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4

Climate Influences on Specific Diseases

The previous chapter reviews the general ways that the emergence and transmission of disease agents can be influenced by climate. The specific mechanisms underlying these linkages vary widely from one disease to another, as does our understanding of these linkages. This chapter focuses on a few specific diseases, chosen because they offer the opportunity to explore a diverse range of vectors, transmission pathways, geographic regions, and relationships to climate. In each case, the disease's impacts and global prevalence are described, as well as the life cycle of the pathogen and vector and the ways that this life cycle can be influenced by climate and other factors. Table 4-1 summarizes the different categories of diseases that are discussed.

DENGUE

Disease description. In terms of the number of human infections occurring globally, dengue is considered to be the most important arthropod-borne viral disease in humans. The symptoms of dengue include fever, severe headache, muscle and bone pain, and occasionally shock and fatal hemorrhage. The average case fatality ratio for dengue hemorrhagic fever is about 5 percent. Dengue is caused by four distinct flavivirus serotypes, and there is only short-lived cross-immunity from each serotype. The variability in the types of virus circulating and the nature of dengue antibodies in the human population interact to alter the frequency of infection and cases of dengue (Gubler, 1988).

There is a global pandemic of dengue, distributed throughout the tropics, and it is estimated that there are roughly 50 million cases of dengue infection



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Page 45 4 Climate Influences on Specific Diseases The previous chapter reviews the general ways that the emergence and transmission of disease agents can be influenced by climate. The specific mechanisms underlying these linkages vary widely from one disease to another, as does our understanding of these linkages. This chapter focuses on a few specific diseases, chosen because they offer the opportunity to explore a diverse range of vectors, transmission pathways, geographic regions, and relationships to climate. In each case, the disease's impacts and global prevalence are described, as well as the life cycle of the pathogen and vector and the ways that this life cycle can be influenced by climate and other factors. Table 4-1 summarizes the different categories of diseases that are discussed. DENGUE Disease description. In terms of the number of human infections occurring globally, dengue is considered to be the most important arthropod-borne viral disease in humans. The symptoms of dengue include fever, severe headache, muscle and bone pain, and occasionally shock and fatal hemorrhage. The average case fatality ratio for dengue hemorrhagic fever is about 5 percent. Dengue is caused by four distinct flavivirus serotypes, and there is only short-lived cross-immunity from each serotype. The variability in the types of virus circulating and the nature of dengue antibodies in the human population interact to alter the frequency of infection and cases of dengue (Gubler, 1988). There is a global pandemic of dengue, distributed throughout the tropics, and it is estimated that there are roughly 50 million cases of dengue infection

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Page 46 TABLE 4-1 Examples of Pathogen Transmission Associated with Environmental Factors Transmission Category Examples of Pathogens Routes/Sources of Transmission Environmental Factors Other Factors Vectorborne Malaria Dengue Lyme disease St. Louis encephalitis Rift Valley fever Hantavirus Routes/Sources of (anthroponotic, indirect) Insect/tick-animal reservoir-humans Rodent-humans (zoonotic, indirect) Rainfall, temp., and relative humidity influencing vector and/or pathogen levels/distribution Vector control Human migration or travel Airborne Influenza Respiratory (anthroponotic, direct) Relative humidity and pathogen survival Level of endemic infection and crowding Water- and food-borne Cryptosporidium Vibrios Fecal-oral (humans and animals) (zoonotic, direct) Naturally occurring (anthroponotic, direct or indirect) Rainfall and water contamination Temp. and salinity influencing growth Management of wastes and water treatment Algal blooms, uncooked shellfish

