Anaplasma phagocytophilum in Ixodes ricinus ticks and human granulocytic anaplasmosis seroprevalence among forestry rangers in Białystok region.
ABSTRACT Human granulocytic anaplasmosis, former ehrlichiosis, is a tick-borne zoonosis of increasing recognition. The aim of the study was: 1) to assess the prevalence of Anaplasma phagocytophilum infection in Ixodes ricinus ticks collected in recreational forests in Bialystok vicinity, the capital of podlaskie voivodship; 2) to evaluate the prevalence of IgG and IgM antibodies to A. phagocytophilum among forestry rangers from the same region.
Of the 372 ticks examined, 54 (14.5%) yield the positive PCR reaction. The highest prevalence was detected in females, up to 27.8% (37/133), almost one third lower in males--9.2% (13/142), followed by nymphs--4.1% (4/97). Human seropositivity study revealed IgG antibodies against A. phagocytophilum in 9 out of 231 individuals (3.9%). No IgM antibodies were found. Sixty-seven individuals 67/231 (29%) reported erythema migrans. IgM anti-Borrelia burgdorferi antibodies were detected in 32 out of 121 (26.4%) persons tested, IgG--in 43 out of 231 (18.6%).
The data obtained show relatively low A. phagocytophilum seroreactivity among professionally exposed to tick group of forestry workers despite high A. phagocytophilum infection level in the competent vector--I. ricinus ticks.
- SourceAvailable from: Monika Halanova[Show abstract] [Hide abstract]
ABSTRACT: Human granulocytic anaplasmosis (HGA) and Lyme borreliosis (LB) are tick-borne and emerging infectious diseases caused by the Anaplasma phagocytophilum and Borrelia burgdorferi species. In Europe, including Slovakia, the principal vector of both pathogens is the common tick - Ixodes ricinus, in which double infections with these pathogens have been reported. The aim of our study was evidence of IgG antibodies against A. phagocytophilum in blood sera of humans with suspects LB from several Clinics of University Hospitals, and the evaluation of the possibility of B. burgdorferi and A. phagocytophilum co-infection in examined patients. The serological method ELISA was used to detect IgM and IgG antibodies against B. burgdorferi. Anti-A. phagocytophilum IgG antibodies were analyzed by the A. phagocytophilum Indirect Immunofluorescence Antibody (IFA) IgG test. A total of 214 human samples (91 men, 123 women) were obtained from patients living in Kosice town and in villages around Kosice (Eastern Slovakia). IgG antibodies against A. phagocytophilum were detected in 15 cases (6 men, 9 women), which represented 7.0 % positivity. Two cases of the co-infection B. burgdorferi with A. phagocytophilum, which equals 0.93 % of the total number, were found.Annals of agricultural and environmental medicine: AAEM 12/2009; 16(2):285-8. · 3.06 Impact Factor
- [Show abstract] [Hide abstract]
ABSTRACT: Streszczenie Wstęp: Celem prezentowanej pracy jest ocena występowania boreliozy, ustalonej diagnozy na podstawie wywiadu, objawów klinicznych ibadań serologicznych, okresu narażenia wmiejscu pracy oraz orzecznictwa ochorobie zawodowej wśród pracowników wybranych nadleśnictw województwa warmińsko-mazurskiego. Materiał imetody: Corocznym badaniom przesiewowym poddano332 pracowni-ków6 nadleśnictw, objętych opieką profilaktyczną przez Centrum Zdrowia Medica wOstródzie. Uwszystkich osób wykonano badania serologiczne, apoziomy przeciwciał klasy IgG oraz IgM wpróbkach surowicy krwi oznaczono testem ELISA. Wynik dodatni kwalifiko-wał pacjenta do wykonania testu potwierdzającego Western-blot oraz ewentualnego ustalenia rozpoznania boreliozy na podstawie wy-wiadu iobjawów klinicznych choroby. Dane przedstawiono zuwzględnieniem podziału na wybrane nadleśnictwa, płeć, okres narażenia wmiejscu pracy oraz genogatunki krętów Borrelia wywołujące chorobę. Wyniki: We wszystkich nadleśnictwach objętych