Emerging Infectious Diseases Volume 16 Issue 1

2010·4.2 MB·English

by  CDC

Peer-Reviewed Journal Tracking and Analyzing Disease Trends pages 1–182
EDITOR-IN-CHIEF
D. Peter Drotman
Managing Senior Editor EDITORIAL BOARD
Polyxeni Potter, Atlanta, Georgia, USA
Dennis Alexander, Addlestone Surrey, United Kingdom
Senior Associate Editor Barry J. Beaty, Ft. Collins, Colorado, USA
Brian W.J. Mahy, Atlanta, Georgia, USA Martin J. Blaser, New York, New York, USA
Christopher Braden, Atlanta, GA, USA
Associate Editors
Carolyn Bridges, Atlanta, GA, USA
Paul Arguin, Atlanta, Georgia, USA
Arturo Casadevall, New York, New York, USA
Charles Ben Beard, Ft. Collins, Colorado, USA
Kenneth C. Castro, Atlanta, Georgia, USA
David Bell, Atlanta, Georgia, USA
Thomas Cleary, Houston, Texas, USA
Charles H. Calisher, Ft. Collins, Colorado, USA
Anne DeGroot, Providence, Rhode Island, USA
Michel Drancourt, Marseille, France
Vincent Deubel, Shanghai, China
Paul V. Effl er, Perth, Australia
Ed Eitzen, Washington, DC, USA
David Freedman, Birmingham, AL, USA
Kathleen Gensheimer, Cambridge, MA, USA
K. Mills McNeill, Kampala, Uganda
Peter Gerner-Smidt, Atlanta, GA, USA
Nina Marano, Atlanta, Georgia, USA
Duane J. Gubler, Singapore
Martin I. Meltzer, Atlanta, Georgia, USA
Richard L. Guerrant, Charlottesville, Virginia, USA
David Morens, Bethesda, Maryland, USA
Scott Halstead, Arlington, Virginia, USA
J. Glenn Morris, Gainesville, Florida, USA
David L. Heymann, London, UK
Patrice Nordmann, Paris, France
Charles King, Cleveland, Ohio, USA
Tanja Popovic, Atlanta, Georgia, USA
Keith Klugman, Atlanta, Georgia, USA
Jocelyn A. Rankin, Atlanta, Georgia, USA
Takeshi Kurata, Tokyo, Japan
Didier Raoult, Marseille, France
S.K. Lam, Kuala Lumpur, Malaysia
Pierre Rollin, Atlanta, Georgia, USA
Bruce R. Levin, Atlanta, Georgia, USA
Dixie E. Snider, Atlanta, Georgia, USA
Myron Levine, Baltimore, Maryland, USA
Frank Sorvillo, Los Angeles, California, USA
Stuart Levy, Boston, Massachusetts, USA
David Walker, Galveston, Texas, USA
John S. MacKenzie, Perth, Australia
David Warnock, Atlanta, Georgia, USA
Marian McDonald, Atlanta, Georgia, USA
J. Todd Weber, Atlanta, Georgia, USA
John E. McGowan, Jr., Atlanta, Georgia, USA
Henrik C. Wegener, Copenhagen, Denmark
Tom Marrie, Edmonton, Alberta, Canada
Founding Editor Philip P. Mortimer, London, United Kingdom
Joseph E. McDade, Rome, Georgia, USA Fred A. Murphy, Galveston, Texas, USA
Barbara E. Murray, Houston, Texas, USA
Copy Editors
P. Keith Murray, Geelong, Australia
Claudia Chesley, Karen Foster, Thomas Gryczan, Nancy Mannikko,
Stephen M. Ostroff, Harrisburg, Pennsylvania, USA
Beverly Merritt, Carol Snarey, P. Lynne Stockton
David H. Persing, Seattle, Washington, USA
Production Richard Platt, Boston, Massachusetts, USA
Carrie Huntington, Ann Jordan, Carole Liston, Shannon O’Connor, Gabriel Rabinovich, Buenos Aires, Argentina
Reginald Tucker Mario Raviglione, Geneva, Switzerland
Leslie Real, Atlanta, Georgia, USA
Editorial Assistant
David Relman, Palo Alto, California, USA
Susanne Justice
Ronald M. Rosenberg, Fort Collins, Colorado, USA
www.cdc.gov/eid
Connie Schmaljohn, Frederick, Maryland, USA
Emerging Infectious Diseases Tom Schwan, Hamilton, Montana, USA
Emerging Infectious Diseases is published monthly by the Centers for Disease Ira Schwartz, Valhalla, New York, USA
Control and Prevention, 1600 Clifton Road, Mailstop D61, Atlanta, GA 30333, Tom Shinnick, Atlanta, Georgia, USA
USA. Telephone [phone], fax [phone], email [email protected]. Bonnie Smoak, Bethesda, Maryland, USA
The opinions expressed by authors contributing to this journal do not necessar- Rosemary Soave, New York, New York, USA
ily refl ect the opinions of the Centers for Disease Control and Prevention or the P. Frederick Sparling, Chapel Hill, North Carolina, USA
institutions with which the authors are affi liated. Robert Swanepoel, Johannesburg, South Africa
All material published in Emerging Infectious Diseases is in the public domain Phillip Tarr, St. Louis, Missouri, USA
and may be used and reprinted without special permission; proper citation, how- Timothy Tucker, Cape Town, South Africa
ever, is required. Elaine Tuomanen, Memphis, Tennessee, USA
Use of trade names is for identifi cation only and does not imply endorsement John Ward, Atlanta, Georgia, USA
by the Public Health Service or by the U.S. Department of Health and Human Mary E. Wilson, Cambridge, Massachusetts, USA
Services.
