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ABSTRACT |
 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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In Kenya, the B. africanus group of snails is represented by B. (africanus) globosus, B. (a.) africanus, B.(a.) nasutus, and B. (a.) ugandae. All, apart from B. (a.) ugandae, are important hosts of S. haematobium in Kenya.10,11 The distribution of B. (a.) globosus and B. (a.) nasutus overlaps in Coastal Kenya and in the Lake Victoria area. Bulinus (a.) africanus is commonly found in higher altitude areas of eastern and central Kenya. Bulinus (a.) ugandae is distributed in limited foci in the Lake Victoria area.12 In the Coast Province of Kenya, B. globosus and B. nasutus can be found occupying a wide diversity of habitats such as quarry pits, streams, drainage canals, dams, and seasonal pools.13 In the Msambweni area, the focus of the present study, transmission of S. haematobium occurs most frequently in small freshwater impoundments, which may dry for varying periods, depending on rainfall. Remarkably, in contrast to the high human prevalence of S. haematobium infection in Msambweni, the proportion of snails shedding S. haematobium cercariae has been previously detected to be only 0.5–1.2%.14
To understand how an area with such a low percentage of snails shedding S. haematobium cercariae could coincide with high human infection prevalence, we characterized the snail population patterns within the area and examined their overlap with human infection patterns. Because snail populations are highly variable temporally, it was also essential to consider both seasonal and spatial trends for factors associated with the presence and density of S. haematobium intermediate-host species, and the snail species that compete with them.15 This report describes the distribution and seasonal fluctuation of the intermediate host snail (B. nasutus) and other snails sharing the same aquatic habitats in Msambweni area. (Similar snail studies were performed some 20 years ago in this same area,14 allowing comparison with the present study.) The spatial and temporal patterns were analyzed and associated with rainfall and environmental determinants as part of a comprehensive study of transmission of S. haematobium in 10 villages. With a companion paper,16 we apply novel mapping and statistical tools to analyze the patterns of local snail and human infection.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and has been previously described in detail.5,14,17 The area has a monsoon-type climate, with the period of January to April–May being hot and dry. The mean monthly temperature varies from 26.3°C 26.6°C, with lows of 23.5°C (July) to 26.9°C (March–April) and highs from 26.7°C (August) to 36.3°C (February). Annual precipitation varies from 900 mm to 1,500 mm, with large yearly and monthly fluctuations. There are usually two rainy seasons, the long rains starting around March and continuing until July, and the short rains beginning in October and lasting through November. Monthly rainfall records for the study period were obtained from the divisional agriculture offices situated near the Msambweni hospital.
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The present study was conducted between March 1984 and July 1987, in addition to February 2001 and May 2003, around nine water bodies: six rain-filled ponds, one rice field, two sites along the banks of the Mkurumji River, and two sites on the seasonal Lukungwi Stream (Figure 1
). A total of 24 sites were monitored with up to five snail sampling sites selected per pond based on human water contact activity. The water bodies studied were Kiziamkala pond, with four sites (1–4); Maridzani pond, with three sites (5–7); Bovo pond (site number 8); Nimbodze pond, with five sites (9–13); Mwachiangwa pond, with three sites (14–16); Mwamagongo pond, with three sites (17–19); a rice field, (site 20); Mkurumji River, with two sites (21 and 22) and Lukungwi Stream, with two sites (23 and 24) (Figure 1).
The major water contact activities included doing laundry, bathing, and swimming, and for young children fishing and playing. Although some alternative water sources (wells, boreholes, piped water stands, and water kiosks) are available, residents appeared to prefer the customary water contact points at the pools where, due to the hot weather conditions for most of the year, they can also bathe and/or swim (Clennon JA and others, unpublished data).17
Ethical oversight. After obtaining informed consent from area residents (or for children from their parents), human infection status and water use activities were monitored under human investigations protocols reviewed and approved by the Ethical Review Board of the Kenya Medical Research Institute (Nairobi, Kenya) and by the Human Investigations Review Board of University Hospitals of Cleveland, Ohio.
