Volume 54, Issue 1 pp. 8-15

Free Access

Observed Prevalence of Tick-borne Pathogens in Domestic Animals in Sicily, Italy during 2003–2005

A. Torina,

A. Torina

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

J. Vicente,

J. Vicente

Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain

Search for more papers by this author

A. Alongi,

A. Alongi

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

S. Scimeca,

S. Scimeca

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

R. Turlá,

R. Turlá

Sanity Local Agency, n. 7 Ragusa, Sicily, Italy

Search for more papers by this author

S. Nicosia,

S. Nicosia

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

V. Di Marco,

V. Di Marco

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

S. Caracappa,

S. Caracappa

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

J. De La Fuente,

J. De La Fuente

Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain

Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, USA

Search for more papers by this author

A. Torina,

A. Torina

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

J. Vicente,

J. Vicente

Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain

Search for more papers by this author

A. Alongi,

A. Alongi

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

S. Scimeca,

S. Scimeca

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

R. Turlá,

R. Turlá

Sanity Local Agency, n. 7 Ragusa, Sicily, Italy

Search for more papers by this author

S. Nicosia,

S. Nicosia

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

V. Di Marco,

V. Di Marco

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

S. Caracappa,

S. Caracappa

Instituto Zooprofilattico Sperimentale della Sicilia, Via G. Marinuzzi n°3, 90129 Palermo, Sicily, Italy

Search for more papers by this author

J. De La Fuente,

J. De La Fuente

Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain

Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, USA

Search for more papers by this author

First published: 23 January 2007

https://doi.org/10.1111/j.1863-2378.2007.00989.x

Citations: 77

J. de la fuente. Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK, USA. Tel.: +405 744 0372; Fax:+405 744 5275; E-mail: [email protected] or [email protected]

Share a link

Email
Wechat
Bluesky

Summary

The objective of this study was to characterize the observed prevalence of tick-borne pathogens (TBP) in domestic animals in Sicily, Italy during 2003–2005. Serological (competitive ELISA and indirect immunofluorescence antibody, n = 3299) and DNA tests (polymerase chain reaction and reverse line blot, n = 2565) were conducted on horse, donkey, cattle, sheep, goat, pig and dog samples. Pathogens analysed included Anaplasma, Ehrlichia, Rickettsia, Babesia and Theileria species, and Coxiella burnetii. The most prevalent TBP were Anaplasma and Babesia species. The results reported herein suggested that cattle could serve as the major reservoir for Babesia and Theileria spp. while for Anaplasma spp. cattle, dogs, sheep and goats may be the most important reservoir species. These results expanded our knowledge about the prevalence of TBP in Sicily and provided information to understand the epidemiology of tick-borne diseases and may help to implement measures to diagnose, treat and control transmission to humans and animals in this region.

Introduction

Tick-borne diseases (TBD) impact human health and animal production and welfare. The development and implementation of control measures for TBD is dependent upon understanding the epidemiology of tick-borne pathogens (TBP) in a particular geographical region (Dehaumont, 2004).

Tick-borne pathogens such as Coxiella burnetti (Caracappa et al., 1986), Theileria spp. (Loria et al., 1999; Sparagano et al., 2000), Rickettsia spp. (Caracappa, 1989), Babesia spp. (Sparagano et al., 2000) and Anaplasma spp. (Caracappa, 1999) have been described in Sicily prior to 2000. However, after the creation of the Centro Nazionale di Referenza per Anaplasma, Babesia, Rickettsia e Theileria (C.R.A.Ba.R.T.) at the Instituto Zooprofilattico Sperimentale della Sicilia in 2003, the prevalence of TBP has been systematically evaluated.

Recent reports from our group have characterized Anaplasma spp. infections in Sicily (de la Fuente et al., 2005a,b,c). However, the updated analysis of the prevalence of other TBP in Sicily has not been reported. The current study was designed to summarize the results obtained by the C.R.A.Ba.R.T. for the characterization of the prevalence of TBP in domestic animals in Sicily.

Materials and Methods

Sample collection

Samples included in the study were supplied to C.R.A.Ba.R.T. for diagnosis or originated from random sampling conducted by the C.R.A.Ba.R.T. to monitor the prevalence of TBP in domestic animals in different provinces of Sicily (mainly in the province of Palermo).

Domestic animals sampled in the study were horses, donkeys, cattle, sheep, goats, pigs and dogs. Blood was collected in sterile tubes with and without anticoagulant (EDTA) and maintained at 4°C until arrival at the laboratory. Plasma and serum were then separated after centrifugation and stored at −20°C. Pathogens analysed were Anaplasma spp., A. marginale, A. phagocytophilum, Ehrlichia spp., E. canis, E. equi, Rickettsia rickettsii, R. conorii, Babesia spp., B. bigemina, B. bovis, B. caballi, B. canis, B. (Theileria) equi, B. microti, Babesia/Theileria spp., T. annulata and Coxiella burnetii.

