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Infection and Immunity, April 2000, p. 2183-2186, Vol. 68, No. 4
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Acquisition of Coinfection and Simultaneous
Transmission of Borrelia burgdorferi and Ehrlichia
phagocytophila by Ixodes scapularis Ticks
Michael L.
Levin and
Durland
Fish*
Department of Epidemiology and Public Health,
Yale School of Medicine, New Haven, Connecticut
Received 1 September 1999/Returned for modification 14 October
1999/Accepted 22 December 1999
 |
ABSTRACT |
The agents of Lyme disease (Borrelia burgdorferi) and
human granulocytic ehrlichiosis (Ehrlichia phagocytophila)
are both transmitted by the tick Ixodes scapularis. In
nature, ticks are often infected with both agents simultaneously. We
studied whether previous infection with either Borrelia or
Ehrlichia in ticks would affect acquisition and
transmission of a second pathogen. Ehrlichia-infected
I. scapularis nymphs were fed upon
Borrelia-infected mice, and Borrelia-infected
I. scapularis nymphs were fed upon Ehrlichia-infected mice. The efficiency with which
previously infected nymphal ticks acquired a second pathogen from
infected hosts was compared to that of uninfected ticks. An average of 51% ± 15% of ticks acquired Ehrlichia from infected mice
regardless of their prior infection status with Borrelia.
An average of 85% ± 10% of ticks acquired Borrelia from
infected mice regardless of their prior infection status with
Ehrlichia. Also, we assessed the efficiency with which
individual nymphs could transmit either agent alone, or both agents
simultaneously, to individual susceptible hosts. An average of 76% ± 9% of Borrelia-infected ticks and 84% ± 10% of
Ehrlichia-infected ticks transmitted these agents to mice
regardless of the presence of the other pathogen. There was no evidence
of interaction between the agents of Lyme disease and human
granulocytic ehrlichiosis in I. scapularis ticks. The presence of either agent in the ticks did not affect acquisition of the
other agent from an infected host. Transmission of the agents of Lyme
disease and human granulocytic ehrlichiosis by individual ticks was
equally efficient and independent. Dually infected ticks transmitted
each pathogen to susceptible hosts as efficiently as ticks infected
with only one pathogen.
| |
INTRODUCTION |
The black-legged tick Ixodes
scapularis is a vector of Borrelia burgdorferi, the
etiologic agent of Lyme disease, as well as Ehrlichia
phagocytophila, the etiologic agent of human granulocytic ehrlichiosis (HGE) (2, 4, 31, 32). In nature, nymphal and
adult ticks are often infected with both agents simultaneously (3,
16, 29, 33). Nymphal or adult ticks can acquire both pathogens
simultaneously from a single coinfected host during either larval or
nymphal feeding (M. Levin, unpublished data). Alternatively, adult
ticks may have acquired pathogens consecutively
one during larval
feeding and a second during nymphal feeding. In nature, the prevalence
of either pathogen in ticks increases significantly from the nymphal to
the adult stage, and consequently, the prevalence of coinfection in
questing adult ticks can be 7 to 10 times higher than in nymphs
(16). This observation suggests that consecutive acquisition
of different pathogens by individual ticks may happen more frequently
than simultaneous acquisition.
Simultaneous infection with these two agents has also been documented
in humans and rodents (16, 18-20). Infection with both agents may result from the bite of a single coinfected tick. However, there is no experimental evidence for simultaneous transmission of
Ehrlichia and Borrelia by individual ticks.
Moreover, the efficiency with which infected ticks can transmit either
E. phagocytophila or B. burgdorferi to
susceptible hosts has not been studied in detail. A recent study found
that some laboratory mice fed upon by small numbers of I. scapularis ticks infected with E. phagocytophila failed
to acquire infection, suggesting that E. phagocytophila may
be transmitted less efficiently than B. burgdorferi
(4). However, all transmission studies of B. burgdorferi published to date also involve groups of infected
ticks (27, 28), and it is therefore not known if all
individual ticks are capable of Borrelia transmission.
Evidence from studies of tick-borne encephalitis suggests that the
efficiency of transmission by a population of infected Ixodes
persulcatus ticks is considerably less than 100% (10).
