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Journal of Clinical Microbiology, November 2000, p. 4208-4210, Vol. 38, No. 11
Institute of Microbiology and Epidemiology,
Fengtai District, Beijing 100071, China,1 and
Department of Pathology, The Johns Hopkins Medical
Institutions, Baltimore, Maryland 212012
Received 17 April 2000/Returned for modification 12 July
2000/Accepted 5 September 2000
A total of 372 adult Ixodes persulcatus ticks were
collected from vegetation in a forest area of Heilongjiang Province in northeastern China, where Lyme disease is known to be endemic. The
ticks were examined for the presence of granulocytic ehrlichiae by
heminested PCR with primers derived from the 16S rRNA gene. Of 310 ticks obtained from the Dahe forestry farm, two pools (each containing
5 ticks) were found positive, with a minimum infection rate of 0.6%.
Ehrlichial DNA was also detected in one female (1.6%) of 62 ticks
collected from the Yulin forestry farm. The overall minimum infection
rate of the 372 I. persulcatus adults was 0.8%. The
nucleotide sequences of 919-bp PCR products from the three positive
tick specimens were identical to each other and very closely related to
the members of the Ehrlichia phagocytophila genogroup. This
is the first identification of granulocytic ehrlichiae in ticks in Asia
and the first report of infection in I. persulcatus anywhere.
Human granulocytic ehrlichiosis
(HGE) was initially described in the United States in 1994 (8) and presents clinically as an acute febrile illness
characterized by fever, headache, chills, myalgia, lethargy, and
arthralgia (28). Laboratory findings suggestive of the
disease mainly include leukopenia, anemia, thrombocytopenia, and
elevated hepatic aminotransferase levels (2, 28). The causative agent of HGE has not yet been fully defined, but 16S rRNA
gene sequence analysis demonstrates that it is closely related to
Ehrlichia equi, the agent of the worldwide equine
granulocytic ehrlichiosis, and Ehrlichia phagocytophila, the
well-recognized pathogen of tick-borne fever of ruminants in Europe
(8, 28). In addition, the HGE agent can cause a form of
granulocytic ehrlichiosis in horses (4, 14, 15) and dogs
(10). It is suggested that the HGE agent, E. equi, and E. phagocytophila may constitute variants of
a single species, now called the E. phagocytophila genogroup.
The granulocytic ehrlichiae have been associated with ixodid ticks that
may act as vectors, including Ixodes scapularis (16, 19) and Ixodes pacificus (5, 12, 25) in the
United States and Ixodes ricinus (11, 22, 27) in
Europe. These ticks are known to transmit Borrelia
burgdorferi, the pathogen of Lyme disease, and recent studies have
indicated that they could be coinfected with B. burgdorferi
and granulocytic ehrlichiae (7, 13, 25). It is suggested
that the natural cycle of granulocytic ehrlichiae is probably similar
to that of B. burgdorferi (28). Ixodes
persulcatus is the vector of Lyme borreliosis (1) and
tick-borne encephalitis in northeastern China, but the occurrence of
Ehrlichia in ticks has not been established for this region.
The objectives of this study were to determine whether or not
ehrlichial DNA is present in I. persulcatus ticks in an area
where Lyme disease is endemic and to provide initial data regarding the
presence of granulocytic ehrlichiae in China.
Tick collection.
Adult I. persulcatus ticks were
collected from a forest area of Heilongjiang Province in northeastern
China in 1997. The collection site is near Mudanjiag located at 50° N
latitude and 128° E longitude, which is a highland city (elevation
from 500 to 600 m above sea level) in the Small Xing-An Mountains.
In the area investigated, I. persulcatus is abundant, and
Lyme borreliosis is known to be endemic, as indicated by a report of
human infection (1) and isolation of B. burgdorferi from ticks (26). In this study, ticks were
collected by dragging a standard 1-m2 flannel flag over
vegetation and were stored alive in the refrigerator until use.
Processing of tick specimens.
Ticks were processed
individually or in pools (each containing five ticks). DNA extraction
was performed by a modification of a method previously described
(16). Briefly, the ticks were placed into micro-tubes and
mechanically crushed with sterile scissors in 50 µl of DNA extraction
buffer (10 mM Tris [pH 8.0], 2 mM EDTA, 0.1% sodium dodecyl sulfate,
500 µg of proteinase K per ml). The samples were incubated for 2 h at 56°C and then boiled at 100°C for 10 min to inactivate the
proteinase K. After centrifugation, the supernatant was transferred to
fresh sterile microtubes and purified by two extractions with an equal
volume of phenol-chloroform. The DNA was precipitated by adding 3 volumes of ice-cold absolute ethanol and 100 µl of 3 M sodium acetate
to the samples and placing them at Heminested PCR amplification.