Serological tests

Serum antibodies were determined for Anaplasma spp., A. phagocytophilum, E. equi, R. rickettsii, B. bigemina, B. bovis, B. caballi, B. canis, B. microti, B. (Theileria) equi and C. burnetii. The anaplasmosis competitive ELISA (cELISA; VMRD Inc., Pullman, WA, USA) was used to detect antibodies against Anaplasma spp. following the manufacturer's instructions. This assay specifically detects the presence of serum antibodies that target the MSP5 protein of Anaplasma spp. (Knowles et al., 1996). Percent inhibition values >30% were considered positive (de la Fuente et al., 2003, 2005c). Indirect immunofluorescence antibody (IFA) test kits for A. phagocytophilum, R. rickettsii, B. caballi, B. microti, B. (T.) equi and C. burnetii (Fuller Laboratories, Fullerton, CA, USA) were used following manufacturer's recommendations. The IFA tests for A. phagocytophilum, R. rickettsii, B. caballi, B. microti and B. (T.) equi use antigens derived from HL-60, Vero and erythrocyte cells infected with the HGE-1 isolate of A. phagocytophilum, the R strain of R. rickettsii and the corresponding Babesia spp., respectively, and samples were considered negative when no fluorescence was detected at 1 : 80, 1 : 50, 1 : 80, 1 : 64 and 1 : 80 dilution of the test serum, as recommended by the manufacturer. The test for C. burnetii use phase I and II antigens with a cut-off dilution of the test serum of 1 : 16. For B. bigemina and B. bovis, IFA tests from VMRD Inc. were used based on antigens derived from infected erythrocytes with cut-off dilution of 1 : 80 and 1 : 40 of the test serum, respectively, as recommended by the manufacturer. Antibodies to B. canis were detected by immunofluorescence using B. canis antigens kindly provided by Dr R. Böse (Institute of Parasitology, School of Veterinary Medicine, Hannover, Germany) with a cut-off dilution of 1 : 40 of the test serum. Fluorescein isothiocyanate-conjugated anti-host species immunoglobulin (Ig)G and/or IgM (Sigma, St Louis, MO, USA or Fuller Laboratories) were used as secondary antibodies.

DNA tests

DNA was extracted from blood samples using the GenElute Mammalian Genomic DNA Miniprep Kit (Sigma). The DNA was resuspended in sterile distilled water and stored at −20°C until used.

PCR analysis for Anaplasma spp. (de la Fuente et al., 2005c,d,e), A. marginale (de la Fuente et al., 2005c,e), A. phagocytophilum (Bown et al., 2003), Ehrlichia spp. (Munderloh et al., 1999), E. canis (Wen et al., 1997), R. rickettsii and R. conorii (Tzianabos et al., 1989), Babesia spp. and Babesia/Theileria spp. (Gubbels et al., 1999; Georges et al., 2001; Nagore et al., 2004), B. bigemina and B. bovis (Figueroa et al., 1993), B. caballi and B. (T.) equi (Battsetseg et al., 2002), B. canis (Carret et al., 1999; Caccio et al., 2002), T. annulata (D'Oliveira et al., 1995) and C. burnetii (To et al., 1996) were conducted as previously described. PCRs were performed with 1 μl (0.1–10 ng) DNA using 10 pmol of each primer and the Ready-To-Go PCR beads (Amersham, Piscataway, NJ, USA). Reactions were performed in an automated DNA thermal cycler for 35 cycles. PCR products were electrophoresed on 1% agarose gels to check the size of amplified fragments by comparison with a DNA molecular weight marker (1 Kb DNA Ladder; Promega Madison, WI, USA). Control reactions were done without the addition of DNA to the reaction to rule out contaminations during PCR.

Reverse line blot (RLB) was used for detection of Babesia/Theileria spp. as previously described (Gubbels et al., 1999; Georges et al., 2001; Nagore et al., 2004; Schnittger et al., 2004).

Statistical analysis

Within-host and between-host comparisons of TBP prevalence obtained with similar diagnostic techniques (serological or DNA tests respectively) were performed by chi-squared tests (spss 13.0 statistical program; SPSS Inc., Chicago, IL, USA). The sampling for B. (T.) equi and B. caballi in horses across the year allowed the statistical estimation of the probability for positive serological, PCR or RLB test results by means of logistic regression. For this purpose, diagnostic entries (n = 65) were grouped in bi-monthly periods as ‘explanatory categorical variable’. The differences were considered statistically significant when P ≤ 0.05.

