Siphonaptera (the Flea) as a Vector of Plague
by JM
Zoology 444
University of Washington
Spring 2003
Abstract
Outbreaks of Plague have declined to a very low level, especially compared to the
Middle Ages. Today, outbreaks of plague are controlled by Integrated Pest Management
programs. These programs rely on detailed information about the disease cycle. Plague
is caused by Yersinia pestis and is transmitted from endemic rodent populations to
humans via fleas. Expression of particular genes by Y. pestis causes blocking of the flea
proventriculus. Starving fleas have altered behavior in that they bite any mammal
searching for a blood meal and are thus able to transmit plague to humans. Management
of endemic rodent flea populations is the principal method for managing plague
outbreaks in humans.
Introduction
Few diseases have made a greater impact on human history than plague. Millions
of people died during the worldwide epidemics of the Middle Ages. During the second
pandemic in the fourteenth century, one-fourth of Europe’s population (and half of
England’s) was killed (Evans 1984, p.296). With better sanitation in urban areas and rat
control, cases of plague declined. The advent of modern medicine and antibiotics
lowered cases of plague even further. It wasn’t until around 1900 that Y. pestis was
identified as the causative agent (Evans 1984, p.296). The rat flea was soon recognized
as the vector of disease. Since that time, plague has largely been controlled; however, it
has not been eradicated. Titball et al. (2003) stated that more than 2000 cases are
reported to the World Health Organization (WHO) each year. Much research has been
done to understand how best to avoid outbreaks of plague. Research has shown that Y.
pestis expresses specific genes depending on which host it is residing. Y. pestis genes
expressed only while in the flea have been shown to interrupt normal flea biology and
behavior (Hinnebusch 2002), making the flea an effective vector. Other research has
focused on controlling flea populations as a means of minimizing risk of plague
outbreaks.
Results
Lifecycle of the Flea
To understand how fleas are effective plague vectors, one must first be familiar
with basic flea biology. The flea lifecycle can be broken into two distinct phases: preparasitic and parasitic. The pre-parasitic stage begins when females lay their eggs in the
nest or burrow of their host. The worm-like larvae hatch and remain in the nest feeding
on skin flakes, dander, and other debris (Gullan 2000, p.369). The larvae require iron,
which they get by eating adult flea feces (Evans 1984, p.294). Finally, the larvae pupate.
The adult, parasitic flea requires a host as a nutritional reservoir. For this reason the
pupae remain in a quiescent state until the host is detected (Gullan 2000, p.311). The
trigger believed to induce emergence from the pupal cocoon is vibration. When the
pupae detect vibrations characteristic of the host, they emerge (Gullan 2000, p.311).
They are now ready to exist as parasites.
During pupation a number of morphological changes take place to make the adult
an effective parasite. First, their bodies are flattened laterally, allowing them to move
forward through host fur (Gullan 2000, p.311). Second, they have backwards pointing
cuticular extensions, called combs (Evans 1984, p.294), that make them very difficult to
remove from host fur. Before the host has to worry about removing fleas from it’s fur,
the newly emerged adults must first find the host. Fleas do not have wings to fly. Instead,
most fleas have very powerful jumping hind legs. Like many jumping insects, the energy
for jumping is stored by compressing or deforming the cuticle. When the flea is ready to
jump, the compression is released in an explosive, spring-like action, propelling the flea
forward (Evans 1984, p.294). An average flea can jump 50 to 100 times it’s own body
length. This tremendous leaping ability helps the newly emerged adults to take up
residence on the host. The final morphological feature important to the parasitic stage is
sucking mouthparts. The stylet, or straw like structure, is derived from the epipharynx
(Gullan 2000, p.29). Fleas only have one stylet. The maxillary laciniae form two cutting
blades (Gullan 2000, p.29) allowing the flea to pierce the host skin and suck blood
through the stylet. The Order comprising the flea is fittingly termed Siphonaptera. As
this name implies, they are sucking (siphon), wingless (aptera) insects.
One behavioral aspect of adult fleas is important to their being an effective vector
of plague. Most species have fairly specific host interactions, meaning they
predominantly feed on one host species. It is common for fleas to rest away from the
host after a blood meal, where they can survive for several weeks (Evans 1984, p.295).
When the flea is again hungry, it will seek for the preferred host. Despite general host
specificity, most fleas are able to feed on a range of host species. Starving fleas will
usually bite whatever mammalian host they can find.
Background on Yersinia pestis and Plague
Y. pestis has a lifecycle as interesting as the flea. Y. pestis is endemic in rodents,
meaning it exists at a low level within the rodent population, causing little or no disease.
The animal host provides a constant reservoir of the bacteria. In western USA, wild
ground squirrels are the reservoir (Gullan 2000, p.365). The disease is initially spread to
humans through flea bites from infected fleas. When humans are infected with the
bacterium, mortality rates are high. This is especially true among the elderly, children,
and when the disease progresses to the pneumonic form (Titball 2003), which is spread
through the air by coughing.
Flea as a Vector
Y. pestis infects and causes disease in fleas. Hinnebusch et al. (2002) explored the
genetic basis of the flea disease. They identified an important toxin: Yersinia Murine
Toxin (YMT). The temperature at which YMT is expressed led them to believe it was
important for bacterial survival in the flea. They inoculated fleas with Y. pestis that was
either wildtype or mutant with respect to the YMT gene. It was shown that the bacteria
were only able to survive in the flea midgut when the wildtype gene was expressed.
