A team of Virginia Tech researchers has discovered that
humans are passing antibiotic resistance to wildlife, especially in protected
areas where numbers of humans are limited.
In the case of banded mongoose in a Botswana study,
multidrug resistance among study social groups, or troops, was higher in the
protected area than in troops living in village areas.
The study also reveals that humans and mongoose appear to be
readily exchanging faecal microorganisms, increasing the potential for disease
"The research identifies the coupled nature of humans,
animals, and the natural environment across landscapes, even those designated
as protected," said Kathleen Alexander, an associate professor of wildlife
in Virginia Tech's College of Natural Resources and Environment. "With few
new antibiotics on the horizon, wide-scale antibiotic resistance in wildlife
across the environment presents a critical threat to human and animal health.
As humans and animals exchange microorganisms, the threat of emerging disease
How the research was
The National Science Foundation-funded research project
investigating how pathogens might move between humans and animals was published
today (April 24, 2013) by EcoHealth.
"Tracking Pathogen Transmission at the Human-Wildlife
Interface: Banded Mongoose and Escherichia coli" is co-authored by Risa
Pesapane of Portsmouth, Va., then a wildlife sciences master's student at
Virginia Tech; microbiologist Monica Ponder, an assistant professor of food
science and technology in Virginia Tech's College of Agriculture and Life
Sciences; and Alexander, who is the corresponding author.
Alexander and Ponder are both affiliated with Virginia
Tech's Fralin Life Science Institute.
Alexander, a veterinarian and researcher with the non-profit
Center for African Resources: Animals, Communities, and Land Use (CARACAL), has
been conducting a long-term ecological study of banded mongoose in the region.
The researchers collected faecal samples from three troops
of banded mongoose living in Botswana's Chobe National Park and three troops
living in villages outside the park.
"Banded mongoose forage in garbage resources and search
for insects in faecal waste, including human sources found in the
environment," said Alexander. "Mongoose contact with other wildlife
and humans, and broad occurrence across the landscape, makes this species an
ideal candidate for evaluating microbial exchange and the potential for
pathogens to be transmitted and emerge at the human-wildlife interface."
Overlap with humans
With the exception of one mongoose troop, all study animals
had some level of their range overlap with human populations. Two of the study
troops had home ranges that included ecotourism facilities in the protected
area, with some contact with humans and development "but at a much lower
level than in the village troops," the article reported.
Fecal samples were collected from these mongoose troops
living in a protected area and in surrounding villages. Human feces were
collected from sewage treatment facilities, environmental spills, and bush latrines
or sites of open-air defecation within mongoose home ranges.
The team used Escherichia coli (E. coli), which is commonly
found in the gut of humans and animals, as a model microorganism to investigate
the potential for microorganisms to move between humans and wildlife. They
evaluated the degree of antibiotic resistance considered an important signature
of bacteria that arise from human sources.
The researchers also extracted data from the local hospital
to assess antibiotic resistance among patients and identify resistance patterns
in the region. Like many places in Africa, antibiotics are widely available and
there are few controls on the dispensing of such drugs.
57% on mongoose have antibiotic
The project screened for nine locally available
antimicrobials, including ampicillin, tetracycline, doxycycline, and
streptomycin, as well as ceftiofur, a veterinary drug not available in the
The researchers discovered 57% of banded mongoose had E-coli
that was antibiotic resistant. "Resistance was identified among individuals
in all sampled troops," the article reports.
The animals were most commonly resistant to ampicillin,
followed by doxycyline, tetracycline, and streptomycin. But it was the
prevalence of multidrug resistance that was most alarming.
"There was a significant difference between troops in
protected area and those outside the park, although not what you might
expect," said Alexander.
One troop in the town of Kazungula, outside the protected
area, had the lowest level of multidrug resistance among sampled mongoose,
while a troop from the protected area living near an ecotourism facility had
the highest levels.
