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A paper by the Harvard Working Group on New and Resurgent Diseases

Only 25 years ago W. H. Stewart, then Surgeon General of the US, told Congress that "the time has come to close the book on infectious disease." With tuberculosis, polio and other killer infections on the decline throughout the industrialised world, Stewart and other public health officials were confident that, thanks to improved hygiene and the development of new drugs and vaccines, the "war" against infectious disease was all but won - at least in the West. As prominent biologist John Cairns wrote in 1975, "During the last 150 years, the Western world has virtually eliminated death due to infectious disease."

At the time, such a claim did not seem wholly unjustified. Yet today infectious diseases remain the leading causes of death in the world, killing more people than heart disease or cancer, while the incidence and spread of these infections, which had been deemed to be "under control", is increasing.

In the US, the incidence of tuberculosis (TB), which had been declining steadily since 1882, rose by 18 percent between 1985 and 1992, with 26,687 cases reported in 1992. Worldwide, in 1991, eight million new TB cases were reported. One-third of the world's population is now estimated to be carrying the infection. While it is dormant in most of these people, the spread of the human immunodeficiency virus (HIV), which destroys the immune cells that keep the TB bacterium under control, is expected to cause many to succumb to the disease. With several strains now resistant to all anti-TB drugs, the World Health Organisation (WHO) admits that the disease "is now out of control in many parts of the world".

Diptheria has reemerged as a major killer of adults in the former Soviet Union, the number of cases more than doubling between 1985 and 1992 in Russia alone. Plague has resurfaced in India, while malaria has returned to regions from which it had supposedly been eliminated and is spreading to previously unaffected areas. Cholera, for the first time in almost a century, has reemerged as a major killer in Latin America.

Epidemics of dengue fever, a viral infection transmitted primarily by the Aedes aegypti mosquito, have swept Venezuela, Brazil, India and Australia for the first time. WHO warns that dengue "is spreading... throughout the globe, affecting tens of millions annually." Cases of the more severe forms, dengue haemorrhagic fever and dengue shock syndrome, are skyrocketing: between 1986-1990, an annual average of 267,692 cases were reported, compared with 29,803 in previous years. Yellow fever, too, is on the increase, the number of cases in Africa alone soaring from a few hundred a year in the late 1940s to an estimated 200,000 today.

Suddenly, the euphoric proclamations of freedom from infection seem, at best, premature; at worst, dangerously hubristic.

Disease Turnover

Few scientists now predict total elimination of infectious disease, maintaining the pattern will be one of "disease turnover". Within mainstream science, medical practitioners generally hold that mutations in viruses and other microbes are responsible for such turnover - new diseases emerging as evolutionary pressures cause pathogens to move from animals to humans, or to convert from innocuous forms into lethal ones.

More researchers, doctors and public health officials, however, are beginning to question this view. Many viruses do show high mutation rates; and viral infection per se undoubtedly plays a role in causing some diseases to persist - influenza, for example. But focusing solely on the evolution of pathogens is to overlook that the genetic makeup of pathogens - whether microorganisms, such as bacteria or viruses, or larger organisms, such as protozoa, fungi and worms - is only one of many factors that contribute to the emergence of disease.

The way these pathogens spread from host to host is one of these factors. To facilitate such a spread, many pathogens require an accomplice, called a vector, which is often an insect. The insect bites an animal infected with the pathogen and ingests some of its blood. When the insect feeds again, it deposits in that subsequent host's tissues pathogens derived from the first host.

Certain "reservoir hosts" may also be required for perpetuating the pathogen. Rodents, for instance, may harbour a microbe without apparent symptoms, while also supporting the fleas, ticks, or other ectoparasites that serve as the vehicle for transmission. The degree of contact between reservoir, vector and pathogen largely determines the prevalence of infection. Whether or not a potential host succumbs to the disease, however, depends on its general state of health and nutrition, as well as its genetic disposition.

Pathways for Disease

Virtually all pathogens regarded as "new" agents of disease have generally resulted not from the pathogens changing but from social conditions and environmental changes that have enabled the pathogens to gain access to new host populations, or to become more virulent in immunocompromised hosts. Marburg and yellow fever viruses, for example, originally were infections of monkeys; Rift Valley fever was an inherited infection of mosquitoes; and hanta virus was maintained in rodent populations. These pathogens transferred to humans because human activity created the opportunity.

In the case of yellow fever, humans serve as hosts for the pathogen mainly when forests are being cleared, bringing people into contact with the mosquitoes that normally live in the canopy along with the monkey reservoir. Humans represent a literal "dead end host" for this pathogen, since each epidemic rapidly exhausts the reservoir of potential susceptible hosts.