∞ Emerging Infectious Diseases is printed on acid-free paper that meets the requirements of
ANSI/NISO 239.48-1992 (Permanence of Paper)
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010
January 2010
On the Cover Dissemination of the bla Carbapenemase
OXA-23
Pieter Claesz (1597–1660) Gene of Acinetobacter baumannii ...................35
Still Life with Turkey Pie (1627) P.D. Mugnier et al.
Oil on wood panel
Controlling the spread of this gene will be diffi cult.
(75 cm × 132 cm)
Rijksmuseum, Amsterdam, the
Netherlands Recombinant Canine Coronaviruses
in Dogs, Europe .................................................41
N. Decaro et al.
About the Cover p. 178
Subtype IIb originates from recombination with porcine
transmissible gastroenteritis virus.
Synopses
Ceftiofur Resistance in Salmonella enterica
Serovar Heidelberg, Canada.............................48
CME ACTIVITY L. Dutil et al.
Public Health Threat of New, Use of this drug in chickens may limit effectiveness of
Reemerging, and Neglected Zoonoses cephalosporins in treating human infections.
in the Industrialized World ..................................1
Healthcare-associated Viral
S.J. Cutler et al.
Gastroenteritis among Children,
Improving our capacity to respond to these pathogens is
essential. United Kingdom .................................................55
N.A. Cunliffe et al.
Laboratory Surge Response to Pandemic Enteric viruses introduced from the community are major
(H1N1) 2009 Outbreak, New York City p. 16 causes.
Metropolitan Area, USA .......................................8
Meningitis Caused by Echovirus
J.M. Crawford et al.
Type 4, Australia ................................................63
Emergency preparedness programs are critical.
P.G. Markey et al.
Projecting Global Occurrence of A strain that emerged in July 2007 caused laboratory-
confi rmed meningitis.
Cryptococcus gattii ...........................................14
D.J. Springer and V. Chaturvedi
Methicillin-Resistant and -Susceptible
This pathogen likely has wider distribution than is
Staphylococcus aureus Infections
currently recognized.
in Dogs ...............................................................69
Research M.C. Faires et al.
Risk factors for MRSA were intravenous catheterization
Travel-associated Pandemic (H1N1) 2009 and receipt of certain antimicrobial drugs.
Infection in 116 Patients, Singapore ................21 300 p. 29
P. Mukherjee et al. 250 Actinobaculum schaalii, a Common
During the pandemic containment phase, regions of Uropathogen in Elderly Patients,
exposure for imported infections changed rapidly. 200 Denmark .............................................................76
S. Bank et al.
150
Severe Pneumonia and Pandemic This organism is identifi ed more often by PCR than by
(H1N1) 2009, San Luis Potosí, Mexico .............27 100 cultivation.
A. Gómez-Gómez et al.
50
Severe pneumonia developed in young adults without Norovirus Gastroenteritis Outbreak
identifi able risk factors. 0 with a Secretor-independent
Week 4 8 12 16 20 24
2008 Susceptibility Pattern, Sweden ........................81
J. Nordgren et al.
Nonsecretors were highly susceptible to norovirus GI.3 in
a foodborne outbreak.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010
Food Reservoir for Escherichia coli
Causing Urinary Tract Infections .....................88
C. Vincent et al. January 2010
Foodborne transmission of extratraintestinal E. coli is
Another Dimension
common.
174 Some Haphazard Aphorisms for Epidemiology
Dispatches
and Life
J.M. Cowden
96 Serologic Cross-Reactivity with Pandemic
p. 93
(H1N1) 2009 Virus in Pigs, Europe
Letters
C.S. Kyriakis et al.
100 Hospitalizations for Pandemic (H1N1) 2009
149 Fatal Pneumonia and Pandemic (H1N1) 2009 in
among Maori and Pacifi c Islanders, New
HIV-Positive Patient
Zealand
A. Verrall et al. 150 Human Herpesvirus 8 in Healthy Blood
Donors, Argentina
103 Pandemic (H1N1) 2009 Surveillance and
Prevalence of Seasonal Infl uenza, Singapore 152 Real-Time PCR for Diagnosis of
Y.-S. Leo et al. Oculoglandular Tularemia
106 Reemergence of Syphilis in Martinique, 154 Increase in Serotype 6C Pneumococcal
2001–2008 Carriage, UK
A. Cabié et al. 155 Oseltamivir- and Amantadine-Resistant
110 Seagulls and Beaches as Reservoirs for Infl uenza Virus A (H1N1)
Multidrug-Resistant Escherichia coli 156 Pandemic (H1N1) 2009 Reinfection, Chile
R.R. Simões et al.
