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Seroprevalence and risk factors associated with Ehrlichia canis, Anaplasma spp., Borrelia burgdorferi sensu lato, and D. immitis in hunting dogs from southern Italy

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Abstract

Canine vector-borne diseases (CVBDs) are caused by a range of pathogens transmitted to dogs by arthropods. The present study investigates Ehrlichia canis, Anaplasma spp., Borrelia burgdorferi sensu lato, and Dirofilaria immitis seroprevalences in hunting dogs from southern Italy. Dogs (no. 1335) were tested using a commercial in-clinic enzyme-linked immunosorbent assay kit. Odds ratios (ORs) were calculated by logistic regression analysis to identify risk factors. Overall, 138/1335 dogs (10.3%) were seroreactive to at least one CVBD pathogen. E. canis, Anaplasma spp., B. burgdorferi s.l., and D. immitis seroprevalences were 7.6, 4.4, 0.3, and 0.2%, respectively. E. canis and Anaplasma spp. co-exposures were found in 30 dogs (2.2%), compared with Anaplasma spp. and B. burgdorferi s.l. co-exposures in 2 dogs (0.1%). Adult age was a risk factor for E. canis (OR 2.35) seroreactivity whereas hunting fur-bearing animals for E. canis (OR 4.75) and Anaplasma spp. (OR 1.87), respectively. The historical presence of tick infestation was identified as a risk factor for positivity to E. canis (OR 2.08) and Anaplasma spp. (OR 2.15). Finally, larger dog pack size was significantly associated with E. canis (OR 1.85) and Anaplasma spp. (OR 2.42) exposures. The results of the present survey indicated that hunting dog populations are at relative risk of CVBDs in southern Italy. Further studies are needed to evaluate the role of hunting dogs in the epidemiology of vector-borne organisms due to sharing common environments with wild, sympatric animal populations.

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References

  • Antognoni MT, Veronesi F, Morganti G, Mangili V, Fruganti G, Miglio A (2014) Natural infection of Anaplasma platys in dogs from Umbria region (Central Italy). Vet Ital 50:45–56

    Google Scholar 

  • Arraga-Alvarado CM, Qurollo BA, Parra OC, Berrueta MA, Hegarty BC, Breitschwerdt EB (2014) Case report: molecular evidence of Anaplasma platys infection in two women from Venezuela. Am J Trop Med Hyg 91:1161–1165

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouza-Mora L, Dolz G, Solórzano-Morales A, Romero-Zuñiga JJ, Salazar-Sánchez L, Labruna MB, Aguiar DM (2017) Novel genotype of Ehrlichia canis detected in samples of human blood bank donors in Costa Rica. Ticks Tick Borne Dis 8:36–40

    Article  PubMed  Google Scholar 

  • Breitschwerdt EB, Hegarty BC, Qurollo BA, Saito TB, Maggi RG, Blanton LS, Bouyer DH (2014) Intravascular persistence of Anaplasma platys, Ehrlichia chaffeensis, and Ehrlichia ewingii DNA in the blood of a dog and two family members. Parasit Vectors 7:298

    Article  PubMed  PubMed Central  Google Scholar 

  • Bush BM (1991) Part 1: Haematology. In: Interpretation of laboratory results for small animal clinicians, 1st edn. Blackwell Scientific Publications, Oxford, UK, pp. 31–220

  • de Caprariis D, Dantas-Torres F, Capelli G, Mencke N, Stanneck D, Breitschwerdt EB, Otranto D (2011) Evolution of clinical, haematologicl and biochemical findings in young dogs naturally infected by vector-borne pathogens. Vet Microbiol 149:206–212

    Article  PubMed  Google Scholar 

  • Cardoso L, Mendão C, Madeira de Carvalho L (2012) Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal—a National serological study. Parasit Vectors 5:62

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardoso L, Cortes HCE, Reis A, Rodrigues P, Simoes M, Lopes AP, Vila-Vicosa MJ, Talmi-Frank D, Eyal O, Solano-Gallego L, Baneth G (2013) Prevalence of Babesia microti-like infection in red foxes (Vulpes vulpes) from Portugal. Vet Parasitol 19:90–95

    Article  Google Scholar 

  • Carpi G, Bertolotti L, Pecchioli E, Cagnacci F, Rizzoli A (2009) Anaplasma phagocytophilum groEL gene heteroneity in Ixodes ricinus larvae feeding on roe deer in northeastern Italy. Vector Borne Zoonotic Dis 9:179–184