Heminested PCR amplifications
were performed with primers designed to amplify the 16S rRNA gene of
the E. phagocytophila genogroup. Primers GE9f
(5'-AACGGATTATTCTTTATAGCTTGCT-3') and GE10r
(5'-TTCCGTTAAGAAGGATCTAATCTCC-3'), previously described by
Chen et al. (8), were applied for the initial amplification.
Two primer pairs were used in the heminested PCR amplification. The
primer pair GE9f and GE2 (5'-GGCAGTATTAAAAGCAGCTCCAGG-3') (17) can specifically produce a 546-bp fragment, and
the primer pair Ehr521 (5'-TGTAGGCGGTTCGGTAAGTTAAAG-3')
(19) and GE10r yields a 441-bp product. The primary
reaction used 3 µl of purified DNA as the template in a total volume
of 30 µl. The heminested PCR was performed with 1 µl of the primary
PCR product as the template in a volume of 30 µl. For either initial
or nested amplification, the reaction mixture contained 200 µM each
deoxynucleoside triphosphate (dATP, dCTP, dGTP, and dTTP), 0.8 U of
Taq polymerase, and 0.5 µM each primer. The PCR
amplification was performed in a Perkin-Elmer 480 thermal cycler. The
cycling conditions were identical for primary and nested
amplifications, which involved the following step-wise procedure:
preheating at 95°C for 2 min; 35 cycles of 94°C for 1 min, 55°C
for 75 s, and 72°C for 1 min; and a final extension at 72°C
for 7 min. Reaction products were then analyzed by agarose gel
electrophoresis or purified for DNA sequencing. A negative control
(distilled water) and a positive control (a plasmid containing the 16S
rRNA gene of the HGE agent [GenBank accession no. U02521]) were
included with each set of amplifications. To minimize contamination,
DNA extraction, the reagent setup, amplification, and agarose gel
electrophoresis were performed in separate rooms.
Cloning of PCR products and DNA sequencing.
PCR products
after nested amplification were purified and then ligated into the
plasmid vector pGEM-T (Promega Corp.) according to the manufacturer's
instructions. The ligation products were transformed into
Escherichia coli XL1-Blue, and white colonies were selected
after growth on Luria-Bertani agar with IPTG
(isopropyl- Nucleotide sequence accession number.
The nucleotide
sequence reported in this study has been deposited in GenBank under
accession no. AF205140.
A total of 372 adult I. persulcatus ticks were examined
for the presence of granulocytic ehrlichiae by heminested PCR with initial primer pair GE9f and GE10r and subsequent primer pair GE9f and
GE2. The prevalences of PCR-positive ticks from the different sources
and by sex are shown in Table 1. The
results are expressed as the positive rate or the minimum positive
rate, obtained by dividing the positive number of specimens by the
total number of ticks examined. The calculation is based on the
assumption that each PCR-positive pool contains at least one tick with
detectable ehrlichiae. Ticks collected from the Dahe forestry farm were
examined in pools, each containing five ticks. Two of 62 pools (310 ticks) were found positive, and the minimum infection rate was 0.6%. Of 62 ticks from the Yulin forestry farm, ehrlichial DNA was detected in one female, with a positive rate of 1.6%. Overall, the minimum positive rate of the 372 ticks was estimated as 0.8%. When the tick
samples were examined with the initial primer set of GE9f and GE10r and
subsequent primer set of Ehr521 and GE10r, exactly the same results
were obtained.
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Granulocytic Ehrlichiae in Ixodes
persulcatus Ticks from an Area in China Where Lyme Disease
Is Endemic
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
20°C for 24 h. The DNA was
pelleted at 10,000 × g for 15 min at 4°C in a
microcentrifuge and washed twice with ice-cold 70% ethanol. After
being dryed, the DNA was resuspended in 50 µl of DNase-free water and
used as a template for PCR amplification.
-D-thiogalactopyranoside), X-Gal
(5-bromo-4-chloro-3-indolyl--D-galactopyranoside), and ampicillin. For sequence analyses, recombinant plasmids were extracted and purified from overnight cultures by using the QIA prep Spin Miniprep kit (QIAGEN). The nucleotide sequence of the plasmid insert
was determined by a dideoxynucleotide cycle sequencing method with an
automated fluorescent ABI PRISM 377 DNA sequencer (Perkin-Elmer, Inc.).