We questioned whether previous infection with either B. burgdorferi or E. phagocytophila in ticks would affect
acquisition and/or transmission of a second pathogen. In order to
determine this, we measured the efficiency with which previously
infected nymphal ticks acquired a second pathogen from infected hosts
and compared it to the efficiency of acquisition by uninfected ticks. We also measured the efficiency with which individual nymphs could transmit either agent alone or both agents simultaneously to individual susceptible hosts.
| |
MATERIALS AND METHODS |
The white-footed mouse (Peromyscus leucopus) is known
to be a major reservoir for B. burgdorferi. It also has been
shown to be susceptible to infection with E. phagocytophila
(5, 16, 21, 32). Therefore, we used white-footed mice as
hosts in our experiments. Two-month-old mice were derived from a
specific-pathogen-free P. leucopus colony maintained in our
laboratory. The maintenance and care of experimental animals complied
with the National Institutes of Health guidelines for the humane use of
laboratory animals. The mice were not exposed to ticks or pathogens
prior to the experiments.
Infected I. scapularis nymphs were produced by allowing
larval ticks to feed upon white-footed mice previously infected with either B. burgdorferi or E. phagocytophila. Both
agents originated from nymphal ticks collected in Westchester County
(N.Y.) and were maintained separately in a laboratory tick-mouse cycle.
The identities of the agents had been previously confirmed by indirect immunofluorescence assay and by DNA sequencing of amplified PCR products (4, 14).
Infection with B. burgdorferi and E. phagocytophila in ticks and mice was determined by PCR. For PCR,
individual nymphal or adult ticks or pools of engorged larvae were
placed in sterile 1.5-cm3 plastic vials, deep frozen in
liquid nitrogen, ground with a sterile plastic pestle, and resuspended
in 100 µl of Tris-borate buffer. DNA was extracted from the ticks
with an IsoQuick nucleic acid extraction kit (ORCA Research Inc.,
Bothell, Wash.) to maximize sensitivity (30). Briefly,
guanidine thiocyanate, a proprietary extraction matrix, and sodium
dodecyl sulfate solution were added to a suspension, and the mixture
was incubated at 65°C for 10 min. After separation of phases by
centrifugation, the DNA was precipitated with sodium acetate and
isopropanol and washed with 70% ethanol. The final DNA pellet was
resuspended in 50 µl of RNase-free water, and 1 2.5-µl aliquot was
used for each PCR test. Primers EHR521 (5'-TGT AGO CGG TTC GOT AAG TTA
AAG-3') and EHR747 (5'-GCA CTC ATC GTT TAC AGC GTG-3') were used to
amplify a 247-bp fragment of 16S ribosomal DNA from E. phagocytophila (24). Primers FLA297 (5'-CGG CAC ATA TTC
AGA TGC AGA CAG-3') and FLA652 (5'-CCT GTT GAA CAC CCT CTT GAA CC-3'),
based on the published nucleotide sequence (6), were used to
amplify a 378-bp fragment of the flagellin gene of B. burgdorferi. The amplification products were visualized in 2%
agarose gels.
Acquisition experiment.
Ten mice were each infected with
Borrelia by allowing 10 I. scapularis nymphs from
a B. burgdorferi-infected cohort to feed on them. Another 10 mice were each similarly infected with Ehrlichia by allowing
10 nymphs from an E. phagocytophila-infected cohort to feed
on them. The infection in the nymphal cohorts prior to the
investigation was assessed by testing representative samples of 25 ticks. The prevalence of infection in the Borrelia-infected cohort was 44.0% ± 10.1%, and the prevalence of infection in the Ehrlichia-infected cohort was 40.0% ± 10.0%.
Two weeks later, 25 nymphs from the B. burgdorferi-infected
cohort were placed on each of five mice previously infected with Ehrlichia. The other five Ehrlichia-infected mice
were each fed upon by 25 uninfected nymphs. Similarly, five B. burgdorferi-infected mice were infested with 25 nymphs from the
Ehrlichia-infected cohort, and 25 uninfected nymphs fed upon
the other five B. burgdorferi-infected mice. The engorged
nymphs were collected and kept at 22°C and 98% relative humidity
until they molted. Freshly moiled adult ticks were individually tested
by PCR for infection.
Transmission experiment.
Single-infected and coinfected
nymphs were produced by allowing larval ticks to feed upon white-footed
mice singly or simultaneously infected with B. burgdorferi
and E. phagocytophila in the course of the previous
experiment. These nymphs were placed individually on single naive mice
and allowed to feed to repletion. The resulting engorged nymphs were
collected and individually tested by PCR for infection.