157 Skin Lesion Caused by ST398 and ST1 MRSA,
113 Serogroup W135 Meningococci, Southeastern Spain
Florida, 2008–2009
159 Identifi cation of a Rotavirus G12 Strain,
T.J. Doyle et al.
Indonesia
116 Human Group A Streptococci Virulence Genes
161 Age-based Human Infl uenza A Virus (H5N1)
in Bovine Group C Streptococci
Infection Patterns, Egypt
M.G. Rato et al.
162 Imported Chikungunya Virus Infection
120 Perceptions and Reactions with Regard to
Pneumonic Plague 164 Bovine Spongiform Encephalopathy Prion
G.J. Rubin et al. in Pigs
123 Rapid Displacement of Dengue Virus Type 1 165 Parvovirus 4 in Blood Donors, France
by Type 4, Pacifi c Region, 2007–2009 166 Otomastoiditis Caused by Mycobacterium
D. Li et al. abscessus, the Netherlands
126 Hepatitis E Epidemic, Uganda 168 Diseases Tracked by Using Google Trends,
E.H. Teshale et al. Spain
130 Novel Human Parechovirus, Sri Lanka 169 Astrovirus MLB1 in Stool Samples from
N.T.K. Pham et al. Children (response)
133 Broiler Chickens and Fluoroquinolone- 170 Optimal Therapy for Multidrug-Resistant
Resistant Escherichia coli, Iceland Acinetobacter baumannii (response)
T.R. Thorsteinsdottir et al.
136 Human Listeriosis Caused by Listeria ivanovii Book Reviews
C. Guillet et al.
139 Acute Encephalopathy Associated with 172 Case Studies in Infectious Disease
Infl uenza A Infection in Adults
p. 113 172 Infectious Disease: Pathogenesis, Prevention
N. Lee et al.
and Case Studies
143 Enterotoxigenic Escherichia coli in Guatemala
and Mexico About the Cover
M. Nicklasson et al.
178 Tasty Bits a Dutch Treat
Commentary
Erratum
177 Vol. 15, No. 11
147 Laboratory Surge Capacity and Pandemic
Infl uenza
M.I. Meltzer et al.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010
Public Health Threat of New,
Reemerging, and Neglected
Zoonoses in the Industrialized World
Sally J. Cutler, Anthony R. Fooks, and Wim H.M. van der Poel
CME ACTIVITY
MedscapeCME is pleased to provide online continuing medical education (CME) for this journal article, allowing clinicians the opportunity
to earn CME credit. This activity has been planned and implemented in accordance with the Essential Areas and policies of the Accreditation
Council for Continuing Medical Education through the joint sponsorship of MedscapeCME and Emerging Infectious Diseases. MedscapeCME
is accredited by the Accreditation Council for Continuing Medical Education (ACCME) to provide continuing medical education for physicians.
MedscapeCME designates this educational activity for a maximum of 0.75 AMA PRA Category 1 Credits™. Physicians should only claim credit
commensurate with the extent of their participation in the activity. All other clinicians completing this activity will be issued a certifi cate of par-
ticipation. To participate in this journal CME activity: (1) review the learning objectives and author disclosures; (2) study the education content;
(3) take the post-test and/or complete the evaluation at http://www.medscape.com/cme/eid; (4) view/print certifi cate.
Learning Objectives
Upon completion of this activity, participants will be able to:
• List animal hosts for different zoonoses
• Identify the type of zoonosis most likely to undergo genetic mutation
• Specify factors that increase the risk for zoonoses now and in the future
• Describe the epidemiology and clinical presentation of rickettsial diseases
Editor
Thomas Gryczan, Technical Writer-Editor, Emerging Infectious Diseases. Disclosure: Thomas Gryczan has disclosed no relevant fi nancial
relationships.
CME Author
Charles P. Vega, MD, Associate Professor; Residency Director, Department of Family Medicine, University of California, Irvine, California,
USA. Disclosure: Charles P. Vega, MD, has disclosed no relevant fi nancial relationships.
Authors
Disclosures: Sally J. Cutler, PhD, has disclosed the following relevant fi nancial relationship: served as an advisor to the Institute of Biomedical
Sciences virology panel. Anthony R. Fooks, MBA, PhD, CBiol, FSB, has disclosed the following relevant fi nancial relationships: received
grants for educational activities from The Wellcome Trust, World Health Organization, University of Oxford Medical Research Fund, UK
Health Protection Agency, and UK Department for Environment, Food and Rural Affairs; served as an advisor or consultant for World Health
Organization, World Health Organization for Animal Health, UK Department for Environment, Food and Rural Affairs. Wim H.M. van der
Poel, PhD, DVM, has disclosed no relevant fi nancial relationships.
