Date: Tue, 09 Dec 1997 18:26:54 -0800
From: Mark Jones <Jones_M-AT-netcomuk.co.uk>
Subject: M-I: DEVELOPMENT, GLOBAL CHANGE, AND THE EPIDEMIOLOGICAL ENVIRONMENT (1 of 4)


By Gretchen C. Daily & Paul R. Ehrlich

Paper number 0062 -- Revised 1995
G.C.D.: Energy and Resources Group Building T-4, Room 100 University of
California Berkeley, California 94720
P.R.E.: Center for Conservation Biology Stanford University Stanford,
California 94305

ABSTRACT

Although improvements in human health represent a crucial aspect of
development worldwide, many trends associated with development and global
change appear to be reducing health security. In this article, we define
the human epidemiological environment and describe key biophysical,
economic, sociocultural, and political factors that shape it. The potential
impact upon the epidemiological environment of aspects of both development
and global change are then examined: the influences of human population
size, mobility, geographic distribution, and nutritional status;
modernization; loss of indigenous medicinal knowledge; microbial evolution
of antibiotic resistance; land conversion and biodiversity loss;
agricultural intensification; stratospheric ozone depletion; and climate
change. Human vulnerability to infectious disease is often strongly and
deleteriously influenced by ongoing, intensifying changes in these factors.
An unprecedented level of communication and cooperation between experts,
institutions, and nations is required to respond to the increasing threat
of epidemic disease, which points to a promising area for enhanced
interdisciplinary collaboration.

When one comes into a city to which he is a stranger, he ought to consider
its situation, how it lies as to the winds and the rising of the sun; for
its influence is not the same whether it lies to the north or to the south,
to the rising or to the setting sun. These things one ought to consider
most attentively, and concerning the waters which the inhabitants use,
whether they be marshy and soft, or hard and running from elevated and
rocky situations, and then if saltish and unfit for cooking; and the
ground, whether it be naked and deficient in water, or wooded and
well-watered, and whether it lies in a hollow, confined situation or is
elevated and cold...

>From these things he must proceed to investigate everything else. For if
one knows all these things well, ... he cannot miss knowing, when he comes
into a strange city, either the diseases peculiar to the place or the
particular nature of the common diseases, or commit mistakes, as is likely
to be the case provided one had not previously considered these matters.
And in particular, as the season and year advances, he can tell what
epidemic disease will attack the city, ... and what each individual will be
in danger of experiencing from the change of regimen. -- Hippocrates, On
Airs, Waters, and Places, cat 400 B.C. (quoted in Garrett 1994, p. 234).

INTRODUCTION

Good health is such an integral part of human well-being that, in many
languages, everyday greetings and meal-time toasts are synonymous with best
wishes for it. In English, the very word "salutation" is derived from the
Latin salutare or salus, which refer to health and safety. People have
always been wary of being unexpectedly stricken by disease.

Although the loss of good health is inherently unpredictable, human
behavior at the individual and societal levels profoundly influences the
incidence of disease. This has been understood since ancient times and,
indeed, the same fundamental factors that determined human vulnerability to
disease early on remain paramount today. The rates and scales over which
these factors now operate are unprecedented, however, greatly disrupting
the epidemiological environment and opening new opportunities for disease
agents.

The epidemiological environment consists of the conditions and processes,
both biophysical and social, that influence the interaction between human
beings and disease agents. It encompasses a complex of interrelated
factors, including:

* the parasites that are actually or potentially pathogenic to Homo
sapiens, defined broadly to include subcellular, unicellular, and
multicellular organisms such as prions , viruses, bacteria, fungi,
protozoa, helminths, and arthropods; ( Whether these proteins could be
considered organisms and, indeed, whether they exist at all is a matter of
debate that extends beyond the bounds of this article (see Prusiner 1995).)

* biophysical determinants of the reproductive success of such parasites,
including conditions such as temperature and moisture, availability of and
transmittancy to vectors and hosts, the evolution of virulence, and
coevolution of human immunity and parasites' resistance to the immune
system and other human defensive measures;

* social determinants of the reproductive success of such parasites,
including the frequency and nature of interpersonal contact, travel and
migration patterns, access to health care and information, pharmaceutical
markets, urbanization, poverty, public health policy, medical training,
funding of medical research, and political leadership.

These factors span virtually the entire human environment. Nonetheless,
their nexus is little appreciated because the pathogenic actors in it are
largely invisible -- out of sight, out of mind (Ornstein and Ehrlich,
1989). Few people are aware that each human being encloses billions of
microorganisms and is surrounded by trillions more. Some of these organisms
play key roles in keeping people alive; others represent lethal threats.
The two kinds do not have to be very different. Some strains of Escherichia
coli, common bacteria that live in the human large intestine, are helpful
in synthesizing vitamins that are essential to people. Other strains may
cause lethal disease.

