Ticks and Tick-Borne Pathogens: Occurrence and Host Associations over Four Years of Wildlife Surveillance in the Liguria Region (Northwest Italy)
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Tick Collection and Identification
2.2. Molecular Analysis for Pathogen Detection
2.2.1. DNA/RNA Extraction
2.2.2. PCR Amplification for TBP Screening
2.2.3. PCR Amplification for TBP Confirmation and Sequencing
2.3. Database and Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Pathogen | Primers | Target Gene | Reference |
---|---|---|---|
Anaplasma spp. | 16SANA-F 5′-CAGAGTTTGATCCTGGCTCAGAACG-3′ 16SANA-R 5′-GAGTTTGCCGGGACTTCTTCT GTA-3′ | 16S rRNA | Stuen et al. [36] |
Borrelia burgdorferi s.l. | FLA1 5′-AGAGCAACTTACAGACGAAATTAAT-3′ FLA2 5′-CAAGTCTATTTTGGAAAGCACCTAA-3′ | FLA | Skotarczak et al. [37] |
Coxiella burnetii | Trans1 5′-TATGTATCCACCGTAGCCAG C-3′ Trans2 5′-CCCAACAACACCTCCTTATTC-3′ | IS1111 | Berri et al. [38] |
Rickettsia spp. | RpCS.877p 5′-GGGGGCCTGCTCACGGCGG-3′ RpCS.1258n 5′-ATTGCAAAAAGTACAGTGAACA-3′ | citrate synthase | Regnery et al. [39] |
Tick-borne encephalitis (TBE) virus | F-TBE 5′-GGGCGGTTCTTGTTCTCC-3′ R-TBE 5′-ACACATCACCTCCTTGTCAGACT-3′ TBE-Probe-WTTGAGCCACCATCACCCAGACACA | 3′ non-coding region | Schwaiger et al. [35] |
Pathogen | Primers | Target Gene | Reference |
---|---|---|---|
Rickettsia spp. | Rr190.70p 5′-ATGGCGAATATTTCTCCAAAA-3′ Rr190.701n 5′-GTTCCGTTAATGGCAGCATCT-3′ Rr190.602n 5′-AGTGCAGCATTCGCTCCCCCT-3′ | OmpA | Oteo et al. [40] |
rompB OF 5′-GTAACCGGAAGTAATCGTTTCGTAA-3′ rompB OR 5′-GCTTTATAACCAGCTAAACCACC-3′ rompB SFG IF 5′-GTTTAATACGTGCTGCTAACCAA-3′ rompB SFG IR 5′-GGTTTGGCCCATATACCATAAG-3′ | OmpB | Choi et al. [41] | |
RpCS.877p 5′-GGGGGCCTGCTCACGGCGG-3′ RpCS.1258n 5′-ATTGCAAAAAGTACAGTGAACA-3′ | Citrate synthase | Regnery et al. [39] | |
Anaplasma spp. | EE1 5′-TCCTGGCTCAGAACGAACGCTGGCGGC-3′ EE2 5′-AGTCACTGACCCAACCTTAAATGGCTG-3′ EE3 5′-GTCGAACGGATTATTCTTTATAGCTTGC-3′ EE4 5′-CCCTTCCGTTAAGAAGGATCTAATCTCC-3′ | 16S-rRNA | Richter et al. [42] |
Coxiella burnetii | sIS1pri F 5′-CGGGTTAAGCGTGCTCAGTAT-3′ sIS1pri R 5′-TCCACACGCTTCCATCACCAC-3′ Tqpro sIS1 (5′-FAM/3′-BHQ1) 5′-AGCCCACCTTAAGACTGGCTACGGTGGAT-3′ | IS1111 | Schets et al. [43] |
Borrelia burgdorferi s.l. | Bor_OspA_F 5′-AATATTTATTGGGAATAGGTCTAA-3′ Bor_OspA_R 5′-CACCAGGCAAATCTACTGA-3′ Bor_OspA_TM (5′-FAM/3′-BHQ1) 5′-TTAATAGCATGYAAGCAAAATGTTAGCA-3′ | OspA | Briciu et al. [44] |
Identified Tick Species | Roe Deer (n Host = 105) | Fallow Deer (n Host = 49) | Chamois (n Host = 2) | Wild Boar (n Host = 61) | Overall |
---|---|---|---|---|---|
Ixodes ricinus | 276 (91.1%) *** | 168 (74.7%) ** | 0 *** | 12 (8.2%) *** | 456 (66.8%) |
Dermacentor marginatus | 0 *** | 0 *** | 0 ns | 108 (73.5%) *** | 108 (15.8%) |
Rhipicephalus sanguineus s.s. | 24 (7.9%) *** | 53 (23.6%) *** | 3 (37.5%) ns | 27 (18.4%) ns | 107 (15.7%) |
Rhipicephalus spp. | 3 (1.0%) ns | 3 (1.3%) ns | 0 ns | 0 ns | 6 (0.9%) |
Haemaphysalis punctata | 0 * | 1 (0.4%) ns | 5 (62.5%) *** | 0 ns | 6 (0.9%) |
Overall number of collected ticks | 303 | 225 | 8 | 147 | 683 |
Identified Pathogen | Tick Species | Host Species | PCR and Sequencing (CRABART): N of Confirmed Positive Pools |
---|---|---|---|
Rickettsia slovaca | Ixodes ricinus | Roe deer | 20 |
Fallow deer | 5 | ||
Dermacentor marginatus | Wild boar | 6 | |
Rhipicephalus sanguineus | Fallow deer | 2 | |
Roe deer | 1 | ||
Rickettsia monacensis | Ixodes ricinus | Roe deer | 13 |
Fallow deer | 4 | ||
Dermacentor marginatus | Wild boar | 1 | |
Rickettsia helvetica | Ixodes ricinus | Roe deer | 3 |
Fallow deer | 1 | ||
Rickettsia massiliae | Ixodes ricinus | Roe deer | 1 |
Rickettsia raoultii | Dermacentor marginatus | Wild boar | 1 |