Microbiologic infections acquired from animals, known characteristics of the hosts. We discuss causal factors that
as zoonoses, pose a risk to public health. An estimated infl uence the dynamics associated with emergence or re-
60% of emerging human pathogens are zoonotic. Of these emergence of zoonoses, particularly in the industrialized
pathogens, >71% have wildlife origins. These pathogens world, and highlight selected examples to provide a com-
can switch hosts by acquiring new genetic combinations prehensive view of their range and diversity.
that have altered pathogenic potential or by changes in
behavior or socioeconomic, environmental, or ecologic
The World Health Organization/Food and Agriculture
Organization/World Organisation for Animal Health
Author affi liations: University of East London, London, UK (S.J. joint consultation on emerging zoonotic diseases, held in
Cutler); Veterinary Laboratories Agency, Addlestone, UK (A.R. Geneva in 2004, defi ned an emerging zoonosis as “a patho-
Fooks); University of Liverpool, Liverpool, UK (A. R. Fooks, W.H.M. gen that is newly recognized or newly evolved, or that has
van der Poel); and Central Veterinary Institute of Wageningen Uni- occurred previously but shows an increase in incidence or
versity and Research Centre, Lelystad, the Netherlands (W.H.M. expansion in geographical, host or vector range” (www.
van der Poel) who.int/zoonoses/emerging_zoonoses/en). Through con-
tinued alterations in human and animal demographics and
DOI: 10.3201/eid1601.081467
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010 1
SYNOPSIS
environmental changes, new and recurring diseases are must be considered on multiple levels. First, pathogens not
likely to continue to emerge. previously known have been identifi ed. For example, alter-
The effects of zoonoses on human health and econom- ation in the processing of cattle feed in the United Kingdom
ics have recently been underscored by notable outbreaks resulted in extended host range and emergence of bovine
such as those involving Nipah virus and severe acute respi- spongiform encephalopathy in cattle (6). Similarly, mixing
ratory syndrome (SARS) coronavirus (CoV). A recent ret- of multiple species under stressful conditions can promote
rospective study of 335 emerging infectious episodes over a species jump such as that witnessed with SARS-CoV
a 64-year period (1940–2004) emphasized the role of wild- (7). New opportunities can be created by climatic changes
life as a source of emerging infections. However, research such as global warming and ecologic alterations facilitated
efforts have typically been focused toward either humans through changed land use and movements of infected hosts,
or economically related species (1). susceptible animals, or disease vectors.
The frequency of these events increased substantially In 1987, 1997–1998, and 2006–2007, outbreaks of
over the period of investigation (2). Such infections are infection with Rift Valley fever virus in Africa were as-
now often perceived as agents of biologic warfare rather sociated with changes in river fl ow and fl ooding resulting
than infections with a long but insidious history in their from damming of rivers or heavy rainfall. Many zoonotic
appropriate ecologic niche. Why then are these infections pathogens fall into the category of generalist agents exhib-
becoming a serious public health concern? The answer is iting extensive host diversity, e.g., Coxiella burnetii, the
a complex multifactorial set of changing circumstances. etiologic agent of Q fever. This bacterium can successfully
To support the growing human population, we have an in- infect hosts ranging from domestic animals to wildlife, rep-
creasing demand for nutritional support, resulting in inten- tiles, fi sh, birds, and ticks.
sive agricultural practices, sometimes involving enormous Others agents have restricted specifi c transmission
numbers of animals, or multiple species farmed within the dynamics because of limited host ranges. These agents
same region. These practices can facilitate infection to include simian immunodefi ciency viruses 1 and 2, which
cross species barriers. are found in chimpanzees and sooty mangabees, and Rift
Additionally, we are witnessing increasing global- Valley virus, which is transmitted by Aedes spp. and Culex
ization, with persons (3), animals, and their products (4) spp. mosquitoes and found in sheep and goats. For many
moving around the world. This movement enables unprec- zoonotic agents, the potential to cause infection in acciden-
edented spread of infections at speeds that challenge the tal hosts, such as humans, exists, but often this represents
most stringent control mechanisms. Furthermore, continual a dead-end host. Pathogens such as Anaplasma spp., Erhli-
encroachment of humans into natural habitats by popula- chia spp., Rickettsia spp., Bartonella spp., West Nile virus,
tion expansion or tourism brings humans into new ecologic and rabies virus can be included in this group.
environments and provides opportunity for novel zoonotic From an epidemiologic point of view, “A reservoir
exposure. Climatic changes have facilitated the expansion should be defi ned as one or more epidemiologically con-
of compatible conditions for some disease vectors, remod- nected populations or environments in which a pathogen
eling dynamics for potentially new, emerging, and reemerg- can be permanently maintained and from which infection
ing zoonoses (5). In the next 2 decades, climate change will is transmitted to the defi ned target species” (8). Converse-
be the most serious issue that dominates reemergence of ly, some zoonoses in specifi c conditions show remark-
pathogens into new regions. able ability for human-to-human transmission beyond the
Climate change also effects evolution of pathogens, confi nes of natural sylvatic cycles. This ability was seen
and where relevant, their vectors. Continual mutation and during a recent outbreak of plague among diamond min-
recombination events give rise to variants with altered ers in the Congo. This outbreak was initiated by an infec-
levels of fi tness to persist and spread. Changing ecologic tion of a miner, which became pneumonic and resulted in
circumstances and pathogen diversity can give rise to vari- 136 secondary cases of pneumonic plague and 57 deaths
ants with altered pathogenic potential. However, the host (9). Transmission of plague is complex and dynamic, with
must not be ignored. Increased longevity and therapies for combinations of stochastic and adaptive mechanisms. As
persons with diseases can modulate host susceptibility and seen in this example, rapid transmission often occurs,
concomitant infections and upset the evolving and dynamic but this is accompanied by slower, localized transmis-
infection balance. sion among enzootic reservoir species, which often use
vector-borne expansion among low-density hosts (10).