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Page 47 worldwide very year (WHO, 1998a). Dengue virus is carried by Aedes aegypti, a mosquito that preferentially feeds on humans and is particularly suited to urban environments. When a mosquito bites an infected person, it acquires the virus through the blood meal. In the insect's gut the virus replicates and spreads to the salivary gland, priming the mosquito for transmission of infection to another person. Climate influences. The abundance of dengue vectors depends in part on the availability of breeding sites, primarily containers such as drums, discarded tires, and leaf axils that are filled with water either manually or by rainfall. Where containers are manually filled for water storage, vector abundance is largely independent of rainfall, as seen in some areas of Bangkok, Thailand (Sheppard et al., 1969). In contrast, in southwestern Puerto Rico a high proportion of available breeding sites are discarded containers such as tires, bottles, and tin cans that become filled with rainfall. In this case there is a clear correlation between rainfall and A. aegypti abundance (Moore et al., 1978). Heavy rainfall tends to overflow containers and can thus discourage vector breeding, while extended drought conditions have in some cases led to higher vector abundance due to an increased use of water storage containers. Saturation deficit, a parameter taking into account both temperature and relative humidity, affects the survival of eggs and adults. Newly laid eggs are subject to desiccation, and adults can experience moisture-related reductions in survival throughout their lifetimes. However, saturation deficits high enough to reduce egg or adult survival, according to the few published studies, are rarely encountered in humid tropical locations (Southwood et al., 1972). Atmospheric moisture also influences the rate of water loss from containers, which in turn affects vector abundance. Temperature affects the potential spread of the virus through each stage in the life cycle of the mosquito. Adult and immature A. aegypti survive in a broad range of temperatures, from about 5°C to 42°C, although temperatures below 20°C reduce or prevent eggs from hatching. Temperature also influences the time required for embryonic, larval, and pupal development and plays a major role in the frequency of biting. Temperature also affects the extrinsic incubation period (EIP), the period between when the mosquito imbibes virus-laden blood and actually becomes infectious. At lower temperatures the EIP is longer and the mosquito is less likely to survive long enough to transmit the virus. In the A. aegypti/dengue system, EIP is a non-linear function of temperature such that even small changes in temperature introduce a seasonality into transmission dynamics (Focks et al., 1995). Recent studies of the distribution and epidemiology of dengue viruses suggest that projected climate warming is generally expected to increase the intensity of transmission. For instance, Patz et al. (1998) estimate that for regions where dengue is already present, a mean temperature increase of about 1°C

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Page 48 increases the aggregate epidemic risk by an average of 31 to 47 percent. Higher infection rates translate into a greater number of individuals who have experienced multiple infections and thereby may have an elevated risk for developing serious dengue illness (Halstead, 1988; Jetten and Focks, 1997). Another possibility to consider, however, is that climate change may lead to lower average atmospheric moisture levels in some regions, which could actually reduce dengue transmission. MALARIA Disease description. Malaria is one of the most common vector-borne diseases in the tropics. The pathogens are protozoan parasites in the genus Plasmodium that are transmitted to humans by the Anopheles mosquito. In humans the malarial parasites infect red blood cells, causing periodic chills and fever, and in some species of Plasmodium the parasites can ultimately cause death. Insufficient vigilance in maintaining mosquito control measures, development of insecticide resistance by the vectors, and the emergence of drug-resistant strains of malaria have contributed to the resurgence of this disease throughout the tropics. Worldwide prevalence of the disease is estimated to be in the order of 300-500 million clinical cases each year, causing over 1 million deaths annually. About 90 percent of these cases occur in sub-Saharan Africa, and most of the others are found in other tropical regions (WHO, 1998b). Humans get malaria from bites of infected female mosquitos. The parasites replicate asexually in the red blood cells of the human host and are responsible for the clinical manifestations of disease. Some of the parasites differentiate into sexual stages that continue the transmission cycle when ingested by another mosquito during a human blood meal. Sexual reproduction of the parasite occurs in the mosquito. Climate influences. Temperature, rainfall, humidity, and wind each play a role in determining the distribution and incidence of malaria. These factors govern the distribution, prevalence, rate of development, life span, and feeding frequency of the Anopheles mosquitos. Temperature also plays a fundamental role in the rate of multiplication of the parasite in the mosquito. Although each species of Anopheles has a different ecology, as a general rule, warmer temperatures mean that the mosquito develops more rapidly and feeds more frequently and earlier in its life cycle and that the parasite within the mosquito develops and multiplies more rapidly. Thus, malaria tends to occur less frequently at higher altitudes and latitudes, at least in part because these regions are associated with colder temperatures. Several studies indicate that malaria has spread or increased in transmission intensity following temperature and/or rainfall variations brought about by El Niño events. These epidemics involve unstable malaria transmission, often in

