Pet-related tick-borne infections constitute an emerging problem in human and veterinary medicine worldwide. In Chile, two pathogens of the Anaplasmataceae family, Anaplasma platys and Ehrlichia canis, have been identified in recent years in dogs and vectors. This epidemiological survey aimed to determine the human and canine seroprevalence of Anaplasma spp. in urban and rural areas of different regions in Chile and to analyze the factors associated with seropositivity.
Methods:
We performed a cross-sectional household-based study in four regions, where healthy adults and their household dogs were included. Households were chosen by double stratified random sampling in urban areas and by convenience sampling in rural areas. Anaplasma seroreactivity was determined by a commercial microimmunofluorescence assay using Anaplasma phagocytophilum antigens. A questionnaire survey was applied to assess risk factors for Anaplasma seropositivity.
Results:
A total of 1105 persons and 905 dogs were included. The overall seroprevalence in humans was 9.4%, ranging from 5.6% in central Chile to 13.7% in the extreme north; in dogs the overall prevalence was 44.0% and ranged from 37.2% in the northern region to 61.1% in central Chile. Risk factors for human seropositivity were lower education and external deworming of dogs, whereas canine seropositivity was associated to urban site, mixed-breed, older animals, and tick infestation.
Conclusions:
This cross-sectional study suggests a broad exposure of both dogs and dog owners to Anaplasma or related agents in Chile. Further epidemiological and clinical studies are necessary to understand the complete spectrum and epidemiology of tick-borne zoonotic infections in the different ecoclimatic regions of Chile.
Get full access to this article
View all access options for this article.
References
1.
AbarcaK, GárateD, LópezJ, Acosta-JamettG. Flea and ticks species from dogs in urban and rural areas in four districts in Chile. Arch Med Vet, 2016; 48:109–115.
2.
AbarcaK, LópezJ, Acosta-JamettG, LepeP, et al.A third Amblyomma species and the first tick-borne rickettsia in Chile. J Med Entomol, 2012; 49:219–222.
3.
AbarcaK, LópezJ, Acosta-JamettG, Martínez-ValdebenitoC. Detection of Rickettsia andeanae in two regions of Chile [in Spanish]. Rev Chilena Infectol, 2013; 30:388–394.
4.
AbarcaK, LópezJ, PerretC, GuerreroJ, et al.Anaplasma platys in dogs, Chile. Emerg Infect Dis, 2007; 13:1392–1395.
5.
AbarcaVK, LópezJ, GonzalezAP, DabanchPJ, et al.Seroepidemiological evidence of human exposure to Anaplasma sp. in Santiago, Chile [in Spanish]. Rev Chilena Infectol, 2008; 25:358–361.
6.
Acosta-JamettG, CleavelandS, CunninghamAA, BronsvoortBM. Demography of domestic dogs in rural and urban areas in Coquimbo region of Chile and its implication for diseases transmission. Prev Vet Med, 2010; 94:272–281.
7.
Acosta-JamettG, CleavelandS, CunninghamAA, ChalmersWS, et al.Urban domestic dog populations as a source of canine distemper virus for wild carnivores in the Coquimbo region of Chile. Vet Microbiol, 2011; 152:247–257.
8.
AllisonRW, LittleSE. Diagnosis of rickettsial diseases in dogs and cats. Vet Clin Pathol, 2013; 42:127–144.
9.
AmusateguiI, TesouroMA, KakomaI, SainzA. Serological reactivity to Ehrlichia canis, Anaplasma phagocytophilum, Neorickettsia risticii, Borrelia burgdorferi and Rickettsia conorii in dogs from northwestern Spain. Vector Borne Zoonotic Dis, 2008; 8:797–803.
10.
Arraga-AlvaradoCM, QurolloBA, ParraOC, BerruetaMA, et al.Case report: Molecular evidence of Anaplasma platys infection in two women from Venezuela. Am J Trop Med Hyg, 2014; 91:1161–1165.
11.
Bouza-MoraL, DolzG, Solorzano-MoralesA, Romero-ZunigaJJ, et al.Novel genotype of Ehrlichia canis detected in samples of human blood bank donors in Costa Rica. Ticks Tick Borne Dis, 2017; 8:36–40.
12.
BowmanD, LittleSE, LorentzenL, ShieldsJ, et al.Prevalence and geographic distribution of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis, and Anaplasma phagocytophilum in dogs in the United States: Results of a national clinic-based serologic survey. Vet Parasitol, 2009; 160:138–148.
13.
Centers for Disease Control and Prevention. Anaplasmosis and ehrlichiosis—Maine, 2008. MMWR Morb Mortal Wkly Rep, 2009; 58:1033–1036.
14.
CetinkayaH, MaturE, AkyaziI, EkizEE, et al.Serological and molecular investigation of Ehrlichia spp. and Anaplasma spp. in ticks and blood of dogs, in the Thrace Region of Turkey. Ticks Tick Borne Dis, 2016; 7:706–714.
15.
CicuttinGL, De SalvoMN, Gury DohmenFE. Molecular characterization of Ehrlichia canis infecting dogs, Buenos Aires. Ticks Tick Borne Dis, 2016; 7:954–957.
