Water >> Application >> Schistosomiasis
Prepared in collaboration with Jolcelyn Davies
Schistosomiasis is a clinical term applied to infection with one of a series of related trematode parasites that are endemic to at least 76 tropical and sub-tropical countries. Four species routinely infect the human host, and several others rarely do so. Many have reservoir hosts, making eradication efforts nearly impossible in some cases. Taken together, these organisms infect some 220 million people throughout the world, while 600 million others remain at risk. All species of schistosomes employ freshwater snails as intermediate hosts that are essential to the completion of their life cycle. The ecology of schistosomiasis includes tropical lotic (lakes and reservoirs) and lentic environments (rivers), and the behavior of people and their domestic animals that live near these aquatic environments. The recent surge in construction of large impoundments throughout many parts of the tropics and China has dramatically increased the health risks associated with acquiring schistosomiasis, and represents a growing concern among public health professionals in those regions. Other parasitic infections, including malaria, trypanosomiasis, and leishmaniasis have also increased in prevalence as a direct result of this activity.
As will be documented, controlling schistosomiasis at the community level is especially daunting, primarily because these parasites are so thoroughly integrated into the ecosystems in which they occur. A notable exception is Japan, where Schistosoma japonicum was eliminated from all of its islands as of 1976, largely based on ecological approaches. It has yet to return to that country and is now considered eradicated. In contrast, most underdeveloped countries do not have the political stability, infrastructure, nor the funding to institute on-going control measures. Instead, civil unrest and war have taken their toll, increasing the likelihood that schistosomiasis will remain a health problem for some time to come in those chaotic environments. Several recent summits have been held on this important health topic. Yet, despite these efforts to draw together, into a single plan, efforts to control these infections, new initiatives are still not in place in areas where they are needed most.
Schistosomes and their intermediate snail hosts are integral parts of the freshwater aquatic environments in which they are found. Many species of schsitosomes infect a wide variety of wild primates and other mammals, in addition to humans. This is particularly true for Schistosoma japonicum in China, in which monkeys in the northern regions, and domestic oxen in the southern regions are significant reservoirs. Each intermediate snail host species lives in a well-defined habitat. For instance, some are found in running waters, while others occupy still water environments. First considerations of the ecology of transmission will therefore focus on the biology of the snail intermediate hosts.
Freshwater snails are in the phylum Mollusca, class Gastropoda. Classification is based primarily on morphological characteristics, such as shell and radula, as well as differences in their anatomy, especially the reproductive systems. The intermediate snail hosts for schistosomiasis are mainly weak-shelled, aquatic animals. All snail species susceptible to infection with Schistosoma mansoni and S. haematobium belong to the family Planorbidae in the subclass Pulmonata. Schistosoma mansoni infects snails in the genus Biomphalaria, and these can also become infected with S. mansoni-S. intercalatum hybrids, S. rodhaini and S. eduardiense. Schistosoma haematobium infects pulmonate snails of the genus Bulinus.
Intermediate snail hosts belong to the family Pomatiopsidae, in the subclass Prosobranchiata, harbor Schistosoma japonicum, S. mekongi, and S. malayensis. This snail group has small conical or sub-conical shells with 4-8 dextral whorls, and rarely exceed 10mm in height. The shell surface may be smooth, have fine axial growth lines, or strong axial ribs. It may also contain a paucispiral ridge or concentric rings on the corneous or calcareous operculum. Prosobranch snails obtain dissolved oxygen directly from the water through a gill. They are dioecious, and must copulation to produce viable eggs. Snails in the genus Neotrichula are susceptible to infection with S. mekongi, while those in the genus Robertsiella are infected by S. malayensis. Schistosoma japonicum is found primarily in amphibious snails of the genus Oncomelania.
Subspecies of Oncomelania are found in Taiwan, China, Japan, the Philippines, and Indonesia. They inhabit shallow waters characterized by lush, littoral macrophyte cover, and do not thrive in permanently flooded areas (i.e., rice paddies) or in riverine environments. They derive oxygen from water by use of gills, and are unable to breathe outside of their aquatic habitats. Many are amphibious, despite this fact. Most amphibious species are restricted to areas of high rainfall and humidity where saturated ground is the rule, and the surrounding vegetation is covered with a persistent film of water. For example, O. hupensis, found in China, seeks out habitats that are flooded for 1-5 months during the rainy season, and spends the rest of the year in habitats with high humidity and residual water flow. Flash floods may transport them from one environment to another, but they often do not survive the journey.