    Article  PubMed  Google Scholar 

  • Corrain R, Di Francesco A, Bolognini M, Ciucci P, Baldelli R, Guberti V (2007) Serosurvey for CPV-2, distemper virus, ehrlichiosis and leishmaniosis in free-ranging dogs in Italy. Vet Rec 160:91–92

    Article  CAS  PubMed  Google Scholar 

  • Costa LM Jr, Rembeck K, Ribeiro MF, Beelitz P, Pfister K, Passos LM (2007) Sero-prevalence and risk indicators for canine ehrlichiosis in three rural areas of Brazil. Vet J 174:673–676

    Article  PubMed  Google Scholar 

  • Courtney CH, Zeng QY (2001) Comparison of heartworm antigen test kit performance in dogs having low heartworm burdens. Vet Parasitol 96:317–322

    Article  CAS  PubMed  Google Scholar 

  • De la Fuente J, Torina A, Naranjo V, Nicosia S, Alongi A, La Mantia F, Kocan KM (2006) Molecular characterization of Anaplsma platys strains from dogs in Sicily, Italy. BMC Vet Res 2:24

    Article  PubMed  PubMed Central  Google Scholar 

  • De Tommasi AS, Otranto D, Dantas-Torres F, Capelli G, Breitschwerdt EB, de Caprariis D (2013) Are vector-borne pathogen co-infections complicating the clinical presentation in dogs? Parasit Vectors 6:97

    Article  PubMed  PubMed Central  Google Scholar 

  • Del Prete L, Maurelli MP, Pennacchio S, Bosco A, Musella V, Ciuca L, Cringoli G, Rinaldi L (2015) Dirofilaria immitis and Angiostrongylus vasorum: the contemporaneous detection in kennels. BMC Vet Res 11:305

    Article  PubMed  PubMed Central  Google Scholar 

  • Duscher GG, Leschnik M, Fuehrer HP, Joachim A (2015) Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. Int J Parasitol Wild 4:88–89

    Article  Google Scholar 

  • Ebani VV, Cerri D, Fratini F, Ampola M, Andreani E (2008) Seroprevalence of Anaplasma phagocytophilum in domestic and wild animals from central Italy. New Microbiol 31:371–375

    CAS  PubMed  Google Scholar 

  • Ebani VV, Bertelloni F, Turchi B, Cerri D (2013) Serological and molecular survey of Anaplasma phagocytophilum in Italian hunting dogs. Ann Agric Environ Med 20:289–292

    PubMed  Google Scholar 

  • Ebani VV, Bertelloni F, Torracca B, Cerri D (2014) Serological survey of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Ehrlichia canis infections in rural and urban dogs in Central Italy. Ann Agric Environ Med 21:671–675

    Article  PubMed  Google Scholar 

  • Ebani VV, Nardoni S, Fognani G, Mugnaini L, Bertelloni F, Rocchigiani G, Papini RA, Stefani F, Mancianti F (2015) Molecular detection of vector-borne bacteria and protozoa in healthy hunting dogs from Central Italy. Asian Pac J Trop Biomed 5:108–112

    Article  Google Scholar 

  • Genchi C, Kramer LH, Rivasi F (2011) Dirofilarial infections in Europe. Vector Borne Zoonotic Dis 10:1307–1317

    Article  Google Scholar 

  • Giangaspero A, Marangi M, Latrofa MS, Martinelli D, Traversa D, Otranto D, Genchi C (2013) Evidences of increasing risk of dirofilarioses in southern Italy. Parasitol Res 12:1357–1361

    Article  Google Scholar 

  • Giudice E, Domina F, Britti D, Di Pietro S, Pugliese A (2003) Clinical findings associated with Borrelia burgdorferi infection in the dog. Vet Res Commun 27:767–770

    Article  PubMed  Google Scholar 

  • Gómez-Morales MA, Selmi M, Ludovisi A, Amati M, Fiorentino E, Breviglieri L, Poglayen G, Pozio E (2016) Hunting dogs as sentinel animals for monitoring infections with Trichinella spp. in wildlife. Parasit Vectors 16:154

    Article  Google Scholar 

  • Greene CE, Straubinger RK, Levy SA (2012) Chapter 43: Borreliosis in: Greene CE, infectious diseases of the dog and cat, 4th edn. Saunders, Elsevier Inc, pp 453–455

    Google Scholar 

  • Hodžić A, Alic A, Fuehrer HP, Harl J, Wille-Piazzai W, Duscher GG (2015) A molecular survey of vector-borne pathogens in red foxes (Vulpes vulpes) from Bosnia and Herzegovina. Parasit Vectors 8:88