badaniem stwierdzono zachorowania na boreliozę. Ogółem dodatnie wyniki badań Western-blot ustalono u120 osób (63,1%badanych), jednak rozpoznanie boreliozy po szczegółowym wywiadzie ibadaniu przedmiotowym ustalono u91 pacjentów (27,4% badanych). Wgrupie pacjentów zrozpoznaną chorobą obecność przeciwciał wklasieIgG stwierdzono u76 osób, wklasieIgM u25 osób, zczego u10 osób– wobu klasach. Wykazano także zmienności wudziale genogatunków wywołujących chorobę, zczego46% stanowiły krętki B.afzeli dla przeciwciał IgG, natomiast wklasie IgM krętki zrodzaju B.burgdorferi stanowiły50% wszystkich przypadków. Jednocześnie potwier-dzono zależność między wydłużeniem okresu narażenia wmiejscu pracy na ukąszenia przez kleszcze azwiększoną zachorowalnością na boreliozę, która wskazała na grupę zponad25-letnim stażem pracy. Wnioski: Praca zawodowa wleśnictwie stwarza szczególnie niebez-pieczne warunki ekspozycji na ukąszenia przez kleszcze, ajednocześnie długość stażu pracy znamiennie zwiększa ryzyko zachorowania na boreliozę. Analiza wyników badań serologicznych wskazuje na różnice reaktywności klas przeciwciał IgG oraz IgM wstosunku do badanych antygenów, potwierdzając tym samym korelację objawów klinicznych boreliozy względem rozpoznanych genogatunków kręt-ków Borrelia. Med.Pr.2014;(65) Słowa kluczowe: borelioza, epidemiologia, serologia, pracownicy lasów, choroba zawodowa Abstract Background: The aim of the study is to assess the incidence of Lyme disease, established diagnosis based on medical history and clinical symptoms, serology, duration of exposure in the workplace and occupational disease certification among forestry workers in selected districts of the Warmia and Mazury region. Material and Methods: The study consisted of annual screening of332 employees in 6 for-est districts under the supervision of the Health Center Medica in Ostróda. Serological tests were performed in all serum samples and IgG and IgM antibodies were determined by ELISA test. Positive results were confirmed by Western-blot test. Diagnosis was made based on medical history and clinical symptoms. Results were presented by the division of selected forest districts, gender, duration of expo-sure in the workplace and genospecies of spirochete Borrelia responsible for the disease development. Results: Lyme disease incidence was found in all selected forest districts. Positive results in Western-blot test were determined in120 people (63.1%of all the surveyed). However, after taking a detailed medical history of the patients Lyme disease was diagnosed in91 people which makes27.4% of all the examined. Among patients with diagnosed disease, IgG antibodies were found in76 people, IgM in25 people, while both IgM and IgG in10 people. There was also variation in the involvement of genospecies generating the disease; spirochete B.afzeli–46% for IgG anti-bodies, whereas spirochete B.burgdorferi– 50% of all cases for IgM antibodies. At the same time the relationship between the extended duration of occupational exposure to tick bites and the increased incidence of Lyme disease was confirmed, indicating the group of workers employed for at least 25 years. Conclusions: Forestry districts of the Warmia and Mazury region, creates extremely dangerous occupational conditions because of exposure to tick bites. At the same time the duration of employment significantly increases the risk of Lyme. The analysis of serological tests results indicated differences in the reactivity of IgG and IgM classes and confirmed the correlation between clinical symptoms of Lyme disease and the variation of genospecies inducing the disease. MedPr2014;65(3)Medycyna pracy 05/2014; 65(3). · 0.32 Impact Factor
- [Show abstract] [Hide abstract]