Oncomelania species copulate daily, but this behavior is not essential for continuous reproduction. Inseminated females store sperm and are capable of producing viable eggs for up to twelve weeks after fertilization without further contact with another snail. Females lay eggs individually, or a short chains of eggs on solid substrates. Eggs are laid mostly at night, or hidden from sunlight, since they require low temperatures and high humidity for optimal development. In tropical ecozones, eggs are produced year-round, but the total number is quite small, averaging 30 to 40. In the subtropics, egg production occurs only during the summer months. The life span of most laboratory-reared Oncomelania ranges from 6-9 months (O. quadrasi) to several years (O. nosophora). In native habitat, O. quadrasi survives for about 9 weeks, while O. nosophora lives somewhat longer; 16 weeks.
Biomphalaria and Bulinus are the two primary genera of snails capable of harboring infections with Schistosoma mansoni and S, haematobium. Both are pulmonate mollusks obtaining oxygen directly from the atmosphere. A small percentage of its oxygen demand is satisfied by diffusion across the epithelium of exposed tissues.
Pulmonates are hermaphroditic, but the male reproductive system may be incompletely developed. They produce viable eggs via self-fertilization or cross-fertilization. Pulmonates can produce up to thousands of eggs in their lifetime. They do not usually lay eggs in temperatures below 180 C. Egg laying behavior increases proportionally with temperatures up to 30-350 C. Above this level, snail and egg mortality rises dramatically. Eggs are laid in clusters within transparent, yellow, gelatinous masses. Biomphalaria eggs are circular or oval, and attached to flat surfaces, while Bulinus eggs are more elongated and are often wrapped around the curved surfaces of plant stems. Egg mass and size are proportional to the size of the parent snail. The mass may exceed 1cm in diameter or length and contain 30 or more eggs. Snail hatching and development is directly linked to temperature.
On average, eggs hatch within 5-10 days, and the hatchlings measure 0.5-1.0mm in length. It takes about 4-12 weeks to reach sexual maturity—most often this occurs when snails have reached 5mm in diameter or height. In the laboratory, Biomphalaria species native to Africa live less than one year, reaching a maximum diameter of 15-20mm. In contrast, those found throughout South America and the Caribbean basin live for two years or more, reaching a maximum diameter of 30mm. In the field, many species of Biomphalaria outlive their laboratory-reared counter-parts.
Some schistosomes that infect humans (e.g., S. mansoni, S. japonicum, and S. mekongi) also infect host species that live in the wild, or are made available within the context of farming practices (e.g., rice paddy agriculture). In most cases, these reservoirs maintain the infection, thus increasing the chances that humans will encounter them, as well. In many areas of China, for example,
S. japonicum has been identified in over 40 different species of wild and domestic animals, and is a serious cause of morbidity and mortality in some of them, especially in cattle and goats. In the Dongting Lake region in the southern province of Hunan, S. japonicum is more prevalent in animals than in humans: 60% of cattle and water buffalo; 24% of pigs; 9% of all domestic dogs. In contrast, only 7% of the people residing in the same areas are infected. In Leyte and the Philippines, reservoir hosts play a role in maintaining the parasite, especially in areas where dense populations of humans exist side-by-side with dense snail population.
In Africa, reservoir hosts are less important. Schistosoma haematobium and S. intercalatum infect some animal species, but none appear to play a significant role in maintaining the parasite with respect to increased human health risk from infection. Humans are mainly responsible for maintaining these infections in the environment through indiscriminant deposition of urine and feces into freshwater. S. mansoni naturally infects rodents, baboons, and insectivores, and in a few instances these animals have served as a source of infection for humans, but these are isolated instances and remain the exception rather than the rule.
In South America, S. mansoni infects rodents, marsupials, and cattle. The role of animals in maintaining the parasite near human habitation is unknown.