Some infections progressed until the proventriculus (the valve connecting the esophagus
and midgut) was blocked. Fleas infected with YMT mutant bacteria were able to clear
the bacteria from their systems. The researchers concluded that wildtype YMT
expression is necessary for the survival of Y. pestis in the flea, and thus subsequent
transmission to mammalian hosts. All infected fleas are capable of transmitting disease
because blood from the flea gut mixes with saliva and is then able to enter the wound.
Blocked fleas are especially efficient at transmitting the disease because bacteria are
more easily dislodged from the proventriculus. Also, the now starving flea tends to bite
many hosts.
Modern Management of Plague
Historically, eliminating the rodent host was the primary method for controlling
plague outbreaks. Though still important in cities, this method is not as useful today
because wild rodent populations predominantly harbor the disease. Modern methods of
plague control focus on controlling flea populations in regions where plague is identified.
Traditional methods include dusting ground squirrel burrows with insecticides and setting
up bait stations with rodent food and insecticide (Davis 1999). These methods are fairly
expensive and difficult to use in areas where people are likely to be. Problems with flea
resistance to the insecticides are also a concern. For these reasons they are only used as
reactive measures (i.e.: after a local outbreak of plague in humans) and often result in the
closures of campgrounds and public parks. With suburban populations pushing farther
into wildlife habitat, plague outbreaks are likely to escalate if a proactive approach is not
found.
Richard Davis (1999) did a study to test the effectiveness of such an approach in
California. He made feed cubes (composed of peanut butter, dry dog food, oatmeal, etc.)
that could be eaten by ground squirrels and used these as a means of administering
Lufenuron. Lufenuron is a chitin inhibitor used to control pet-infesting fleas. The drug is
absorbed into the mammal’s blood where it then enters the flea when it eats. The next
generation of fleas is unable to synthesize their chitin exoskeleton and die as a result.
Because the drug targets an insect specific molecule (chitin), it has a very low toxicity in
humans and other mammals. The problem has been administering the drug to wild
rodents. Davis (1999) used his feed cubes as a method to administer Lufenuron to
ground squirrels. Rather than setting up a bait station to attract the ground squirrels, the
feed cubes were placed near occupied ground squirrel burrows. Observations were made
to ensure that the ground squirrels were eating the cubes completely (receiving the full
dose). Next, ground squirrels were trapped live from this area and a neighboring, isolated
area where no drug was administered. Blood tests were done to determine the dose of
Lufenuron in each ground squirrel. The number of fleas on each ground squirrel were
also counted. The fleas were removed, identified to species, and tests were done to
determine the viability of their eggs. The study covered a two-year span. During the first
year two doses were administered with feed cubes and four doses were administered the
second year. The result was that ground squirrels were infested with fewer fleas after
repeated administration of Lufenuron via the feed cubes. Flea levels were analogous to
or better than the target levels of other insecticide programs. From the blood analysis
Davis (1999) determined that the feed cube dosage could be increased to provide longer
lasting flea control. His study was successful because of natural flea behavior. Adult
fleas receiving a blood meal containing Lufenuron are largely unaffected because they
don’t molt anymore. However, they are the means of administering the drug to future
generations. Lufenuron is excreted in adult feces, which are then eaten by larval fleas.
To maintain control of the flea population, Lufenuron would need to be administered
every year. The cost of materials and labor to make and administer the feed cubes was
about 90% less than traditional reactive insecticide measures. Parks and campgrounds
can be left open to the public because the treatment poses almost no risk to humans. It
was concluded that this method of flea control was a safe, cost effective, and proactive
part of an Integrated Pest Management program.
Conclusion
Plague has been with mankind for centuries. Research over the past century has
been very effective in eliminating the disease as a major cause of death to humans. It is
unlikely that plague will be entirely eliminated because bacterial agents are difficult, if
not impossible, to eradicate completely. Study of the bacteria was especially important in
understanding how the flea is transformed into an effective vector. This, however, is
largely irrelevant in controlling the spread of the disease. The study of flea development
and behavior has played a critical part in understanding how to control plague outbreaks.
Because larvae feed on adult fecal matter, it is possible to safely administer Lufenuron to
control flea populations with little danger to flea hosts and people. Access to areas where
Y. pestis is detected can also be restricted to ensure the disease is not transmitted to
people. I was unable to find any articles describing whether feed cube administration
was continued in California. The major assumption of the study conducted by Davis
(1999) was that plague outbreaks would decrease if endemic rodent flea populations were
controlled. I found no studies or data to support this and feel this would be an interesting
area of continued research.
References
Davis, Richard M. 1999. Use of Orally Administered Chitin Inhibitor (Lufenuron) to
Control Flea Vectors of Plague on Ground Squirrels in California. J. Med.
Entomol. 36(5): 562-567.
Evans, Howard E. Insects: A Textbook of Entomology. Addison-Wesley Publishing Co.
Reading, Mass: 1984.
Gullan, P.J., P.S. Cranston. The Insects: An Outline of Entomology. 2nd Ed. Blackwell
Science Ltd. London: 2000.
Hinnebusch, B.J., A.E. Rudolph, P. Cherepanov, J.E. Dixon, T.G. Schwan, A. Forsberg.
2002. Role of Yersinia Murine Toxin in Survival of Yersinia pestis in the Midgut
of the Flea Vector. Science. 296: 733-735.
Titball, R.W., J. Hill, D.G. Lawton, K.A. Brown. 2003. Yersinia pestis and Plague.
Biochem. Soc. Transactions. 31(1): 104-107.