16.
CicuttinGL, TarragonaEL, De SalvoMN, MangoldAJ, et al.Infection with Ehrlichia canis and Anaplasma platys (Rickettsiales: Anaplasmataceae) in two lineages of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) from Argentina. Ticks Tick Borne Dis, 2015; 6:724–729.
17.
CleavelandS, MeslinFX, BreimanR. Dogs can play useful role as sentinel hosts for disease. Nature, 2006; 440:605.
18.
Costa-JuniorLM, RembeckK, PassosLM, RibeiroMF. Factors associated with epidemiology of Anaplasma platys in dogs in rural and urban areas of Minas Gerais State, Brazil. Prev Vet Med, 2013; 109:321–326.
19.
DayMJ. One health: The importance of companion animal vector-borne diseases. Parasit Vectors, 2011; 4:49.
20.
DíazFE, Martínez-ValdebenitoC, LópezJ, WeitzelT, et al.Geographical distribution and phylogenetic analysis of Rhipicephalus sanguineus sensu lato in northern and central Chile. Ticks Tick Borne Dis, 2018; 9:792–797.
21.
DoudierB, OlanoJ, ParolaP, BrouquiP. Factors contributing to emergence of Ehrlichia and Anaplasma spp. as human pathogens. Vet Parasitol, 2010; 167:149–154.
22.
DugatT, LagreeAC, MaillardR, BoulouisHJ, et al.Opening the black box of Anaplasma phagocytophilum diversity: Current situation and future perspectives. Front Cell Infect Microbiol, 2015; 5:61.
23.
EbaniVV, BertelloniF, TorraccaB, CerriD. 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, 2014; 21:671–675.
24.
EvasonM, StullJW, PearlDL, PeregrineAS, et al.Prevalence of Borrelia burgdorferi, Anaplasma spp., Ehrlichia spp. and Dirofilaria immitis in Canadian dogs, 2008 to 2015: A repeat cross-sectional study. Parasit Vectors, 2019; 12:64.
25.
FarkasR, GyurkovszkyM, LukacsZ, AladicsB, et al.Seroprevalence of some vector-borne infections of dogs in Hungary. Vector Borne Zoonotic Dis, 2014; 14:256–260.
LastaCS, dos SantosAP, MessickJB, OliveiraST, et al.Molecular detection of Ehrlichia canis and Anaplasma platys in dogs in Southern Brazil. Rev Bras Parasitol Vet, 2013; 22:360–366.
30.
LópezJ, AbarcaK, MundacaMI, CaballeroC, et al.Molecular identification of Ehrlichia canis in a dog from Arica, Chile [in Spanish]. Rev Chilena Infectol, 2012; 29:527–530.
31.
LópezJ, RiveraM, ConchaJC, GaticaS, et al.Serologic evidence for human ehrlichiosis in Chile [in Spanish]. Rev Med Chil, 2003; 131:67–70.
32.
MaggiRG, KramerF. A review on the occurrence of companion vector-borne diseases in pet animals in Latin America. Parasit Vectors, 2019; 12:145.
33.
MaggiRG, MascarelliPE, HavengaLN, NaidooV, et al.Co-infection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasit Vectors, 2013; 6:103.
34.
MáttarS, ParraM. Detection of antibodies to Anaplasma, Bartonella and Coxiella in rural inhabitants of the caribbean area of Colombia. Rev MVZ Córdoba, 2006; 11:781–789.
35.
McCownME, MonterrosoVH, CardonaW. Surveillance for Ehrlichia canis, Anaplasma phagocytophilum, Borrelia burgdorferi, and Dirofilaria immitis in dogs from three cities in Colombia. J Spec Oper Med, 2014; 14:86–90.
36.
McMahanCS, WangD, BeallMJ, BowmanDD, et al.Factors associated with Anaplasma spp. seroprevalence among dogs in the United States. Parasit Vectors, 2016; 9:169.
37.
MonjeLD, FernandezC, PercaraA. Detection of Ehrlichia sp. strain San Luis and Candidatus Rickettsia andeanae in Amblyomma parvum ticks. Ticks Tick Borne Dis, 2019; 10:111–114.
38.
MoroPL, ShahJ, LiO, GilmanRH, et al.Short report: Serologic evidence of human ehrlichiosis in Peru. Am J Trop Med Hyg, 2009; 80:242–244.
39.
MovillaR, GarciaC, SiebertS, RouraX. Countrywide serological evaluation of canine prevalence for Anaplasma spp., Borrelia burgdorferi (sensu lato), Dirofilaria immitis and Ehrlichia canis in Mexico. Parasit Vectors, 2016; 9:421.
40.
MüllerA, MontiG, OtthC, SepulvedaP, et al.“Candidatus Neoehrlichia chilensis” sp. nov.: Molecular detection and characterization of a novel Anaplasmataceae in wild rodents from Valdivia, southern Chile. Transbound Emerg Dis, 2018; 65:357–362.
41.