The complex interaction of events that can result in the emergence of a new disease is well illustrated by Oropouche fever, a nonfatal disease which causes severe headaches, muscle pains and occasionally meningitis. Frequent epidemics have occurred in Brazil where hundreds of thousands have been affected. The first outbreaks followed the building of a highway in the 1950s from Belem on the coast to Brasilia in Amazonia. Soon after construction, researchers isolated the Oropouche virus in the blood of highway workers and discovered that it was the same as that found in the blood of a sloth on the side of the Belem-Brasilia highway. Writer Ann Gibbons records in Science magazine in 1993 that the connection between the virus, the sloth and the epidemic took 19 years of epidemiological detective work: 1980 researchers had the answer: in that year, they isolated the virus from biting midges (Culicoides paraensis), which proved to be the missing link. The forest-dwelling midges, it seems, had gone through a population explosion when the settlers started clearing the forest and planting cacao for chocolate. After the farmers harvested their cacao beans, they discarded the hulls in piles that were an ideal breeding ground for the midge which spread the virus to humans along the Amazon roads.

The aetiology of Brazil's Oropouche epidemics cannot be reduced to a single cause. Rather, they resulted from a complex dialectic between a pathogen and its environment, where human activity - the colonisation of the Amazon region, the cultivation of cacao, and subsequent environmental changes that encouraged the proliferation of Culicoides and their interaction with humans - created the opportunity for Oropouche to become a disease in humans. Attempts to "explain" Oropouche through a narrow focus on viral evolution are thus highly misleading, not least because they render invisible the role that specific economic and environmental forces played in creating the disease.

What is true for Oropouche is true for many diseases. Most bacteria are not pathogens, most arthropods are not disease vectors, and most mammals are not a source of human disease. If they emerge as agents of disease, it is more often than not because of environmental change, which today results primarily from human activity. In continent after continent, country after country, both old and modern technologies and ways of living have created new niches for pathogens. As economies become increasingly international, environments degraded and growing sections of society impoverished, the pace of this change increases.

Travelling Pathogens

The concern is not just with sporadic cases of travellers being struck down with tropical illnesses. The large-scale movement of goods and people around the globe increases the probability of vectors (often insects) and nonhuman carriers of disease being introduced into areas where neither previously existed - frequently with fatal results. The reintroduction of cholera to South America in the 1990s is thought to have resulted from a freighter discharging ballast water from China into Peruvian coastal waters. The water carried the cholera vibrio which flourished in algal blooms enriched with nitrogen and phosphorous from sewage and fertilisers. Algae are filtered and eaten by molluscs, crustaceans and fish that are, in turn, eaten by people. Once it entered Latin America, the infection spread rapidly, encouraged by rapid urbanisation and IMF- and World Bank-imposed cutbacks in sanitation and public health programmes. By December 1994, millions of Latin Americans had become ill, and thousands had died. Reported cases are thought to be only a fraction of those infected.

Current development policies have also contributed to the spread of disease by undermining local livelihoods and forcing people to migrate in search of work. The resurgence of malaria, for example, has been greatly exacerbated not only by the building of irrigation schemes, creating drainage problems that increase the opportunities for vector mosquitoes to breed, but also by migrant workers bringing the pathogen into areas where it previously did not exist. Non-immune migrants entering endemic areas may fuel another kind of outbreak. Political and economic oppression has exacerbated the problem, as more and more people are forced to move within and between countries. The effect is that diseases once limited to small regions of the globe are no longer confined.

The increase in yellow fever has generated the fear that in Africa the disease will be carried from savannah areas and forest fringes, where it is currently confined, to the major cities, where the mosquito vector is plentiful but the virus as yet absent. Migration from rural to urban areas, spurred by current development policies, could bring the virus to the vector, risking an urban epidemic. And in Latin America, public health officials fear that the stage is set for a major outbreak of yellow fever: as in Africa, the risk is that urban mosquitoes will pick up the virus from rural migrants seeking work in the cities. Air travel could then spread the disease still further afield to countries such as the US, where the mosquito vector is now firmly established in the southeast of the country. According to the US Institute of Medicine, a future yellow fever outbreak in New Orleans alone could cause 10,000 to die within 90 days, and 100,000 to become ill. Jim Le Duc, a WHO virologist and epidemologist, warns of the spread of yellow fever that "we could be in for a major worldwide catastrophe".

Published (slightly abridged) with permission of Edward Goldsmith.

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