ABSTRACT: Worldwide, ticks are important vectors of human and animal pathogens. Besides Lyme Borreliosis, a variety of other bacterial and protozoal tick-borne infections are of medical interest in Europe. In this study, 553 questing and feeding Ixodes ricinus (n = 327) and Dermacentor reticulatus ticks (n = 226) were analysed by PCR for Borrelia, Rickettsia, Anaplasma, Coxiella, Francisella and Babesia species. Overall, the pathogen prevalence in ticks was 30.6% for I. ricinus and 45.6% for D. reticulatus. The majority of infections were caused by members of the spotted-fever group rickettsiae (24.4%), 9.4% of ticks were positive for Borrelia burgdorferi sensu lato, with Borrelia afzelii being the most frequently detected species (40.4%). Pathogens with low prevalence rates in ticks were Anaplasma phagocytophilum (2.2%), Coxiella burnetii (0.9%), Francisella tularensis subspecies (0.7%), Bartonella henselae (0.7%), Babesia microti (0.5%) and Babesia venatorum (0.4%). On a regional level, hotspots of pathogens were identified for A. phagocytophilum (12.5-17.2%), F. tularensis ssp. (5.5%) and C. burnetii (9.1%), suggesting established zoonotic cycles of these pathogens at least at these sites. Our survey revealed a high burden of tick-borne pathogens in questing and feeding I. ricinus and D. reticulatus ticks collected in different regions in Belarus, indicating a potential risk for humans and animals. Identified hotspots of infected ticks should be included in future surveillance studies, especially when F. tularensis ssp. and C. burnetii are involved.PLoS ONE 01/2013; 8(1):e54476. · 3.53 Impact Factor
Anaplasma phagocytophilum in Ixodes ricinus ticks and human granulocytic anaplasmosis seroprevalence among forestry rangers in Białystok region
· Advances in Medical Sciences · Vol. 51 · 2006 ·
* CORRESPONDING AUTHOR:
Department of Infectious Diseases
Medical University of Białystok
ul. urawia 14, 15-540 Białystok, Poland
Tel: +48 85 7409479, Fax: +48 85 7416421
e-mail: firstname.lastname@example.org (Anna Grzeszczuk)
Received 14.06.2006 Accepted 21.07.2006
Anaplasma phagocytophilum in Ixodes ricinus ticks
and human granulocytic anaplasmosis seroprevalence among
forestry rangers in Białystok region
Department of Infectious Diseases, Medical University of Białystok, Poland
Purpose: Human granulocytic anaplasmosis, former ehrli-
chiosis, is a tick-borne zoonosis of increasing recognition.
The aim of the study was: 1) to assess the prevalence of
Anaplasma phagocytophilum infection in Ixodes ricinus ticks col-
lected in recreational forests in Białystok vicinity, the capital of
podlaskie voivodship; 2) to evaluate the prevalence of IgG and
IgM antibodies to A. phagocytophilum among forestry rangers
from the same region.
Results: Of the 372 ticks examined, 54 (14.5%) yield the
positive PCR reaction. The highest prevalence was detected in
females, up to 27.8% (37/133), almost one third lower in males
– 9.2% (13/142), followed by nymphs – 4.1% (4/97). Human
seropositivity study revealed IgG antibodies against A. phago-
cytophilum in 9 out of 231 individuals (3.9%). No IgM antibod-
ies were found. Sixty-seven individuals 67/231 (29%) reported
erythema migrans. IgM anti-Borrelia burgdorferi antibodies were
detected in 32 out of 121 (26.4%) persons tested, IgG – in 43 out
of 231 (18.6%).
Conclusions: The data obtained show relatively low A. pha-
gocytophilum seroreactivity among professionally exposed to
tick group of forestry workers despite high A. phagocytophilum
infection level in the competent vector – I. ricinus ticks.
Key words: Anaplasma phagocytophilum, Ixodes ricinus, ticks,
antibodies, human granulocytic anaplasmosis, forestry rangers,
Białystok region, Poland.
Anaplasma phagocytophilum is a unique bacterium infect-
ing and multiplying successfully in granulocytes of broad range
of hosts, including domestic and wild animals – canids, horses,
sheep, cattle, European bisons and rodents, as well as humans.