Many species of schistosome are infectious primarily to animals, and pose no major health threat. S. mattheei is a parasite of sheep, cattle, and wild animals in South Africa, S. bovis is found in the cattle of southern Europe, Iraq, and much of Africa, S. margrebowiei is prevalent in African antelope and S. rodhaini infects carnivores, primarily rodents, in central Africa. Lastly, S. curassoni is found in domesticated ruminants in West Africa. Only one or two human cases have been detected with any of these species. Because they are often abundant near human settlements, the cercariae of these organisms and others, as well (e.g., S. bovis, S. spindale, and Schistosomatium douthitti) often penetrate human skin, but almost invariably fail to develop further. A condition known as “swimmer’s itch” is the usual result from repeated exposures to them. In addition, bird schistosomes can also cause this condition (e.g., Heterobilharzia americana, Orientobilharzia turkestanica, and O. turkenstanicum). Due to the presence of cross-reacting antigens among all schistosome species, it is possible that constant exposure to non-human cercariae imparts some degree of immunity against the ones that do cause disease.
Regions where abundant numbers of reservoir hosts are prevalent are known as “hot spots.” These ecological zones are where higher rates of infection in humans occur, due to the convergence of environmental factors that favor transmission, such as ideal snail habitat, suitable buffalo and cattle habitat, and a close proximity to large numbers of humans. Remote sensing can be useful in classify some hot spots, identifying land where grazing most often occurs, calculating the area, and determining suitable snail habitats. In one such study, as one might suspect, a strong correlation was found between distance and optimal transmission sites for Onchomelania snails. The shorter the distance between snail habitat and grazing pasture for water buffalo, the greater the probability of producing a hot spot. It is important to note, however, that hot spots constitute only a small fraction of most cattle grazing ranges.
Random sampling has been used to identify relationships between environments without snails, environments with snails, the densities of snail populations, and the impact of seasonal environmental change on each environment. There are four environmental factors that affect the density and viability of snail populations.
No single method of control of schistosomiasis, regardless of location, has been shown to work because of the large number of environmental variables involved in its transmission. Nevertheless, at least four approaches to controlling infection have proven effective at the community level: 1. Control of snails, 2. public health education, 3. sanitation, and 4. community-based chemotherapy employing praziquantel.
Controlling populations of snail hosts through the use of molluscicides at one time was considered the only effective way to preventing large-scale infection in communities living near aquatic habitats. With the advent of safe drugs, such as praziquantel, this strategy has declined in popularity. Yet, it can still play a crucial role in controlling the spread of the disease. Since the size of snail populations, rates of infection, and the production of cercariae are strongly influenced by the local climate, rates of transmission of schistosomiasis are in a constant state of flux. Snail control, when appropriate, is only employed at certain times during the year. Several methods are used to control snail populations.
Selective molluscicide treatment in snail-infested bodies of water at main human contact points is the preferred way to approach controlling snail populations. Metallic salts, such as copper sulfate, were among the first agents used, and were most effective when applied to standing bodies of water. Copper sulfate was introduced by dragging burlap sacks filled with large CuSO4 crystals behind slow moving boats. This compound worked well enough, but it also limited algal growth, that in turn affected growth patterns of fish that served as primary sources of protein. Newer molluscicides, such as nicotinanilide, organotin, dibromo-nitraozo-benzene, sodium pentachlorophenate, tritylmorpholine, sodium dichloro-bromopheno, niclosamide, and acetamide analogs replaced copper sulfate, as these were deemed safer to the environment.
Niclosamide is the only remaining commercially available molluscicide. While niclosamide is biodegradable, its “side effects” included the death of many fish species, as well as the targeted snail populations. It acts by depleting glycogen stores, and is the drug of choice for some adult tapeworm infections in humans. It also used be a drug of choice for schistosomiaisis, but too many suffered from the same side effect of depletion of glycogen stores. This led in some cases to coma, an unacceptable outcome of treatment. Its use is limited by cost, as well. Plant-derived molluscicides have proven too variable in their effectiveness and are difficult to manufacture.
Laboratory and field experiments employing microbial pathogens to snails and snail-specific metazoan parasites give a hint as to possible future control strategies for schistosomiasis. In one instance, when Biomphilaria glabrata was sequentially infected, first with S. mansoni, then with the trematode, Ribeiroia guadeloupensis, the double infection resulted in the elimination of the human pathogen, while retaining infection with the snail parasite. In another experiment, it was shown that Microsporidium spp. can interfere with the development of the sporocyst stage of S. mansoni. More of these kinds of associations most likely exist in nature, and discovering them may result in the development of a useful adjunct to current control strategies.
