Global climate change is expected to intensify ENSO-related climate variability (WHO et al., 2003), which in turn offers a means to study the effects of climate variability on infectious disease (see Haines in Chapter 1). In his workshop presentation, Jean-Paul Chretien, of the U.S. Department of Defense, described key examples of such research, which examined connections between ENSO-related weather extremes and two infectious diseases: RVF and chikungunya fever (see Chretien in Chapter 2).

El Niño and Rift Valley fever An acute mosquito-borne viral disease, RVF primarily affects livestock (e.g., cattle, buffalo, sheep, goats) but can also be transmitted to humans through direct contact with the tissue or blood of infected animals, as well as by mosquito bites. Outbreaks of RVF among animals can spread to humans. The largest reported human outbreak, which occurred in Kenya during 1997-1998, resulted in an estimated 89,000 infections and 478 deaths (CDC, 2007b). For decades, RVF outbreaks have been associated with periods of heavy rainfall, which occur during El Niño; this observation led researchers to develop an operational model for RVF risk based on vegetation density (a marker for rainfall) as measured by satellite (see Figure SA-7A; Linthicum et al., 1999).

During the El Niño event of 2006-2007, above normal rainfall resulted in anomalous vegetation growth in East Africa, northern Australia, and parts of eastern China, and drought and diminished vegetation growth in southeastern Australia and northern South America. Above normal rainfall and anomalous vegetation growth in eastern Africa created ideal ecological conditions for the emergence of mosquito vectors of RVF, resulting in an outbreak of the disease in East Africa from December 2006 to May 2007 (see Figure SA-7B; A. Anyamba, personal communication, April 2008).10

Throughout the autumn of 2006, this model identified high risk for RVF in the same area affected by the 1997 epidemic, leading the U.S. Army Medical Research Unit (USAMRU) in Kenya to intensify its surveillance of local mosquitoes. Positive results provided early warning of a pending epidemic, enabling the Kenyan government—in concert with international partners including the Centers for Disease Control and Prevention (CDC) and the World Health Organization (WHO)—to mount a timely and targeted response, Chretien said (see CDC, 2007b).

La Niña and chikungunya fever Another mosquito-borne viral disease, chikungunya fever, is rarely fatal, but can cause severe joint pain, prolonged disability, and complications including protracted fatigue and arthritis (CDC, 2007b). A

10Moisture is required for egg development. Flooding often occurs following periods of heavy precipitation, enabling full development of the larvae and an increase in the mosquito population, thus spreading the virus during their next bloodmeal (WHO, 2007).

^ FIGURE SA-7A Using satellites to track Rift Valley fever. g g; NOTE: Scientists have discovered that the combination of warmer-than-normal equatorial Pacific Ocean temperatures associated with El Niño g;

Í and rising sea surface temperatures in the western equatorial Indian Ocean can trigger outbreaks of Rift Valley fever in eastern Africa. This c

$ February 1998 image of sea surface temperature and vegetation (above), from the Advanced Very High Resolution Radiometer (AVHRR) §

jj onboard the National Oceanic and Atmospheric Administration's (NOAA) polar-orbiting weather satellites, illustrates the close relationship —

^ between ocean temperature (warmer-than-normal ocean temperatures are shown in red, cooler-than-normal temperatures shown in blue), rain- 5"

fall, and their impacts on land vegetation (greener-than-normal vegetation shown in light green). The two warm pools of water (highlighted in o the boxes) affect atmospheric circulation patterns such that there is an increase in rainfall over a large area of eastern Africa, which can lead °

to large-scale outbreaks of mosquito-bome diseases (NASA Goddard Space Flight Center, 2000). ^

SOURCE: NASA Goddard Space Flight Center, Scientific Visualization Studio (2000). ^

FIGURE SA-7B January 2007 combined global Nomialized Difference Vegetation Index (NDVI) (depicted over land surfaces) and sea surface temperature (SST) (depicted over oceans) anomaly mosaic. NDVI and SST data are collected daily by several satellites in an ongoing fashion as part of NASA's and NOAA's global climate observing efforts. According to the Global Inventory Modeling and Mapping Studies (GIMMS) Group at the NASA Goddard Space Flight Center, the El Niño event of 2006-2007 was manifest by anomalous warming (~+2°C) of SSTs in the equatorial eastern Pacific Ocean with corresponding anomalous warming (—i-l°C) in the equatorial western Indian Ocean. Such El Niño events result in anomalous displacement of global tropical precipitation yielding regional patterns with above normal rainfall in some areas and severe drought in other areas. These anomalies in precipitation are illustrated through biospheric response patterns represented by satellite derived vegetation index anomalies over land surfaces.