Recent and projected future changes in the epidemiological environment pose
a major threat to health security, which is presently manifesting itself in
a variety of ways (Ehrlich and Ehrlich, 1970, pp. 148-151; 1972, pp.
181-184; Ehrlich et al., 1977, pp. 606-609; Leaf, 1989). Old diseases such
as malaria (e.g., Pearce, 1995), tuberculosis (Bloom and Murray, 1992;
Brown, 1992), bubonic plague (Altman, 1994; Burns, 1994), and cholera
(Glass et al., 1992) are resurgent; the new epidemic of AIDS is creating
formidable public health problems; some strains of old bacterial enemies
may be becoming more deadly (Nowak, 1994); "miracle" drugs are losing their
potency; and a variety of nasty viruses such as Ebola appear to be lurking
in the wings (e.g., MacKenzie, 1995; Morell, 1995; Altmann, 1995). Malaria
was once thought to be on the way toward eradication (Garrett, 1994, p.
31), yet now there are between 300 and 500 million cases annually,
resulting in as many as 2.7 million deaths (Nussenzweig and Long, 1994).

These problems mark the second major round in a coevolutionary (Ehrlich and
Raven, 1965) battle between Homo sapiens and its parasitic enemies. The
first began with the agricultural revolution, some 10,000 years ago. This
led to the development of towns and cities where human populations grew to
a size and density at which they could sustain epidemics of diseases such
as measles, smallpox, flu, cholera, and polio (Black, 1966, 1975). It also
led to concentrations of human and animal wastes ideal for the propagation
of protozoan and helminth parasites (Inhorn and Brown, 1990).

After World War II, many believed that the first round was ending in
victory for humanity with the defeat of microbial pathogens through the use
of sanitation, water purification, vaccination, antibiotics, and
pesticides. Indeed, in 1969 U.S. Surgeon General William H. Stewart
testified before Congress that it was time to "close the book on infectious
disease" (Fisher, 1994); like most physicians of his day, he was deeply
ignorant of the nature of the epidemiological environment.

As the human population has increased to unprecedented size, it has
dramatically changed this vast, tumultuous, little understood world. Some
of these alterations have been to our benefit; many are already clearly
deleterious and promise to become more so in the future. Alterations in the
epidemiological environment have been little examined, and do not fit into
the heuristic framework by which other aspects of human activity and the
environment have been explored (Ehrlich and Holdren, 1971; Holdren and
Ehrlich, 1974; Ehrlich and Ehrlich, 1990).

In our view, in no aspect of the human environment are the economic costs
of environmental deterioration clearer, of greater importance to those
concerned with development, or more threatening to the human future.
Consider the warning of the late Howard Temin, who received the Nobel Prize
for his discovery of retroviruses (which include HIV): "...it is not
surprising that a major new epidemic has accompanied the dramatic
post-World War II social changes -- the greater urbanization and enormous
population increases in Africa, the rise of freer lifestyles in North
America and Europe, and the growth of jet travel everywhere. If anything,
the surprise might be that there has been only one major new epidemic"
(Temin, 1989, p. 1).

In this paper, we examine the impact on this hidden environment of both
development and global change. These two aspects of the increase in scale
of the human enterprise are so tightly interrelated as to make any
classification of their elements quite arbitrary. We have structured our
inquiry around three categories of changes: (i) those in biophysical and
social characteristics of the human population; (ii) those in human tactics
and strategies for controlling disease; and (iii) dramatic alterations of
the biophysical environment, collectively referred to as "global change"
(Lovejoy, 1993), that for the most part represent unintended consequences
of the first category.

CHANGES IN CHARACTERISTICS OF THE HUMAN POPULATION

Population Size

For successful establishment in a host population, a parasite must achieve
a basic reproductive rate of greater than one (Macdonald 1952, May and
Anderson, 1979). In general, this means that each infected individual, on
average, infects more than one other individual. This, in turn, means that
a threshold or critical community size is necessary for the perpetuation of
most epidemic diseases. The precise threshold for disease establishment is
determined by complex characteristics of both the parasite and the host,
such as whether transmission is direct or mediated through a vector and/or
animal reservoirs; seasonality in transmission; incubation, latent, and
infectious periods of the host; the existence and duration of acquired host
immunity; reproductive requirements of the parasite; and so on (Anderson
and May 1991).