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Page 49 desert and highland fringes. In northern Pakistan, higher temperatures associated with El Niño correlated with increased malaria incidence (Bouma et al., 1994). Malaria outbreaks in the former Punjab province of India were more likely in the year after an El Niño with a relative risk of 4.5, and in El Niño years in Sri Lanka with a relative risk of 3.6 (Bouma and van der Kaay, 1996). There was a highly consistent association between El Niño years and outbreaks of malaria in Venezuela (Bouma and Dye, 1997) and Colombia (Bouma et al., 1997). Linblade et al. (1999) found that in the highland region of southwestern Uganda during the El Niño event of 1997-1998, an increase in rainfall was positively correlated with an increase in vector density and incidence of malaria (almost three times the mean incidence of the preceding five years). These associations are strong and consistent and imply that ENSO forecasts may have value in predicting disease risk in particular regions, even though the mechanisms underlying these associations are not always apparent. At present, there is insufficient evidence to clearly attribute an increase in malaria incidence or its geographic spread to long-term global warming patterns. While some studies have predicted that global climate change could potentially lead to widespread increases in malaria transmission by expanding mosquito habitat range and “vectorial capacity” (Martens et al., 1999), other models have projected only a negligible extension in potential malaria transmission due to climate change (Rogers and Randolph, 2000; these studies are discussed further in Chapter 5). Regardless, these models can only simulate the potential transmission risk; actual occurrence of the disease is determined largely by socioeconomic factors. For instance, historically malaria was common in temperate regions but is no longer found in such regions because of environmental sanitation, mosquito control (e.g., draining swamps that breed some species of Anopheles), and lifestyle changes that allow people to minimize exposure to mosquitos (e.g., by screening houses and using air conditioning). Similarly, Reiter (2000) emphasizes that an increase in the potential malaria burden due to future warming trends could be offset by other factors, especially human interventions, as documented by the fact that during the warming trend of the past three centuries, the geographic distribution of malaria diminished rather than increased. ST. LOUIS ENCEPHALITIS Disease description. St. Louis encephalitis is an acute inflammation of the brain caused by a mosquito-transmitted virus in the family Flaviviridae. Mild infections cause fever and headache, but more severe infections may cause encephalitis, with symptoms of headache, high fever, neck stiffness, stupor, disorientation, coma, and paralysis. The disease occurs in North America, and the virus is closely related to the Japanese encephalitis virus of Asia and West Nile virus of Africa, Eurasia, Australia, and North America. The original epidemic in St. Louis County, Missouri in 1933 was associated with an extremely dry sum-

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Page 50 mer, during which the city's open sewage ditches did not flush and mosquito breeding was unusually abundant (Kinsella, 1935). There have been 4,478 reported human cases of St. Louis encephalitis in the United States since 1964, with an average of 128 cases reported annually (Shope and Tsai, 1998). One in 338 infected people becomes sick, and the case-fatality ratio is between 2 percent in young people and 23 percent in persons over 70 (Monath, 1980). The urban mosquito vector of St. Louis encephalitis is Culex pipiens, which maintains the virus in a life cycle involving several species of wild birds. The mosquito is infected when it takes a blood meal from a viremic bird. The virus multiplies in the mosquito, and after an extrinsic incubation of about two weeks, the virus appears in the saliva and can be transmitted either to another bird or to a person. The virus also has a rural cycle in the western United States, where the Culex tarsalis mosquito is the major vector. This mosquito breeds in flood waters and is abundant in irrigated fields and riverine flood plains, and thus excess rainfall and abundant snowmelt can favor its breeding (Monath, 1980). Climate influences. Temperature has a major influence on the development of the Culex mosquito and St. Louis encephalitis virus in the mosquito. Epidemics occur primarily in southern latitudes where the mean June temperature is 21°C or above. Monath and Tsai (1987) compared retrospectively 15 urban U.S. outbreaks of St. Louis encephalitis, and found statistically significant associations with increased precipitation and temperature in January, decreased temperature in April, and increased temperature in May. Seven of 15 epidemic years had all of these characteristics, as contrasted to only two of the 130 non-epidemic years. Reeves et al. (1994) studied the ecology of St. Louis encephalitis in mosquitos of California by comparing the warm southern San Joachim Valley with the colder northern Sacramento Valley. Based on their findings about the dynamics of mosquito infection and life cycles, they predicted that if a 5°C warming were to occur, St. Louis encephalitis would become less prevalent in the warmer south and would be distributed farther north in California, Oregon, and Washington. This prediction, however, did not take into account socioeconomic factors that might modify exposure of persons to infected mosquitos. RIFT VALLEY FEVER Disease description. Rift Valley fever (RVF), first described in 1930 during an epizootic among domestic livestock in the Rift Valley of Kenya, is a potentially fatal disease of humans that results from infection with RVF virus (Daubney et al., 1931). During the past half-century, dozens of animal and human outbreaks of RVF have occurred, mostly in sub-Saharan Africa (Meegan and Bailey, 1988). Transport of infected mosquitos or animals into Egypt resulted in outbreaks during 1977-1978 and again in 1993-1994 along the Nile River. Symptoms of RVF range from unnoticeable or mild disease in adult sheep

