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Impact of the Crayfish Procambarus Clarkii on Schistosoma Haematobium Transmission in Kenya

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Impact of the Crayfish Procambarus Clarkii on Schistosoma Haematobium Transmission in Kenya Am. J. Trop. Med. Hyg., 61(5), 1999, pp. 751±759 Copyright q 1999 by The American Society of Tropical Medicine and Hygiene IMPACT OF THE CRAYFISH PROCAMBARUS CLARKII ON SCHISTOSOMA HAEMATOBIUM TRANSMISSION IN KENYA GERALD M. MKOJI, BRUCE V. HOFKIN, ARMAND M. KURIS, ALLAN STEWART-OATEN, BENJAMIN N. MUNGAI, JIMMY H. KIHARA, FRANCIS MUNGAI, JOSEPHAT YUNDU, JANE MBUI, JUMA R. RASHID, CURTIS H. KARIUKI, JOHN H. OUMA, DAVY K. KOECH, AND ERIC S. LOKER Biomedical Sciences Research Center and Clinical Research Center, Kenya Medical Research Institute, Nairobi, Kenya; Department of Biology, University of New Mexico, Albuquerque, New Mexico; Department of Biological Sciences, University of California, Santa Barbara, California; Division of Vector-Borne Diseases, Ministry of Health, Nairobi, Kenya Abstract. The Louisiana red swamp cray®sh, Procambarus clarkii, which was introduced into east Africa in the 1950s or 1960s, has since widely dispersed. Previous work by our group has shown that P. clarkii can reduce populations of the molluscan intermediate hosts of human schistosomes through predatory and competitive interac- tions. Here, we investigate whether cray®sh can reduce populations of Bulinus africanus and consequently, Schisto- soma haematobium prevalence in school children. Children from 6 primary schools in the Machakos and Kitui Districts of Kenya were selected for study. Schools were divided into 3 experimental-control pairs. At experimental schools, cray®sh were introduced into nearby aquatic habitats harboring Bulinus africanus snails and serving as S. haematobium transmission sites. Snail habitats near control schools did not receive cray®sh. Six months after cray®sh introduction, all infected children were treated with praziquantel. Children were then monitored quarterly for 2 years, at which time infection and reinfection rates were compared statistically between the paired schools. In one such pair, cray®sh failed to establish, resulting in neither snail control nor a reduction in transmission. At the second pair of schools, the numbers of snails were decreased by the presence of cray®sh, but a clear difference in infection rates in children could not be detected, primarily because drought conditions kept overall transmission rates low. At the third school pair, cray®sh established well in experimental habitats, snail numbers decreased precipitously, and children at the experimental school were signi®cantly less likely to acquire S. haematobium infections than children at the control school. Our results indicate that under certain environmental circumstances, P. clarkii exerts a signi®cant impact on the transmission of human schistosomiasis in Kenya. Important questions remain regarding the impact of P. clarkii on Kenyan freshwater ecosystems, not the least of which is its potential to signi®cantly in¯uence the epidemiology of schistosomiasis in east Africa. Human schistosomiasis remains an intractable problem in man schistosomes.12 Consequently, we examined the ability much of the developing world.1 In Kenya, both the intestinal of this cray®sh to affect pulmonate snails in the genera and urinary forms of the disease, caused by Schistosoma Biomphalaria and Bulinus, known to transmit S. mansoni mansoni and S. haematobium, respectively, affect an esti- and S. haematobium, respectively. Cray®sh eradicated or mated 3.5 million individuals, with 12 million more at risk greatly reduced snail populations in both laboratory and in for infection (Ministry of Health, Kenya, unpublished data). ®eld enclosures,13,14 as well as in small-scale ®eld trials.15 In Traditionally, control efforts have relied heavily on anthel- addition to being voracious snail predators, cray®sh also minthics such as praziquantel and/or the use of molluscicides compete with snails by consuming aquatic plants used by to control the gastropod intermediate hosts of the schisto- snails as refuge, oviposition sites, and food.13 some. Such strategies, however, require sustained effort to Although we believe that P. clarkii can signi®cantly re- prevent a rapid return to pre-intervention infection rates. duce or eliminate populations of medically important pul- Chemotherapy, for instance, must be repeated regularly and monate snails, this does not necessarily translate into re- by itself cannot prevent reinfection.2 Likewise, mollusci- duced human infection rates. In this report, we investigate cides, inevitably short term in their effects, must be reapplied whether or not cray®sh introduced into natural foci of S. frequently to maintain effective control and pose obvious haematobium transmission signi®cantly reduced such trans- environmental concerns.3,4 mission. Our results indicate that under certain conditions, As an alternative to chemical intervention, the use of nat- the presence of P. clarkii can dramatically reduce S. hae- ural enemies of snails has frequently been mentioned as a matobium