Two weeks after the feeding by infected nymphs, the mice were infested
with uninfected larval ticks for xenodiagnosis. The
infection status of
individual mice was assessed using 20 engorged
xenodiagnostic larvae
per mouse (four pools of five ticks). The
tick pools were tested for
both pathogens by PCR. Our previous
study had shown that feeding
density influences the acquisition
of
B. burgdorferi in
larval
I. scapularis (
15). Therefore, the
mice
were infested with a large number of larvae (approximately
200) in
order to maximize the sensitivity of xenodiagnosis. The
xenodiagnostic
larvae were derived from a colony of
I. scapularis maintained in our laboratory by allowing them to feed on uninfected
mice and rabbits for several generations. Representative samples
of
ticks from the colony are regularly tested to ensure that the
colony is
free of both tick-borne pathogens. Xenodiagnosis was
performed only on
mice from which individual replete nymphs that
tested positive for
either pathogen were
collected.
Differences in prevalence of infection were analyzed using
2 and analysis of variance (ANOVA)
statistics.
| |
RESULTS AND DISCUSSION |
Acquisition experiment.
An average of 19 (12 to 23) nymphal
ticks fed to repletion on each of the 20 infected mice and were tested
for both agents as adults. When nymphs from the
Borrelia-infected cohort fed upon five mice infected with
Ehrlichia, 39 of the resulting adult ticks tested PCR
positive and 47 tested PCR negative for B. burgdorferi (Table 1). The prevalence of
Borrelia infection in adult ticks (45.3% ± 10.6%) did not
differ from that in the same cohort of nymphs tested prior to feeding
(44.0% ± 19.9%). When nymphs from the Ehrlichia-infected
cohort fed upon five mice infected with B. burgdorferi, 48 of the resulting adult ticks tested PCR positive and 47 tested PCR
negative for Ehrlichia (Table
2). Again, the difference in
Ehrlichia infection between nymphal ticks prior to feeding
(40.0% ± 19.6%) and the resulting adult ticks (50.5% ± 10.1%) was
not statistically significant.
Nymphs may be able to acquire pathogens not only from an infectious
host but also from infected ticks during cofeeding (
7,
22,
23,
25). However, transmission by cofeeding did not
increase the
prevalence of either
B. burgdorferi or
Ehrlichia in our experiment. Therefore, we assume that the ticks which tested
positive for
B. burgdorferi after feeding on mice (Table
1)
were
infected with
B. burgdorferi prior to feeding. The same
assumption
applies to the adult ticks that tested positive for
Ehrlichia (Table
2).
A total of 44 ticks from the
Borrelia-infected cohort
acquired
Ehrlichia during feeding upon five infected mice
(Table
1).
The efficiency of
Ehrlichia acquisition by
nymphal ticks from
the same cohort varied among individual mice but did
not differ
between ticks that were or were not previously infected with
B. burgdorferi (
P
2 = 0.98). On the average,
approximately 50% of nymphs from the
Borrelia-infected cohort
acquired
Ehrlichia from
infected mice regardless of their prior
infection status with
B. burgdorferi (Table
1).
When a cohort of exclusively uninfected nymphs fed upon the second
group of five mice infected with
Ehrlichia, a total of
43 of
96 resulting adult ticks (44.8% ± 10.0%) acquired the infection.
Individual mice transmitted
Ehrlichia to 30.0 to 60.1% of
feeding
ticks. The difference in acquisition of
Ehrlichia by a cohort
of
B. burgdorferi-infected nymphs and a cohort of uninfected nymphs
was not statistically significant (
PANOVA = 0.22).
A total of 81 ticks from the
Ehrlichia-infected cohort
acquired
Borrelia during feeding upon five infected mice
(Table
2).
The efficiency of
B. burgdorferi acquisition by
nymphal ticks
from the same cohort varied among individual mice but did
not
differ between ticks that were or were not previously infected
with
Ehrlichia (
P2 = 0.97).
An average
of 85.3% ± 7.2% of nymphs from the
Ehrlichia-infected cohort acquired
B. burgdorferi
from infected mice regardless of their prior infection
status with
Ehrlichia (Table
2).
When a cohort of exclusively uninfected nymphs fed upon an additional
five mice infected with
B. burgdorferi, a total of 88
of 105 resulting adult ticks (83.8% ± 7.1%) acquired the infection.
Individual mice transmitted
B. burgdorferi to 73.9 to 90.5%
of
feeding ticks. The difference in acquisition of
B. burgdorferi by a cohort of
Ehrlichia-infected nymphs
and a cohort of uninfected
nymphs was not statistically significant
(
PANOVA = 0.37).