Snail sampling. Snail sampling was conducted by one man searching each site for five minutes using a standard flat wire-mesh scoop with a mesh size of 2 mm.18 Snails were taken to the laboratory at Msambweni Hospital, separated by species, and tested for cercarial shedding. Species confirmation for B. nasutus was carried out by genetic mapping19 at the Natural History Museum (London, London, United Kingdom) and at Hebrew University (Jerusalem, Israel) (Hamburger J, Hoffman O, unpublished data). The snails were placed individually in flat-bottomed glass vials (height = 7.5 cm, Diameter = 2.5 cm) containing clear, filtered, pond water and exposed to indirect sunlight for a maximum duration of four hours. Snails that did not shed cercariae on the first exposure were re-exposed on the second day. Cercariae were categorized either as those of S. haematobium or those of other trematodes (non-S. haematobium cercariae), as described by Frandsen and Christensen.20
Other parameters recorded at each site during every snail collection were water temperature (at a depth of 15 cm), water pH and conductivity (Oakton portable meters; Fisher Scientific, Pittsburgh, PA), turbidity (visual scale), site condition (dry or having water), water level, and the presence or absence of vegetation such as water lilies (Nymphaea spp.), sedge (Cyperus exaltatus Retz). or various species of grass.
Mapping and statistical analysis. All snail collection sites were located using a global positioning system (GPS) (GeoExplorer II; Trimble, Sunnyvale, CA) and identified on an Ikonos (Space Imaging, Atlanta, GA) satellite image acquired on March 4, 2001 at 7:45 AM. The 25-km2 study area is centered around 4.464°S and 39.449°E.
The image and GPS readings were imported into ArcView version 3.3 and ArcGIS version 8.3 (Environmental Systems Research Institute, Redlands, CA). Statistical spatial analyses were conducted using point pattern analysis.21 Specifically, we used a weighted K-function (second-order analysis) to detect global clustering,22,23 and the Getis and Ord24 Gi*(d) statistic to detect local clustering of snails and cercarial shedding. (For details on the mapping and spatial statistic analysis, see Clennon and others.16)
Correlation, homogeneity chi-square (continuity adjusted), analysis of variance, and linear regression analyses were conducted using SPSS version 11.5.0 (SPSS, Inc., Chicago, IL).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Bulinus nasutus, the intermediate host for S. haematobium in this study area, was the most common snail, accounting for more than two-thirds of all snails collected, with L. purpureus accounting for most of the rest (25%) of all snails.
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). Only at Maridzani was there complete species overlap (i.e., more than a single specimen of each of the four common snail species found). In the Mkurumji River, only M. tuberculata was found. Spatial statistical analysis of the distribution of B. nasutus in the study area, using a weighted K-function, demonstrated significant clustering of snails through distances of less than 1 km, with peak clustering at a distance of 400 meters. This is less than the distance between any two ponds, indicating that the clustering effect is in force around individual ponds. The global statistical result was supported by the subsequent application of Gi*(d) testing to detect local clustering. Gi*(d) was > 3.0 (P < 0.01) for all Nimbodze pond sites, but not significant for any other sites. This implies that the observed global clustering effect noted for B. nasutus snails was primarily due to the high numbers of snails found in the five collection sites of Nimbodze pond.
Cercarial shedding.
Only B. nasutus snails were found to shed S. haematobium cercariae, and the percentage of shedding snails within the ponds ranged from 0.2% in Bovo pond to 2.5% in Nimbodze pond (Table 2). Overall, 1.2% of the B. nasutus recovered in the Msambweni area shed S. haematobium cercariae. Nimbodze pond accounted for 73 (60%) of the 122 S. haematobium cercariae shedders. In contrast, 9.1% of B. nasutus, 0.7% of L. purpureus, 3.9% of B. forskalii, and 9.5% of M. tuberculata shed other, non-S. haematobium cercariae, with B. nasutus accounting for more than 90% of non-S. haematobium cercariae shedders within all ponds (Table 2). As for the shedding of S. haematobium cercariae, most of the snails shedding non-S. haematobium cercariae were collected from Nimbodze pond.
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); only Nimbodze pond was comparable in terms of overall numbers of B. nasutus shedding S. haematobium cercariae. Analysis of environmental variables, including pH, water temperature, and water conductivity, indicated no obvious differences between site 17 and the two other sites at Mwamagongo that would explain this difference in shedding prevalence for S. haematobium cercariae. However, our observations did show that site 17 was the most intensely used human water contact site of the three Mwamagongo locations (Clennon JA and others, unpublished data).
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2 = 5.43, P > 0.1 and 2 = 7.83, P > 0.1, respectively). However, site 7 at Maridzani had two months of high shedding prevalence in June and July of 2001, making its overall prevalence significantly higher than that of the other Maridzani sites (2 = 15.9, P < 0.01). At Mwamagongo, site 17 had significantly fewer non-S. haematobium cercariae (2 = 15.9, P < 0.0001). However, when examined more closely, this pattern resulted from very high numbers of uninfected B. nasutus collected at the site during July–August 2001. When the data from September 2001 were analyzed, the time when most non-S. haematobium cercariae from Mwamagongo were collected, no significant relationship between the Mwamagongo site and number of non-S. haematobium shedders was found (2 = 1.86, P > 0.3).