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Page 51 and cattle to abortion among pregnant ungulates and fatalities in young animals (Shimshony and Barzilai, 1983). Human disease may be mild but can involve abrupt onset of high fever, severe headache, myalgia, and incapacitation for several days (Peters and Meegan, 1981). Some patients develop fatal hemorrhagic fever or encephalitis. There is a 1 percent case fatality rate in humans. Low-level endemic transmission occurs regularly throughout much of the African continent, but most of this remains unrecognized due to inadequate surveillance and health care facilities (Meegan and Bailey, 1988). RVF virus is transmitted by mosquitos to both domestic animals and people. Although more than 30 mosquito species are potential vectors, certain floodwater Aedes species that emerge from temporary ground pools following seasonal rains are recognized as the important enzootic vectors (McIntosh and Jupp, 1981). Epizootic transmission often occurs during periods of heavy rainfall in East Africa (Davies et al., 1985) when particular Culex species become infected. Transmission of RVF virus depends on complex interactions among mosquito vectors, non-human vertebrates, and human hosts, all of which are linked to various environmental factors (Wilson, 1994). Mosquitos perpetuate transmission either by direct infection of eggs or by acquiring infection during a blood meal and transmitting it during a subsequent feeding. Not only is species-specific mosquito abundance important, but densities of certain vertebrates, especially domestic ungulates, are crucial factors in zoonotic outbreaks. Such outbreaks induce protective immunity in all infected animals, thus reducing the number of susceptible animals after an epizootic. Human proximity to infected animals and mosquitos partly determines disease risk to people. Aedes mosquitos that infect animals rarely bite humans, so abundance of other mosquitos (notably Culex species) may be important for human disease. Climate influences. Studies of climate variability and RVF activity have focused on precipitation and epizootics. Periods of excessive rainfall are believed to increase the egg hatching and larval survival of certain African Aedes floodwater mosquito species. Extensive transmission to humans, however, would seem to require the buildup of Culex populations. Recently, Linthicum et al. (1999) analyzed the historical pattern of eight recognized RVF outbreaks in East Africa since 1950 and claimed that each followed periods of abnormally high rainfall. Using Pacific and Indian ocean sea surface temperature anomalies and satellite-based vegetation indices, these authors suggest that outbreaks may be predicted up to five months in advance of their occurrence. Whether this association is strong and consistent enough to allow such forecasts remains to be seen. HANTAVIRUS Disease description. In 1993 an outbreak of acute respiratory distress with a high fatality rate (>50 percent) occurred in the population of the Four Corners