Emerging, Reemerging, and Neglected Zoonoses Other zoonoses, given correct circumstances, can result
Data for this review were identifi ed in PubMed searches in human-to-human transmission. These zoonoses include
and relevant journal articles and excluded those studies not those that cause Ebola fever, infl uenza A, plague, tulare-
published in English. Emerging or reemerging pathogens mia, and SARS (11).
2 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010
Public Health Threat of Zoonoses
New or emerging virulence traits can evolve and re- for acquiring tularemia (caused by Francisella tularensis)
sult in large-scale transmission and concomitant alteration in disease-endemic areas where lagomorph reservoirs may
of pathogenicity. This new pathogenicity may include in- be killed by mowers or hedge trimmers (17).
creased invasiveness, enhanced spread, toxin production, or For some infections, zoonotic transmission occurs in-
antimicrobial drug resistance. Y. pestis has shown a resur- directly through food. Human brucellosis is not usually
gence in regions such as Madagascar, with isolates show- acquired through animal contact but is transmitted more
ing a marked increase in resistance to antimicrobial agents often by consumption of infected animal products such as
(12). Similarly, a recently evolved outer surface protein A unpasteurized dairy products (18). Salmonella spp. have
serotype of a Lyme borreliosis spirochete (Borrelia garinii repeatedly caused outbreaks of salmonellosis after per-
serotype 4), has shown particularly aggressive tendencies sons have eaten uncooked eggs (19). Hepatitis E virus has
and is often associated with hyperinvasive infection (13). been transmitted through consumption of uncooked deer
Concern has also been noted about increasingly frequent meat (20).
isolation of Corynebacterium ulcerans carrying the diph- Exposure routes may be airborne, as demonstrated for
theria toxigenic phage. several outbreaks of Q fever (21). An ongoing airborne Q
Mutation is the ultimate source of genetic variation, fever outbreak in the Netherlands related to goat farming
on which natural selection, genetic drift, gene fl ow, and has raised awareness of this previously neglected zoonosis
recombination act to shape the genetic structure of popu- (22). How humans were exposed to these animals would
lations. This factor is especially notable in viruses, which not have been apparent; the exposures were identifi ed by
have relatively small genomes and short generation times, epidemiologic mapping of the distribution of cases. These
particularly among viruses with more error-prone RNA ge- examples underscore the necessity of gathering compre-
nomic replication (14). However, most mutations are del- hensive patient data to effectively diagnose zoonoses.
eterious and under pressure of innate and adaptive host im-
munity, viruses probably always experience selection for Recreational Zoonoses
mutation rates >0. The upper limit on mutation rates will Sporting activities can expose humans to zoonotic in-
be determined by factors such as natural selection, genomic fections. Hunting wildlife has been associated with infec-
architecture, and the ability to avoid loss of viability or ge- tions such as brucellosis and tularemia (23). Less obvious
netic information, albeit, that a loss of genetic information routes arise from activities such as water sports. Leptospira
and increased specialization is observed in co-evolution spp.–infected animals excrete viable organisms in their
with a host (15). urine, which can persist in aquatic environments for pro-
According to evolutionary theory, higher mutation longed periods. After a triathlon event in 1998, a total of
rates should be favored in a changing environment, such as 52 of 474 athletes tested were diagnosed with leptospiro-
altered host immune defenses. However, in experimental sis (24). Suspicion of water sport–related infections with
settings, artifi cially increased mutation rates are often as- hepatitis A and Leptospira spp. led to closure of an area of
sociated with lower virus titers. In addition, a complex re- Bristol, United Kindom, where docks were used for recre-
lationship exists between underlying mutational dynamics ational water activities (25).
and the ability to generate antigenic variation, which in turn Horses are now moved from countries in Europe to
has serious implications for the epidemiologic potential of warmer regions (e.g., United Arab Emirates) to prolong
the virus. the racing season during the winter. Hunting activities have
Evolutionary changes are not always a prerequisite for promoted large-scale export of animals such as hares (pos-
viral emergence in a new host. Some viruses (e.g., poxvi- sible reservoirs of tularemia and brucellosis) from Poland
ruses), have a wide host range and show a relatively low and the movement of potentially rabies-infected raccoons
mutation rate. However, in other viruses such as Venezu- in the United States. In other countries such as the United
elan equine encephalitis virus, evolutionary change is es- Kingdom, pheasants are bred and released for shooting in
sential for effi cient infection and transmission to new hosts the fall and provide plentiful hosts for questing ticks and
(16). Because most viruses replicate poorly when trans- increasing their abundance. Importation of pheasants into
ferred to new hosts, greater variation is more likely to assist the United Kingdom from France was associated with in-
viral adaptation to its new host. troduction of a mild zoonotic infection (Newcastle virus
All too frequently, the diagnosis of zoonotic disease disease) in 2007 (26).
