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Dissemination of Antibiotic-Resistant Bacteria
across Geographic Borders
Iruka N. Okeke1,2,a and Robert Edelman2,3
1
Department of Microbiology and Immunology, 2Center for Vaccine Development, and 3Department of Medicine, University of Maryland School of Medicine, Baltimore
The development of antibiotic-resistant (AR) bacteria in any country is of global importance. After their initial selection and
local dissemination, AR bacteria can be transferred across international borders by human travelers, animal and insect vectors,
agricultural products, and surface water. The sources and routes of importation of strains of AR bacteria are most often
unknown or undetected, because many bacteria carrying resistance genes do not cause disease, and routine surveillance often
does not detect them. Control of international dissemination of AR bacteria depends on methods to reduce selection pressure
for the development of such bacteria and improved surveillance to detect their subsequent spread.
The risk of transmission of antibioticresistant (AR) bacteria from one country
to another grows as the “global village”
shrinks. Strains can be imported into a
country and disseminated before their
presence is recognized, and countries
vary in their capacity to detect and deal
with resistant bacteria once introduced.
For these reasons, the emergence of an
AR bacterial strain in one location becomes a global problem. In recent Scandinavian studies, greater genetic relatedness existed between Enterococcus faecium
and Salmonella enterica isolated from humans in different countries than between
strains isolated from humans and animals
in the same country [1, 2]. These findings
Received 5 October 2000; revised 27 December 2000;
electronically published 5 July 2001.
a
Present affiliation: Department of Biomedical Sciences,
University of Bradford, Bradford, West Yorkshire, United
Kingdom.
Reprints or correspondence: Dr. Robert Edelman, Center
for Vaccine Development, University of Maryland School of
Medicine, 685 W. Baltimore St., Baltimore, MD 21201
([email protected]).
Clinical Infectious Diseases 2001; 33:364–9
2001 by the Infectious Diseases Society of America. All
rights reserved.
1058-4838/2001/3303-0015$03.00
suggest that the transmission of some AR
bacteria across borders may be even more
important than the spread of AR resistant
bacteria within countries.
An example of the international dissemination of clinically important AR
bacteria is the introduction and spread
of African and Asian penicillinase-producing Neisseria gonorrhoeae (PPNG) in
Great Britain in the 1970s. Before then,
PPNG was virtually unknown in Britain,
and treatment of gonorrhea was usually
carried out empirically with penicillin. In
the subsequent decade, PPNG became
endemic in Britain, and penicillin could
no longer be used empirically [3]. More
recently, Smith et al. [4] have shown that
the majority of cases of infection due to
quinolone-resistant Campylobacter in
Minnesota in 1996–1997 were associated
with international travel.
Other clinically important bacterial species that combine the dual risk of emerging antibiotic resistance and international
transmission include staphylococci, Streptococcus pneumoniae, Mycobacterium tuberculosis, and both pathogenic and commensal enteric bacteria (reviewed in [5–
364 • CID 2001:33 (1 August) • Okeke and Edelman
8]). The transmission of nonpathogenic
AR bacteria is also important because
they can serve as reservoirs of resistance
genes that may be transferred to pathogens. The magnitude of the problem is
summarized by the World Health Organization: “antimicrobial resistance is a
global problem, affecting developed and
developing countries, and rapidly spreading between continents through international travel” [9]. In this article, we
provide a review of and perspective on
this expanding public health problem.
SELECTION OF AR BACTERIA
IN INDUSTRIALIZED
COUNTRIES
In many industrialized countries, overprescription of antibiotics [10, 11] and
the increasingly popular use of disinfectants for routine hygiene have been
shown to contribute to the selection pressure for AR bacteria [12, 13]. Perhaps
even greater pressure is exerted by the
use of approximately 50% of the antibiotics produced in developed countries
for veterinary medication or growth pro-
motion in animal husbandry. Large-scale
farming practices such as the inclusion
of poultry waste in cattle fodder may provide conditions suitable for the exchange
of AR organisms by livestock and consequently increase the chance that these
organisms will be transmitted to humans
[14, 15]. In hospitals, day-care centers,
and nursing homes, AR bacteria are efficiently transmitted to inmates and their
contacts, increasing local prevalence and
the possibility that AR organisms will be
exported [16–18].