A number of predator/competitor snail species are receiving more and more attention as potential control agents, as well. In well-controlled situations, such as small, artificial ponds, experiments carried out in Grenada, Martinique, Guadelupe, Puerto Rico, and St. Lucia showed that Ampullariidae (Pomacea glauca and Marisa cornuarietis) and Thiaridae (Tarebia granifera and Melanoides tuberculata) snails out-competed Biomphalaria spp. for space and resources. Competitor snail species were also used successfully as a follow up measure after molluscicide use in some rivers of central Venezuela.
The strong disk snail, Marisa cornuarietis, is not susceptible to infection with human schistosomes, and thus can be used as a potential competitor to snails that do. Fortunately, this snail has a voracious appetite for littoral macrophytes. When introduced into situations in which Biomphilaria were already present, it consumed large quantities of littoral macrophytes, and eliminated the dominant food source for Biomphilaria snails. In addition, strong disk snails consumed the eggs of Biomphilaria, as well, adding insult to injury. A significant reduction in population densites of Biomphilaria spp. from most experimental ponds occurred after only several years. In the two to three succeeding years, native snails could no longer be demonstrated. In another related experiment, competitor and native snail species coexisted in heavily eutrophicated ponds, whereas in sparsely vegetated ones, strong disk snails replaced the original population. Conditions that favored maintaining the competition were easy to maintain at low cost.
In central China, the Three Gorges Dam, when completed, will permanently alter the flow of the Yangtze River. The project will result in a dam 180 m high, and generating 18,000 megawatts of electricity. One of the “side effects” will be the displacement of some 2 million people. The lake is expected to grow between two existing endemic areas for Schistosoma japonicum. Increased transmission rates are anticipated, compared to those before the construction of other dam. In Ghana, when Lake Volta was created, infection rates were significantly increased. Lateral canals are an integral part of the Three gorges dam, and will undoubtedly facilitate the spread of Oncomelania from one irrigation system to another. Large influxes of people and domestic animals, such as water buffalo, following completion of the project will become the new targets of the parasite.
Approximately 500,000 to 1 million Brazilians exhibited signs of severe schistosomiasis in the 1950s, but over the course of the past 30 years a sharp decline in the number of cases has been recorded. This is due largely to the rapid economic development of Brazil, accompanied by a strong political will to prevent the spread of infectious diseases of all kinds. In 1984, a parasitological survey was conducted among schoolchildren ages 7-14 in Vicosa, Brazil. A recently developed housing project had the lowest prevalence of all sites tested. Commercial districts had a slightly higher prevalence. The least-developed area in Vicosa, in which either primitive or non-existent sanitation was the case, had the highest prevalence, and the highest average egg count. Interestingly, the high egg counts appeared in clusters, in which families were forced to live in close proximity to each other. Following community treatment, it was shown that within 6-10 months, most children had re-acquired high concentrations of eggs. This is a typical feature of most parasitic infections in endemic regions, regardless of the parasite. Hence, mass treatment for S. mansoni with praziquantel would be ineffective by itself, unless accompanied by significant changes in sanitation.
China and Japan both had endemic schistosomiasis at one time. Today, China still has the infection, while, as pointed out earlier, Japan does not. Japan solved their problem using several approaches, none of which involved either drugs or vaccines. Water buffalo were the commonly used animal in rice paddy farming. By switching to horses, a far less susceptible host, the incidence in the reservoir went down significantly. Littoral vegetation was removed from the sides of canals feeding irrigation projects and the incidence went down further. Finally the institution of good sanitary practices in controlling human excrement finally brought the number of infected people down below the limit necessary for transmission. In 1976, Japan declared itself schistosome-free, both in its citizens and in its animals. All of this effort required well-coordinated public health education, remarkable outreach to farmers, and extensive knowledge of the ecology of the snails that are involved in the parasite’s life cycle. Most importantly, there was the political will to do so, a stable government to implement and coordinate control programs, and more than adequate funding for them, insuring their success.
The situation is different in China, a much larger and geographically more diverse land-mass. Management must be tailored to specific ecozones. Community control boards, especially in the southern portions of the country, with aggressive public health educational components were established after the cultural revolution of 1966-1976, in conjunction with leading schistosomiasis control groups (e.g., WHO and The World Bank) at each administrative level. Each control group consisted of officers from the offices of public health, water resources, agriculture, planning, and finance. In addition to having a well-organized program, the World Bank contributed a $71 million loan to the project.