RESULTS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Results of heminested PCR for the identification of
granulocytic ehrlichiae in I. persulcatus ticks with initial
primer pair GE9f and GE10r and subsequent primer pair GE9f and GE2
The primary PCR product (amplified with primer GE9f and GE10r) of each
positive specimen was respectively reamplified with subsequent primer
sets GE9f-GE2 and Ehr521-GE10r. For all nested PCR amplicons, both DNA
strands were sequenced twice. As a result, a specific nucleotide
sequence 919 bp long was obtained for each tick specimen. The
ehrlichial 16S rDNA sequences determined from the three positive tick
samples were identical to each other and all differed from the
corresponding sequences of the HGE agent, E. phagocytophila,
and E. equi by 4 bases, respectively, but at different
positions (Table 2). A variable region
was discovered near the 5' end of 16S rRNA gene at positions 76 to 84 (according to the HGE agent [GenBank accession no. U02521]). It is
remarkable that the G at position 77 or 80 was unique to the
Ehrlichia variant in I. persulcatus. In contrast,
there is an A at both positions for all known granulocytic ehrlichia
variants (data not shown).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
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Granulocytic Ehrlichia DNA was amplified from I. persulcatus collected in a forest area of Heilongjiang Province in northeastern China, where Lyme disease is known to be highly endemic. To our knowledge, this is the first detection of granulocytic ehrlichiae in ticks in Asia and the first report of infection in I. persulcatus anywhere. I. scapularis. and I. pacificus have been identified as potential vectors of the HGE agent and E. equi in the United States (3, 6, 12, 23). The E. phagocytophila genogroup has been found in I. ricinus ticks from many European countries (11, 22, 27). The findings of this study add to the evidence that the E. phagocytophila genogroup is specifically associated with the I. persulcatus complex. I. persulcatus ticks are distributed over an extensive area from Russia to eastern Asia, where about one-fifth of the human population of the world resides. The presence of granulocytic ehrlichiae in northeastern China suggests a potential health threat to both humans and animals in the area, where I. persulcatus ticks are abundant. Detailed epidemiological studies are required to investigate the distribution of ticks infected with ehrlichiae, to determine the animal reservoirs of the ehrlichial agents, and especially to detect ehrlichiae in patients with acute febrile illnesses following tick bite in areas where Lyme disease is endemic.
The overall minimum infection rate of granulocytic ehrlichiae in I. persulcatus adults in this study was 0.8%, which is comparable to that in adult I. pacificus ticks from California (5) and in free-living adult I. ricinus ticks from areas in Switzerland where tick-borne fever is endemic (21). The percentage reported in this study might have been falsely reduced, because ticks were examined in pools, and some pools might contain more than one positive tick. However, even if every tick in the positive pools had harbored detectable ehrlichiae, the overall prevalence would have only gone up to 3.0%. A higher prevalence of the E. phagocytophila genogroup was reported in I. scapularis in the United States (16, 19, 25) and I. ricinus in some European countries (11, 24, 27). This discrepancy in the rates of positivity could be due to differences in sampling approaches, tick species, and ehrlichial life cycle; to geographic and seasonal variations among infected ticks; or to limits of PCR sensitivity.
Sequence analysis of PCR products from tick samples revealed a granulocytic ehrlichia variant that slightly differs from members of the E. phagocytophila genogroup (Table 2). The sequence variants of the granulocytic ehrlichia 16S rRNA gene have previously been detected in ticks in many places (7, 17, 20). It is unlikely that the 16S ribosomal DNA variants represent different Ehrlichia species. The specific sequence polymorphism of the Ehrlichia variant identified in this study has not been reported before, and whether the variant can cause disease in humans and animals remains to be determined.
I. persulcatus is abundant in northeastern China and is known as the vector of B. burgdorferi, the agent of Lyme disease (1). Studies elsewhere have demonstrated that ixodid ticks are coinfected with B. burgdorferi and the HGE agent ((7, 13, 25), and simultaneous human infection with the two agents has been reported (9, 18, 29). Coinfection may explain variations in clinical manifestations in humans and animals as a consequence of tick bites. The identification of granulocytic ehrlichiae in I. persulcatus suggests the probability of coinfection and cotransmission of the two agents in the area. Further studies are needed to investigate this phenomenon, and the possible occurrence of ehrlichiosis should be considered in the differential diagnosis of febrile patients with a history of tick bite in northeastern China, particularly when clinical symptoms and signs are atypical for Lyme disease.
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ACKNOWLEDGMENTS |
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This study was supported by a grant from the National Natural Science Foundation of China (no. 39970655).
We are grateful to Xu Rong-Man for identification of ticks.
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FOOTNOTES |
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* Corresponding author. Mailing address: Beijing Institute of Microbiology and Epidemiology, 20 Dong-Da-Jie St., Fengtai District, Beijing 100071, People's Republic of China. Phone: (086) 10-63862060. Fax: (086) 10-63812060. E-mail: caowc{at}nic.bmi.ac.cn.
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Journal of Clinical Microbiology, November 2000, p. 4208-4210, Vol. 38, No. 11
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Heo, E.-j., Park, J.-h., Koo, J.-r., Park, M.-s., Park, M.-y., Dumler, J. S., Chae, J.-s.
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