Seasonal patterns of snail density.
For our study sites, variation in snail density over time followed the changes in water level due to seasonal and inter-annual rainfall fluctuation (Figure 2). The highest snail density was observed between July and November, with a peak in September–October 2001, but since February 2002, snail populations have remained low.
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In 2001, all study ponds contained water throughout the year, except for Bovo and Mwamagongo, which were dry from February to April and again from November to December. However, in 2002, with the lack of rains, most ponds dried out. Maridzani pond was the only pond that contained water at least at one site throughout the two-year duration of this study. As of May 2003, Mwamagongo has been dry since November 2001 (19 months), Nimbodze since March 2002 (15 months), Kiziamkala since October 2002 (7 months), and Mwachiangwa since November 2002 (6 months). In comparison, for a period with more consistent rainfall, the data for B. nasutus and rainfall in Msambweni during 1984–198714 are shown in Figure 2B.
Overall, no significant relationship between rainfall and snail numbers was found when the complete 2001–2003 data were used. This result is not surprising since most of the sites experienced significant periods of complete dryness between March 2002 and May 2003, and no snails were recovered at these sites during this period. However, for the initial 2001–2002 period alone, when rainfall was correlated with snail density, a significant four-month lag in the snail population response to rainfall was found. Factoring in the four-month lag produced a significant relationship between total snail numbers and total rainfall (r = 0.90, P < 0.0001). In comparison, data collected in the same area between 1984 and 198714 showed a significant relationship between snail density and total rainfall with only a two-month lag (r = 0.43, P < 0.01). This discrepancy between the two time-lag periods is likely due to the more consistent level of rainfall that the region experienced during the mid-1980s, and indicates that longer-term precipitation patterns affect the relationship between the peak rainfall and peak snail populations in any given year.
Although snail density did not vary from site-to-site within individual ponds, there was significant variation between ponds in the timing and magnitude of peak snail populations (Table 3). Mwamagongo, which had the highest total number of snails, produced large numbers of snails only during July, August, and September 2001 before drying in October–November 2001. In contrast, Nimbodze, the pond with the next highest total, produced large numbers of snails from July 2001 through January 2002. Site 17 at Mwamagongo was particularly productive, with more than 500 snails collected at the site during each of its peak months. Most of the other ponds also had peak snail populations during the summer of 2001, although the duration of high snail populations varied for each water body: Kiziamkala, August to November; Bovo, only in August and September; and Maridzani, which appears to be more resistant to drying than the other sites, showing a slightly different pattern, a small peak in February–March of 2001 and then a longer period with high populations May to October. Interestingly, the population of M. tuberculata in Maridzani peaked from December 2001 to February 2002, long after the population peaks of B. nasutus and L. purpureus.
The cercarial shedding pattern followed the temporal changes in snail density (Figure 3); the correlation was positive and highly significant (r = 0.64, P < 0.0001, by log-transformed data). The pattern of non-S. haematobium cercariae shedding by B. nasutus also closely followed that of S. haematobium cercariae shedding over time (Figure 3).
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shows a contour map of the numbers of S. haematobium cercariae-shedding snails by location over the first 13 months of observation, before most sites went dry. The observed patterns in the abundance of shedding snails indicates a strong pool-specific and seasonal variation in transmission risk, with only a limited number of sites active overall, and only a few sites active at any given time.
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Vegetation.
Vegetation type was significantly associated with presence of several snail species. Both B. nasutus and L. purpureus were positively associated with the presence of water lilies (Nymphaea spp.) (2 = 57.1 and 29.1, respectively, P < 0.001), and negatively with a sedge (Cyperus exaltatus) (2 = 5.4, P < 0.02 and 12.4, P < 0.0001, respectively). Bulinus forskalii was positively associated with sedge (2 = 5.4, P < 0.02) and M. tuberculata was negatively associated with grass (2 = 4.3, P < 0.04). These statistical associations, and particularly the positive association with the presence of lilies, was confirmed in the field by repeated observations of more snails resting on the underside of lily pads than in association with any other vegetation type.
Dissolved ions (conductivity).