Results

Horses

Serological (n = 551) and DNA (PCR or RLB, n = 358) tests were done for TBP on horse samples (Table 1). For both serological and DNA tests, the observed prevalence of A. phagocytophilum was lower (χ² = 90.15, P = 0.00 and χ² = 89.63, P = 0.00 respectively) than of B. caballi and B. (T.) equi. The latter did not differ in prevalence (χ² = 0.01, P = 0.91). A tendency to seasonality was observed for prevalence of A. phagocytophilum, B. caballi and B. (T.) equi (Figs 1a and b). However, statistically higher (P < 0.05) seasonal prevalence was detected during spring for B. caballi only (Fig. 1b).

Table 1. Prevalence of tick-borne pathogens in domestic animals in Sicily during 2003–2005

Pathogen	Method	Positive	Negative	n	Prevalence (%)	SE
Horses
A. phagocytophilum	IFA	12	142	154	7.79	2.16
A. phagocytophilum	PCR	0	111	111	0.00	0.00
B. caballi	IFA	109	83	192	56.77	3.58
B. caballi	PCR	29	91	120	24.17	3.91
B. (T.) equi	IFA	113	88	201	56.22	3.50
B. (T.) equi	PCR	40	87	127	31.50	4.12
E. equi	IFA	3	1	4	75.00	21.65
Donkeys
A. phagocytophilum	IFA	14	60	74	18.92	4.55
A. phagocytophilum	PCR	0	73	73	0.00	0.00
B. caballi	IFA	57	24	81	70.37	5.07
B. caballi	PCR	0	43	43	0.00	0.00
B. (T.) equi	IFA	30	51	81	37.04	5.37
B. (T.) equi	PCR	1	42	43	2.33	2.30
Babesia/Theileria spp.	RLB	9	31	40	22.50	6.60
T. annulata	PCR	0	33	33	0.00	0.00
Cattle
Anaplasma spp.	cELISA	627	470	1097	57.16	1.49
A. marginale	PCR	14	128	142	9.86	2.50
A. phagocytophilum	PCR	13	65	78	16.67	4.22
A. phagocytophilum	IFA	27	141	168	16.07	2.83
B. bigemina	PCR	1	12	13	7.69	7.39
B. bigemina	IFA	58	153	211	27.49	3.07
B. bovis	PCR	2	57	59	3.39	2.36
B. bovis	IFA	72	239	311	23.15	2.39
Babesia/Theileria spp.	RLB	138	216	354	38.98	2.59
Babesia/Theileria spp.	PCR	4	18	22	18.18	8.22
C. burnetii	PCR	0	9	9	0.00	0.00
T. annulata	PCR	12	82	94	12.77	3.44
Sheep
Anaplasma spp.	cELISA	151	66	217	69.59	3.12
Anaplasma spp.	PCR	14	48	62	22.58	5.31
A. marginale	PCR	3	88	91	3.30	1.87
A. phagocytophilum	PCR	3	87	90	3.33	1.89
A. phagocytophilum	IFA	17	136	153	11.11	2.54
Babesia spp.	PCR	2	14	16	12.50	8.27
Babesia/Theileria spp.	RLB	57	141	198	28.79	3.22
Babesia/Theileria spp.	PCR	4	37	41	9.76	4.63
C. burnetii	PCR	1	17	18	5.56	5.40
C. burnetii	IFA	0	37	37	0.00	0.00
T. annulata	PCR	0	21	21	0.00	0.00
Goats
Anaplasma spp.	cELISA	10	12	22	45.45	10.62
A. marginale	PCR	3	13	16	18.75	9.76
A. phagocytophilum	PCR	0	48	48	0.00	0.00
A. phagocytophilum	IFA	0	13	13	0.00	0.00
Babesia spp.	PCR	1	12	13	7.69	7.39
Babesia/Theileria spp.	RLB	3	24	27	11.11	6.05
Babesia/Theileria spp.	PCR	18	5	23	78.26	8.60
C. burnetii	PCR	0	7	7	0.00	0.00
T. annulata	PCR	0	49	49	0.00	0.00
Pigs
Anaplasma spp.	PCR	1	27	28	3.57	3.51
Ehrlichia spp.	PCR	0	97	97	0.00	0.00
B. bigemina	PCR	0	18	18	0.00	0.00
Babesia spp.	PCR	0	23	23	0.00	0.00
Babesia/Theileria spp.	RLB	0	8	8	0.00	0.00
Babesia/Theileria spp.	PCR	0	194	194	0.00	0.00
T. annulata	PCR	0	20	20	0.00	0.00
Dogs
A. phagocytophilum	IFA	39	48	87	44.83	5.33
A. phagocytophilum	PCR	0	2	2	0.00	0.00
Anaplasma spp.	PCR	12	18	30	40.00	8.94
B. canis	IFA	16	112	128	12.50	2.92
B. canis	PCR	5	2	7	71.43	17.07
B. microti	IFA	0	8	8	0.00	0.00
B. canis	IFA	1	2	3	33.33	27.22
Babesia/Theileria spp.	PCR	0	8	8	0.00	0.00
C. burnetii	IFA	2	23	25	8.00	5.43
E. canis	PCR	0	51	51	0.00	0.00
Ehrlichia spp.	PCR	1	4	5	20.00	17.89
R. conorii	PCR	7	44	51	13.73	4.82
R. ricketsii	IFA	1	31	32	3.13	3.08
R. ricketsii	PCR	0	4	4	0.00	0.00

