculte des Sciences, B.P. 28/S, 80000 Agadir, Morocco E-mail: [email protected], Fax: +212-8-22-01-00 D. Rondelaud Laboratoire d'Histopathologie Parasitaire, Faculte de MeÂdecine, 2, rue du Docteur Raymond Marcland, F-87025 Limoges Cedex, France

country by the World Health Organization (WHO): Bulinus truncatus and Planorbarius metidjensis (Doumenge et al. 1987). The ®rst species was considered an usual intermediate host of Schistosoma haematobium in North Africa. The role of the second species was discussed for a long time because of the con¯icting results regarding its experimental infection. A previous note by Moukrim et al. (1995) demonstrated that P. metidjensis from the province of Agadir (South Morocco) can be experimentally infected with a local strain of S. haematobium and display cercarial shedding for 70 days. However, these results were obtained using a single snail population and it was useful to determine whether another population(s) of P. metidjensis from South Morocco might harbor S. haematobium infections, as snail populations are scarce in the districts where human cases of schistosome infection have occurred (Moukrim et al. 1993). In view of these initial results, the following two questions arose. Can other populations of P. metidjensis from the Agadir province ensure the complete larval development of S. haematobium when experimentally infected? If the answer is armative, are the characteristics of infection identical when the origins of the snail populations used for experiments di€er? To answer these two questions we undertook a comparative study in which juvenile planorbids from three populations were experimentally infected and the shedding of cercariae was studied. The ®rst population of P. metidjensis was living at Sidi Belkacem (100 km north of Agadir town) in a spring located in the same bed as Oued Tafsrert. The second had colonized an irrigation system at Imouzzer (60 km northeast of Agadir town). The third population was living in a source near the village of Ida Ou Gnidif (115 km south of Agadir town). Adult P. metidjensis were collected from these sites, transported to the laboratory under isothermal conditions, and placed in breeding containers until they had laid eggs. The latter gave rise to the juvenile snails (2±3 mm in diameter) used in the experiment. The eggs of S. haematobium were

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obtained from the urine of a 14-year-old boy from Targa N'Touchka (district of A Baha, province of Agadir). The urine was collected during a mass screening program carried out by the Department of Epidemiology, Service of Infrastructure of Provincial Ambulatory Actions of Agadir (Ministry of Public Health, Morocco). Experimental infections were performed using 58 or 60 snails from each population (see Table 1). Each snail was exposed to 2 miracidia in a 35-mm-diameter petri dish for 4 h. The planorbids from the 3 groups were then raised in aquaria containing sediment and water from their site of origin (5 snails/l of water). The temperature ¯uctuated between 24° and 26 °C, and arti®cial lighting of 3,000 lux intensity at the surface of the aquaria was provided for a 12-h period (from 8 a.m. to 8 p.m.). At day 35 the survivors were isolated in 35-mm-diameter petri dishes with 2.5 ml of water and a piece of lettuce. Snail dishes were placed under the same experimental conditions described for the aquaria. They were exposed every 3 days to a 5,000-lux light source for 6 h to detect cercaria-shedding snails (CS snails). Every day a cercaria count was performed between 4 p.m. and 6 p.m. using 25 CS planorbids from each population, and the water in the dish was changed until snail death. Another cercaria count was performed hourly for 3 consecutive days using 10 CS planorbids from each population during week 2 of the shedding period. The parameters studied were (a) the survival rate of snails when the ®rst cercarial shedding occurred; (b) the prevalence of infection, calculated using the ratio between the number of CS snails and that of surviving P. metidjensis; (c) the shell diameter of CS snails at the ®rst shedding; (d) the shell diameter of CS snails at death; (e) the time between exposure and the ®rst shedding; (f) the duration of the shedding period; (g) the total number of cercariae shed by each CS snail over the ®rst 60 days of the shedding period; and (h) the mean number of cercariae shed per snail per day. The values and SD were calculated according to the hour or day of

the shedding period. The mean daily values recorded for cercarial production during the ®rst 90 days of the shedding period were compared using the autocorrelation test to detect any rhythm in cercarial shedding (Broom 1979). The mean values obtained for the other parameters were compared by the chi-square test and one-way analysis of variance. Table 1 shows the general characteristics of infection. Comparison of the mean values did not demonstrate any signi®cant di€erence between the three populations in the survival rate of snails when the ®rst shedding occurred or in the prevalence of infection. The shell diameter of CS snails at the ®rst cercarial shedding was signi®cantly lower in the Imouzzer planorbids (F ˆ 7.10; P < 0.05) as compared with the Sidi Belkacem snails. However, at snail death there was no signi®cant di€erence in shell diameter between the three snail groups. The time between exposure and the ®rst cercarial shedding was signi®cantly greater in the Ida Ou Gnidif snails (F ˆ 6.71; P < 0.05), whereas the mean duration of the shedding period was signi®cantly higher in the Imouzzer snails (F ˆ 30.1; P < 0.01). The total number of cercariae per CS snail was signi®cantly lower in the Ida Ou Gnidif snails (F ˆ 66.55; P < 0.01). Lastly, the mean number of cercariae per CS snail per day was signi®cantly lower in the Ida Ou Gnidif (F ˆ 21.8; P < 0.01) and Imouzzer (F ˆ 27.52; P < 0.01) planorbids than in the Sidi Belkacem snails. Figure 1 shows the existence of successive periods of high production. The ®rst was heavier than the other two periods in the three snail groups and occurred between day 1 and day 16 of the shedding period. The second appeared during week 3. Finally, a third period began during week 7 for the Sidi Belkacem and Ida Ou Gnidif planorbids. The correlograms show a rhythm in daily cercarial production, with the periodicity being 18±20 days in the three snail groups. Cercariae of S. haematobium were shed between 8 a.m. and 6 p.m., with a peak occurring between 11 a.m. and 1 p.m. (data not shown).