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Page 52 area of New Mexico, Arizona, Colorado, and Utah. The cluster of cases was caused by a newly recognized virus that was given the name Sin Nombre virus, a hantavirus (Nichol et al., 1993). The disease, hantavirus pulmonary syndrome (HPS), was soon recognized over a wide area of North and South America. Patients with HPS typically exhibit fever and muscle aches lasting three to five days; shortness of breath and coughing symptoms then develop rapidly, requiring hospitalization and ventilation. Since first identified in May 1993, 260 cases of HPS have been reported in the United States, with the peak, 80 cases, occurring in 1993. The Sin Nombre virus is a rodent-borne pathogen belonging to the bunyavirus family of RNA viruses. Deer mice (Peromyscus maniculatus) are the most common reservoir in the southwestern United States, and they shed virus in their urine, droppings, and saliva (Childs et al., 1994). The virus is mainly transmitted to people when they breathe in contaminated air. Molecular tests of archived postmortem tissues from humans and rodents revealed that HPS was not a new disease, but that it was only newly recognized as a result of this unusual cluster of cases in 1993. Climate influences. Data from an ongoing study of Peromyscus rodents revealed that in 1993 populations of this animal in some parts of New Mexico were as much as 10 times greater than average (Parmenter et al., 1993). The hypothesis was advanced that the unusually heavy rainfalls occurring during the 1992-1993 El Niño led to an abundant food supply for rodents, followed by a rodent population explosion. Deer mice readily entered homes and farm buildings, which resulted in greater exposure of humans to hantavirus-infected rodent excreta. To test this hypothesis, investigators used satellite imagery and precipitation estimates to identify environmental conditions that were associated with the sites where HPS cases occurred (Glass et al., 2000). The clustering of cases was found to be associated with areas of heavy vegetation, but the data failed to fully support the connections between El Niño and HPS risk as proposed above. Also, at this point such associations may be confounded by the fact that more people have begun taking actions (such as rodent-proofing their houses) to mitigate risk of exposure to the virus. LYME DISEASE Disease description. Lyme disease is caused by a spirochete bacterium (Borrelia burgdorferi) that is transmitted by tick bites. The disease typically presents with a characteristic “bull's-eye” rash, accompanied by symptoms such as fever, fatigue, headache, and muscle and joint aches; although some infected individuals show no signs of illness. It is rarely, if ever, a primary cause of death. Lyme disease occurs throughout many areas of the northeastern United States and parts of the northern Midwest (especially Wisconsin and Minnesota)

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Page 53 and is found at lower frequencies in the southeastern states and on parts of the West Coast, especially northwestern California. Lyme disease is also found in parts of Europe and eastward across Asia (Dennis, 1998). The annual number of cases in the United States per year has increased about 25-fold since national surveillance for the disease began in 1982. A mean of approximately 12,500 cases was reported annually to the Centers for Disease Control and Prevention from 1993 to 1997. In all areas where Lyme disease occurs, ticks of the genus Ixodes appear to be the vector responsible for most transmission. The predominant vector in the eastern United States is the deer tick (Ixodes scapularis) and in the western United States the western black-legged tick (Ixodes pacificus). The tick has three motile stages (larvae, nymphs, adults), and each of these stages must find, attach to, and feed on the blood of a vertebrate to eventually molt to the next stage or, in the case of adult females, to reproduce. Mated and blood-fed female ticks lay perhaps 2,000 to 3,000 eggs, which hatch into larvae and begin another generation. Adult ticks in North America feed predominantly on large vertebrates, particularly white-tailed deer (Odocoileus virginianus). Abundance of deer has been linked to abundance of ticks in infested areas. The principal reservoir of the spirochete, however, is the white-footed mouse (Peromyscus leucopus). Larval or nymphal ticks become infected while feeding on an infected mouse and are then capable of transmitting infection to another vertebrate during a subsequent blood meal. Occasionally, a tick will bite and feed on a human, sometimes resulting in Lyme disease (Dennis, 1998; Wilson, 1998). Climate Influences. Many factors appear to influence the spatial and temporal patterns of Lyme disease risk. Transmission among natural hosts and humans is determined by local abundance and survival of ticks, the percentage of ticks that are infected, abundance of hosts, human activity in tick habitats, and people's knowledge and awareness of Lyme disease prevention. A few studies have demonstrated how micro-climate influences the survival and activity of deer ticks (e.g., Bertrand and Wilson, 1996), suggesting that climate patterns may be important in determining Lyme disease risk; but research thus far has not yet fully elucidated the contributions of climate and other factors to transmission dynamics. Climate change scenarios often forecast that some regions of the United States may become warmer and moister, leading to speculation that the range of deer ticks carrying Lyme disease might expand. However, the current distribution of the deer tick and of Lyme disease in the Unites States spans a wide range of climatic conditions, and deer ticks are already abundant in parts of the country where cold extremes are common. Extremely cold regions of North America and Northern Europe could perhaps support survival of local Ixodes ticks if climate warming were to occur, but whether this would translate to new cases of Lyme disease is highly speculative. If the range of ticks were to expand, this

