Ixodid ticks and zoonotic tick-borne pathogens of the Western Balkans

Kapo, Naida; Zuber Bogdanović, Ivana; Gagović, Ema; Žekić, Marina; Veinović, Gorana; Sukara, Ratko; Mihaljica, Darko; Adžić, Bojan; Kadriaj, Përparim; Cvetkovikj, Aleksandar; Djadjovski, Igor; Potkonjak, Aleksandar; Velo, Enkelejda; Savić, Sara; Tomanović, Snežana; Omeragić, Jasmin; Beck, Relja; Hodžić, Adnan

doi:10.1186/s13071-023-06116-1

Parasites & Vectors

Table 2 Zoonotic tick-borne pathogens affecting animals in the Western Balkans

From: Ixodid ticks and zoonotic tick-borne pathogens of the Western Balkans

Country	Pathogen	Host^a	Prevalence (%)	Method	References
Albania	Anaplasma spp./Ehrlichia spp.	Rh. bursa Rh. sanguineus,	12.5–14.3	PCR, RLBH	[17]
	E. canis	Rh. sanguineus	3.6	PCR	[17]
	Rickettsia IRS3	Rh. bursa, Hy. marginatum	6.2–43.3	PCR	[17]
	R. helvetica	Rh. sanguineus, Rh. bursa	3.6–6.2	PCR	[17]
	R. conorii	Rh. sanguineus, Rh. bursa, Hy. marginatum	3.1–26.6	PCR	[17]
	C. burnetii	Cattle, sheep, goat	9.1	ELISA	[22]
	B. garinii	Dog	49.4	ELISA	[21]
	CCHFV	Rh. bursa, Hy. marginatum, cattle, sheep, goat	0.03–88.3	IFAT, ELISA, PCR	[27,28,29,30,31,32]
Bosnia and Herzegovina	B. divergens	Cattle, I. ricinus	n/a	Blood smear, PCR-Seq	[36, 37]
	A. phagocytophilum	D. reticulatus, dog	1.1–4.9	PCR-Seq, mf qPCR	[40, 44]
	A. phagocytophilum	Dog	24	qPCR	[41]
	A. phagocytophilum/A. platys	Dog	0.5	qPCR	[41]
	A. phagocytophilum/A. platys	Dog	20.4	SNAP 4Dx	[41]
	E. canis/E. ewingii	Dog	0.2	SNAP 4Dx	[41]
	R. monacensis	I. ricinus	1.1	PCR-Seq	[44]
	R. helvetica	I. ricinus	5.7	PCR-Seq	[44]
	R. raoultii	D. reticulatus	5.7	PCR-Seq	[44]
	R. slovaca	D. reticulatus, D. marginatus	8.0	PCR-Seq	[44]
	F. tularensis subsp. holarctica	D. marginatus	1.1	PCR-Seq	[44]
	TBEV (Bosnia lineage)	I. ricinus	n/a	Isolation, PCR, genome seq	[45, 227]
	CCHFV	Hy. marginatum^b, cattle, sheep	0.4^a–15.0	IFAT, ELISA, RT-PCR	[46, 47]
Croatia	B. microti	Rodent	3.3–14.0	RT-PCR, PCR-Seq	[79, 221]
	Anaplasma spp.	Dog, rodent	4.5–6.2 (dogs), 1.65 (rodents)	SNAP 4Dx, PCR	[49, 70, 71]
	A. phagocytophilum	I. ricinus, various animals	< 38.0	IFAT, PCR-Seq	[50, 75, 77]
	A. phagcytophilum	Horse	Case report	PCR-Seq	[75, 220]
	A. phagocytophilum	Dog	0.3–10.5%	PCR-Seq	[50, 72]
	Ehrlichia spp.	Rodent	0.8	PCR-Seq	[49]
	E. canis	Dog	0.46	SNAP 4Dx	[70, 71]
	N. mikurensis	Dog	4.6	PCR-Seq	[50]
	Rickettsia spp.	Rodent	1.8–4.3	RT- PCR	[63]
	SFG Rickettsiae	Ticks from sheep, goat, cattle	1.6	PCR-Seq	[65]
	R. helvetica	I. ricinus, D. reticulatus	6.2–10.0	PCR-Seq	[48, 68]
	R. raoultii	I. ricinus	0.08	PCR	[48]
	R. slovaca	D. reticulatus, D. marginatus	2.0–60.0	PCR-Seq	[48, 65, 66, 68]
	R. conorii	Dog, cattle, goat, sheep, ticks	23–51.0	IFAT, PCR-Seq	[61, 66, 68, 145]
	R. aeshlimanii	Hy. marginatum	26.1–64.7	PCR-Seq	[65, 66]
	R. rhipicephali	Rh. turanicus	9.1	PCR-Seq	[66]
	R. felis-like	Hae. sulcate from sheep, goats	19.6–26.0	PCR-Seq	[67]
	F. tularensis	Rodent	0.8	PCR-Seq	[49]
	C. burnetii	Dog, cattle, sheep, goat, brown bear, rodents	< 16.4	CFT, IFAT, PCR-Seq	[49, 61, 222]
	B. burgdorferi s.l	I. ricinus, Dog	0.4–0.7 (dogs)	SNAP 4Dx, IFAT	[70, 71]