is delayed through lack of clinical suspicion or failure to
obtain adequate clinical histories. Some zoonotic infec- Role of Companion Animals
tions are unusual (e.g., scabies infection after handling of Companion animals have many forms of contact and
pet guinea pigs). Other infections may have a less obvious opportunities to transmit multiple zoonoses. The sexual
animal link. Mowing lawns is believed to be a risk factor stage of the life cycle of Toxoplasma spp. occurs in cats,
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010 3
SYNOPSIS
thus exposing humans to infection in situations in which pathogens than transporting, selling, and eating the butch-
hygienic measures have not been observed. Cats also ered meat (33).
serve as reservoir for Bartonella henselae, the etiologic Zoonotic pathogens from wildlife may infect humans
agent of cat-scratch fever (27). Cowpox virus can also be with little or no human-to-human transmission (e.g., avian
transmitted to humans by contact with cats (28). Animal infl uenza virus and Hendra virus). Alternatively, increased
bites can result in zoonotic infections, typifi ed by infec- travel or migration and increased between-person contacts
tion with Pasteurella multocida. Even in the absence of a have facilitated emergence of simian immunodefi ciency
bite, contact with animals (e.g., licking of wounds) can re- virus/HIV/AIDS in Africa. Increased exposure to wild-
sult in infection. More recently, attention has focused on caught animals and high mutation rates of many RNA vi-
transmission of Rickettsia felis into the human environ- ruses have increased their predominance among emerging
ment by cat fl eas (29). zoonoses transmitted from human to human; RNA viruses
Dogs are the most likely source when humans become from bush meat may therefore play a possible role in future
infected with rabies virus and are potential sources of Toxo- disease emergence.
cara spp. This emerging threat is becoming apparent with
importation of rescued dogs and global movement of dogs Globalization and Livestock Movement
with their owners, which has resulted in several cases of Large-scale movement of persons, livestock, food, or
leishmaniasis in the absence of sand fl y vectors. Dogs can goods is now commonplace and provides increasing op-
be a source of methicillin-resistant Staphylococcus aureus portunities for rapid spread of pathogens. Trichinellae in
and could play a role in zoonotic spread of genetic elements horsemeat have been transported across the Pacifi c Ocean
responsible for antimicrobial drug resistance (30). Contact and infected consumers in other parts of the world. Dis-
with dogs in Mediterranean regions has been implicated as carded tires provide new habitats for mosquitoes in addi-
a likely source of infection in recent cases of Mediterranean tion to their usual ecologic niches. The World Organisation
spotted fever reported in traveling humans (31). for Animal Health and the Food and Agriculture Organisa-
Cats and dogs can introduce plague or rabies into hu- tion implement strict control of animal movement. Trans-
man environments and have been associated with Q fever port of animals can result in mingling of different species
in humans and dermatophytosis (ringworm). Scavenger in crowded and stressful conditions. This mingling can
habits of these animals bring them into contact with many suppress immune responses to persistent infections and in-
zoonotic agents, and close living relationships with humans crease pathogen shedding. Under such circumstances, sus-
such as sharing meal plates or beds offer many opportuni- ceptible species can readily become infected (34).
ties for disease transmission.
Pet rats have recently been incriminated as the source Tourism
of Leptospira icterrohemoragiae infection in their owners. Tourism has exponentially increased in recent years.
Psittacine birds are an established risk factor for acquisi- This fi nding has resulted in increasing numbers of import-
tion of Chlamydophila psittaci. During recent years, the ed zoonoses, such as a variety of rickettsial spotted fevers,
market for exotic pets has greatly increased. This increase brucellosis, melioidosis, genotype I hepatitis E (35), tick-
has resulted in transmission of several unusual organisms, borne encephalitis (36), and schistosomiasis (37).A rapid
such as exotic Salmonella spp., which are often associated increase in cases of African tick bite fever has been associ-
with pet reptiles. Media attention was captured after an out- ated with travelers to sub-Saharan Africa and the eastern
break of monkeypox in America that affected >70 persons Caribbean. This disease, which is caused by R. africae, is
in 2003. After infected African rodents had been imported transmitted by a particularly aggressive Amblyomma sp.
for the pet trade, the infection spread into native North tick; >350 imported cases have been observed in recent
American black-tailed prairie dogs and was subsequently years (31). Infection sequalae, such as subacute neuropa-
disseminated among humans (32). thy, may be found long after travel when tick bite fever es-
chars have disappeared (37). An estimated >1 million inter-
Bush Meat national journeys are made each day, and a staggering 700
Zoonotic diseases associated with hunting and eating million tourists travel on an annual basis. Detailed travel
wildlife is of increasing global concern. Bush meat is con- histories of patients who show clinical signs and symptoms
sidered a delicacy by many and has resulted in its growth of disease are needed.