IFA, indirect immunofluorescence antibody; PCR, polymerase chain reaction; RLB, reverse line blot; cELISA, competitive ELISA.

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Seasonal prevalence of *Anaplasma phagocytophilum*, *Babesia caballi* and *B. (T.) equi* in horses in Sicily. (a) Seroprevalence determined by indirect immunofluorescence antibody. (b) Prevalence determined by PCR. Values represent mean ± SE.

Donkeys

A similar number of serological (n = 236) and DNA (n = 232) tests were conducted on donkey samples (Table 1). Similar to results obtained for horses, the seroprevalence was higher for B. caballi (χ² = 41.24, P = 0.00) and B. equi (χ² = 6.24, P = 0.01) than for A. phagocytophilum. However, in donkeys the seroprevalence was higher for B. caballi than for B. (T.) equi (χ² = 18.10, P = 0.00).

Cattle

Cattle are the most abundant domestic species in Sicily. Therefore, the number of serological (n = 1787) and DNA (n = 771) tests was comparatively high (Table 1). Anaplasma spp. presented higher (P < 0.05) seropre-valence than other TBP analysed. However, Babesia/Theileria spp. had the highest prevalence using DNA tests (χ² = 35.46, P = 0.00). By PCR, the prevalence of A. phagocytophilum and T. annulata was higher than that of B. bovis (χ² = 6.07, P = 0.01 and χ² = 3.83, P = 0.05 respectively).

Sheep

A total number of 407 and 537 serological and DNA tests, respectively, were conducted with sheep samples (Table 1). By PCR, Anaplasma spp. displayed higher prevalence than A. marginale (χ² = 13.88, P = 0.00) and A. phagocytophilum (χ² = 13.69, P = 0.00). The seroprevalence of Anaplasma spp. was also higher than that of A. phagocytophilum (χ² = 68.93, P = 0.00).

Goats

In 183 DNA tests (Table 1), the prevalence of Babesia/Theileria spp. was higher than that of Anaplasma spp. (χ² = 12.81, P = 0.00). The prevalence of A. marginale was higher than that of A. phagocytophilum (χ² = 9.44, P = 0.00). In the 35 serological tests conducted (Table 1), the seroprevalence of Anaplasma spp. was higher than that of A. phagocytophilum (χ² = 7.34, P = 0.00).

Pigs

Only DNA tests (n = 388) were done on pig samples (Table 1). Of them, a single positive result was obtained for Anaplasma spp. without significant differences for prevalence when compared with other TBP analysed.

Dogs

Serological (n = 283) and DNA (n = 158) tests were done for TBP on dog samples (Table 1). By PCR, the prevalence of R. conorii was higher than that of E. canis (χ² = 6.51, P = 0.01). Serologically, the prevalence of A. phagocytophilum was higher than that of R. ricketsii (χ² = 18.23, P = 0.00), B. canis (χ² = 28.43, P = 0.01) and C. burnetti (χ² = 10.16, P = 0.00) respectively.

Pathogens

The analysis of pathogen species was done for those that were analysed in most domestic animals (Fig. 2). The most notable results were that (a) the seroprevalence of Anaplasma spp. was higher in sheep, followed by cattle and goats and it was zero in donkeys, (2) the highest seroprevalence of A. phagocytophilum was found in dogs and (3) the highest prevalence of A. phagocytophilum, Babesia/Theileria spp. and T. annulata was found in cattle.