SOURCE: Data processing and analysis: Jennifer Small, Edwin Pak, Assaf Anyamba, Compton J. Tucker, GIMMS Group, NASA Goddard Space Flight Center.


string of outbreaks along the Kenyan coast in 2004 apparently spread to several western Indian Ocean islands and to India, resulting in the largest chikungunya fever epidemic on record (Chretien et al., 2007). Upon investigation, Chretien and coworkers discovered that at the time of the initial outbreaks in Kenya, a regional drought—corresponding to the La Niña phase of ENSO—had gripped the region. "There is some evidence that suggests that there may be a connection [between the drought and the chikungunya fever epidemic]," Chretien observed. "We know from the outbreak investigations in [Kenya], that domestic water wasn't being changed as frequently as usual because of the drought, and it wasn't being protected properly from the peridomestic mosquitoes that transmit chikungunya virus." Also, he noted, previous experimental studies in Kenya found that warm conditions can accelerate viral development within the mosquito (Chretien et al., 2007).

In addition to ENSO-associated weather anomalies, other short-term variations in climate, including drought, temperature, and wind patterns, have also been linked with changes in infectious disease incidence and geographic range:

Drought and diarrheal disease While diarrheal disease is frequently associated with periods of heavy rainfall and flooding and the subsequent contamination of water supplies with fecal bacteria (NRC, 2001), Haines described findings from a recent review of cross-sectional studies from 36 low- and middle-income countries that correlate increased incidence of diarrhea in young children with decreased rainfall (Lloyd et al., 2007). Because the vast majority of freshwater is used for irrigation, rather than for personal consumption, the relationship between these variables is unclear. Haines noted that handwashing behavior has been shown to decline when freshwater is less available (Curtis and Cairncross, 2003).

Temperature and food poisoning Comparing data from 16 sites in industrialized countries, investigators examined the incidence of sporadic cases of food poisoning (rather than outbreaks, which tend to be triggered by specific contamination incidents) attributed to the bacterium Salmonella. They found that such cases rose in a linear relationship to the previous week's temperature (Kovats et al., 2004). The lag in time suggests that temperature exerts this effect by accelerating bacterial replication in prepared food, Haines observed. Similar patterns of seasonal incidence also occur in cases of gastroenteritis caused by another bacterial agent Campylobacter (Kovats et al., 2005; Louis et al., 2005; Tam et al., 2006). However, unlike salmonellosis, seasonal patterns of Campylobacter infection in humans are not completely attributable to food-borne transmission of the pathogen, according to speaker Rita Colwell of the University of Maryland.

In a study conducted in England and Wales, Colwell and colleagues found that an increased incidence of Campylobacter gastroenteritis was associated with higher temperatures in districts supplied primarily with surface water, while those


with the lowest incidence received mainly groundwater (Louis et al., 2005). The researchers therefore hypothesized that water ingested by poultry was the source of the seasonal increase in cases of human Campylobacter gastroenteritis and noted that surface water may be especially prone to contamination with the pathogen in the spring, when cattle and sheep give birth and are put out to pasture.

Wind-borne disease The annual arrival of dry, dust-laden winds—thought to render mucosal membranes vulnerable to infection—heralds the onset of epidemic meningococcal meningitis in West Africa (Sultan et al., 2005). There is some evidence that the geographical distribution of meningococcal meningitis in West Africa has expanded in the recent past, possibly as a result of changes in land use and climate (Molesworth et al., 2003; see Haines in Chapter 1).

Coccidioidomycosis—a fungal disease caused by inhaling the spores of Coccidioides immitis—along with meningococcal meningitis, can travel across continents in spore-laden desert dust clouds (Flynn et al., 1979; Garrison et al., 2003; NRC, 2001). The winds pick up these spores, along with dry, dusty soils, and transport them hundreds of miles (NRC, 2001; Schneider et al., 1997).

High winds and extreme weather have also been linked to the emergence, reemergence, and long-distance transport of vector-borne pathogens such as bluetongue and the citrus tristeza virus (IOM, 2003, 2008; NRC, 2001). Asian soybean rust, a pathogenic fungus, was apparently blown into the United States from South America by Hurricane Ivan in 2004 (Schneider et al., 2005). This nonnative plant pathogen has now become established in soybean-growing areas of the United States and Canada.

Synergies and Threshold Effects of Climate Change on Infectious Disease Emergence

In addition to the short-term observations of the effects of climate variation on the range and transmission of infectious disease described in the previous section, workshop participants considered the apparent near-term and long-range impacts of climate change on infectious diseases in several illustrative contexts: plant communities and crops; aquatic and marine environments; the Arctic; and central Asian ecosystems that have long served as incubators for plague epidemics. A common theme uniting these diverse accounts was the recognition that climate does not act gradually or entirely predictably upon ecosystems, but combines with other influences to produce threshold effects. Although typically expressed in terms of population dynamics (e.g., explosions, migrations, extinctions), such threshold effects also include the emergence of infectious diseases.


