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Epidemiologic Reviews
Copyright © 1996 by The Johns Hopkins University School of Hygiene and Public Health
All rights reserved
Vol. 18, No. 1
Printed in U.S.A.
Impact of Technology on the Emergence of Infectious Diseases
Robert F. Breiman
INTRODUCTION
Technologic advances during this century have led
to unparalleled improvements in comfort, productivity, and life span. There has also been negative impact
from technology as shown by increases in fatal and
nonfatal trauma (e.g., motor vehicle injuries), coronary
artery disease (promoted by more sedentary lifestyles),
and environmental degradation (resulting from a variety of factors including land use, motor vehicle exhaust, and refrigerants). Other events, like massive
urbanization (as a result of mechanization of farming
practices and industrialization), have had substantial
but less tangible negative effects. The burst of technologic advancements has also been accompanied by
new weapons of war with dramatic destructive impact.
In the field of medicine, changes in technology have
provided immeasurable benefits to society. Catastrophic and epidemic diseases have been prevented
and/or controlled by improvements in sanitation and
hygiene and by introduction and widespread use of
vaccines and antimicrobial and other drugs. Improvements in intensive care, surgical techniques, cancer
therapy, and therapy for a variety of chronic diseases
(like diabetes mellitus and heart disease) have led to
prolonged survival and better quality of life for millions of people. The impact of technology on the
practice of medicine is among the most salutary
changes that has occurred during the twentieth century.
While some of the most spectacular successes of
technology have been in the area of prevention and
treatment of infectious diseases, there have been negative effects (often indirect) as well. Societal changes
resulting from mass urbanization are clearly linked to
the age of technology. These events have led to the
widespread use of illicit intravenous drugs, which in
turn has contributed to the spread of serious bloodReceived for publication November 13, 1995, and accepted for
publication May 21, 1996.
From the Respiratory Diseases Epidemiology Section, MS-C09,
Childhood and Respiratory Diseases Branch, Division of Bacterial
and Mycotic Diseases, National Center for Infectious Diseases,
Centers for Disease Control and Prevention, 1600 Clifton Road,
Atlanta, GA 30333. (Reprint requests to Dr. Breiman at this address.)
borne pathogens like human immunodeficiency virus
and hepatitis viruses, and to increased incidence of
subacute bacterial endocarditis. The same changes
have led to increasing numbers of persons who, without permanent homes, are often squeezed into
crowded and unclean living spaces facilitating transmission of tuberculosis and diarrheal and respiratory
infections.
Accelerating technologic advancement is an ineluctable part of our balance of life, and, up to now at least,
the benefits appear to outweigh the negatives. The
focus of this presentation is to consider ways that
technology has had a direct effect on the potential for
causing epidemic infectious diseases and has contributed to the emergence of some diseases by providing
supportive environments for growth or dissemination
of microorganisms.
THE PARADIGM
Legionnaires' disease is a model infectious disease
for demonstrating the effects of technology, because a
variety of man-made devices have provided ideal settings for multiplication of the etiologic agent while
also providing effective means for disseminating the
organism to humans. The bacteria have probably existed for thousands of years, but human disease was
not recognized until 1976 and likely occurred rarely, if
at all, before the latter half of this century.
Legionellae live in water and are facultative intracellular bacteria—unable to grow outside of cells,
unless a complex set of nutritional needs are met in
laboratory growth media, a condition unlikely to be
achieved in nature (1). The evolution of legionellae in
natural aquatic environments over thousands of years
has depended upon the presence in water of amoebae
and protozoa that routinely ingest other ubiquitous
bacteria (like Pseudomonas species) as food (2-4).
Unlike a myriad of other aquatic organisms that are
destroyed by amoebae, legionellae have the capacity
to evade microbicidal processes and to "parasitize"
amoeba, meeting the bacterium's complex nutritional
requirements. The organism multiplies intracellularly
until the host amoeba, stuffed with legionellae, bursts
open, releasing dozens of newly formed legionellae
Impact of Technology
into the water (figure 1). The new organisms then look
to other amoebae to "trick" into ingesting them as
food; thus, legionellae might be thought of as "Trojan
horse" bacteria.