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Page 54 could set the stage for expansion of disease, but many other factors that contribute to human risk would also have to develop (e.g., competent reservoirs, human behavior, seasonal activity patterns). Although climate is important, various other factors appear to be primarily responsible for risk of this vector-borne disease. The range of factors that presently limit distribution of the vector remain poorly understood, but research suggests that microclimate, abundant hosts, and suitable vegetation and soil habitat are important. The tick has not yet become established or widespread in apparently appropriate environments in many areas of the United States, thus indicating that even where suitable microclimate, host, pathogen, and human contact conditions appear to exist, Lyme disease may not be present. INFLUENZA Disease description. Influenza or “flu” is a viral infection of the respiratory tract that affects millions of people globally every year. Influenza is highly contagious and can cause severe complications such as pneumonia, particularly in children, the elderly, and other vulnerable groups. Numerous influenza global epidemics, or “pandemics,” have been documented, with three occurring in the twentieth century. Some estimates of mortality from the Spanish flu pandemic of 1918-1920 are greater than 50 million people worldwide. Pandemics in 1957 and 1968 together killed more than 1.5 million people (WHO, 1999a). The World Health Organization (WHO) has developed a sophisticated international program for influenza surveillance and vaccine preparation. Surveillance is maintained by 110 international influenza centers, which continually isolate influenza virus from humans and animals, so that emerging strains are rapidly identified. They provide human isolates to WHO collaborating centers, where the virus is characterized genetically. Results from the influenza network are reviewed biannually, and a recommendation for the antigenic composition of the next year's influenza vaccine is given to vaccine manufacturers (WHO, 1999b). Vaccines for specific strains of influenza are produced and used worldwide, but at present there is too little use of vaccine for it to have an effect on large-scale transmission patterns. Influenza is transmitted person to person in aerosol droplets, typically through coughing and sneezing. Viruses causing influenza are typed as A, B, or C. Currently there are three different influenza strains circulating worldwide, two subtypes of influenza A and one of influenza B. Influenza type A viruses constantly change, enabling them to evade the immune system of its host, such that people are susceptible to influenza infection throughout life. One mechanism, antigenic “drift,” is a series of mutations that occur gradually over time. The other type of change is the more abrupt antigenic “shift,” in which a new subtype of the virus suddenly emerges by incorporation of a gene from an animal host influenza strain. Antigenic shift occurs infrequently, but when it happens

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Page 55 large numbers of people, and sometimes an entire population, are vulnerable to infection because they have no antibodies that recognize the virus. Influenza B viruses occur almost exclusively in humans, whereas all human influenza A viruses infect avian species, and a few subtypes infect other animals, particularly pigs and horses. There is evidence that the three pandemic influenza strains of the twentieth century arose from the incorporation of genetic material from animal influenza viruses (Webster et al., 1992). Climate influences. Influenza has a clear seasonal cycle, occurring in North America mainly in late fall, winter, and early spring. The peak number of reported cases averaged over five seasons from 1994 to 1999 occurred in mid-December through February. It is reasonable to assume that the disease transmission cycle is influenced by climate, but the actual driving mechanisms are not well understood and have been the subject of few quantitative studies. Annual influenza outbreaks do not appear to correlate with mean winter or monthly temperature (Langford and Bentham, 1995). The interannual variability in the virulence of influenza strains makes interpretation of the relevant data difficult. One common explanation for influenza's seasonal cycle is that there is more indoor crowding in the winter, which leads to greater disease transmission. Evidence for the effect of crowding includes the fact that flu epidemics tend to correlate with the start of school and peak during winter holidays, and that outbreaks occur frequently on cruise ships and other “contained” environments. However, laboratory studies of influenza transmission in mice show that, even under identical crowding conditions, flu transmission can still show a seasonal component. This may be due to the effects of humidity on the survival rate of the virus contained in the aerosolized droplets spread by coughing and sneezing (Schulman and Kilbourne, 1963). Flu is often regarded as a “high-latitude” disease, yet it does occur every year in the tropics. Recent outbreaks occurring on cruise ships have shown that flu can be introduced from the Southern Hemisphere (Australia) and lead to outbreaks even in the middle of the summer (Miller et al., 2000b). More research is needed to gain a better understanding of the basis of the climatic influences on influenza. Particularly useful would be additional animal model studies in which dose and environmental conditions can be controlled. There are many ways that global warming could conceivably impact influenza transmission. For instance, warming may change bird migration patterns and thus patterns of interaction between humans and infected animals; if warmer weather reduces indoor crowding, this could reduce virus transmission; higher relative humidity and ultraviolet flux could impair virus survival and slow the spread of disease. Other factors that may have greater influence on future transmission patterns include changes in population density, urbanization, and increased air travel.