Anaplasma phagocytophilum | Ixodes ricinus | Fallow deer | 3 |
B. burgdorferi s.l. | Ixodes ricinus | Roe deer | 1 |
Coxiella burnetii | Ixodes ricinus | Roe deer | 0 |
Host | Tick Species | N Ticks | Tested Pools | Rickettsia slovaca % [95% CI] | Rickettsia monacensis % [95% CI] | Rickettsia helvetica % [95% CI] | Rickettsia massiliae % [95% CI] | Rickettsia raoultii % [95% CI] | Anaplasma sp. % [95% CI] | Borrellia sp. [95% CI] |
---|---|---|---|---|---|---|---|---|---|---|
Chamois | Haemaphysalis punctata | 5 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Chamois | Rhipicephalus sanguineus s.s. | 3 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Roe deer | Ixodes ricinus | 263 | 103 | 19.42 [12.28–28.38] | 11.65 [6.17–19.47] | 2.91 [0.60–8.28] | 0.97 [0.02–5.29] | 0 | 0 | 0.97 [0.02–5.29] |
Roe deer | Rhipicephalus sanguineus s.s | 24 | 3 | 33.33 [0.84–90.57] | 0 | 0 | 0 | 0 | 0 | 0 |
Roe deer | Rhipicephalus spp. | 3 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Wild boar | Dermacentor marginatus | 106 | 50 | 12.00 [4.53–24.31] | 2.00 [0.05–13.65] | 0 | 0 | 2.00 [0.05–13.65] | 0 | 0 |
Wild boar | Ixodes ricinus | 12 | 8 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Wild boar | Rhipicephalus sanguineus s.s. | 28 | 3 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Fallow deer | Haemaphysalis punctata | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Fallow deer | Ixodes ricinus | 167 | 36 | 13.89 [4.67–29.50] | 8.33 [1.75–22.47] | 2.78 [0.07–14.53] | 0 | 0 | 8.33 [1.75–22.47] | 0 |
Fallow deer | Rhipicephalus sanguineus s.s. | 51 | 12 | 8.33 [0.21–38.48] | 0 | 0 | 0 | 0 | 0 | 0 |
Fallow deer | Rhipicephalus spp. | 5 | 3 | 33.33 [0.84–90.57] | 0 | 0 | 0 | 0 | 0 | 0 |
Factors | Category | n° Pool | Rickettsia spp. Prevalence | Chi Square | p Value |
---|---|---|---|---|---|
Host | Chamois | 2 | 0.00% | 10.83 | 0.01 |
Roe deer | 107 | 34.58% | |||
Wild boar | 61 | 13.11% | |||
Fallow deer | 52 | 21.15% | |||
Tick species | Dermacentor marginatus | 50 | 12.73% | 6.28 | 0.04 |
Ixodex ricinus | 147 | 37.42% | |||
Rhipicephalus spp. | 23 | 5.85% | |||
Season | Autumn | 37 | 0.00% | 25.67 | <0.0001 |
Spring | 30 | 7.69% | |||
Winter | 155 | 34.84% | |||
Area | East | 12 | 0.00% | 4.28 | 0.04 |
West | 210 | 26.67% |
Parameter | Baseline | OR | 95% CI OR | Wald χ2 | p-Value χ2 |
---|---|---|---|---|---|
host | Roe deer | 3.2 | 1.4–7.4 | 10.1384 | 0.0015 |
season | winter | 12.9 | 2.9–57.0 | 11.9671 | 0.0005 |
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Guardone, L.; Nogarol, C.; Accorsi, A.; Vitale, N.; Listorti, V.; Scala, S.; Brusadore, S.; Miceli, I.N.; Wolfsgruber, L.; Guercio, A.; et al. Ticks and Tick-Borne Pathogens: Occurrence and Host Associations over Four Years of Wildlife Surveillance in the Liguria Region (Northwest Italy). Animals 2024, 14, 2377. https://doi.org/10.3390/ani14162377
Guardone L, Nogarol C, Accorsi A, Vitale N, Listorti V, Scala S, Brusadore S, Miceli IN, Wolfsgruber L, Guercio A, et al. Ticks and Tick-Borne Pathogens: Occurrence and Host Associations over Four Years of Wildlife Surveillance in the Liguria Region (Northwest Italy). Animals. 2024; 14(16):2377. https://doi.org/10.3390/ani14162377
Chicago/Turabian StyleGuardone, Lisa, Chiara Nogarol, Annalisa Accorsi, Nicoletta Vitale, Valeria Listorti, Sonia Scala, Sonia Brusadore, Ilaria Nina Miceli, Lara Wolfsgruber, Annalisa Guercio, and et al. 2024. "Ticks and Tick-Borne Pathogens: Occurrence and Host Associations over Four Years of Wildlife Surveillance in the Liguria Region (Northwest Italy)" Animals 14, no. 16: 2377. https://doi.org/10.3390/ani14162377