The main goal was to reduce prevalence in humans and bovines (such as cattle and water buffalo) by 40%. The program uses two approaches. The first prong was community-based treatment with praziquantel of all humans in a given region, regardless of whether or not they were infected, and treatment of domestic bovines with the same drug. Praziquantel has been produced in China since 1978. The second prong was comprised of two sub-sections: selective treatment of infected individuals, only, with praziquantel, and snail control employing environmental modification methods. Mass chemotherapy was employed only after significant flooding events (e.g., Hunan Province, July 1996), or when the prevalence in a given community was higher than 15%. Selective treatment was used when the prevalence was between 3% and 5%, or when individuals between 7-14 years of age were diagnosed, and where the prevalence was less than 3%. A third prong attacked irrigation ditches in rice fields, clearing their banks of littoral vegetation. Non-commercial ponds were filled in.
The World Bank was also involved in researching the impact/cost analysis of the use of praziquantel, the economic assessment of different control strategies, the development of new procedures in diagnosis (such as antigen/antibody detection), cercarial detection, and liver exams with ultrasound B. All of these approaches proved effective in reducing the prevalence in provinces where non-primate reservoirs were not present.
Today, an extensive education program remains in place, where each school routinely holds lectures on the life cycle of S. japonicum and hookworms, and gives recommendations as to the necessary precautions to take in order to avoid infection with them.
Over the past 20 years throughout the tropics, wide spread dam construction has been the rule. While dams allow for the possibility of creating massive irrigation schemes, large reservoirs for supplying drinking water, and, in some cases, the generation of hydroelectric power, they also have inadvertently increased snail habitat, and mosquito and black fly breeding sites. For example, in Senegal, recently constructed dams and irrigation projects have led to the spread of S. mansoni into previously uninfected areas. However, even in these seemingly intractable situations, innovative management practices have occasionally saved the day. Many dams can be controlled with respect to water flow regimins, permitting intermittent drying out of littoral zones of impoundments. Stranding snails and mosquito larvae on dry lakeshores effectively limits the population densities of unwanted vector and intermediate host species. This was the case for the Tennessee Valley Authority project in the United States in the 1930’s that through this single approach eliminated malaria from those parts of the south without the use of insecticides or chemotherapy.
Reservoirs and adjacent irrigation schemes with the following characteristics favor the spread and maintenance of snails and mosquitoes:
Poor water management also includes the lack of proper maintenance (e.g., failure to repair leaking water faucets, etc.). Effective draining of waste and excess water is essential. Distribution systems require continual maintenance, the availability of spare parts, and frequent inspections. Although all of this activity is difficult to execute, it is essential to disease prevention.
Irrigation canals play an important role in snail breeding. These habitats are often created in ancillary drainage systems associated with rice farming, and represent refuges for snail populations between wet seasons. Irrigated rice fields aren’t in themselves ideal snail habitat, because water temperatures routinely exceed tolerance limits for optimal snail reproduction. In the canals themselves, reducing snail populations through manipulation of water velocity and construction of deeply “v” shaped concrete banks are two effective approaches that have proven useful in snail control. However, not all species of snails respond similarly to the same control strategy. For example, some species cannot maintain a presence in environments with water flows above a certain velocity. For Biomphalaria and Bulinus, the velocity is quite low, approximately 0.3m/sec.. Most snail species can withstand velocities in excess of 0.5m/sec., while velocities exceeding 1m/sec. dislodge all snails. In the case of Oncomelania spp., prolonged drought (i.e., draining water from its aquatic niche for several weeks) leads to dehydration and death. In contrast, Planorbid and bulinid snails can survive quite well under these conditions.
Sanitation is key to prevention of a number of water-borne infections, but it is paramount to reducing infection from all species of schistosomes, because it is spread through human contact with water, and not from the act of drinking. Although this seems like an obvious statement of fact, nonetheless, prevalence rates are significantly lower where safe drinking water is maintained by good public health practices. Likewise, the consumption of rainwater, when available, is encouraged. For example, in the Virgin Islands, corrugated tin roofs aid in collection. Chemical treatment, filtration, and simple overnight storage are effective methods of treating rainwater. But what actually keeps schistosomiasis out of the Virgin Islands is the lack of permanent bodies of standing water. Just a few hundred miles away in St. Lucia and Puerto Rico, however, endemic foci of infection still persist, because of the existence of extensive freshwater habitats. High quality latrines help raise sanitation standards, but too many countries lack the funds to purchase and then maintain them.