	B. afzelii	I. ricinus, rodent	2.0–21.5	PCR, PCR–RFLP, PCR-Seq	[49, 83, 91]
	B. garinii	I. ricinus	4.0	PCR-Seq	[223]
	B. burgdorferi s.s	I. ricinus	0.3–0.8	PCR-Seq, RLBH	[69, 223]
	B. valaisiana	I. ricinus	0.5–12.0	PCR-Seq, RLBH	[69, 223]
	B. lustaniae	I. ricinus	0.6	PCR-Seq	[69]
	B. spielmanii	I. ricinus	0.06	PCR-Seq	[69]
	B. miyamotoi	Rodent	3.7	PCR-Seq	[48, 49]
	TBEV	Ticks, animals	< 39.0	PCR, PCR-Seq, RT-PCR	[63, 115]
	BHAV	Bears, sheep	68.0 (bears), 100 (sheep)	HI, ELISA	[94, 222]
Montenegro	E. canis	Dog	19.3	IFAT, ELISA	[119]
	R. conorii	Dog	73.4	IFAT, ELISA	[119]
	C. burnetii	Sheep, dog	1.2–5.0	IFAT	[119, 120]
North Macedonia	E. canis	Dog	18.7–45.0	ELISA, PCR	[132, 133]
Serbia	CCHFV	Tick, cattle, sheep, goat	14.6–80.0	ELISA	[130, 131]
	B. microti	I. ricinus, dog	1.4–1.9	PCR-Seq	[161, 165,166,167]
	B. venatorum Anaplsma spp.	I. ricinus Ticks	2.8 19.35	PCR-Seq PCR	[165] [166]
	A. phagocytophilum	I. ricinus, D. reticulatus, Hae. concinna, dog, golden jackal	0.9–15.5	IFAT, PCR-Seq, mf qPCR	[158, 161, 163, 165, 166, 174, 176, 178, 179]
	N. mikurensis	I. ricinus	4.2	PCR-Seq	[12, 165, 166]
	E. canis	Dog	Case report, 16%	IFAT, PCR-Seq	[152, 180]
	R. monacensis	I. ricinus	14.8–22.5	PCR-Seq, mf qPCR	[165, 166, 172,173,174,175]
	R. helvetica	I. ricinus	7.4–54.0	PCR-Seq, mf qPCR	[172,173,174,175]
	R. raoultii	D. reticulatus	5.6	PCR-Seq, mf qPCR	[165, 172]
	R. conorii	Rh. sanguineus, Dog	44.8	IFAT, PCR-Seq	[176, 177]
	R. massiliae	Rh. sanguineus	0.8	PCR-Seq	[165]
	F. tularensis	I. ricinus	3.8	PCR/RFLP	[159]
	C. burnetii	I. ricinus, D. reticulatus, Hae. concinna, Rh. Sanguineus	3.8–62.9	PCR-Seq	[174, 183]
	B. burgdorferi s.l	I. ricinus, dog, rodent	8.1–54.2	DF, IFAT, ELISA, WB, PCR	[146, 147, 150,151,152, 154,155,156, 174, 176]
	B. afzelii	I. ricinus	7.0–75.0	Isolation, PCR-Seq, PCR/RFLP, RT-PCR	[151, 152, 158,159,160, 178]
	B. garinii	I. ricinus, D. reticulatus, red fox	0.8–4.9	Isolation, PCR-Seq, PCR/RPLF	[12, 152, 158,159,160,161,162, 178]
	B. burgdorferi s.s	I. ricinus, red fox	0.8–22.2	PCR-Seq, PCR/RFLP	[12, 152, 159, 178]
	B. valaisiana	I. ricinus	1.4–3.8	Isolation, PCR-Seq, PCR/RFLP, mf qPCR	[158, 160,161,162,163, 178]
	B. lusitaniae	I. ricinus, red fox	1.6–11.3	Isolation, PCR-Seq, PCR/RFLP, mf qPCR	[12, 151, 158, 160,161,162,163, 178]
	B. bavariensis	I. ricinus	2 isolates	Isolation, PCR-Seq	[162]
	B. miyamotoi	I. ricinus	1.6–6.0	PCR-Seq, mf qPCR	[160, 163]
	TBEV (EU subtype)	Horse, cattle, roe deer, wild boar, dog	2.5–17.5	Isolation, ELISA, PCR-Seq	[184, 185]

CFT Complement fixation test, DF dark field microscopy, ELISA enzyme-linked immunosorbent assay, HI hemagglutination inhibition assay, IFAT indirect immunofluorescence test, mf qPCR microfluidic real-time PCR, PCR-RFLP restriction fragment length polymorphism-PCR, PCR-Seq PCR followed by DNA sequencing, qPCR real-time PCR, RLBH reverse line blot hybridization, RT-PCR reverse transcription PCR, s.l. sensu lato, s.s. sensu stricto, WB western blot
^aD. Dermacentor, Hae. Haemaphysalis, Hy. Hyalomma, I Ixodes, Rh. Rhipicephalus
^bTick pool

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