Discussion

Tick-borne pathogens are endemic in Sicily as well as in other regions of Italy and Europe (Cringoli et al., 2002; Tassi et al., 2002; Parola, 2004; Sambri et al., 2004; Bernabeu-Wittel and Segura-Porta, 2005; Stanek, 2005). The observed prevalence was generally lower when estimated by DNA tests than with serological tests. Similar differences have been found in other studies and may reflect the absence of detectable levels of bacteremia in some animals (de la Fuente et al., 2005b).

The results of the observed prevalence reported herein suggest that cattle could serve as the major reservoir for Babesia and Theileria spp. while for Anaplasma spp., cattle, dogs, sheep and goats may be the most important reservoir species. We have previously shown that in Sicily infections with Anaplasma spp. occur in cattle and sheep (de la Fuente et al., 2005a,b, 2005c). The Anaplasma cELISA used in this study detects antibodies to A. marginale, A. phagocytophilum and A. ovis (Dreher et al., 2005). The PCR products were not sequenced in this study but it is known that the A. marginale PCR also detects the presence of A. ovis DNA (de la Fuente et al., 2005b). Therefore, it is likely that cattle were the major reservoir for A. marginale, dogs for A. phagocytophilum and sheep and goats for A. ovis. This possibility agrees with the difference between observed seroprevalence of Anaplasma spp. and A. phagocytophilum in cattle, sheep and goats and the host range reported for A. marginale, A. phagocytophilum and A. ovis (Kocan et al., 2004).

The most prevalent TBP in our study were Anaplasma and Babesia species. Anaplasma phagocytophilum can infect a wide range of vertebrate species including domesticated and wild animals and humans with an impact on animal and human health (Hofmann-Lehmann et al., 2004; Dumler et al., 2005; de la Fuente et al., 2005a,d, 2005e; Naranjo et al., 2006). Evidence of infection with A. phagocytophilum were found in all domestic animals studied, except for goats and pigs. However, the PCR sample positive for Anaplasma spp. in one pig could correspond to A. phagocytophilum. Infections with A. phagocytophilum have been reported in wild boar in Europe (Hulinska et al., 2004). Anaplasma marginale, which is endemic in Sicily where it causes economic loss to the cattle industry (Caracappa, 1999), had a high observed seroprevalence in cattle confirming previous reports in Sicily (de la Fuente et al., 2005b,c). Babesia spp. could also alter animal health and affect cattle production (Bock et al., 2004). As reviewed for other regions of the world (Kocan et al., 2003; Bock et al., 2004; Dumler et al., 2005; Stanek, 2005), our results suggest an increased risk for animal and human health for the most prevalent TBP identified in Sicily, Anaplasma and Babesia species.

The tick vectors for the TBP analysed herein are present in Sicily and have been found infected with these pathogens (Loria et al., 1999; Sparagano et al., 2000; Georges et al., 2001; de la Fuente et al., 2005b; Torina et al., 2006). The higher prevalence of B. caballi during spring in horses agrees with the seasonal abundance of the tick vectors Rhipicephalus spp. and Hyalomma m. marginatum (Torina et al., 2006).

The results reported herein expand our knowledge about the prevalence of TBP in Sicily. The knowledge of prevalence of TBP in domestic animals is important to understand the epidemiology of TBD and may help to implement measures to diagnose, treat and control transmission to humans and animals (Dehaumont, 2004; Bratton and Corey, 2005).

Acknowledgements

This research was funded by The Ministry of Health, Italy. Dr R. Böse (Institute of Parasitology, School of Veterinary Medicine, Hannover, Germany) is acknowledged for providing B. canis antigens for IFA test.