TRANSMISSION OF NEWLY
SELECTED AR BACTERIA
FROM DEVELOPED TO
DEVELOPING COUNTRIES
All of the antibiotics in clinical use today
have been developed in industrialized
countries. With rising costs of drug development, newer, patent-protected drugs
are expensive and are used sparingly, if at
all, in developing countries. However, AR
organisms tend to spread rapidly in tropical developing countries, once introduced
[19, 20]. As a result, AR bacterial strains
selected in the developed world theoretically could be introduced into the developing world before the drug to which they
are AR is available.
DEVELOPING COUNTRIES
AS RESERVOIRS OF AR
BACTERIA
For many bacterial genera, the problem
of antibiotic resistance is more pronounced in developing countries, where
several factors select for antibiotic resistance genes and encourage dissemination of AR strains (reviewed in [19, 21,
22]). Antibiotic pressure is enhanced by
the use of subtherapeutic doses of antimicrobial agents, that are often of substandard quality. Poor infection control
practices and sanitation allow AR organisms to be spread from person to person,
magnifying the effect of their selection or
importation. Infections are also likely to
be improperly treated or untreated in developing countries, making it likely that
AR organisms, when present, will spread.
The warm and humid tropical climate is
conducive to propagation of bacteria
[23]. This, combined with the low level
of sanitation in many developing countries, particularly in urban slums, provides an efficient means for the dissemination of these strains throughout the
community, and thus increases the likelihood that they will be exported [19].
POTENTIAL ROUTES
OF IMPORTATION
International Travel by Humans
Short-term travelers. Because travel is
quicker, more convenient, and cheaper
than ever, the number of persons crossing
borders has increased remarkably [24].
This provides greater opportunity for
both pathogenic and nonpathogenic varieties of AR bacteria to be carried further
distances and less chance that these bacteria will be detected before they are implanted in another country [24]. In addition, the high population densities in
most port cities make it likely that AR
bacteria will spread rapidly once introduced [25].
The importance of travel in the dissemination of AR bacteria is demonstrated by the study of Murray et al. [26],
who showed that visitors to Mexico acquired AR flora without ingesting antibiotics and returned with these organisms to the United States. Similarly,
Cobelens et al. [27] showed that the risk
of infection with M. tuberculosis, which
may be drug-resistant, was high among
long-term travelers to areas of endemicity.
Immigrants and other long-term travelers. Kenyon et al. [28] recently observed a correlation between the increase
in pediatric tuberculosis patients and immigration from countries of endemicity
into California. Most of the source cases,
mainly parents of the children, were foreign-born, and 92% of cases were linked
to a country where tuberculosis is en-
demic [28]. Other categories of travelers
who are important as vehicles for the importation of AR organisms include refugees and relief workers [29, 30], as well
as patients referred internationally for
specialized health care [31].
Transmission aboard airplanes and
ships. Transmission of pathogenic and
AR microbes aboard airplanes can occur,
as demonstrated by aerosol infection of
multiply-resistant M. tuberculosis during
long-distance air travel [32, 33]. Even
though modern jet planes have air-purification systems superior to those found
in most buildings, risk factors such as
close proximity to highly infectious cases
and long-distance travel appear to increase the chance of person-to-person
transmission of M. tuberculosis [33, 34].
Foodborne bacteria, including Shigella
sonnei and Vibrio cholerae, have been
transmitted by contaminated meals served
during international flights or aboard
cruise ships [34–37].