Infection may be subclinical or manifesting as a non specific
febrile disease, called granulocytic anaplasmosis, tick fever or
pasture fever in sheep [1-3]. A. phagocytophilum is transmitted
by ticks from Ixodes persulcatus complex, which in Europe is
mainly I. ricinus [1,4]. Ticks and tick-borne diseases are endemic
in north-eastern Poland. This region has also the highest
incidence of tick-borne encephalitis in Poland – 7.8/100 000 vs
0.46/100 000 for the whole country in 2005 and Lyme borreliosis
(63.1 vs 11.5) . Ecological and socio-economical changes in
our region lead to increased ticks abundance and therefore
augmented exposure of human population to tick transmitted
Forestry workers constitute the professional group greatly
exposed to ticks. The aim of the study was: 1) to assess the
prevalence of A. phagocytophilum infection in I. ricinus ticks
collected in recreational forests in Białystok vicinity, the capital
of podlaskie voivodship; 2) to evaluate the prevalence of IgG
and IgM antibodies to A. phagocytophilum among forestry rang-
ers from the same region.
Material and methods
Host seeking ticks were collected by flagging lower vegeta-
tion in different forested areas in Białystok vicinity – Pietrasze,
Strzelnica, Dzikie and in Knyszyn Primeval Forest – Bobrowa,
Korytne, Supraśl-Pólko, Królowy Most and in Biebrza National
Reserve, Tab. 1. Collected ticks were individually evaluated
prior to DNA extraction by a qualified entomologist with regard
to species and gender according to Siuda . The ticks were
killed in hot water, placed in separate vials (adult) or pooled by
2-5 (nymphs) and fixed in 70% ethanol for further investigation
by PCR for the presence of A. phagocytophilum.
Human study population
Study participants were recruited from the following forest
inspectorates localized in Białystok vicinity: Dojlidy, Supraśl,
Czarna Białostocka, Waliły in July, August 2004 or 2005. Serum
samples were collected from 231 forestry workers, 40 females
and 191 males, aged 49±12 years. The questionnaire regarding
age, length and character of employment in the forest, Lyme
borreliosis and tick-borne encephalitis history, ticks exposure
and actual complains such as fever, arthralgia, mialgia was filled
by a physician.
DNA was extracted by the ammonium hydroxide lysis
(NH4OH) according to Rijpkema et al. . Lysates were stored
in -20°C until examination.
Polymerase Chain Reaction
PCR was performed according to Pancholi et al. . The
primers EHR 521 (5’-TGT AGG CGG TTC GGT AAG TTA
AAG-3’) and EHR 747 (5’-GCA CTC ATC GTT TAC AGC
GTG-3’) were used to amplify the 16S rRNA (rrs) gene frag-
ment specific for A. phagocytophilum. The tick lysates from posi-
tive reactions obtained in our previous investigation  served
as a positive control and the double distilled water as a negative
control in each PCR run. All PCR reactions were carried out
in Perkin Elmer GeneAmp PCR System 9700 thermal cyclers.
Amplification products were analyzed after electrophoresis in a
2% agarose gel stained with ethidium bromide. DNA bands of
247 base pairs (bp) were considered positive results. All positive
samples were confirmed with nested PCR reaction amplifying
rrs gene according to Massung .
phagocytophilum IgM and IgG antibodies were detected by
indirect immunofluorescence technique applying commercial
kits with HL60 cells infected with the human isolate of A. phago-
granulocytic anaplasmosis (HGA) Anti-A.
cytophilum (Focus technologies HGE IFA IgG /IgM Test Kit,
USA). The serum screening dilution was 1:64 according to the
manufacturer and results 1:64 were considered positive.
Lyme borreliosis In order to examine the anti-Borrelia
burgdorferi serological response Borrelia recombinant IgG and/
/or IgM kits (Biomedica, Austria) applying MiniBoss were used,
according to the producer.
Statistical analysis was performed with Pearson’s
p 0.05 was considered significant.