prevalence in primary school children. Although sustainable means of schistosomiasis control.5±7 Over the important questions exist regarding the impact of P. clarkii past decade we have investigated the potential of several on Kenyan freshwater ecosystems, this introduced species is such putative control agents in Kenya.8 Our results indicate likely to remain well-established in Kenya. Consequently, that of the organisms evaluated, the Louisiana red swamp the epidemiology of schistosomiasis in east Africa may be cray®sh, Procambarus clarkii, was the most effective in signi®cantly altered by the presence of P. clarkii. terms of controlling snail populations. Procambarus clarkii was initially introduced into Kenya MATERIALS AND METHODS for aquacultural purposes, probably in the 1960s,9,10 but pos- sibly as early as the late 1950s.11 Since that time, this exotic Study area and site selection. The study was conducted crustacean has dispersed widely, and is now present within in the Machakos-Kitui area of Kenya, within the Athi River all major drainage basins in the country.10 As part of a snail drainage basin. Both S. mansoni and S. haematobium are survey in Kenya, we observed that P. clarkii rarely if ever endemic to this area,16±18 with members of the Bulinus afri- coexisted with known molluscan intermediate hosts of hu- canus species group serving as intermediate hosts for S. hae- 751 752 MKOJI AND OTHERS administrators, teachers, and residents in a series of village meetings. Approval from villagers was granted in all cases. Study subjects. The subjects at each school were children 7±16 years old. Since all schools included in the study were located in a part of Kenya inhabited by the Kamba people, these children were relatively homogeneous in terms of eth- nicity and cultural practices. Ethical approval for the study was granted by the Ethical Review Committee of the Kenya Medical Research Institute and the Human Research Review Committee of the University of New Mexico (Approval # HRRC 92±163). A signed informed consent form was ob- tained from all participating children and their parents or guardians. At each school, 150±200 children were selected at random to participate. This followed an initial screening of a single urine sample from each child in January 1994 to determine his or her infection status. Snail and cray®sh sampling. After identifying study sites and selecting study children, monthly snail sampling began in March 1994 at all snail habitats in the 6 localities. Per- manent sampling stations, each 10 meters long, were estab- lished along the shoreline of each snail habitat at both ex- perimental and control study sites. At monthly intervals, a standard snail scoop was used to sample along the length of each sampling station for 5 min. Total snail counts for each species per habitat per sampling period were then recorded. FIGURE 1. Map of Kenya showing the location of the paired Immediately after collection, snails of the B. africanus group study sites. A refers to Ikotamwithe and Nzangathi in the Kitui dis- were isolated in small vials and screened for schistosome trict. In the Machakos district, B refers to Kataluni and Matuu and C refers to Kwandoo and Kisukioni. cercariae. Snails releasing mammalian schistosome cercariae were noted. All snails were returned to the site from which they had been originally collected. Snail collections contin- ued in this manner until the study was terminated in January matobium. Except where noted, all further references to 1997. snails refer to B. africanus. The area lies within the known Between June and July 1994, approximately 4 months af- geographic range of P. clarkii in Kenya,10 but cray®sh had ter initiation of snail sampling, cray®sh collected from a dam never been introduced into the snail habitats used for the near Thika, approximately 25 km northeast of Nairobi, were present study. introduced into the snail habitats of localities designated as To be considered, a potential study site needed to have 1) experimental sites. Permission for this activity was granted a local school, 2) high enough disease prevalence for a cray- by Kenya's Department of Fisheries. No cray®sh were re- ®sh effect to be detected, 3) at least one human-made water leased into control snail habitats. Stocking density was a impoundment harboring snails, 4) no other ongoing schis- low-end density for standard aquacultural stocking between tosomiasis study, and 5) agreement of local people and au- 1 and 2 cray®sh/m2. After stocking, experimental habitats thorities. Ultimately, the 6 sites with the highest prevalence were sampled monthly for cray®sh until the study ended in that met the above criteria were selected for study. Impound- January 1997. During each sampling session, 20 meat-baited ments were selected as study habitats because they are usu- traps were placed in the water body for 1 hr. The traps, ally isolated and, once introduced, cray®sh would remain constructed of wire and covered with nylon mesh (mesh size con®ned within the habitats. Also, cray®sh in Kenya appear 1 3 1 cm), were 45 cm long with a diameter of 20 cm. Traps to be well-adapted to such habitats.
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