The highest levels of conductivity were recorded in Kiziamkala and Maridzani ponds; their high conductance was though to be due to their proximity to the ocean. High conductivity was also recorded in the rice field, possibly due to application of agricultural fertilizers. Snail species differ in their tolerance to increasing ion concentrations: high conductivity was negatively correlated with L. purpureus (r = –0.53, P < 0.0001) while correlating positively with B. forskalii (r = 0.18, P < 0.01). For example, there were no L. purpureus in Kiziamkala pond and only relatively few occurring in the neighboring Maridzani pond (Table 1). However, B. forskalii appeared at these ponds in larger numbers than in all the other habitats. The observed high conductivity in these ponds did not appear to have a limiting effect on B. nasutus.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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In our study area, most B. nasutus snails, and particularly those shedding S. haematobium cercariae, were found in Nimbodze pond, the location that was most strongly associated also with clustering of human infection.17 Conversely, no B. nasutus snails were collected at Mwachiangwa pond, and only a few Lanistes were recovered there. It is likely that chemical, physical, and biologic factors determine the species diversity and snail density to be found in a particular water body at a given period of time. The ecologic conditions for transmission of schistosomiasis in favorable snail habitats can vary considerably from site to site and area to area, even within short distances.25 To determine the environmental conditions that may inhibit snail survival or development, further investigations of water composition, e.g., measurements of specific dissolved ions,26,27 need to be carried out at these and comparison ponds. In other areas of the Coast Province of Kenya, abundance of B. globosus has been linked to water temperature, and rapid growth of B. globosus populations has been tied to unseasonable rains during the cooler months.14 In our study area, we did not find a significant link between snail abundance and water temperature, perhaps reflecting the narrow range of temperatures observed.10
One factor that was significantly associated with snail density was the presence of horizontal vegetation, namely water lilies (Nymphaea spp.). Most snails were observed resting on the underside of the lilies, areas probably rich in oxygen due to photosynthesis. The water lilies also provide egg-laying surfaces, shelter from the sun, and food for many species of snails. For food, the snails feed on the microflora and decaying plant matter of the water lily leaves.28 Aquatic macrophytes may also protect snails from predators such as birds. A pitfall that may result in an overemphasis of the importance of water lily leaves is that they are much easier to sample than a dense stand of grass or sedges. For our study area, the presence of water lilies was an effective indicator for the presence of both B. nasutus and L. purpureus. This association deserves further study in other transmission areas. If validated, it is possible that aerial remote sensing, whether by satellite or by less expensive aerial photography, may offer effective means for detection of likely transmission sites.
During long periods of drought, temporary ponds dry up and the snails estivate.29,30 As the rains arrive and the ponds fill up, snails are triggered out of estivation and repopulate the water bodies.14 However, this effect of rainfall on snails depends on the intensity with which the rains fall; our experience suggests that heavy downpours over a short period of time will fill up snail habitats and have a marked influence on snail populations, while small amounts of rain over a long period of time, which has been the pattern in the study area since 2002, do not result in a sufficient amount of water to refill ponds that have dried. Published reports on the length of estivation period do not indicate survival of snails beyond 6–12 months.29–31 However, it appears that many of our ponds, including Nimbodze pond (which was had the greatest B. nasutus abundance and most frequent S. haematobium cercariae production), have been dry for periods that extend beyond the published survival records of aestivated Bulinus or other snails. While survival is likely to be extended in moist areas and under vegetation, the prolonged drought may have drastic long-term impacts on snail populations and cercariae shedding in our study area. This, in turn, may result in changes in human infection patterns and the age distribution of schistosomiasis.17
The finding of a large number of snails shedding non-S. haematobium cercariae merits further study because it may be associated with infection of domestic livestock and possibly transmission to humans of zoonotic parasites. Bulinus forskalii is reported to be an intermediate host of Paramphistomum phellerouxi, an amphistome parasite of grazing animals, in Zambia,32 and is known to transmit S. bovis. Bulinus globosus has also been associated with transmission of Calicophoron microbothrium, another intestinal amphistome parasite of domestic animals, especially cattle.33 A case of Paragonimus-like eggs in humans was reported in Natal Province of South Africa by Proctor and Gregory,34 and similar eggs were obtained from cats in Durban area. They were thought to belong to Paragonimus kellicotti, which only rarely infects humans. In these South African studies, M. tuberculata was the only prosobranch snail found in the area, and was therefore suspected to be the intermediate host. Lanistes carinatus is reported to transmit the rat lung-worm Angiostrongylus cantonensis in Egypt.35
