Technology, climate changes foster emerging diseases threat

Health officials embrace progress, but plan for outbreaks needed.

Since the 20th century, fears about climate change and its effects on human health have dominated international headlines.

Ecosystem instability exacerbated by changes in seasonality, ocean warming and altered rainfall patterns are purported to be influencing infectious disease pathogen prevalence, transmission profiles and host susceptibility — particularly among vector-borne diseases. Media reports about outbreaks of diseases once thought to be confined to tropical and subtropical climates appearing in temperate regions were heralded by many as irrevocable evidence that global warming is real.

Outbreaks — including resurgences of malaria in the traditionally cooler, higher altitudes of Africa and dryer semi-arid regions of India; chikungunya fever in Italy; and dengue fever and West Nile virus in the United States — have prompted epidemiologists and public health officials to question the role climate change plays in infectious disease patterns and transmission.

“This is the first case of an epidemic of tropical disease in a developed European country,” Roberto Bertollini, MD, MPH, director, special program on health and environment, WHO regional office for Europe, said in a 2007 interview with The New York Times after the chikungunya fever outbreak in the province of Ravenna, Italy. “Climate change creates conditions that make it easier for this mosquito to survive, and it opens the door to diseases that didn’t exist here previously. This is a real issue.”

“There are many complex behavioral factors and environmental factors, so it’s hard to say that the climate change has caused a particular outcome,” Kristie L. Ebi, PhD, MPH, consulting professor in the department of medicine at Stanford University in California, told Infectious Disease News.

“Climate change studies require long-time series to determine the effects of climate variability on disease, which we do not have,” Menno J. Bouma, MD, a researcher and lecturer at the London School of Hygiene and Tropical Medicine, said in an interview. “These scenarios are hard to reproduce in laboratories, and in general, people are exposed to a number of uncontrolled experiences. These are very serious limitations.”

Factors such as population growth and changing land use patterns also play important roles in interacting with weather’s effect on infectious disease transmission, making it harder to tease out the direct effects of weather, according to Mercedes Pascual, PhD, professor of ecology and evolutionary biology at the University of Michigan in Ann Arbor.

“This does not mean that climate change is not important,” Pascual said. “It’s informative to understand the interactions between these factors, rather than saying one factor is important and we should not worry about the others, or we cannot do predictions because scenarios are multifactorial.”

Paul Reiter, PhD, a medical entomology professor at the Pasteur Institute in Paris, who has more than 40 years experience studying vector-borne diseases — first with the CDC’s dengue branch and then as a member of the WHO expert advisory committee on vector biology and control — said the Intergovernmental Panel on Climate Change (IPCC) and WHO reports on climate change and infectious disease have spread misinformation.

“We are just beginning to understand climate, and in many ways we are on very shaky ground. We build models in order to try to understand the role of climate on infectious diseases better, but models should never be relied on to make predictions,” Reiter said.

Looking at the various environmental, sociodemographic and biological factors that have contributed to recent emerging infections and shifts in the distribution of diseases more closely can help public health officials better understand infectious disease ecology and develop more adaptive approaches to the challenges that climate change pose.

Malaria in the highlands and desert fringes

Malaria and dengue fever are the two major vector-borne diseases of global concern when it comes to studying the effects of climate variability, according to Ebi. “These diseases currently affect millions of people, with malaria have a serious mortality risk to children, particularly in parts of Africa,” she said.

Approximately 100 million people are living in areas where higher temperatures could affect their risk of contracting malaria, Bouma said.

“If you look at places that matter the most to understanding the role of climate variability in malaria, it will be at the edges of the distribution of disease — in highlands and also in desert fringes — where rainfall and temperature limit transmission,” Pascual said.

The role of local temperature change on malaria incidence in the Kenyan highlands during the past 30 years and its possible connection to global climate change has been a matter of debate for the past decade.

Although a clear relationship exists between altitude and temperature, and researchers know that temperature plays a role in both the development of the malaria-causing Plasmodium parasite and the Anopheles vector, these relationships are not linear.

Multiple studies using different data sets and methodologies have reached conflicting results, and a scientific consensus on the role of temperature in malaria’s resurgence has not been reached.

“Many factors influence a disease like malaria, and climate is just one,” Pascual said. Factors such as population growth, changing land use patterns and the development of insecticide resistance can act synergistically with climate, making the development of scenarios difficult, she added.

Yet, these factors are not given the attention by influential organizations such as the IPCC and WHO, according to Reiter. Claims that warming temperatures are contributing to malaria moving to higher altitudes in Africa are “a terrible dishonesty,” he said.

The often repeated pretense that people living in the Africa highlands were safe from malaria to begin with is false, according to Reiter, who said historical texts document at least 10 major malaria epidemics in the Kenya highlands between World War I and the advent of DDT and antimalarial drugs in the 1950s and 1960s.