Importation with Livestock
or Agricultural Products
In Europe, the glycopeptide avoparcin,
used in animal feeds, has provided selection pressure for vancomycin-resistant
enterococci [15, 38]. Although avoparcin
is not used in animal husbandry in the
United States [39] or developing countries, the potential exists for importation
of AR European strains with livestock or
animal fodder [40].
AR commensal gastrointestinal flora is
likely acquired from contaminated food.
Up to 70% of fruits and vegetables eaten
in the United States are imported from
tropical countries, and many are consumed uncooked [41]. Food from developing countries is often contaminated
with AR bacteria [42, 43]. Iceberg lettuce
imported from Spain was responsible for
outbreaks of AR S. sonnei dysentery in
different parts of Europe [44]. Similar
outbreaks occurred recently in the United
States and Canada, with parsley from
Mexico being strongly implicated [45].
Dissemination of Resistant Bacteria • CID 2001:33 (1 August) • 365
Table 1.
International transmission of antibiotic-resistant bacteria.
Reference(s)
Resistant organism
Antibiotic resistance
Route of importation
Likely mode of importation
[57]
Escherichia coli
b-Lactams, mediated by plasmidborne SHV-5 b-lactamase gene
Indian subcontinent to United
Kingdom
Human travel
[58, 59]
Salmonella typhi
Multiple antibiotics
Developing countries (mainly South
Asia) to United States and Canada
Human travel
[31]
MRSA
Multiple antibiotics
Great Britain to The Netherlands
Human travel (health workers)
[60]
MRSA
Multiple antibiotics
Brazil to Portugal
Unknown
[45]
Shigella sonnei
Ampicillin, TMP-SMX, streptomycin
Mexico to United States
Imported food (parsley)
[4]
Campylobacter jejuni
Quinolones
[61]
Streptococcus pneumoniae 6B Multiple antibiotics
NOTE.
Europe and Asia to United States
Human travel
Spain to Iceland
Unknown
MRSA, methicillin-resistant Staphylococcus aureus; SHV-5, sulphydryl variable-5; TMP-SMX, trimethoprim-sulfamethoxazole.
Wildlife and Animal Pests
Wildlife provides a reservoir for potential
transfer of AR bacteria across international borders. In a recent report, resistance among enteric bacteria from bank
voles and wood mice—which presumably
had no direct contact with antibiotics, humans, or antibiotic-exposed animals—was
shown to be highly prevalent [46]. Souza
et al. [47] also demonstrated that isolates
of Escherichia coli from a wide variety of
wild mammals were resistant to antibiotics, and Kadavy et al. [48] found multiply resistant Providencia species colonizing natural oil fly larvae. These data
demonstrate the abundance of multiply
resistant bacteria in the wild. Just as important, transfer across borders was demonstrated by migrating birds in Sweden
that were found to carry enteric organisms resistant to multiple antibiotics
[49]. Pet birds imported from tropical
countries can also carry AR organisms,
because they are frequently treated with
antibiotics [50]. Insect and rodent pests
have the capacity to act as vehicles for
AR organisms as well [51]. The public
health importance of such transfers depends on the frequency of contact between imported wildlife or pests and resident humans, livestock, or food.
Surface Water
Several studies have been conducted to
identify environmental reservoirs of AR
bacteria. In areas where such organisms
exist in high densities, they may find their
way into bodies of water via sewage runoff [52]. Sternes [53] identified vancomycin-resistant enterococci in the water
of the Rio Grande, which runs along the
border of the state of Texas. They speculated that Mexico was a possible source
of the organisms because of the easy
availability of antibiotics in that country.
Further evidence of the role of flowing
water in the dissemination of AR bacteria
is provided by the observation that environmental organisms isolated downstream of wastewater discharge into the
Arga River in Spain were more likely to
carry resistance genes than those isolated
from upstream areas [54].