References

Battsetseg, B., S. Lucero, X. Xuan, F. C. Claveria, N. Inoue, A. Alhassan, T. Kanno, I. Igarashi, H. Nagasawa, T. Mikami, and K. Fujisaki, 2002: Detection of natural infection of Boophilus microplus with Babesia equi and Babesia caballi in Brazilian horses using nested polymerase chain reaction. Vet. Parasitol. 107, 351–357.
10.1016/S0304-4017(02)00131-0
PubMed Web of Science® Google Scholar
Bernabeu-Wittel, M., and F. Segura-Porta, 2005: Rickettsioses. Enferm. Infecc. Microbiol. Clin. 23, 163–172.
10.1157/13072167
PubMed Web of Science® Google Scholar
Bock, R., L. Jackson, A. De Vos, and W. Jorgensen, 2004: Babesiosis of cattle. Parasitology 129, S247–S269.
10.1017/S0031182004005190
PubMed Web of Science® Google Scholar
Bown, K. J., M. Begon, M. Bennett, Z. Woldehiwet, and N. H. Ogden, 2003: Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerg. Infect. Dis. 9, 63–70.
10.3201/eid0901.020169
PubMed Web of Science® Google Scholar
Bratton, R. L., and R. Corey, 2005: Tick-borne disease. Am. Fam. Physician. 71, 2323–2330.
PubMed Web of Science® Google Scholar
Caccio, S. M., B. Antunovic, A. Moretti, V. Mangili, A. Marinculic, R. R. Baric, S. B. Slemenda, and N. J. Pieniazek, 2002: Molecular characterisation of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Vet. Parasitol. 106, 285–292.
10.1016/S0304-4017(02)00112-7
CAS PubMed Web of Science® Google Scholar
Caracappa, S., 1989: Rickettsiosi: Epidemiologia, Diagnostica di Laboratorio Negli Animali e Nei Prodotti di Origine Animale. Instituto Zooprofilattico Sperimentale della Sicilia, Tipografia Litografia Emilio Bono, Torino, Italy.
Web of Science® Google Scholar
Caracappa, S., 1999: Livestock production and animal health in Sicily, Italy. Parassitologia 41 (Suppl. 1), 17–23.
PubMed Google Scholar
Caracappa, S., G. Tumino, F. Campo, and F. Scarlata, 1986: Q fever in Sicily. Acta Medit. Patol. Inf. Trop. 5, 345–350.
Google Scholar
Carret, C., F. Walas, B. Carcy, N. Grande, E. Precigout, K. Moubri, T. P. Schetters, and A. Gorenflot, 1999: Babesia canis canis, Babesia canis vogali, Babesia canis rossi: Differentiation of the three subspecies by a restriction fragment length polymorphism analysis on amplified small subunit ribosomal RNA genes. J. Eukaryot. Microbiol. 46, 298–303.
10.1111/j.1550-7408.1999.tb05128.x
CAS PubMed Web of Science® Google Scholar
Cringoli, G., D. Otranto, G. Testini, V. Buono, G. Di Giulio, D. Traversa, R. Lia, L. Rinaldi, V. Veneziano, and V. Puccini, 2002: Epidemiology of bovine tick-borne diseases in southern Italy. Vet. Res. 33, 421–428.
10.1051/vetres:2002028
PubMed Web of Science® Google Scholar
D'Oliveira, C., Van der Weide, M., M. A. Habela, P. Jacquiet, and F. Jongejan, 1995: Detection of Theileria annulata in blood samples of carriers by PCR. J. Clin. Microbiol. 33, 1665–2669.
PubMed Web of Science® Google Scholar
Dehaumont, P., 2004: OIE International standards on antimicrobial resistance. J. Vet. Med. B 51, 411–414.
10.1111/j.1439-0450.2004.00784.x
CAS PubMed Web of Science® Google Scholar
Dreher, U. M., De La Fuente, J., R. Hofmann-Lehmann, M. L. Meli, N. Pusterla, K. M. Kocan, Z. Woldehiwet, U. Braun, G. Regula, K. D. C. Staerk, and H. Lutz, 2005: Serologic cross-reactivity between Anaplasma marginale and Anaplasma phagocytophilum. Clin. Diagn. Lab. Immunol. 12, 1177–1183.
CAS PubMed Web of Science® Google Scholar
Dumler, J. S., K. S. Choi, J. C. Garcia-Garcia, N. S. Barat, D. G. Scorpio, J. W. Garyu, D. J. Grab, and J. S. Bakken, 2005: Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg. Infect. Dis. 11, 1828–1834.
10.3201/eid1112.050898
PubMed Web of Science® Google Scholar
Figueroa, J. V., L. P. Chieves, G. S. Johnson, and G. M. Buening, 1993: Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Vet. Parasitol. 50, 69–81.
10.1016/0304-4017(93)90008-B
CAS PubMed Web of Science® Google Scholar