2 test and
Of the 372 ticks examined, 54 (14.5%) yield the posi-
tive PCR reaction. The highest prevalence was detected in
females, up to 27.8% (37/133), almost one third lower in males
– 9.2% (13/142), followed by nymphs – 4.1% (4/97). The overall
infection rate varied depending on the collection site; among
adults from 27.3% in Dzikie to 11.8% in Białystok-Pietrasze;
differences in nymphs were less pronounced – from 0% to
IgG antibodies against A. phagocytophilum were detected
in 9 out of 231 individuals (3.9%), Tab. 2. A. phagocytophilum
antibodies were detected in employee from 3 forest inspector-
ates – Supraśl 2/36 (5.5%), Dojlidy 3/39 (7.7%) and Czarna
Białostocka 4/72 (5.6%). No seropositive individuals were found
neither in ednia 0/30 nor in Waliły 0/45 inspectorates. Such
a low prevalence of specific antibodies might not allow finding
any significant differences depending on sex, age, length and
character of forestry employment – field or office work, Lyme
borreliosis serological status and history (erythema migrans),
and actually reported complains (fever, arthralgia, mialgia).
Surprisingly, no significant differences were detected between
individuals reporting tick bites in the last year – 6/147 (2.6%)
and those denying it – 3/63 (1.3%). Thus regression analysis was
Table 1. Anaplasma phagocytophilum infection rate in host seeking Ixodes ricinus ticks collected in different forested areas in north-eastern
No positive I. ricinus/No tested (% positive)
4/49 (8.2)10/85 (11.8)
5/24 (20.8) 13/52 (25.0)
0/4 nc2/11 (18.2)
1/28 (3.6) 6/49 (12.2)
0/5 nc3/11 (27.3)
13/142 (9.2)*50/275 (18.1)#
Białystok – Pietrasze
Białystok – Strzelnica
Supraśl – Pólko
nc – not calculated, No<10; * – difference statistically significant between females and males; # – difference statistically significant between adults
Anaplasma phagocytophilum in Ixodes ricinus ticks and human granulocytic anaplasmosis seroprevalence among forestry rangers in Białystok region
not possible. IgM antibodies against A. phagocytophilum were
not detected in any person evaluated.
Sixty-seven individuals 67/231 (29%) reported erythema
migrans in their medical history. Twelve foresters had erythema
migrans in the year of examination, but only 3 out of 10 persons
tested had IgM antibodies to B. burgdorferi. IgM anti-Borrelia
burgdorferi antibodies were detected in 32 out of 121 (26.4%)
persons tested, IgG – in 43 out of 231 (18.6%), however, the
results were not confirmed by Western Blot tests, Tab. 2.
Our results show pretty high A. phagocytophilum infection
rate in I. ricinus ticks collected in north-eastern Poland, reach-
ing 18.1% average in adults and even 40% among females in
certain locations (Królowy Most). The frequency of infection
significantly raises from nymphal to adult stage of ticks. This
observation points to the role of little rodents and small,
and intermediate mammals, harboring I. ricinus larvae, in
A. phagocytophilum circulation in nature since this bacterium is
not transovarially transmitted [1,4]. A. phagocytophilum infec-
tion rate demonstrated in our study is similar to that found in
mid-eastern Poland . Slovac research conducted in suburban
forest near Košice revealed 12.5% adult ticks infected with
A. phagocytophilum . Several other Polish studies showed
the A. phagocytophilum infection rates ranging from 0% in
Szczecin province (Głębokie Public Bath and Landscape Park
in Ińsko) , 13.1% in Lublin province , 14% in Tricity For-
est on the Baltic coast  and to 16% in Białowiea Primeval
Despite the high A. phagocytophilum infection rate in I. rici-
nus ticks, a very low presence of antibodies (3.9%) was revealed
in the present study. Beginning the investigation among forestry
workers and choosing the summer months, which followed
the highest tick activity, higher prevalence and eventually
acute granulocytic anaplasmosis cases detection was expected.