In Msambweni, further studies will be needed to determine the role of sympatric non-host snails in controlling schistosomiasis transmission by local bulinid snails. The non-host snails may act as biologic control agents for the intermediate hosts by either competing for space and food or by acting as predators.15 Marisa cornuarietis has been reported to act as a predator for all stages of Bulinus and Biomphalaria, and has been used as part of schistosomiasis control measures in Puerto Rico and other Caribbean islands.36 In addition, some of the non-host snails may protect the intermediate host snails from infection with schistosome miracidia by acting as decoys. Upatham, in a laboratory experiment in St. Lucia, found that two non-host snails, Physa marmorata and Drepanotrema surinamensis could prevent infection of susceptible Biomphalaria glabrata with S. mansoni miracidia to a certain degree.37
The results of our combined human and snail mapping studies indicate that transmission patterns of urinary schistosomiasis are closely related to the abundance and spatial distribution of host snails, and that travel distance to transmission sites likely plays an important role in determining human risk for infection. For schistosomiasis control programs to be successful, an effective understanding of the spatial and temporal variations in snail densities will be important for determining both the location and timing of control interventions. The use of GIS to integrate remotely-sensed area data on climate and terrain38 with other risk markers that can be readily determined at ground level (e.g., aquatic flora) has the potential to improve the effectiveness of site selection for control intervention. However, variability in rainfall patterns, compounded by the ability for the snail intermediate hosts to estivate for several months, complicates the design of predictive transmission models.39,40 Although snail abatement combined with population-based drug therapy has the potential to strongly suppress transmission, it is likely that successful control of schistosomiasis at Msambweni (and other areas having similar transmission features) will need to be tailored according to the prevailing environmental and weather patterns.
Received October 30, 2003. Accepted for publication December 30, 2003.
Acknowledgments: We thank Anthony Chome, Charles Nganga, Jackson Muinde, Robin Bundi, Idi Masemo, and Joyce Bongo for their invaluable contributions to the field work; Grace Nguma for data entry and management; and Dr. Evelin Grijalva for providing valuable comments. This paper is published with the kind permission of the Director of Medical Services, Ministry of Health, Kenya.
Financial support: This research was supported by the National Institutes of Health under grants AI-45473 (National Institute of Allergy and Infectious Diseases) and TW/ES01543 (Fogarty International Center).
Authors’ addresses: H. Curtis Kariuki and Eric M. Muchiri, Division of Vector Borne Diseases, Ministry of Health, PO Box 20750, Nairobi, Kenya, Telephone: 254-20-725-833, Fax: 254-20-720-030, E-mail: schisto{at}wananchi.com. Julie A. Clennon, Melinda S. Brady, and Uriel Kitron, Division of Epidemiology and Preventive Medicine, Department of Veterinary Pathobiology, University of Illinois, 2001 South Lincoln Avenue, Urbana, IL 61802, Telephone: 217-333-2449, Fax: 217-244-7421, E-mails: jaclenno{at}uiuc.edu, msbrady{at}uiuc.edu, and ukitron{at}uiuc.edu. Robert F. Sturrock, 92 Brennand Road, Dongara, Western Australia, 6525, Australia, Telephone: 61-8-9339-0560, E-mail: sturrock{at}iprimus.com.au. John H. Ouma, Kenya Medical Research Institute, Mbagathi Road, Nairobi, Kenya, Telephone: 254-20-722-541, Fax: 254-20-720-030. Saidi Tosha, Malick Ndzovhu, and Peter Mungai, c/o Case Western Reserve University/Division of Vector-Borne Diseases/Kenya Medical Research Institute Filariasis-Schistosomiasis Research Unit, PO Box 8, Msambweni, Kenya, Telephone: 254-40-52267, E-mail: dvbdcwru{at}wananchi.com. Orit Hoffman and Joseph Hamburger, Helminthology Unit, Hadassah Medical School, Hebrew University of Jerusalem, PO Box 12272, Jerusalem, 91120, Israel, Telephone: 972-2-675-8082, Fax: 972-2-6757425, E-mail: hambu{at}cc.huji.ac.il. Cara Pellegrini, Department of Medicine, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104, Telephone: 215-62-2200, E-mail: drpelle3{at}yahoo.com. Charles H. King, Center for Global Health and Diseases, Wolstein Research Building, Room 4126, Case Western Reserve University School of Medicine, 10900 Euclid Avenue, Cleveland, OH 44106-7286, Telephone: 216-368-4818, Fax: 216-368-4825, E-mail: chk{at}po.cwru.edu.
Reprint requests: Charles H. King, Center for Global Health and Diseases, Wolstein Research Building, Room 4126, Case Western Reserve University School of Medicine, 10900 Euclid Avenue, Cleveland, OH 44106-7286.
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
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= rainfall.