While evolution of the capacity to avoid intracellular destruction and to multiply intracellularly has ensured survival of the species, the bacteria are present
in extremely low numbers in most natural aquatic
settings (5, 6). The bacteria are thermophilic, amplifying their numbers only at temperatures between 2 5 42°C (7, 8). This water temperature range is unusual in
nature; however, this century has seen the invention
and widespread use of a number of devices that utilize
and maintain water within this range. Cooling towers
5
and evaporative condensers are heat rejection devices
used in the process of efficiently providing refrigeration of air for large buildings and for cooling water for
a variety of industrial processes, without the use of
chemical refrigerants. These devices generally have
sizable reservoirs, within which the water temperature
is maintained between 25-35°C for maximum efficiency.
Whirlpool spas also often maintain the water temperature within the ideal range. Recirculated water
within cooling towers and whirlpool spas contains
abundant organic and inorganic material and microorganisms, providing ideal environments for the multiplication of organisms and for evading biocidal com-
B
„*
^
FIGURE 1. Four phases of ingestion and multiplication of Legionella pneumophila serogroup 1 within the amoeba Echinamoeba exudans
by transmission electron microscopy. Photos courtesy Dr. Barry S. Fields.
Epidemiol Rev Vol. 18, No. 1, 1996
6
Breiman
pounds that may be added to the water. Plumbing
systems, particularly in large buildings, may deliver
warm or hot water within the ideal temperature range
for legionellae. Thus, amplification of legionellae can
occur within plumbing systems as well.
Cooling towers, evaporative condensers, whirlpools,
spas, and showers produce aerosols containing fine
droplets of water. Similar aerosols are produced by
other devices like ultrasonic or cool-mist humidifiers,
and respiratory therapy devices, that use potable water
from plumbing systems. If legionellae are present in
the water, these devices have the capacity to disseminate aerosols in which the bacteria are contained
within water droplets 1-5 JU, in diameter (9). Inhaled
droplets of this size can reach alveoli, where they are
usually retained (10, 11).
Technology creates the capacity for legionellae to
reach the lower respiratory tract—the evolution of the
organism in natural aquatic environments enables it to
cause disease. Having reached the alveoli, legionellae
are rapidly met by the front line of the human host
defense mechanism at this level, the alveolar macrophages (12). Like amoebae, human alveolar macrophages ingest microorganisms and have a wide range
of internal microbicidal mechanisms. Just as in aquatic
environments, legionellae are able to avoid a variety of
steps employed by alveolar macrophages for killing
bacteria, and as in amoebae, multiply actively within
the cells (12, 13). The cells eventually burst, spilling
out large numbers of bacteria capable of destroying
more host cells, producing additional toxic effects,
and, if other host defense responses are not produced
in a timely fashion, causing pneumonia and systemic
illness (Legionnaires' disease).
There are a variety of unanswered questions regarding the epidemiology of Legionnaires' disease; these
are key to developing effective strategies for its prevention. The incidence of disease appears to be relatively low (six persons per 100,000 adult population
per year) (14) despite widespread use of devices capable of transmitting disease. There are thousands of
cooling towers in use in the United States, with legionellae present in 30-50 percent at any one particular
time (15). While epidemics of Legionnaires' disease
have been linked unequivocally to cooling towers
(16-19), the attributable risk of these devices (and
other aerosol-producing devices associated with Legionnaires' disease) for transmitting disease is unknown; nonetheless, the proportion of cooling towers
that actually transmit disease appears to be exceedingly low. Reliably identifying factors promoting (and
predictive of) disease transmission is a critical part of
developing an effective and efficient public health
response to this disease.
Numerous other infectious diseases have either
newly emerged or have become more common as a
result of technology. The emergence of some infectious diseases has been particularly influenced by
changes having to do with municipal water systems,
housing, transportation, commerce, food and nutrition,
and with medical technology itself. Examples of the
impact of these events, by no means complete, are
highlighted in the sections below.