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Page 56 CRYPTOSPORIDIUM Disease description. Cryptosporidium, one of the most significant causes of waterborne disease in the United States and perhaps throughout the world, is an enteric protozoan that infects the intestinal tract and causes severe diarrhea. Cryptosporidium is an obligate parasite; it completes a complex life cycle in the epithelial cells and produces thousands of egg-like structures known as oocysts. The organism is transmitted by the fecal-oral route; individuals become infected when oocysts are washed into water supplies from sewage or animal wastes. First diagnosed in humans in 1976, it is well recognized as a cause of severe diarrheal illness worldwide (Fayer, 1997). Populations with compromised immune systems are most severely affected, with up to a 50 percent mortality rate reported in some outbreaks (Rose, 1997). Incidence of Cryptosporidium infections in the U.S. population varies widely depending on geographic location. In North America there have been 12 waterborne outbreaks of Cryptosporidium. The largest outbreak in the United States occurred in Milwaukee, Wisconsin, in 1993, when 400,000 people became ill and 100 died due to contamination of the water supply with fecal wastes (MacKenzie et al., 1994). There is a greater prevalence of infection in populations in Asia, Australia, Africa, and South America; and cryptosporidium has also been associated with drinking water outbreaks in the United Kingdom, Japan, and Holland (Smith and Rose, 1998). Climate influences. The role of climate has not been clearly elucidated in the transmission of Cryptosporidium. Data on drinking water outbreaks (from all infectious agents) in the United States from 1971 to 1994 demonstrated a distinct seasonality, a spatial clustering in key watersheds, and a statistical association with extreme precipitation (Rose et al., 2000). This suggests that land use in key watersheds is an important factor, facilitating transport of fecal contaminants from both human sewage and animal wastes into waterways and drinking water supplies during heavy precipitation. The occurrence of Cryptosporidium in surface waters has been reported in 4 to 100 percent of samples examined (Lisle and Rose, 1995). Groundwater, once thought to be a more protected source, has shown between 9.5 and 22 percent of samples to be positive for Cryptosporidium (Hancock et al., 1998). Correlations between increased rainfall and increased Cryptosporidium oocyst concentrations in river water have been reported (Alterholt et al., 1998). In the Milwaukee outbreak, spring rains and storm runoff were suspected to wash both human and animal wastes into Lake Michigan, overwhelming the drinking water treatment process. The Oxford/Swindon Cryptosporidium outbreak in the United Kingdom was also associated with a rainfall event (Rose, 1997), and rainfall was implicated in a waterborne outbreak of giardiasis, a diarrheal disease caused by the similar protozoan Giardia (Weniger et al., 1983). Researchers in Brazil