The bottom line is that human population size and density are key variables
in epidemiology, influencing the rate of introduction of new parasites into
the population, their chances of becoming established, the rate of their
spread, the evolution of their virulence, and the capacity of human
cultural evolution to defend against them. Paleolithic groups were probably
relatively free of virulent epidemic disease (Cohen, 1989; Inhorn and
Brown, 1990). It was not until a critical community size was reached in
early agricultural societies that parasites previously confined to nonhuman
animals were able to exploit Homo sapiens. Examples of such diseases
include smallpox, influenza, and measles, which are thought to have evolved
from monkey pox, avian flu, and rinderpest or canine distemper,
respectively (Fenner et al., 1974). Measles apparently could not get a
foothold in human populations until there were aggregations of about
200,000 to 500,000 people (Bartlett, 1957; Black, 1966).

Today's 5.7 billion people represent a brand new environment for pathogens
and potential pathogens (Mitchison, 1993). It is the densest population the
world has ever seen, and it contains large numbers of immune-compromised
people due primarily to malnourishment, the presence of immunosuppressive
pollutants in the environment (Ross et al., 1992; Repetto, 1992; Colborn et
al., 1996) and, increasingly, to AIDS. That vulnerable portion of the
population makes an especially favorable environment for the evolution of
virulence in viruses, bacteria, and fungi that in the past were viewed as
benign (e.g., Sternberg, 1994; Georgopapadakou and Walsh, 1994). For a
parasite, evolving host specificity to humans would amount to winning the
biggest jackpot in history.

It is not clear, at present, how HIV-1 (the virus that causes the most
serious form of AIDS) first entered the human population, but one
possibility is that it was the result of a transfer by a vector (e.g., a
mosquito or tick) from another primate. Such events are thought to occur
very rarely (Humphery-Smith et al., 1993), but increased human numbers make
more probable such "jumps" from other species.

Moreover, population growth is accompanied by large families, which
increase the vulnerability of populations by presenting arrays of
immune-similar individuals. As viruses colonize individuals in such
families sequentially, they may evolve greater virulence, as was the case
in rural Senegal where the case fatality rate was higher in children who
caught the measles from relatives than among those that contracted the
disease from nonrelatives (Garenne and Aaby, 1990). Immune-similarity of
individuals may also have contributed to the near extinction over recent
centuries of native Americans and their cultures (Roberts, 1989). Black
(1992, 1994) has argued that the decimation of these populations by disease
was due not just to a lack of immunological experience that made them
highly susceptible, but also to a relative lack of genetic variability
tracing to their rapid expansion after the genetic "bottleneck" of the
trans-Bering invasion. Sadly, the genetic mixing through immigration that
might protect isolated cultures would probably simultaneously destroy them
(Black, 1994).

Population Mobility: Rapid Transportation

The movement of people has always been an important mode of spread of
disease. The legacy of merchants, explorers, and conquistadores extends far
beyond that assessed by most historians (McNeill, 1976). European sailors
brought smallpox, measles, and swine flu to the New World; the first
epidemics of leprosy in Europe followed the expansion of the Roman Empire;
the black death of fourteenth-century Europe made its way from central Asia
via the Silk Road; and cholera was carried unwittingly by traders and
armies into Europe from India in the early 1800s. As we write, world health
authorities are declaring states of emergency in Central America, and port
cities throughout Latin America are on alert, due to the rapid spread of
dengue fever (New York Times, 1995; UPI, 1995).

The spread of epidemics is clearly greatly facilitated by the development
of high-speed modern transport systems. In recent years, indices of the
amount of international travel were highly associated with the spread of
AIDS (Darrow et al., 1986). Steamships alone made it possible to transport
bubonic plague to all major ports in the world at the end of the last
century, something that could not have occurred earlier because all of the
susceptible passengers on plague-infested, slow-moving sailing ships would
generally have died before the ships reached ports (McNeill, 1976). People
carrying dengue fever on airplanes have represented an important mode of
its recent spread (Monath, 1993). Rapid transportation helps the spread of
antibiotic-resistant strains of bacterial pathogens (Tauxe et al., 1990).

Modern high-speed transport also plays a role in the distribution of
recreational drugs; large supplies produced in the "golden triangle" of
southeast Asia or the mountains of South a flow easily into rich and poor
nations around the world. Almost everywhere, sharing of needles by addicts
contributes to the propagation of infectious diseases. The problem is
especially serious because narcotic addicts are often immune-compromised,
making their bodies ideal environments for the multiplication of numerous
pathogens (e.g., Cherubin, 1971; Levine and Sobel, 1991).