as a commercial enterprise. Tracking, capturing, handling,
butchering in the fi eld, and transporting of carcasses involve Changed Land Use and Urbanization
risks of cross-species transmission. Particularly high risks Deforestation and development of natural habitats have
are associated with hunting nonhuman primates. The act of been seen on a global scale to accommodate intensifi cation
butchering is a greater risk factor for acquiring bloodborne of agriculture and living areas for humans. As a result, eco-
4 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010
Public Health Threat of Zoonoses
logic habitats have been disrupted, reservoir abundance has risk for acquiring leptospirosis. Wilderness camping ac-
changed, and transmission dynamics have been altered. Re- tivities have been associated with hantavirus infection after
duced host abundance may force vectors to seek alternative inhalation of aerosolized urine excretions of rodents. Other
hosts, increasing opportunities for disease transmission, as sporting activities such as hunting have been associated
demonstrated by increases in human cases of Lyme borreli- with brucellosis and tularemia. Travel to other countries
osis, ehrlichiosis, spotted fevers, and anaplasmosis. Devel- opens a range of new potential zoonotic exposures through
opment of forests to provide rubber plantations in Malaysia direct contact or indirectly through fomites, food, or arthro-
has been correlated with increases in schistosomiasis (37). pod vectors. Increasingly exotic locations are being sought
Wildlife may modify feeding practices as a consequence with associated exotic zoonoses. Some tourists consume
of changing land use, bringing them closer to humans and local delicacies, such as aborted animal fetuses in Ecuador,
livestock. This modifi cation was suggested to have been which are a source of brucellosis (39).
instrumental in the Nipah virus outbreak that affected pigs
and humans in Malaysia in 1999. Nipah virus persists as Conclusions and Future Prospects
a serious problem in many rural areas of Bangladesh and Many zoonoses can be considered opportunistic infec-
India, where infected bats living near human dwellings, tions. Increasing demands for protein necessitate increased
urinate in date palm sap, which is later consumed raw by levels of farming. Food can provide a vehicle for spread of
humans (38). pathogens from animals to humans. Contact with animals
Human population growth has been associated with during farming, hunting, or by animal bites can increase
reshaping of population demographics. Increasing from 1 transmission of diseases (e.g., rabies and tularemia). Ar-
billion at the beginning of the 20th century to 6 billion by thropod vectors can transmit diseases on an immense scale
the end of the century, current predictions forecast a hu- to other hosts as in cases of West Nile fever and plague.
man population of ≈10 billion by 2050. This prediction is Changing patterns of farming, life style, and trans-
accompanied by a staggering increase in urbanization of portation infl uence the dynamics of pathogen ecology.
the population from 39% in urban environments in 1980 Pathogens are subjected to changes by many intrinsic and
to 46% in 1997 and a predicted 60% by 2030. This high- extrinsic factors. Mutation, recombination, selection, and
density clustering of the human population paves the way deliberate manipulation can result in new traits acquired by
for potential outbreaks on an immense scale (5). pathogens and result in potential epidemic consequences.
Reemergence of diseases through opportunistic host
Public Health Risks of Reemerging switching is likely to continue as a major source of human
and Neglected Zoonoses infectious disease. Strategies to improve public health have
Many areas are now experiencing a reemergence of focused on improved surveillance in regions of perceived
zoonotic pathogens, partly resulting from collapse of pub- high likelihood of disease (reemergence). These strategies
lic health programs during political upheavals. Often, these include improved detection of pathogens in reservoirs,
areas increasingly appeal to those seeking adventurous or early outbreak detection, broad-based research to identify
unusual holiday destinations. factors that favor reemergence, and effective control (i.e.,
Delay in development of clinical signs and often in- quarantine and improved hygiene) (40).
sidious onset can challenge appropriate diagnosis and pa- To recognize and combat zoonotic diseases, the epi-
tient management. Furthermore, movements of animals demiology of these infections must be understood. We
used for agricultural trade, sport, and as companions also need to identify pathogens, their vertebrate hosts, and their
offer opportunities for further dissemination of infections. methods of transmission. Identifi cation should include
Brucellosis-free countries have seen reintroductions asso- knowledge of spatiotemporal disease patterns and their
ciated with movement of infected livestock. Movement of changes over time. These features can be used to identi-
pets throughout Europe has been associated with an alarm- fy dynamic processes involved in pathogen transmission
ing increase in diseases such as leishmaniasis. Moreover, (Figure), which can be used to account for observed disease
pets can harbor ectoparasites such as ticks, fl eas, and lice. patterns and ultimately forecast spread and establishment
All of these parasites, especially ticks, are notorious vec- into new areas.
tors of multiple zoonotic agents. Armed with information on expected disease patterns,
We are at risk for airborne transmission of zoonoses we can address whether change has occurred beyond that
by many factors (e.g., from travel to farms, consumption of which would normally be expected. However, this analysis
food, and mowing the lawn, which as been associated with may not be suitably responsive to control new and emerg-
tularemia). Visiting petting farms or having family pets in- ing zoonoses. Improved detection may be achieved through
creases the likelihood of potential zoonotic infections, es- use of syndromic approaches rather than searching for spe-
pecially if pets are exotic. Water sports may increase the cifi c pathogens.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010 5
SYNOPSIS
Acknowledgments
Climate
We thank Eric Fevré for helpful comments during the draft-
change
influencing ing of this manuscript and MedVetNet for support.