Likewise, many countries lack the funds, or do not realize the inherent need to implement health education programs that inform the populace of ways to protect themselves from schistosomiasis. Currently, in countries that have been able to implement such programs, they tend to emphasize the control of human behavior as they relate to the spread of schistosomiasis. Earlier versions of these programs stressed the need for snail control and the attendant reduction of transmission. Educated, informed people are able to adopt control strategies at the personal level, even if it requires reducing their contact with contaminated water sources, or making water safe to drink.
With the exception of some countries (Brazil, China, the Dominican Republic, the Philippines, Egypt, Iran, Morocco, Iraq, Puerto Rico, St. Lucia, Tunisia and Venezuela), the majority of the 76 endemic countries are still unable to adopt and execute health policies that might reduce transmission of the parasite. This is mostly due to the lack of sufficient funds. Control programs that work exist in all endemic countries with per capita incomes over $1000 (US). For the most part, countries without control programs are the least developed. The current thrust of most effective control strategies is towards preventing the development of chronic, severe pathology.
Development of resistance to praziquantel in some regions over the past 10 years, particularly in Egypt, has motivated some phamaceutical companies to initiate a new surge of research for schistosome drugs that act at more than one point in a biochemical pathway. Some are pursuing preventive therapies, as well. In this regard, a thin film of dibutyl phthalate or hexachlorophene on skin will protect against penetration for approximately 4 hours. Many are interested in exploiting natural products such as artemether, a plant-derived anti-malarial drug, for use against schistosomes, as well. In China, early drug trial results indicate it is a worthwhile area for further research.
Medical Ecology has benefited greatly from the growth and development of new technologies such as Geographic Information Science (GIS). GIS allows for computer-based manipulation of data collected from a wide variety of satellites. These data can be transformed into a variety of visual presentations. Some of the more successful ones including maps that are color-coded to display quantitative information. Land surface features such as altitude, surface temperature profiles, patterns of precipitation, and vegetation cover and types have been presented in this fashion. Determining by remote sensing the patterns of vegetation in a given tropical region has permitted accurate estimates regarding the range of habitat for a number of aquatic snail species. These data are periodically correlated with selected ground observations in order to validate GIS satellite reflectometry information. Patterns of disease transmission that could otherwise never be observed have been revealed in this way. Remote sensing data can also be linked to mathematical models that attempt to predict the potential for outbreaks of infection for a wide variety of infectious agents.
With regard to schistosomiasis, these two approaches have become important tools in ecological and epidemiological research. For example, the impact of dam construction and irrigation schemes on snail habitats, before, during, and after completion of those environment-altering activities. The latter facilitates decisions about control strategies by predicting results that can only cover specific areas during certain periods of time. It can also help discern the cost and impact of chemotherapy strategies on transmission, infection, and morbidity; the cost effectiveness of snail control; water supply; health education; and the usefulness of rapid assessment methods capable of identifying communities and individuals at high risk for Schistosomiasis.
The study of population genetics has also become a significant tool in disease control. Studies have led to the discovery that the level of infection is controlled by one major gene locus, Sm1. This breakthrough explains field observations that the distribution of hepatosplenomegaly is nonrandom. There are also indications that another gene locus, Sm2, is responsible for the development of fibrosis.
A vaccine, ultimately, is anticipated to be the most effective form of Schistosomiasis treatment and control. If proved to be effective and inexpensive enough for worldwide distribution, it would eliminate the need for snail and reservoir host control. Thus far, the vaccine based on irradiated cercariae offers almost complete protection in experimental animals. The first generation vaccines were directed against infection and/or worm fecundity. Currently there is a natural balance, tempering anti-schistosomal responses by stimuli down-regulating the granulomatous reaction against eggs in the tissue. Research promises to improve the understanding of cytokine interaction in the development of pathology and immunity, looking for a way to induce maximum levels of immunity without enhancing egg-associated reactions.