    Article  PubMed  PubMed Central  Google Scholar 

  • Hovius KE (2013) Canine borreliosis. In: Beugnet F. Guide to vector borne diseases of pets. Merial, Lyon, pp 219–229

    Google Scholar 

  • Kohn B, Silaghi C, Galke D, Arndt G, Pfister K (2011) Infection with Anaplasma phagocytophilum in dog in Germany. Res Vet Sci 91:71–76

    Article  CAS  PubMed  Google Scholar 

  • Kordick SK, Breitschwerdt EB, Hegarty BC, Southwick KL, Colitz CM, Hancock SI, Bradley JM, Rumbough R, Mcpherson JT, MacCormack JN (1999) Coinfection with multiple tick-borne pathogens in a walker hound kennel in North Carolina. J Clin Microbiol 37:2631–2638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krupka I, Knauer J, Lorentzen L, O’Connor TP, Saucier J, Straubinger RK (2009) Borrelia burgdorferi sensu lato species in Europe induce diverse immune responses against C6 peptides in infected mice. Clin Vaccine Immunol 16:1546–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laflamme DP (1997) Development and validation of a body condition score system for dogs. Canine Pract 22:10–15

    Google Scholar 

  • Latrofa MS, Dantas-Torres F, de Caprariis D, Cantacessi C, Capelli G, Lia RP, Breitschwerdt EB, Otranto D (2016) Vertical transmission of Anaplasma platys and Leishmania infantum in dogs during the first half of gestation. Parasit Vectors 9:269

    Article  PubMed  PubMed Central  Google Scholar 

  • Little SE, Heise SR, Blagburn BL, Callister SM, Mead PS (2010) Lyme borreliosis in dogs and humans in the USA. Trends Parasitol 26:213–218

    Article  PubMed  Google Scholar 

  • Mackenstedt U, Jenkins D, Roming T (2015) The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. Int J Parasitol Wildl 4:71–79

    Article  Google Scholar 

  • Mannelli D, Cerri D, Buffrini L, Rossi S, Arata T, Innocenti M, Grignolo MC, Bianchi G, Iori A, Tolari F (1999) Low risk of Lyme borreliosis in a protected area on the Thyrrhenian coast, in central Italy. Eur J Epidemiol 15:371–377

    Article  CAS  PubMed  Google Scholar 

  • McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L (2008) Heartworm disease in animals and humans. Adv Parasitol 66:193–285

    Article  PubMed  Google Scholar 

  • Mircean V, Dumitrache MO, Gyorke A, Pantchev N, Jodies R, Mihalca AD, Cozma V (2012) Seroprevalence and geographic distribution of Dirofilaria immitis and tick-borne infections (Anaplasma phagocytophilum, Borrelia burgdorfei sensu lato, and Ehrlichia canis ) in dogs from Romania. Vector Borne Zoonotic Dis 7:595–604

    Article  Google Scholar 

  • O’Connor TP (2015) SNAP assay technology. Top Companion Anim Med 30:132–138

    Article  PubMed  Google Scholar 

  • Otranto D, Dantas -Torres F (2010) Canine and feline vector-borne disease in Italy: current situation and perspectives. Parasit Vectors 3:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D, Paradies P, Testini G, Latrofa MS, Weigl S, Cantacessi C, Mencke N, de Caprariis D, Parisi V, Capelli G, Stanneck V (2008) Application of 10% imidacloprid 50% permethrin to prevent Ehrlichia canis exposure in dogs under natural conditions. Vet Parasitol 153:320–328

    Article  CAS  PubMed  Google Scholar 

  • Otranto D, Capelli G, Genchi C (2009) Changing distribution patterns of canine vector borne disease in Italy. Leishmaniosis vs. Dirofilariosis. Parasit Vectors 2(Suppl 1):S2

    Article  Google Scholar 

  • Otranto D, Testini G, Dantas-Torres F, Latrofa MS, Vissotto de Paiva Diniz PP, de Caprariis D, Lia RP, Mencke N, Stanneck D, Capelli G, Breitschwerdt EB (2010) Diagnosis of canine vector-borne disease in young dogs: a longitudinal study. J Clin Microbiol 48:3316–3324

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D, Dantas-Torres F, Brianti E, Traversa D, Petric D, Genchi C, Capelli G (2013) Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 6:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Otranto D, Cantacessi C, Pfeffer M, Dantas-Torres F, Brianti E, Deplazes P, Genchi C, Guberti V, Capelli G (2015) The role of wild canids and felids in spreading parasite to dogs and cats in Europe. Part I: protozoa and tick-borne agents. Vet Parasitol 213:12–23