Municipal water systems
Municipal water systems provide potable water to
homes on a scale unimaginable before this century;
however, these same systems can be efficient conduits
for causing epidemics. Most water supplies in developed countries are effectively treated in municipal
water treatment facilities. In some circumstances, the
treatment may be ineffective because of faulty procedures or resistance of an organism to routine procedures. In large urban areas, distribution of contaminated water can adversely affect huge numbers of
people. An example of the potential magnitude of
impact occurred in Milwaukee, Wisconsin, in 1993,
when an estimated 400,000 residents experienced gastrointestinal symptoms, including chronic diarrhea attributed to Cryptosporidium oocysts. Over 4,000 people required hospitalization during that outbreak (20).
Before this outbreak, Cryptosporidium was believed to
cause human disease only among the immunosuppressed, children attending day-care centers, and animal workers. Subsequently, smaller outbreaks have
occurred in other cities. While their precise role in
transmitting cryptosporidiosis is currently the focus of
intense scientific study, municipal water systems may
be responsible for the emergence of what has become
a common gastrointestinal infection in many cities in
the United States.
In developing countries, large outbreaks of cholera
have been traced to municipal water systems (21). As
with some outbreaks of cryptosporidiosis in the United
States, cholera outbreaks have been traced to ineffective decontamination, as well as to introduction of the
organism resulting from ineffective sewage treatment.
While less is known about the epidemiology of
non-tuberculous mycobacteria, there is some evidence
that technology may have provided mechanisms for
transmission of some mycobacterial species in a manner similar to that for legionellae. Non-tuberculous
mycobacteria, like Mycobacterium avium complex,
cause illness in immunosuppressed persons. These
pathogens have become increasingly familiar to
health-care providers in the era of acquired immunodeficiency syndrome and with increasing numbers of
patients receiving long-term immunosuppressing therEpidemiol Rev Vol. 18, No. 1, 1996
Impact of Technology
apy. M. avium complex can be found in water (22, 23)
and may also be present in soil and in certain types of
food (24). A potentially symbiotic or parasitic relation
with amoebae (as with legionellae) has been hypothesized for these organisms. Studies evaluating transmission of M. avium complex in domestic settings are
ongoing, but there is some evidence that disease may
be linked to inhalation or ingestion of contaminated
water (25).
An epidemiologic study evaluating immunosuppressed patients with systemic infection due to another
non-tuberculous mycobacteria, Mycobacterium haemophilum, showed that patients with M. haemophilum
disease were more likely to have had recent plumbing
work and to have seen brown or rusty appearing water
in the home. M. haemophilum requires iron for
growth—it was hypothesized that changing water
pressures brought on by plumbing work caused "biofilm" (layers of slime on internal surfaces of pipes
containing diverse populations of microorganisms)
plaques containing the bacteria to disengage from the
inner surfaces of pipes. Immunosuppressed patients
were then exposed to the organism by inhaling aerosols into the respiratory tract or ingesting contaminated water (26). Microbiologic studies confirming
these findings have not been done.
Housing and transportation
Epidemics of respiratory infection can be facilitated
in settings that are overcrowded, particularly where
there is faulty or inadequate ventilation. Although they
are energy efficient, tightly sealed homes and buildings may provide appropriate settings for person-toperson transmission of respiratory pathogens (including Mycobacterium tuberculosis), viruses, and
bacteria (like Streptococcus pneumoniae (27)). Transmission of M. tuberculosis has been documented
aboard airplanes (28, 29). This is a particular problem
aboard airplanes that use predominantly recirculated
air. There is substantial sharing of air among passengers, especially on long flights. Because it brings
people together from around the globe, puts them in a
closed space for up to 12 hours, and then disperses
them to a variety of locations, air travel has markedly
increased the potential for rapid introduction and
spread of respiratory pathogens worldwide. Air travel
can also facilitate transmission of influenza virus (30,
31) and may heighten the potential for a new global
pandemic of this disease. Air travel may be particularly likely to play a role in the rapid spread of newly
emerging respiratory pathogens. Ensuring adequate
fresh-air exchanges for airplane ventilation is encouraged to diminish the risk of transmission of respiratory
pathogens.
Epidemiol Rev Vol. 18, No. 1, 1996
7
Vector-borne diseases may be expected to emerge
as a result of transporting insects to new environments.