Plant Disease

According to speaker Karen Garrett of Kansas State University, climate change has the potential to produce huge—and largely unanticipated—impacts on agricultural and natural systems by altering patterns of plant infections. These effects include the direct consequences of crop diseases, such as declining food supplies; indirect effects on agricultural productivity, such as reduced soil formation (and thereby lower crop yields) resulting from more frequent tillage to remove infected plant residue; and health risks associated with increased pesticide usage. While efforts to understand these potential impacts typically focus on ecosystems, populations, and communities, Garrett and coworkers study plant responses to infectious disease at the molecular level, in order to understand and model genetic constraints for pathogen and plant adaptation to climate change (see Garrett in Chapter 2 for specific examples of these studies in various crop plants and plant communities).

Extending such observations to predict the repercussions of climate change on plant disease at the ecosystem level requires consideration of a broad range of influences on each member of the disease triad. Moreover, Garrett explained, any such perturbation may cross a threshold to an unexpectedly dramatic response. Many diseases, such as potato late blight, the disease that caused the Irish potato famine in the mid-nineteenth century, exhibit compound interest increases during a growing season, so that a slightly longer growing season can result in much higher regional inoculum loads. "The effects of climate change will be most important when there are thresholds and interactions that produce unanticipated large responses, and one of the most important effects might be that the systems will change more rapidly than in the past," Garrett observed.

Considerable resource investments will be needed to improve our understanding of the various and interacting factors that influence plant disease, she said. These include long-term, large-scale records of pathogen and host distributions (currently lacking even for agriculturally-important diseases); models of regional processes that incorporate disease dynamics; data and models that describe the dispersal of pathogens and vectors; and integrated, multidisciplinary, international collaborative networks for data collection and synthesis.

Research is also needed to identify and improve the introduction of disease resistance genes, a proven and promising strategy for responding to changes in disease threats to crops. In the tropics, where climate change is viewed as a considerable threat to food security due to the likelihood of greater climate variability, and where resources for crop protection are limited, efforts to characterize genetic resources are especially important. The Consultative Group for International Agricultural Research (CGIAR, 2008) currently undertakes such efforts on a "shoestring budget," Garrett reported.


Aquatic and Marine Environments

Two speakers at this workshop offered different perspectives on the direct and indirect influences of climate change in aquatic ecosystems. Leslie Dierauf of the U.S. Geological Survey (USGS) described the apparent impacts of climate and disease trends for a broad cross-section of aquatic and marine species and ecosystems, while Colwell discussed ecological and climatological factors that influence cholera, a water-borne infectious disease of considerable public health significance.

Aquatic and marine wildlife Marine life has suffered significant increases in the frequency and number of novel disease epidemics over the past few decades due to a variety of factors including, but not limited to, the disruption of ocean ecosystems by climate variability and warming water temperatures (Harvell et al., 1999). Much like their human counterparts in drought- or storm-stricken areas, marine mammals are being forced out of their home ranges by warming-induced population declines in plankton. As they follow their food to new territories, migrant marine mammals both encounter and introduce novel disease agents. Mass die-offs of certain species (e.g., seals, dolphins, porpoises) have occurred when these animals were exposed to morbilliviral diseases, such as distemper, for the first time during their annual migrations. Phocine distemper virus, identified as the cause of a die-off of harbor and gray seals in northern European coastal waters, is thought to have been transmitted to these species by harp seals that migrated to this region in response to overfishing-induced food shortages around their native Greenland in the late 1980s (Harvell et al., 1999).

The effects of climate variability on the health and disease of aquatic (freshwater-dwelling) and marine (ocean-dwelling) organisms are frequently exerted through the food web, as shown in Figure SA-8. In addition to these relationships, Dierauf emphasized that because aquatic and marine ecosystems are interconnected, infectious diseases of fish and wildlife may have the opportunity to move from freshwater sources to intertidal zones to marine environments, affecting species that may have not encountered these disease agents before. She also noted the particular vulnerability of coastal and intertidal zones to the effects of extreme weather, both directly as a result of damaging winds and water and indirectly though runoff from inland floods. On the U.S. Gulf Coast where, she said, "two hurricanes can turn an intertidal seagrass area into a mudflat," a majority of such areas—which act as buffers between ocean and land, and between fresh and marine waters—have been lost in recent years.

Examples of emerging infectious diseases along the aquatic-marine continuum, and their potential links to climate change, are presented in Box SA-2. Noting the lack of evidence-based literature on the effects of climate change and wildlife health, Dierauf joined the chorus of workshop participants calling for

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