SURVEILLANCE
OF IMPORTATION OF AR
BACTERIA
In some instances, dissemination of AR
organisms between countries has been inferred from the isolation in both countries
of identical AR clones or promiscuous
genetic material encoding antibiotic resistance. For example, genetic evidence
suggests that the global dissemination of
methicillin resistance in staphylococci
began with the distribution of very few
AR clones [6]. Another example is the
spread of a plasmid carrying a gentamicin-resistance gene among enteric bacteria isolated in Venezuela and the United
States [55].
366 • CID 2001:33 (1 August) • Okeke and Edelman
Clinical or epidemiological evidence
can also be used to infer transfer of AR
organisms between countries. For example, AR pathogens endemic in many
developing countries have been recovered from recent returnees in the United
States and Europe who were presumed
to be infected during their visits abroad
(table 1) [3, 36, 56]. When strains causing
infections show unusual antibiotic resistance patterns, they may have been imported from countries where such resistance is commonplace [57].
The reports listed in table 1 undoubtedly describe a small fraction of the actual
number and variety of clinically significant
importations of AR organisms that have
occurred and do occur internationally.
Confirmatory evidence of the transfer of
antibiotic resistance is difficult to obtain.
First, because surveillance of antibiotic resistance by clinical laboratories in many
countries is poor or lacking altogether, it
is often impossible to prove that crosstransfer has occurred [62]. In some countries, because susceptibility testing is rarely
conducted or documented, local resistance
patterns are not known, and imported AR
strains pass undetected. Second, even
when more sophisticated molecular tests
are available, the detection of identical resistance genes in strains from different
countries may be insufficient to infer
cross-transfer. Similar or identical genes
may appear in different geographic locations as a result of separate evolutionary
events [63]. Finally, tracking important
strains may be difficult, because bacterial
strains are constantly evolving during dissemination [2].
Initial detection of antibiotic resistance
is conventionally carried out by antibiotic
susceptibility tests of cultured organisms.
The inherent difficulty in cultivating some
species and bacterial variants (such as
small-colony variants of staphylococci
[64] and viable but nonculturable bacteria
[65, 66]) makes both detection and antibiotic susceptibility testing difficult. Genotypic identification of such organisms is
not yet used routinely in most clinical laboratories [57, 67]. Even when bacteria can
be cultivated, isolates from developing
countries are often unavailable for analysis. Few developing countries have operational surveillance systems, and many
do not have functional clinical microbiology laboratories [68, 69].
include indiscriminate use or overuse of
antibiotics, high population density, environmental reservoirs, inadequate surveillance, and poor infection control.
The technology exists for screening
every person, animal, or food item entering a country for bacteria resistant to antibiotics of clinical importance [69, 72].
Such screening, however, would be expensive, impractical, and unpopular
among exporters and tourists [33]. There
are also the difficult questions of whether
to screen before or after travel and what
to do when someone “fails” the screening
test. A far more practicable approach
would be to provide support for (1) the
global control of antimicrobial resistance
(including reducing selection pressure and
improving infection control and hygiene),
(2) vaccination, (3) good surveillance, (4)
and efficient travelers’ education [41, 73,
74].
WHAT WE CAN LEARN
FROM THE NOSOCOMIAL
SPREAD OF AR BACTERIA?
ACKNOWLEDGMENT
14.
Dr. Okeke thanks Dr. James Kaper for
mentorship and support.
15.
Although the organisms causing AR hospital-acquired and community-acquired
infections often differ, much can be
learned from the dissemination of nosocomial AR bacteria, particularly as the
organisms spread within and between
different institutions [70]. Factors that
have been instrumental in the nosocomial spread of AR bacteria are antimicrobial pressure, inadequate detection and
reporting by clinical laboratories, asymptomatic carriage, environmental reservoirs, intrahospital and interhospital
transfer of colonized persons, inadequate
infection-control precautions, and inadequate compliance with hand washing
and barrier precautions [71].
As in hospitals, the selection pressure
in countries varies. The countries with
higher prevalences of AR bacteria tend to
have features similar to hospitals at risk of
acquiring AR organisms. These features
6.
7.
8.
9.
10.
11.
12.
13.
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