At least one sampled mongoose in this particular troop in
the protected area was resistant to each of the 10 antibiotics screened in the
As is common of mongoose that live near humans, the troop
near the ecotourism facility utilized the opportunities presented by its human neighbours,
setting up residence in the drain fields of the open septic tanks servicing the
employee accommodations and foraging around employee living quarters, including
eating food remains from dishes left outside. One interaction between the
employees resulted in an unexpected finding — the kitchen staff fed raw meat
waste from commercially produced chickens to mongoose.
"This may be how the mongoose developed resistance to
ceftiofur," said Alexander.
The one troop living in an undisturbed region of the park
was resistant to only ampicillin. "These findings reinforce the
significance of human impacts to natural environments, even when human numbers
are low," said Alexander.
The article reports that mongoose were resistant to the same
antibiotics as humans in the region, but at a lower level. Of human faecal
samples collected in the mongoose home ranges, 80.3% were resistant to at least
one antibiotic. Of the human clinical samples screened at the local hospital,
89.9% of various isolated bacteria species were resistant to at least one
"This work identifies direct support for the
possibility that direct human faecal contamination of the environment is an
important potential source of microbial exposure and transmission to wildlife
living in these areas," said Ponder, who was with the US Centers for
Disease Control and Prevention before coming to Virginia Tech.
"Ecotourism developments are important for conservation
and economic growth, but the associated human waste, which includes garbage as
well as faeces and waste water, may expose wildlife to human-associated
pathogens and antibiotic resistance, ultimately increasing future threats to
human health," said Alexander.
The project was funded by a National Science Foundation
(NSF) Dynamics of Coupled Natural and Human Systems award, the Morris Animal
Foundation, and the WildiZe Foundation. The NSF Scholarships in Science,
Technology, Engineering, and Mathematics program also provided partial
financial support for Pesapane.
"The impact of microbial exchange and antibiotic
resistance accumulation in mongoose may extend through food webs," the
researchers conclude. "Mongoose are eaten by a large number of avian,
reptile, and mammalian predators including domestic dogs. Thus, the cascading
effects of exposure of wildlife species to human waste-associated microbes can
impact an array of susceptible species across an ecosystem and in turn increase
human exposure, coupling humans and natural systems in complicated ways."
They recommend closed sewage systems, wildlife-proofed trash
receptacles, and prohibiting feeding poultry and livestock products from
kitchen waste to either wildlife or domestic animals.
"As we change our natural environments, these
modifications can in turn impact our own health," said Alexander. "We
are working with the Botswana Ministry of Health and Ministry of Environment,
Wildlife, and Tourism to minimize these impacts and develop sustainable approaches
to the protection of human, wildlife, and ecosystem health."
Pesapane said the research experience reinforced that
"the issue of global sustainability and health is multifaceted, and an
interdisciplinary approach is vital to achieving progress in managing health
threats at this complex interface."
Pointing out the interconnectedness of human health and
wellbeing and conservation of natural resources, she said, "We cannot
begin to address issues of conservation without also improving quality of life
in neighbouring communities.
"The Virginia Tech/CARACAL program under the NSF-funded
program embodied this concept with expanded program focus beyond research in
the Chobe region to include educational outreach and partnered efforts with the
Government of Botswana to improve the quality of life for the citizens of
Botswana," she added.
Pesapane, who completed her master's in wildlife science at
Virginia Tech in December 2011, is now project director of Rural System Inc.
"My experience with the Alexander lab, its non-profit affiliate CARACAL,
and my education in the fish and wildlife conservation department at Virginia
Tech provided a solid foundation for an inspiring career in global
conservation," she said.
"Our next step," Alexander said, "is to begin
to unravel the interdependent natural and human drivers of microorganism
exchange, emergence of disease, and spread of antibiotic resistance among
wildlife and across environments. This will be essential to our ability to
effectively manage this interface and protect the health of humans, wildlife,
and environments on which we depend."
(Picture: banded mongoose from Shutterstock)