“What’s upsetting is that organizations like the IPCC, which is supposed to be the gold standard on these things, have been repeating this misinformation,” Reiter said.

Although temperature plays a role in disease transmission, he said it is usually not the dominant role.

Changing of land-use patterns, human behavior

Changing land-use patterns and human behavior, such as the clearing of previously dense forests for subsistence farming and increased population density that occurred after colonists left the region in the 1960s, are more likely driving malaria’s re-emergence.

“Anopheles gambiae, the most predominant malaria vector in that area of the world, breeds in open sunlit pools of water, which simply were not present when the area was dense forest,” Reiter said. “Once people came and cleared the forest, it created a beautiful environment for the mosquito.”

The situation in the semi-arid regions of Rajasthan and Gujarat in northwest India and the Punjab regions of Pakistan is similar to that of the African highlands. Attempts to eradicate malaria through the use of pesticides and antimalarials in the 1960s and 1970s have failed. Similar to the highland regions of Africa, malaria population dynamics are characterized by strong seasonality and variation in outbreak sizes from year to year, Pascual said.

Low immunity among the general population due to inconsistent exposure to the pathogen results in intermittent outbreaks that tend to place larger burdens on the health care system.

To complicate matters further, irrigation systems developed to stimulate agricultural production to meet growing food demands have resulted in higher numbers of the malaria vector Anopheles mosquito, but these numbers do not necessarily translate to more cases of malaria.

“Desert fringe malaria has changed because of irrigation. These regions are desperately trying to get areas irrigated and increase the food supply,” Bouma said. “We see reduced risk in certain areas because more people can live in warmer drier locations with irrigation, but the amount of people is not going down. The relative risk per person might go down, when the risk for the population as a whole is increasing.”

Using statistical analyses, Pascual and colleagues have found that irrigation systems tend to reduce the coupling between large rainfall events and the size of epidemics, making them more difficult to predict. Increases in wealth in regions that have better irrigation and agricultural systems could lead to better malaria control efforts with residual insecticide spraying, but these transient improvements mask the true burden of disease in the event of anomalous weather conditions.

“Regardless of the specific mechanism, in areas where the risk itself persists for anomalous climatic conditions, it would be beneficial to incorporate predictions of this risk based on climate variability, using remote sensing tools in the planning of spray interventions,” Pascual and colleagues wrote in Malaria Journal.

“The complexity of transmission cycles is challenging,” Ebi said. “Climate change is one of several drivers, and we need to be able to tease out how these different drivers interact — synergistically, antagonistically or whether they exist side by side.”

Dengue fever in the United States

Perhaps the largest emerging US infectious disease threat is the vector-borne dengue fever, transmitted by the Aedes aegypti mosquito, whose natural range includes Texas and Florida.

Although it is plausible that rising temperatures could extend A. aegypti’s range northward to other regions of the country, “dengue fever is more difficult to predict using weather as a variable,” Bouma said.

Infectious disease specialists and public health officials are more worried about cases imported from travelers, which have become increasingly frequent in the past decade due to the convergence of multiple factors, not just weather.

In the 1980s, global trade and commerce brought a second dengue vector to the United States — the A. albopictus mosquito, which is better able to survive and thrive in the cooler temperate climates than A. aegypti. Reiter first recognized A. albopictus in Memphis in 1982 while working with the CDC’s dengue branch and in 1985 discovered that the mosquitoes were hitching rides in used tires imported from their native Southeast Asia.

A. albopictus has since spread to the Northeast and Midwest regions of the United States, but Reiter said although it can spread dengue, A. albopictus is not as efficient a vector as A. aegypti.

However, public health officials warn that if a mutation were to occur from a strain of the virus imported by a traveler, dengue could theoretically establish a wider US distribution.

On Sept. 15, the CDC issued an outbreak notice urging US travelers in the Caribbean, Central and South America to protect themselves against mosquito bites after more than 890,000 cases of dengue were reported to the Pan American Health Organization, including 10,840 cases of severe dengue hemorrhagic fever and dengue shock syndrome.

Although large in scale, the outbreak is not entirely surprising. Dengue cases in these regions have increased fourfold since the 1980s, according to the CDC, with the rise attributable to increasing urbanization, the proliferation of man-made water-holding containers that facilitate A. aegypti breeding and lax mosquito control policies.

In August 2009, the continental United States saw its first reported case of dengue fever since 1945 in a New York woman who had just returned from a trip to Key West, Fla. After two more cases were identified in Key West, CDC and Florida Department of Health investigations revealed that 5.4% of 240 residents included in a serosurvey had evidence of a recent infection. In a separate sampling of specimens from 21 residents, 42.9% tested positive for dengue.

That same year, the CDC classified dengue as a nationally reportable disease. Since that time, at least 57 cases have been reported in Key West, but health officials said improved surveillance and testing may account for the increase because conditions in South Florida have always been conducive to A. aegypti transmission.