Table 1 Experimental infections of Planorbarius metidjensis with Schistosoma haematobium: general characteristics of infection (CS snails Cercaria-shedding snails) Snail population

Sidi Belkacem

Imouzzer

Ida Ou Gnidif

Number of snails at exposure Number and % of surviving snails when the ®rst shedding occurred Number of CS snails and prevalence of infection Mean shell diameter of CS snails at the ®rst shedding (mm) Mean shell diameter at snail's death (mm) Mean time between exposure and the ®rst cercarial shedding (days) Mean duration of shedding period (days) Mean total number of cercariae per CS snail Mean number of cercariae per CS snail per day

60 58 (98.3%) 38 (65.1%) 5.1 ‹ 0.8

58 53 (91.4%) 34 (64.1%) 4.2 ‹ 0.9*

60 59 (96.7%) 37 (62.7%) 4.9 ‹ 0.8

5.7 ‹ 0.7

5.4 ‹ 0.9

5.4 ‹ 0.9

44.9 ‹ 0.8

44.8 ‹ 1.0

45.5 ‹ 1.0*

57.9 ‹ 34.2 3,343.6 ‹ 940.2

111.6 ‹ 34.9** 3,346.6 ‹ 1,165.5

53.3 ‹ 37.7 1,398 ‹ 745.1**

70.8 ‹ 32.5

35.7 ‹ 20.5**

32.2 ‹ 17.6**

* P < 0.05; ** P < 0.01 versus the Sidi Belkacem population

241 Fig. 1 Experimental infections of Planorbarius metidjensis with Schistosoma haematobium: numerical distribution of cercariae over the ®rst 60 days of the shedding period and corresponding correlograms

The survival rate, the prevalence of infection, and the rhythm of daily cercarial production were comparable in the three groups of P. metidjensis. However, two slight di€erences in parasite development were noted between these three snail populations. The ®rst concern was the low values recorded for the total number of cercariae in the Ida Ou Gnidif planorbids. The second di€erence was the longer duration of the shedding period observed in the Imouzzer planorbids, whereas the total number of cercariae shed by this group was comparable with that of the Sidi Belkacem population. Two perhaps complementary hypotheses may be proposed to explain this ®nding. As cercarial production could be used as an indicator for estimating the compatibility between the intermediate host and the parasite (Frandsen 1979; Combes 1985), it may be suggested that the compatibility between the snail and the parasite would be lower in the Ida Ou Gnidif population. Another assumption

would be to admit a low developmental rate of S. haematobium sporocysts in the Ida Ou Gnidif and Imouzzer snails, as has been demonstrated by Ward et al. (1988) in Biomphalaria glabrata displaying a low cercarial production of Schistosoma mansoni. The mechanism causing these di€erences is more dicult to interpret. The more valid hypothesis would be to relate these di€erences to the frequency of natural encounter between the strain of P. metijdensis and that of S. haematobium in the ®eld, as has been demonstrated by Rondelaud (1993) in the system Lymnaea truncatulaFasciola hepatica. According to this author, several changes in the characteristics of Fasciola infection, such as a large decrease in the total number of cercariae shed by L. truncatula, were noted when the natural encounter between the snail and the parasite was scarce or exceptional. Further complementary experiments must be performed to verify these hypotheses.

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In conclusion, our results show that despite some di€erences in parasite development, the di€erent populations of P. metidjensis can ensure the complete development of S. haematobium and maintain local transmission in the South of Morocco. These results suggest that P. metidjensis can be considered an usual intermediate host of S. haematobium in North Africa.

References Broom DM (1979) Methods of detecting and analyzing activity rhythms. Biol Beh 1: 3±18 Combes C (1985) L'analyse de la compatibilite schistosomes/ mollusques vecteurs. Bull Soc Pathol Exot Filiales 78: 742±746 Doumenge JP, Mott KE, Cheung C, Villenave D, Chapuis O, Perrin MF, Reaud-Thomas G (1987) Atlas of global distribution of schistosomiasis. World Health Organization, Parasitic Diseases Program. Presses Universitaires, Bordeaux

Frandsen F (1979) Studies on the relationship between Schistosoma and their intermediate hosts. I. The genus Bulinus and Schistosoma haematobium from Egypt. J Helminthol 53: 15± 29 Ministry of Public Health of Morocco (1996) DonneÂes eÂpideÂmiologiques des maladies sous surveillance. Bull Epidemiol 20: 24± 38 Moukrim A, Zekhnini A, Rondelaud D (1993) Observations eÂcologiques sur les hoÃtes intermeÂdiaires de Schistosoma haematobium Bilharz dans la province d'Agadir (Maroc). Bull Soc Fr Parasitol 11: 223±230 Moukrim A, Zekhnini A, Rondelaud D (1995) A comparative study of the shedding of cercariae of Schistosoma haematobium in newborn Bulinus truncatus and Planorbarius metidjensis. Parasitol Res 81: 537±539 Rondelaud D (1993) Variabilite interpopulationnelle de l'infestation fasciolienne chez le mollusque Lymnaea truncatula MuÈller. In¯uence du contact preÂalable de la population avec le parasite. Bull Soc Zool Fr 118: 185±193 Ward RD, Lewis FA, Yoshino PT, Dunn TS (1988) Schistosoma mansoni: relationship between cercarial production levels and snail host susceptibility. Exp Parasitol 66: 78±85