Other Polish studies in forestry rangers demonstrated higher
levels of seropositivity from 17.7% (20/113) to 20.0% (13/63) in
mid-eastern Poland and 9.6% (46/478) in northern and north-
-eastern Poland [11,16,17]. Analogically to our results, very low
A. phagocytophilum seropositivity – 1.5% was detected in Eng-
lish farmers , nevertheless south-western German data from
Baden-Württemberg forestry workers show seroprevalence
ranging from 5% to 16% in various counties . Northern
Italy investigation showed 8.8% (16/181) sera positive by IFA,
although the authors considered only one of them – 0.6%, truly
positive since confirmed by Western blot . However, applica-
tion of Western blot is not required for granulocytic anaplasmo-
sis diagnosis according to ESCMID Study Group . All three
above studies demonstrated anti-B. burgdorferi seropositivity
surpassing those of A. phagocytophilum from 3 to 20 times [11,
19,20], however, the anti-B. burgdorferi assays results should
be interpreted with caution since they where not followed by
Western blot, what is required for Lyme borreliosis diagnostics
. The reasons of such low levels of A. phagocytophilum sero-
positivity are unclear. One of the factors may be very variable
year to year tick infection rate observed in our region during 4
years period . Another factor, postulated by Massung and
co-workers in USA, is presence of A. phagocytophilum variants
non-pathogenic for humans , however, the latter hypothesis
require closer characterization of strains postulated.
The results obtained show relatively high A. phagocy-
tophilum infection rate in I. ricinus ticks and very low seropo-
sitivity among forestry rangers, a professional group highly
exposed to ticks.
I would like to thank Dr Joanna Stańczak from Medical
Academy of Gdańsk, Institute of Maritime and Tropical Medi-
cine for her help in conducting the above study.
1. Dumler JS, Walker DH. Tick-borne ehrlichioses. Lancet Inf Dis,
2. Dumler JS, Barbet AF, Bekker CPJ, Dasch GA, Palmer GH, Ray
SG, Rikihisa Y, Rurangirwa FR. Reorganization of genera in the families
Rickettsiaceae and Anaplasmataceae in the order Rickettsiales; unification
of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and
Ehrlichia with Neorickettsia; description of five new species combinations;
and designation of Ehrlichia equi and HGE agent as subjective synonyms
of Ehrlichia phagocytophila. Int J Syst Evol Microbiol, 2001; 51: 2145-65.
3. Grzeszczuk A, Barat N, Bakken SJ, Dumler JS. Anaplasmosis in
humans. In: Parola P, Raoult D, editors. Rickettsial diseases old and new.
Taylor & Francis Group, LLC, in press.
4. Strle F. Human granulocytic ehrlichiosis in Europe. Int J Med
Microbiol, 2004; 293 (Suppl. 37): 27-35.
5. Meldunki PZH. http://www.pzh.gov.pl
6. Siuda K. Ticks of Poland (Acari: Ixodidae). Part II: Systematic
and distribution (in Polish). Polskie Towarzystwo Parazytologiczne, War-
7. Rijpkema S, Golubic D, Molkenboer M, Verbreek-De Kruif N,
Schellekens J. Identification of four groups of Borrelia burgdorferi sensu
Table 2. Prevalence of IgG against A. phagocytophilum and IgG/IgM against B. burgdorferi among forestry workers in north-eastern
Erythema migrans (No=231)
lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region
of northern Croatia. Exp Appl Acarol, 1996; 20: 23-30.
8. Pancholi P, Kolbert CP, Mitchel PD, Reed KD, Dumler JS,
Bakken JS, Telford SR III, Persing D. Ixodes dammini as a potential vec-
tor of human granulocytic ehrlichiosis. J Infect Dis, 1995; 172: 1007-12.
9. Grzeszczuk A, Stańczak J, Kubica-Biernat B, Racewicz M, Kru-
minis-Łozowska W, Prokopowicz D. Human anaplasmosis in north-east-
ern Poland: seroprevalence in humans and prevalence in Ixodes ricinus
ticks. Ann Agric Environ Med, 2004; 11: 99-103.
10. Massung RF, Slater K, Owens JH, Nicholson WL, Mather TN,
Solberg VB, Olson JG. Nested PCR for detection of granulocytic ehrli-
chiae. J Clin Microbiol, 1998; 36: 1090-5.