Nonetheless, the CDC warns that the risk of dengue spreading from these areas is high due to increased volume of tourists. US health care providers should maintain a high index of suspicion for dengue in patients returning from areas where the disease circulates who are exhibiting the following signs and syptoms: acute febrile illness, thrombocytopenia, leukopenia, hemoconcentration, rash and eye pain.

Despite these warnings, if an outbreak were to occur in the United States, it is unlikely that it would result in serious morbidity and mortality, as sequential infection and immune phenomenon are greater determinants of disease severity. “Disease serotype and whether a person has been previously infected are more likely to influence the likelihood of a dengue epidemic,” Bouma said.

Responding to shifts in infectious disease ecology

“What’s really important is improving public health prevention programs, including education and awareness, improving surveillance programs and ensuring the public health organizations and institutions are prepared for potential changes in disease distribution,” Ebi said.

“It’s fairly clear for some diseases that climate variability can have an effect, but the extent to which it does have an effect is entirely dependent on our public health systems,” she said. – by Nicole Blazek

For more information:

• Alonso D. Proc Biol Sci. 2011;278:1661-1669.
• Baeza A. Malar J. 2011;10:190.
• Gould EA. Trans R Soc Trop Med Hyg. 2009;103: 109-121.
• McMichael AJ. J Intern Med. 2011;270:401-413.
• Omumbo JA. Malar J. 2011;10:12.
• Reeza G. Euro J Public Health. 2009;19:236-237.
• Reiter P. Environ Health Perspect. 2001;109:141-161.
• Rose JB. Environ Health Perspect. 2001;109:211-221.
• Rosenthal E. As earth warms up, tropical virus moves to Italy. The New York Times. Dec. 23, 2007.

Disclosures: Drs. Bertollini, Bouma, Ebi, Pascual and Reiter report no relevant financial disclosures.

Is global warming’s effect on emerging and shifting disease patterns overemphasized?

We should be sure to keep the role of climate in proper perspective and consider the wide range of effects it may have.

In many fields, we are looking closely at intersections with climate change. It is a timely topic and it is not really a question of the correct amount of emphasis as being sure that we keep the role of climate in a proper perspective and consider the wide range of effects that it might have. We know that some infectious diseases are sensitive to climate. But, if our goal is to understand how climate affects disease processes, it is important to not confound climate sensitivity with the assumption that climate change will increase disease. The best starting point is to assume that climate change will shift the distribution of diseases to higher latitudes. This means that disease might increase toward the poles, but decrease near the equator. Of course, from a public health perspective, we are concerned with the areas where disease will increase, but from a scientific perspective, the areas where disease will decrease are equally interesting. We also know that diseases are sensitive to many other things besides climate. For human diseases, economy is the overwhelming factor and can easily trump climate effects.

Kevin Lafferty is a research ecologist at USGS, Western Ecological Research Center. Disclosure: Lafferty reports no relevant financial disclosures.

We should continue to try to understand the full range of factors affecting future disease risks.

Given that the climate is changing it is very reasonable to ask whether and to what extent those changes will affect the distribution and burden of infectious diseases. Most attention to date has been directed at vector-borne diseases (eg malaria), reflecting that the distribution and abundance of the arthropod vectors typically is very climate dependent. Some, but rather less, attention has been paid to impacts on diseases with a significant environmental component, such as cholera. My own impression of that body of work is that it does indicate possible impacts of climate change, but these are likely to occur to any significant degree only over time scales of decades. That’s a helpful conclusion indicating that these impacts should be borne in mind but are rather less urgent than faster moving problems such as the spread of antibiotic resistance. That said, the work I refer to has concentrated on what I might call the direct impacts of climate change.

There are also likely to be indirect impacts on infectious diseases, mediated by changes in human behavior, housing, agricultural practices, food availability, water supplies and so on. It is easy to imagine that these indirect impacts could be much more important than the direct impacts. However, they are much harder to evaluate. One of the attractions of attempting to predict the future impact of climate change is that sophisticated projections of spatial and temporal changes in climate variables are available. These are relatively easy to plug into epidemiological models. No such projections exist for factors such as changes in agricultural practices or human behavior etc., which remain far more uncertain. Other potentially important factors such as migration, civil unrest or economic problems – to which climate change could contribute but will obviously not be the only driver – are essentially unpredictable at present. So they tend to get ignored. I expressed this in the

Philosophical Transactions (Taylor LH. Phil Trans R Soc. 2001;356:983-989.) paper as the projection of infectious disease risks being very much ‘the art of the possible.’ In summary, my personal view is that we should continue to try to understand the full range of factors affecting future disease risks, including climate amongst these, but also how they are influenced by climates and, indeed, by anything else.

Mark Woolhouse is a professor at the Center for Immunology, Infection and Evolution at the University of Edinburgh. Disclosure: Woolhouse reports no relevant financial disclosures.

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