    Article  PubMed  Google Scholar 

  • Pennisi MG, Caprì A, Solano-gallego L, Lombardo G, Torina A, Masucci M (2012) Prevalence of antibodies against Rickettsia conorii, Babesia canis, Ehrlichia canis and Anaplasma phagocytophilum antigens in dogs from the Stretto di Messina area (Italy). Ticks Tick Borne Dis 3:314–317

    Article  Google Scholar 

  • Perez M, Bodor M, Zhang C, Xiong Q, Rikihisa Y (2006) Human infection with Ehrlichia canis accompanied by clinical signs in Venezuela. Ann N Y Acad Sci 1078:110–117

    Article  CAS  PubMed  Google Scholar 

  • Petrie A, Watson P (2013) Experimental design and clinical trials. In: Petrie A, Watson P (eds) Statistics for veterinary and animal science, 3rd edn. John Wiley & Sons, Ltd, Oxford, pp 77–103

    Google Scholar 

  • Piantedosi D, Veneziano V, Di Muccio T, Foglia Manzillo V, Fiorentino E, Scalone A, Neola B, Di Prisco F, D’Alessio N, Gradoni L, Oliva G, Gramiccia M (2016) Epidemiological survey on Leishmania infection in red fox (Vulpes vulpes) and hunting dogs sarin the same rural area in southern Italy. Acta Parasitol 61(4):769–775

    Article  PubMed  Google Scholar 

  • Pipia AP, Varcasia A, Tosciri G, Seu S, Manunta ML, Mura MC, Sanna G, Tamponi C, Brianti E, Scala A (2014) New insights onto cardiopulmonary nematodea of dogs in Sardinia, Italy. Parasitol Res 113:1505–1059

    Article  CAS  PubMed  Google Scholar 

  • Qurollo BA, Chandrashekar R, Hegarty BC, Beall MJ, Stillman BA, Liu J, Thatcher B, Pultorak E, Cerrito B, Walsh M, Breitschwerdt EB (2014) A serological survey of tick-borne pathogens in dogs in North America and the Caribbean as assessed by Anaplasma phagocytophilum, A. platys, Ehrlichia canis, E. chaffeensis, E. ewingii, and Borrelia burgdorferi species-specific peptides. Infect Ecol Epidemiol 20:4

    Google Scholar 

  • Ramos RA, Latrofa MS, Giannelli A, Lacasella V, Campbell BE, Dantas-Torres F, Otranto D (2014) Detection of Anaplasma platys in dogs and Rhipicephalus sanguineus group ticks by a quantitative real-time PCR. Vet Parasitol 205:285–288

    Article  CAS  PubMed  Google Scholar 

  • Renè-Martellet M, Lebert I, Chêne J, Massot R, Leon M, Leal A, Badavelli S, Chalvet-Monfray K, Ducrot C, Abrial D, Chabanne L, Halos L (2015) Diagnosis and incidence risk of clinical canine monocytic ehrlichiosis under field conditions in southern Europe. Parasit Vectors 8:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Rizzoli A, Hauffe HC, Carpi G, Vourc HG, Neteler M, Rosa R (2011) Lyme borreliosis in Europe. Euro Surveill 16(27):19906

    PubMed  Google Scholar 

  • Sainz Á, Roura X, Miró G, Estrada-Peña A, Kohn B, Harrus S, Solano-Gallego L (2015) Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe. Parasit Vectors 8:75

    Article  PubMed  PubMed Central  Google Scholar 

  • Santoro M, Veneziano V, D'Alessio N, Di Prisco F, Lucibelli MG, Borriello G, Cerrone A, Dantas-Torres F, Latrofa MS, Otranto D, Galiero G (2016) Molecular survey of Ehrlichia canis and Coxiella burnetii infections in wild mammals of southern Italy. Parasitol Res 115:4427–4431

    Article  PubMed  Google Scholar 

  • Solano-Gallego L, Trotta M, Razia L, Furlanello T, Caldin M (2006) Molecular survey of Ehrlichia canis and Anaplasma phagocytophilum from blood of dogs in Italy. Ann N Y Acad Sci 1078:515–518

    Article  CAS  PubMed  Google Scholar 

  • Sparagano OA, de Vos AP, Paoletti B, Cammà C, de Santis P, Otranto D, Giangaspero A (2003) Molecular detection of Anaplasma platys in dogs using polymerase chain reaction and reverse line blot hybridization. J Vet Diagn Investig 15:527–534

    Article  Google Scholar 

  • Stańczak J, Gabre RM, Kruminis-Łozowska W, Racewicz M, Kubica-Biernat B (2004) Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Ann Agric Environ Med 11:109–114