Thus, previous infection with
B. burgdorferi or
E. phagocytophila in nymphal
I. scapularis did not affect
the ability of the
ticks to acquire a second pathogen from infected
hosts.
Transmission experiment.
A total of 98 mice were successfully
fed upon by individual nymphal ticks. Of those 98 nymphs, 89 were
infected with either B. burgdorferi or E. phagocytophila or both as detected by PCR performed on the
engorged ticks (Table 3). Xenodiagnostic
results showed that 31 of 38 (81.6%) ticks infected with only B. burgdorferi transmitted the spirochete to mice compared to 70%
(21 of 30) transmission success when ticks were simultaneously infected
with both Borrelia and Ehrlichia (Table 3). This
difference between the two groups of ticks was not statistically
significant (P2 = 0.27). When ticks
were infected with Ehrlichia only, 18 of 21 (85.7%)
transmitted it to susceptible mice, as determined by xenodiagnosis (Table 3). Of 30 dually infected ticks, 18 (83.3%) transmitted Ehrlichia. Thus, there also was no difference in the
efficiency of transmission of E. phagocytophila between
ticks infected with one or both pathogens
(P2 = 0.82). The efficiency of
transmission did not differ significantly between B. burgdorferi and Ehrlichia either in ticks infected with
one pathogen (P2 = 0.69) or in
dually infected ticks (P2 = 0.22).
In another study of pathogen transmission by individual
I. scapularis ticks, six of seven nymphs that fed to repletion
transmitted
B. burgdorferi to hamsters (
26).
However, the ticks themselves
were not examined, and it was not known
whether the nontransmitting
ticks were infected. Our data show that
only 70 to 81% of infected
I. scapularis nymphs transmit
B. burgdorferi to susceptible hosts
even when fed to
repletion. The efficiency of transmission of
E. phagocytophila by infected ticks is 83 to 86% and is not
significantly
different from that of
B. burgdorferi. The
differential infectivity
of ticks is likely to be related to the
variability of pathogen
concentration among infected ticks (
1,
11-13,
17). This has
been shown to occur in ticks transmitting
spring-summer tick-borne
encephalitis virus (
8,
9).
Of 30 ticks infected with
Borrelia and
Ehrlichia
simultaneously, 20 successfully transmitted both pathogens while 4 failed
to transmit either (Fig.
1). Our
results suggest that transmission
of the agents of Lyme disease and HGE
by individual ticks is equally
efficient and independent. Simultaneous
infection with the agents
of Lyme disease and HGE has been observed
both in human patients
and in wild animals (
16,
18-20).
Mixed infections in hosts may
originate either from the bite of a
single tick infected with
two pathogens or from multiple bites of
singly infected ticks.
Simultaneous transmission of
B. burgdorferi and
Babesia microti by individual
I. scapularis nymphs has been previously reported
(
26).
The present study provides evidence that dually infected
ticks are
capable of simultaneous transmission of
B. burgdorferi and
E. phagocytophila and that infection of ticks with one of
these pathogens does not interfere with transmission of the other.
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FIG. 1.
Transmission of B. burgdorferi and E. phagocytophila by individual I. scapularis nymphs
simultaneously infected with both pathogens.
|
|
There was no evidence of interaction between the agents of Lyme disease
and HGE in
I. scapularis. The presence of either agent
in
ticks did not interfere with acquisition of the other agent
from an
infected host. Transmission of the agents of Lyme disease
and HGE by
individual ticks was equally efficient and independent.
Dually infected
ticks transmitted each pathogen to susceptible
hosts as efficiently as
ticks infected with only one pathogen,
and most dually infected ticks
were able to transmit both pathogens
to a susceptible
host.
| |
ACKNOWLEDGMENTS |
This research was sponsored by grants from the G. Harold and
Leila Y. Mathers Charitable Foundation, the National Institutes of
Health, National Institute of Allergy and Infectious Diseases (AI28956), and USDA cooperative agreement 58-1265-5023.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Epidemiology and Public Health, Yale School of Medicine, 60 College
St., P.O. Box 208034, New Haven, CT 06520-8034. Phone: (203) 785-3525. Fax: (203) 785-3604. E-mail: durland.fish{at}yale.edu.
Editor:
D. L. Burns
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Infection and Immunity, April 2000, p. 2183-2186, Vol. 68, No. 4
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