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Page 57 suggested that waterborne transmission of Cryptosporidium was related to the seasonality of the cases associated with rainfall (Wuhib et al., 1994). Waterborne disease due to any fecal-oral agent such as Cryptosporidium is not only influenced by climate. The incidence of infection in the animal or human population and the type of animal waste handling and sewage treatment will influence the likelihood of oocysts ending up in the environment. The size and hydrology of the watershed and the type and reliability of drinking water treatment will influence the impact on the drinking water. Thus, human, infrastructure, and engineering factors all play important roles in the possibility of waterborne disease. CHOLERA AND OTHER VIBRIOS Disease description. Cholera is a diarrheal disease caused by the human pathogenic bacterium, Vibrio cholera. Vibrios, including the other pathogenic species—V. parahaemolyticus, V. vulnificus, and V. alginolyticus—commonly occur in marine and estuarine waters, frequently in association with planktonic copepods. The primary mechanism for transmission of disease is through ingestion of contaminated water or seafood. Chlorination and filtration have effectively eliminated cholera from the water supply in many countries. Currently, the only source of cholera in the United States is contaminated shellfish (fewer than five cases per year). A cholera pandemic has been ongoing for at least the past 40 years in developing nations of Asia, Africa, and Latin America. In 1998 the number of reported cholera cases worldwide almost doubled. As many as 72 percent of the cholera cases were from Africa (211,748 cases). There was also a dramatic increase in cholera in Central and South America, from 17,760 in 1997 to 57,106 in 1998. Similarly, cases in Asia more than doubled in 1998 compared to 1997, with notable increases in Afghanistan, India, Cambodia, Malaysia, Nepal, and Sri Lanka (WHO, 1999c). One of the mysteries of cholera epidemics has been that cholera bacteria do not show up in cultures from environmental samples between epidemics; thus, it was difficult to identify the reservoir of bacteria that could initiate a new outbreak. Recently though, immunofluorescent assays have revealed that vibrios are present in the environment even when they cannot be cultured. The vibrios appear to enter a non-culturable phase induced primarily by unfavorable conditions such as low temperature (Colwell and Grimes, 2000). Higher temperatures, in turn, lead to increased numbers of vibrios. Climate influences. Colwell (1996) hypothesized that a 1990 El Niño event that brought warm waters to the coastal waters off Peru fostered the growth of vibrios and thus contributed to an outbreak of cholera in January 1991 in Peru and neighboring countries (Mata, 1994). Similarly, an association was found

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Page 58 between sea surface temperature in the Bay of Bengal and cholera cases reported in Bangladesh (Colwell, 1996). Sea surface height was also found to be associated with cholera outbreaks and may be an indicator of incursion of plankton-laden water inland (Lobitz et al., 2000). More recently, Pascual et al. (2000) carried out a time-series analysis of an 18-year cholera record from Bangladesh and found a significant association between ENSO and the interannual variability of cholera, likely mediated by regional climate variables such as temperature. The confirmation that V. cholerae occurs in aquatic environments in association with zooplankton and phytoplankton, and the associations found between cholera cases and sea surface temperature and sea surface height, combine to provide evidence that some cholera epidemics are indeed influenced by climate. Other vibrios that cause human disease also have growth characteristics dependent on climate. V. vulnificus, acquired by eating uncooked or undercooked shellfish, causes primary septicemia and gastroenteritis. V. vulnificus proliferates at warmer temperatures and thus could be influenced by climate-induced increases in water temperature. O'Neill et al. (1992) showed that in a New England estuary subject to extreme seasonal temperature fluctuations, there was a strong correlation between levels of V. vulnificus recovered from oysters and water temperature and salinity. Motes et al. (1998) investigated the temperature and salinity parameters of waters associated with oysters linked to V. vulnificus infections and found that abundance of this pathogen is directly related to water temperature. Vibrio parahaemolyticus, the second most common vibrio disease in humans after V. cholerae, is a frequent food-borne pathogen in Japan. It typically causes acute gastroenteritis when associated with eating uncooked or undercooked shellfish. V. parahaemolyticus is the first known example of a human pathogenic bacterium whose growth fluctuates with environmental temperatures. In 1973, Kaneko and Colwell (1973) reported that V. parahaemolyticus overwinters in Chesapeake Bay sediment and enters the water column only when temperatures exceed 14°C. They also observed that V. parahaemolyticus abundance was proportional to the concentration of zooplankton in the water column, especially copepods. Watkins and Cabelli (1985) observed a similar relationship in Narragansett Bay, Rhode Island. They determined that nutrients associated with waste water stimulated phytoplankton. The phytoplankton supported larger numbers of grazing zooplankton with a resultant increase in the abundance of the associated V. parahaemolyticus. From an ecological perspective, it is probable that V. parahaemolyticus behaves in a manner similar to that described for V. cholerae because both are estuarine bacteria that associate with copepods, both have reasonably strict temperature and salinity requirements, and both can accidentally enter human hosts and cause disease. Hence, it is likely that climate fluctuations conducive to their growth (warmer temperatures and intermediate salinities) lead to increased incidence of disease.