11. Tomasiewicz K, Modrzewska R, Buczek A, Stańczak J, Maciukajć
J. The risk of exposure to Anaplasma phagocytophilum infection in mid-
eastern Poland. Ann Agric Environ Med, 2004; 11: 261-4.
12. Derdáková M, Halánova M, Stanko M, Štefan iková A,
isláková, Pet’ko B. Molecular evidence for Anaplasma phagocytophilum
and Borrelia burgdorferi in Ixodes ricinus ticks from eastern Slovakia. Ann
Agric Environ Med, 2003; 10: 269-71.
13. Skotarczak B, Rymaszewska A. Prevalence of etiological agent
of human ehrlichiosis (HGE) in ticks from west-north Poland. (in Polish)
Wiad Parazytol, 2001; 47: 95-101.
14. Stańczak J, Gabre RM, Kruminis-Łozowska W, Racewicz M,
Kubica-Biernat B. Ixodes ricinus as a vector of Borrelia burgdorferi sensu
lato, Anaplasma phagocytophilum and Babesia microti in urban and sub-
urban forests. Ann Agric Environ Med, 2004; 11: 109-14.
15. Grzeszczuk A, Stańczak J, Kubica-Biernat B. Serological and
molecular evidence of human granulocytic ehrlichiosis focus in the
Białowiea Primeval Forest (Puszcza Białowieska), north-eastern Poland.
Eur J Clin Microbiol Infect Dis, 2002; 21: 6-11.
A, Polak J, Dutkiewicz J. Risk of tick-borne bacterial diseases among
workers of Roztocze National Park (south-eastern Poland). Ann Agric
Environ Med, 2005; 12: 127-32.
17. Stańczak J, Grzeszczuk A. Seroprevalence of Anaplasma phago-
cytophilum among forestry rangers in northern and north-eastern Poland.
Ann NY Acad Sci, 2006, in press.
18. Thomas DR, Sillis M, Coleman TJ, Kench SM, Ogden NH,
Salmon RL, Morgan-Capner P, Softley P, Meadows D. Low rates of ehr-
lichiosis and Lyme borreliosis in England farmworkers. Epidemiol Infect,
1998; 121: 609-14.
19. Oehme R, Hartelt K, Backe H, Brockmann S, Kimmig P. Foci of
tick-borne diseases in souhwest Germany. Int J Med Microbiol, 2002; 291
(Suppl. 33): 22-9.
20. Cinco M, Barbone F, Grazia Ciufolini M, Mascioli M, Aguero
Rosenfeld M, Stefanel P, Luzzati R. Seroprevalence of tick-borne infec-
tions in forestry rangers from north-eastern Italy. Clin Microbiol Infect,
2004; 10: 1056-61.
21. Brouqui P, Bacellar F, Baranton G, Birtles RJ, Bjoërsdorff A,
Blanco JR, Caruso G, Cinco M, Fournier PE, Francavilla E, Jensenius M,
Kazar J, Laferl H, Lakos A, Lotric Furlan S, Maurin M, Oteo JA, Parola
P, Perez-Eid C, Peter O, Postic D, Raoult D, Tellez A, Tselentis Y,Wilske
B. Guidelines for the diagnosis of tick-borne bacterial diseases in Europe.
Clin Microbiol Infect, 2004; 10: 1108-32.
22. Grzeszczuk A, Stańczak J. Highly variable year to year preva-
lence of Anaplasma phagocytophilum in Ixodes ricinus ticks in north-east-
ern Poland. Four years follow-up. Ann NY Acad Sci 2006, in press.
23. Massung RF, Mauel MJ, Owens JH, Allan N, Courtney JW, Staf-
ford KC 3rd, Mather TN. Genetic variants of Ehrlichia phagocytophila,
Rhode Island and Connecticut. Emerg Infect Dis, 2002; 8: 467-72.
16. Cisak E, Chmielewska-Badora J, Zwoliński J, Wójcik-Fatla