Exotic arthropods Translocation
pets of infected A.R.F. is supported by the United Kingdom Department for
animals or
persons Environment, Food and Rural Affairs (Defra grant SEV3500).
Exotic foods
(bush meat) Dr Cutler is a reader in microbiology and infectious disease
Tourism
at the School of Health and Bioscience of the University of East
Infection of
humans or London. Her research interest is bacterial zoonoses, particularly Q
Companion animals fever, brucellosis, rickettsiosis, leptospirosis, and relapsing fever
animals
Changes in borreliosis.
land use
Alteration in
livestock Pathogen References
management adaptation to
practices Acquisition new host
of new species 1. Daszak P, Epstein JH, Kilpatrick AM, Aguirre AA, Karesh WB,
virulence Cunningham AA. Collaborative research approaches to the role of
traits wildlife in zoonotic disease emergence. Curr Top Microbiol Immu-
nol. 2007;315:463–75. DOI: 10.1007/978-3-540-70962-6_18
Figure. Factors infl uencing new and reemerging zoonoses. 2. Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and
re-emerging pathogens. Emerg Infect Dis. 2005;11:1842–7.
3. Colizza V, Barrat A, Barthélemy M, Vespignani A. The role of the
airline transportation network in the prediction and predictability of
global epidemics. Proc Natl Acad Sci U S A. 2006;103:2015–20.
Human disease surveillance must be associated with
DOI: 10.1073/pnas.0510525103
enhanced longitudinal veterinary surveillance in food-pro- 4. Fèvre EM, Bronsvoort BM, Hamilton KA, Cleaveland S. Animal
ducing animals and wildlife. Prompt detection and insti- movements and the spread of infectious diseases. Trends Microbiol.
2006;14:125–31. DOI: 10.1016/j.tim.2006.01.004
gation of control measures such as vaccination are pivotal
5. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman
to prevent disease spread. Novel molecular methods (e.g.,
JL, et al. Global trends in emerging infectious diseases. Nature.
DNA microarrays) offer unprecedented opportunities for 2008;451:990–4. DOI: 10.1038/nature06536
rapid detection. However, these methods require optimi- 6. Mahy BW, Brown CC. Emerging zoonoses: crossing the species bar-
rier. Rev Sci Tech. 2000;19:33–40.
zation and validation before they can be used in routine
7. Stavrinides J, Guttman DS. Mosaic evolution of the severe acute
microbiology laboratories. Cloned antigens or attenuated
respiratory syndrome coronavirus. J Virol. 2004;78:76–82. DOI:
vaccines can be rapidly modifi ed into appropriate antigenic 10.1128/JVI.78.1.76-82.2004
forms. However, for identifi cation of specifi c pathogens, 8. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying
reservoirs of infection: a conceptual and practical challenge. Emerg
more research will be needed to provide timely manage-
Infect Dis. 2002;8:1468–73.
ment of a new or emerging disease threat.
9. Outbreak news. Plague, Democratic Republic of The Congo. Wkly
Approaches for identifi cation of pathogen replication Epidemiol Rec. 2006;81:397–8.
in vectors are more likely to offer substantial benefi ts for 10. Girard JM, Wagner DM, Vogler AJ, Keys C, Allender CJ, Drickam-
er LC, et al. Differential plague-transmission dynamics determine
control of zoonoses. These methods are inappropriate for
Yersinia pestis population genetic structure on local, regional, and
human vaccines, which must adhere to stricter legislative
global scales. Proc Natl Acad Sci U S A. 2004;101:8408–13. DOI:
criteria. However, control of zoonotic infections in res- 10.1073/pnas.0401561101
ervoir hosts has a pronounced protective effect in human 11. Bengis RG, Leighton FA, Fischer JR, Artois M, Mörner T, Tate CM.
The role of wildlife in emerging and re-emerging zoonoses. Rev Sci
populations. Use and development of antiviral drugs are
Tech. 2004;23:497–511.
other useful possibilities, but these drugs are likely to be
12. Galimand M, Carniel E, Courvalin P. Resistance of Yersinia
too expensive for use in large disease outbreaks and emer- pestis to antimicrobial agents. Antimicrob Agents Chemother.
gence of drug resistance may result in concomitant loss of 2006;50:3233–6. DOI: 10.1128/AAC.00306-06
13. Michel H, Wilske B, Hettche G, Göttner G, Heimerl C, Reischl U, et
therapeutic options for these agents.
al. An ospA-polymerase chain reaction/restriction fragment length
We do not know which zoonosis will be the next seri-
polymorphism-based method for sensitive detection and reliable dif-
ous public health threat. However, as we increase efforts ferentiation of all European Borrelia burgdorferi sensu lato species
to improve the capacity to respond to this pathogen, we and OspA types. Med Microbiol Immunol. 2004;193:219–26. DOI:
10.1007/s00430-003-0196-8
will also increase the likelihood that we can effi ciently
14. Duffy S, Shackleton LA, Holmes EC. Rates of evolutionary change
and effectively respond to new, reemerging, or neglected
in viruses: patterns and determinants. Nat Rev Genet. 2008;9:267–
zoonoses in the future. 76. DOI: 10.1038/nrg2323
6 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 1, January 2010