    PubMed  Google Scholar 

  • Stillman BA, Monn M, Liu J, Thatcher B, Foster P, Andrews B, Little S, Eberts M, Breitschwerdt EB, Beall MJ, Chandrashekar R (2014) Performance of a commercially available in-clinic ELISA for detection of antibodies against Anaplasma phagocytophilum, Anaplasma platys, Borrelia burgdorferi, Ehrlichia canis, and Ehrlichia ewingii and Dirofilaria immitis antigen in dogs. JAVMA 245:80–86

    Article  PubMed  Google Scholar 

  • Thrustfield M (1995) Veterinary epidemiology. Blackwell Science Ltd, London, pp 138–188

    Google Scholar 

  • Tolnai Z, Sreter-Lancz Z, Sreter T (2015) Spatial distribution of Anaplasma phagocytophilum and Hepatozoon canis in red foxes (Vulpes vulpes) in Hungary. Ticks Tick Borne Dis 6:645–648

    Article  CAS  PubMed  Google Scholar 

  • Torina A, Caracappa S (2006) Dog tick-borne disease in Sicily. Parassitologia 48:145–147

    CAS  PubMed  Google Scholar 

  • Torina A, Vicente J, Alongi A, Scimeca S, Turlà R, Nicolsia S, Di Marco V, Caracappa S, de la Fuente J (2007) Observed prevalence of tick-borne pathogens in domestic animals in Sicily, Italy during 2003-2005. Zoonoses Public Health 54:8–15

    Article  CAS  PubMed  Google Scholar 

  • Torina A, Alongi A, Naranjo V, Scimeca S, Nicosia S, Di Marco V, Caracappa S, Kocan KM, de la Fuente J (2008) Characterization of Anaplasma infections in Sicily, Italy. Ann N Y Acad Sci 1149:90–93

    Article  CAS  PubMed  Google Scholar 

  • Trotta M, Fogliazza A, Furlanello T, Solano-Gallego L (2009) A molecular and serological study of exposure to tick-borne pathogens in sick dogs from Italy. Clin Microbiol Infect 15(Suppl 2):62–63

    Article  CAS  PubMed  Google Scholar 

  • Veronesi F, Galuppi R, Tampieri MP, Botoli C, Mammoli R, Piergili Fioretti D (2011) Prevalence of Anaplasma phagocytophilum in fallow deer (Dama dama) and feeding ticks from an Italy preserve. Res Vet Sci 90:40–43

    Article  CAS  PubMed  Google Scholar 

  • Westmoreland LS, Stoskopf MK, Maggi RG (2016) Prevalence of Anaplasma phagocytophilum in North Carolina eastern black bears (Ursus americanus ). J Wildl Dis 52:968–970

    Article  PubMed  Google Scholar 

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Acknowledgements

The study was supported by the management committees of the hunting districts of Salerno (ATC SA 1) and Avellino (ATC AV) and partially funded by the grant from the Ministry of Health of the Italian Republic (IZSME 01/14 RC).

The authors thank the following veterinaries for their cooperation: Claudio Amore, Pasquale Apicella (ASL Salerno), Loredana Avallone, Gennaro Barra, Raffaele Bevilacqua, Annalisa Bianco, Gaetano Bove (ASL Salerno), Antonio Bufalo, Giacomo Calabria, Vincenzo Cardamone, Francesco Celano, Domenico Crocetta, Cristina Cucciniello, Susanna De Luca, Giovanni De Lucia, Lucio De Maria, Anna Fiorella Desiderio, Enrico Di Blasi, Antonio Fimiani, Alfonso Gallo, Saverio Giordano, Enrico Lanaro, Cosimo Manna, Paola Napolitano, Carmine Palo, Gerardo Paraggio (ASL Salerno), Agnese Parrilli, Luca Pericolo, Gaetano Petta, Simona Pisano, Giovanni Russo (ASL Salerno), Antonio Raffaele, Vincenzo Raimondi, Enrico Renzulli, Antonio Ricco, Giampiero Sepe, Pierluigi Vitale, and Antonio Zotti.

The authors thank Eng. Tullio Panico (CIRAM) for his technical assistance.

This manuscript is dedicated to the memory of Dr. Enrico Lanaro, friend and colleague of many of the coauthors.

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Piantedosi, D., Neola, B., D’Alessio, N. et al. Seroprevalence and risk factors associated with Ehrlichia canis, Anaplasma spp., Borrelia burgdorferi sensu lato, and D. immitis in hunting dogs from southern Italy. Parasitol Res 116, 2651–2660 (2017). https://doi.org/10.1007/s00436-017-5574-z

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