De La Fuente, J., E. J. Golsteyn Thomas, R. A. Van Den Bussche, R. G. Hamilton, E. E. Tanaka, S. E. Druhan, and K. M. Kocan, 2003: Characterization of Anaplasma marginale isolated from North American bison. Appl. Environ. Microbiol. 69, 5001–5005.
10.1128/AEM.69.8.5001-5005.2003
CAS PubMed Web of Science® Google Scholar
De La Fuente, J., A. Lew, H. Lutz, M. L. Meli, R. Hofmann-Lehmann, V. Shkap, T. Molad, A. J. Mangold, C. Almazán, V. Naranjo, C. Gortázar, A. Torina, S. Caracappa, A. L. García-Pérez, M. Barral, B. Oporto, L. Ceci, G. Carelli, E. F. Blouin, and K. M. Kocan, 2005a: Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim. Health Res. Rev. 6, 75–89.
10.1079/AHR2005104
CAS PubMed Google Scholar
De La Fuente, J., A. Torina, S. Caracappa, G. Tumino, R. Furlá, C. Almazán, and K. M. Tocan, 2005b: Serologic and molecular characterization of Anaplasma species infection in farm animals and ticks from Sicily. Vet. Parasitol. 133, 357–362.
10.1016/j.vetpar.2005.05.063
CAS PubMed Web of Science® Google Scholar
De La Fuente, J., A. Torina, V. Naranjo, S. Caracappa, J. Vicente, A. J. Mangold, D. Vicari, A. Alongi, S. Scimeca, and K. M. Kocan, 2005c: Genetic diversity of Anaplasma marginale strains from cattle farms with different husbandry systems in the Province of Palermo, Sicily. J. Vet. Med. B 52, 226–229.
10.1111/j.1439-0450.2005.00851.x
CAS PubMed Web of Science® Google Scholar
De La Fuente, J., A. Torina, V. Naranjo, S. Caracappa, V. Di Marco, A. Alongi, M. Russo, A. R. Maggio, and K. M. Kocan, 2005d: Infection with Anaplasma phagocytophilum in a seronegative patient in Sicily, Italy: case report. Ann. Clin. Microbiol. Antimicrob. 4, 15.
10.1186/1476-0711-4-15
CAS PubMed Google Scholar
De La Fuente, J., V. Naranjo, F. Ruiz-Fons, U. Höfle, I. G. Fernández de Mera, D. Villanúa, C. Almazán, A. Torina, S. Caracappa, K. M. Kocan, and C. Gortázar, 2005e: Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Dis. 5, 390–401.
10.1089/vbz.2005.5.390
PubMed Web of Science® Google Scholar
Georges, K., G. R. Loria, S. Riili, A. Greco, S. Caracappa, F. Jongejan, and O. Sparagano, 2001: Detection of haemoparasites in cattle by reverse line blot hybridization with a note on the distribution of ticks in Sicily. Vet. Parasitol. 99, 273–286.
10.1016/S0304-4017(01)00488-5
CAS PubMed Web of Science® Google Scholar
Gubbels, J. M., A. P. De Vos, M. Van der Weide, J. Viseras, L. M. Schouls, E. De Vries, and F. Jongejan, 1999: Simultaneous detection of bovine Theileria and Babesia spp. by reverse line blot hybridization. J. Clin. Microbiol. 37, 1782–1789.
CAS PubMed Web of Science® Google Scholar
Hofmann-Lehmann, R., M. L. Meli, U. M. Dreher, E. Gönczi, P. Deplazes, U. Braun, M. Engels, J. Schüpbach, K. Jörger, R. Thoma, C. Griot, K. Stärk, B. Willi, J. Schmidt, K. M. Kocan, and H. Lutz, 2004: Concurrent infections with vector-borne pathogens as etiology of fatal hemolytic anemia in a cattle herd from Switzerland. J. Clin. Microbiol. 42, 3775–3780.
10.1128/JCM.42.8.3775-3780.2004
PubMed Web of Science® Google Scholar
Hulinska, D., K. Langrova, M. Pejcoch, and I. Pavlasek, 2004: Detection of Anaplasma phagocytophilum in animals by real-time polymerase chain reaction. APMIS 112, 239–247.
10.1111/j.1600-0463.2004.apm11204-0503.x
CAS PubMed Web of Science® Google Scholar
Knowles, D. P., S. Torioni de Echaide, G. H. Palmer, T. C. McGuire, D. Stiller, and T. F. McElwain, 1996: Antibody against an Anaplasma marginale MSP5 epitope common to tick and erythrocyte stages identifies persistently infected cattle. J. Clin. Microbiol. 34, 2225–2230.
PubMed Web of Science® Google Scholar
Kocan, K. M., J. De La Fuente, A. A. Guglielmone, and R. D. Meléndez, 2003: Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin. Microbiol. Rev. 16, 698–712.
10.1128/CMR.16.4.698-712.2003
PubMed Web of Science® Google Scholar
Kocan, K. M., J.De La Fuente, E. F. Blouin, and J. C. Garcia-Garcia, 2004: Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 125, S285–S300.
10.1017/S0031182003004700