Modern transport also helps to move animals that are potential vectors or
disease reservoirs around the world, which combined with projected climate
change could further degrade the epidemiological environment (Soule, 1995;
Dobson and Carper, 1992). In Uganda a century ago an agricultural officer
introduced the shrub Lantana camera for use as an ornamental hedge. The
Lantana provided excellent moist habitat for tsetse flies, and an increase
in sleeping sickness followed. Perhaps the most spectacular recent case of
the transfer of a dangerous vector was the moving from Asia to the United
States of a mosquito (Anopheles albopictus; the Asian tiger mosquito)
capable of transmitting dengue. The mosquito larvae apparently survived a
ship journey in water collected in old tires (Craven et al., 1988; Monath,
1993). Soon after its introduction, A. albopictus was found to be carrying
another potentially dangerous virus, that of La Crosse encephalitis (Francy
et al., 1990; Henig, 1995). The usual vector of this disease is a woodland
mosquito that relatively rarely bites human beings. George Craig of Notre
Dame, perhaps America's greatest authority on mosquitoes, considers the
combination of that virus and the aggressive tiger mosquito especially
worrying (Henig, 1995). Dengue has returned to Mexico just south of the
border of the United States (Rohter, 1995), from where the tiger mosquito
could move it north into areas in which its normal vector cannot survive
the cold winters.

Modern transportation systems certainly improve the epidemiological
environment by making it relatively easy to move food to the hungry and
medical personnel, drugs, and vaccines to the ill. But even here they are a
two-edged sword, because they are susceptible to disruption during
epidemics by fear and by the disease itself (Ehrlich and Ehrlich, 1970; p.
150). Truck drivers and pilots are generally loath to enter plague areas.

Population Distribution: Urbanization and Suburbanization

As nations develop, they are characterized by relatively larger urban
populations (Gizewski and Homer-Dixon, 1995). This can improve access to
health care, food, and clean water. For example, in urban areas of poor
nations, a minimum of 170 million people do not have access to clean
drinking water, but an estimated 855 million lack that access in rural
areas (World Bank, 1992). About 35 percent of the population of developing
nations (1.5 billion people) now live in cities, so this suggests that the
water-supply element in the epidemiological environment has been somewhat
improved by urbanization, even among the poor. Only some 15 percent of
urbanites in poor countries may suffer bad drinking water, while over a
quarter of the 3 billion who live in the countryside do. (These data may
overstate the quality of drinking water in many cities in developing
countries, however; much depends on such things as what is meant by "a
minimum of 170 million people" and interpretation of the statement that
"many of those who officially have access still drink polluted water";
World Bank, 1992, p. 47).

Urbanization does not have only positive effects on the epidemiological
environment, however (e.g., Morse, 1991). Cities above all bring large
numbers of people into intimate contact. In 1950 only New York, London, and
Shanghai had populations of over 10 million. By the start of the 21st
century, 23 cities will have surpassed that number, and more than half of
all human beings are projected to be city dwellers by 2010 (United Nations,
1987). This sudden concentration of humanity would greatly facilitate
disease transmission even if all urbanites were well fed and supplied with
clean water, adequate shelter, and access to health care. But that is
hardly the case, and it will be difficult to achieve given the tremendous
rate of growth in demand for such resources and services.

In poor countries, urban inhabitants very often lack clean water and
adequate sanitation. In Uganda, unskilled urban workers often spend 10
percent of their income on small quantities of poor-quality water (Bradley,
1993b). Yet even poor quality water can be important for use in washing to
restrict the direct fecal oral transmission of diseases (Bradley, 1993b).

A problem afflicting cities in rich and poor nations alike is the lack of
control of disease reservoirs (e.g., rodents) and vectors (e.g.,
mosquitoes). Rats, for example, are all too common in New York and other
cities in the United States. Urbanization has contributed to the great
spread of dengue fever (Anonymous, 1995c) by bringing large numbers of
people into close association with the household mosquito Aedes aegypti,
the vector of the causative virus (Monath, 1993). A. aegypti breeds in
water standing in containers, and everything from coke bottles to old tires
that can hold small pools help support it in third-world slums.

The anonymity associated with large-scale movement and urbanization is
associated with behavior that tends to be suppressed in small communities.
In both rich and poor nations, urban conditions may promote drug use,
prostitution, and greater sexual promiscuity in general, especially among
homosexual men (Symons, 1978, although time-series data on this point are
lacking). Interestingly, for diseases transmitted sexually or through the
sharing of needles, lack of acquired immunity in recovered hosts permits
persistence in low-density populations. In such cases, a principal
criterion for persistence is a threshold average number of partners, rather
than a general threshold host density (Anderson and May 1991; Thrall et
al., 1993).


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