In 1986, the Asian mosquito, Aedes albopictus, was
introduced into the United States in a shipment of
tires, and it has since adapted to a variety of settings,
establishing itself in over 20 states. The introduction
of this mosquito, with the capability of transmitting a
variety of encephalitides, may contribute to a change
in the epidemiology of these infectious diseases in
North America.
Food safety
The impact of technology on food production, distribution, and processing has also contributed to the
spread of infectious diseases. For example, in 1985 a
failure in the pasteurization of milk at one dairy plant
may have led to over 190,000 infections with Salmonella (32). In 1994, an epidemic of illness due to
Salmonella serotype enteritidis was confirmed in 80
persons (but may have affected several thousand people) following ingestion of a contaminated ice cream
product distributed nationally (33).
International trade has increased the potential for
global spread of food-borne pathogens. For example,
outbreaks of gastrointestinal illness caused by Salmonella species in the United States have been attributed
to contamination of cantaloupes with the organism as
a result of farming practices in Mexico and failure to
thoroughly clean the melons before cutting them (34,
35).
New methods for storing foods have also resulted in
the emergence of some food-borne pathogens. Outbreaks of botulism have resulted from changes in the
preparation of fermented food among Alaska Natives.
Traditional fermentation procedures involved placing
food in porous containers placed into holes dug into
the cool permafrost. However, practices among some
Alaska Natives changed with the availability of plastic
sealed bags and wraps. Containers were often placed
above ground or within sheds, where fermentation
would proceed at warmer temperatures in airtight environments, encouraging growth of Clostridium botulinum (36). Outbreaks of meningitis due to Listeria
monocytogenes, an organism that thrives in refrigerated environments, have resulted from contaminated
food products, particularly cheeses, vegetables, and
under cooked meats, processed or stored at cool temperatures for long periods (37).
Medical technology
While the successes of medical technology are undisputed, the emergence of some infectious diseases
has clearly been a side effect. Use of immunosuppress-
8
Breiman
ing drugs, like corticosteroids, cyclosporin, and azathioprine, has increased susceptibility of patients to a
variety of bacterial, fungal, viral, and parasitic infectious diseases, including Legionnaires' disease (38),
systemic cytomegalovirus infections (39), disseminated coccidioidomycosis (40), and mycobacterial infections (41). Surgical procedures, implantable devices (like intravenous catheters), and injections have
led to systemic or deep tissue infections with a host of
organisms like Staphylococcus epidermidis, Mycobacterium fortuitum/chelonae (42), and Malassezia (43),
that would rarely have found their way past epidermal
layers.
Antimicrobial drugs have had a tremendous role in
limiting the impact of devastating infectious disease.
Ironically, widespread use of these drugs (44), often
for conditions that do not respond to their use, has led
to the emergence of pathogens, like Enterococcus
(45), 5. pneumoniae (46, 47), and Staphylococcus aureus (48) with decreased susceptibility to many or all
available drugs. This has limited the effectiveness of
these drugs or, in some cases, rendered them ineffective.
Transfusion of blood or blood products has been
associated with a variety of diseases including acquired immunodeficiency syndrome, hepatitis, malaria, and trypanosomiasis. Blood storing practices
may have an impact on transmission of some pathogens. For example, Yersinia enterocolitica, which can
grow slowly in cold, iron-enriched environments (like
stored blood), has been noted in packed red blood cells
stored at 4°C for longer than 25 days, resulting in
blood transfusion-associated systemic infections (49).
SUMMARY
Not all new threats from microorganisms result
from changes within the microorganisms themselves.
Innovative, progressive changes introduced by humans can provide advantages to microbes which, in
turn, threaten the population. In most cases, advantages are provided unwittingly as a by-product of
technology, and can be corrected when the problem is
recognized. An end to progress is neither a practical
nor desirable solution. Alertness (i.e., surveillance) for
the emergence of new diseases and to changes in
disease patterns will continue to be critical to ensure
timely implementation of public health measures.
ACKNOWLEDGMENTS
Drs. Robert V. Tauxe, David Addiss, and Mitchell S.
Cohen provided particularly helpful suggestions.
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