Web of Science® Google Scholar
Loria, G. R., S. Riili, F. Vitale, A. Greco, and O. Sparagano, 1999: Clinical and laboratory studies on theileriosis outbreaks in Sicily, Italy. Parassitologia 41, 63–67.
PubMed Google Scholar
Munderloh, U. G., S. J. Jauron, V. Fingerle, L. Hayes, J. M. Hautman, C. Nelson, B. W. Huberty, G. G. Ahlstrand, D. Greig, and M. A. Mellencamp, 1999: Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. J. Clin. Microbiol. 37, 2518–2524.
10.1128/JCM.37.8.2518-2524.1999
CAS PubMed Web of Science® Google Scholar
Nagore, D., J. García-Sanmartín, A. L. García-Pérez, R. A. Juste, and A. Hurtado, 2004: Detection and identification of equine Theileria and Babesia species by reverse line blotting: epidemiological survey and phylogenetic analysis. Vet. Parasitol. 123, 41–54.
10.1016/j.vetpar.2004.04.010
PubMed Web of Science® Google Scholar
Naranjo, V., F. Ruiz-Fons, U. Höfle, I. G. Fernández de Mera, D. Villanúa, C. Almazán, A. Torina, S. Caracappa, K. M. Kocan, C. Gortázar, and J. De La Fuente, 2006: Molecular epidemiology of human and bovine anaplasmosis in southern Europe. Ann. N. Y. Acad. Sci., 1078 in press.
10.1196/annals.1374.013
PubMed Web of Science® Google Scholar
Parola, P., 2004: Tick-borne rickettsial diseases: emerging risks in Europe. Comp. Immunol. Microbiol. Infect. Dis. 27, 297–304.
10.1016/j.cimid.2004.03.006
PubMed Web of Science® Google Scholar
Sambri, V., A. Marangoni, E. Storni, F. Cavrini, A. Moroni, M. Sparacino, and R. Cevenini, 2004: Tick borne zoonosis: selected clinical and diagnostic aspects. Parassitologia 46, 109–113.
CAS PubMed Google Scholar
Schnittger, L., H. Yin, B. Qi, M. J. Gubbels, D. Beyer, S. Niemann, F. Jongejan, and J. S. Ahmed, 2004: Simultaneous detection and differentiation of Theileria and Babesia parasites infecting small ruminants by reverse line blotting. Parasitol. Res. 92, 189–196.
10.1007/s00436-003-0980-9
PubMed Web of Science® Google Scholar
Sparagano, O., G. R. Loria, M. J. Gubbels, A. P. De Vos, S. Caracappa, and F. Jongejan, 2000: Integrated molecular diagnosis of Theileria and Babesia species of cattle in Italy. Ann. N. Y. Acad. Sci. 916, 533–539.
10.1111/j.1749-6632.2000.tb05332.x
CAS PubMed Web of Science® Google Scholar
Stanek, G., 2005: Tick-borne pathogens in Central Europe. Wien. Klin. Wochenschr. 117, 373–380.
10.1007/s00508-005-0368-1
PubMed Web of Science® Google Scholar
Tassi, P., G. Carelli, and L. Ceci, 2002: Tick-borne diseases (TBDs) of dairy cows in a Mediterranean environment: a clinical, serological, and hematological study. Ann. N.Y. Acad. Sci. 969, 314–317.
10.1111/j.1749-6632.2002.tb04398.x
CAS PubMed Web of Science® Google Scholar
To, H., N. Kako, G. Q. Zhang, H. Otsuka, M. Ogawa, O. Ochiai, S. V. Nguyen, T. Yamaguchi, H. Fukushi, N. Nagaoka, M. Akiyama, K. Amano, and K. Hirai, 1996: Q fever pneumonia in children in Japan. J. Clin. Microbiol. 34, 647–651.
10.1128/JCM.34.3.647-651.1996
CAS PubMed Web of Science® Google Scholar
Torina, A., C. Khoury, S. Caracappa, and M. Maroli, 2006: Ticks infesting livestock on farms in Western Sicily, Italy. Exp. Appl. Acarol. 38, 75–86.
10.1007/s10493-005-5629-1
PubMed Web of Science® Google Scholar
Tzianabos, T., B. E. Anderson, and J. E. McDade, 1989: Detection of Rickettsia rickettsii DNA in clinical specimens by using polymerase chain reaction technology. J. Clin. Microbiol. 27, 2866–2868.
10.1128/jcm.27.12.2866-2868.1989
CAS PubMed Web of Science® Google Scholar
Wen, B., Y. Rikihisa, J. M. Mott, R. Greene, H. Y. Kim, N. Zhi, G. C. Couto, A. Unver, and R. Bartsch, 1997: Comparison of nested PCR with immunofluorescent-antibody assay for detection of Ehrlichia canis infection in dogs treated with doxycycline. J. Clin. Microbiol. 35, 1852–1855.
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume54, Issue1

February 2007

Pages 8-15

Observed Prevalence of Tick-borne Pathogens in Domestic Animals in Sicily, Italy during 2003–2005

Summary

Introduction