Muñoz-LealS, ClemesYS, LopesMG, AcostaICL, et al.Novel Ehrlichia sp. detected in Magellanic penguins (Sphenicus magellanicus) and in the seabird tick Ixodes uriae from Magdalena Island, southern Chile. Ticks Tick Borne Dis, 2019a; 10:101256.
42.
Muñoz-LealS, LopesMG, MarciliA, MartinsTF, et al.Anaplasmataceae, Borrelia and Hepatozoon agents in ticks (Acari: Argasidae, Ixodidae) from Chile. Acta Trop, 2019b; 192:91–103.
43.
Muñoz-LealS, MarciliA, Fuentes-CastilloD, AyalaM, et al.A relapsing fever Borrelia and spotted fever Rickettsia in ticks from an Andean valley, central Chile. Exp Appl Acarol, 2019c; 78:403–420.
44.
NicholsonWL, AllenKE, McQuistonJH, BreitschwerdtEB, et al.The increasing recognition of rickettsial pathogens in dogs and people. Trends Parasitol, 2010; 26:205–212.
45.
PantchevN, SchnyderM, VrhovecMG, SchaperR, et al.Current surveys of the seroprevalence of Borrelia burgdorferi, Ehrlichia canis, Anaplasma phagocytophilum, Leishmania infantum, Babesia canis, Angiostrongylus vasorum and Dirofilaria immitis in dogs in Bulgaria. Parasitol Res, 2015; 114(Suppl 1):S117–S130.
46.
ParkJH, HeoEJ, ChoiKS, DumlerJS, et al.Detection of antibodies to Anaplasma phagocytophilum and Ehrlichia chaffeensis antigens in sera of Korean patients by western immunoblotting and indirect immunofluorescence assays. Clin Diagn Lab Immunol, 2003; 10:1059–1064.
47.
ParolaP, PaddockCD, RaoultD. Tick-borne rickettsioses around the world: Emerging diseases challenging old concepts. Clin Microbiol Rev, 2005; 18:719–756.
48.
ParolaP, PaddockCD, SocolovschiC, LabrunaMB, et al.Update on tick-borne rickettsioses around the world: A geographic approach. Clin Microbiol Rev, 2013; 26:657–702.
49.
Perez-MacchiS, PedrozoR, BittencourtP, MullerA. Prevalence, molecular characterization and risk factor analysis of Ehrlichia canis and Anaplasma platys in domestic dogs from Paraguay. Comp Immunol Microbiol Infect Dis, 2019; 62:31–39.
50.
Perez-OsorioCE, Zavala-VelazquezJE, Arias LeonJJ, Zavala-CastroJE. Rickettsia felis as emergent global threat for humans. Emerg Infect Dis, 2008; 14:1019–1023.
51.
Perez VeraC, KapiainenS, JunnikkalaS, AaltonenK, et al.Survey of selected tick-borne diseases in dogs in Finland. Parasit Vectors, 2014; 7:285.
52.
Poo-MuñozDA, Elizondo-PatroneC, EscobarLE, AstorgaF, et al.Fleas and ticks in carnivores from a domestic-wildlife interface: Implications for public health and wildlife. J Med Entomol, 2016; 53:1433–1443.
53.
R-Development-Core-Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: The R Foundation for Statistical Computing. 2018. Available at http://www.R-project.org
54.
RichardsAL. Worldwide detection and identification of new and old rickettsiae and rickettsial diseases. FEMS Immunol Med Microbiol, 2012; 64:107–110.
55.
SalbAL, BarkemaHW, ElkinBT, ThompsonRC, et al.Dogs as sources and sentinels of parasites in humans and wildlife, northern Canada. Emerg Infect Dis, 2008; 14:60–63.
56.
SantosAS, AlexandreN, SousaR, NuncioMS, et al.Serological and molecular survey of Anaplasma species infection in dogs with suspected tickborne disease in Portugal. Vet Rec, 2009; 164:168–171.
57.
Tinoco-GraciaL, Quiroz-RomeroH, Quintero-MartinezMT, Renteria-EvangelistaTB, et al.Prevalence of Rhipicephalus sanguineus ticks on dogs in a region on the Mexico-USA border. Vet Rec, 2009; 164:59–61.
58.
VieiraTS, VieiraRF, NascimentoDA, TamekuniK, et al.Serosurvey of tick-borne pathogens in dogs from urban and rural areas from Parana State, Brazil. Rev Bras Parasitol Vet, 2013; 22:104–109.
59.
WassL, GrankvistA, MattssonM, GustafssonH, et al.Serological reactivity to Anaplasma phagocytophilum in neoehrlichiosis patients. Eur J Clin Microbiol Infect Dis, 2018; 37:1673–1678.
60.
WeitzelT, JiangJ, Acosta-JamettG, Martínez-ValdebenitoC, et al.Canine seroprevalence to Orientia species in southern Chile: A cross-sectional survey on the Chiloe Island. PLoS One, 2018; 13:e0200362.
61.
WeitzelT, Martínez-ValdebenitoC, Acosta-JamettG, JiangJ, et al.Scrub typhus in continental Chile, 2016–2018. Emerg Infect Dis, 2019; 25:1214–1217.
62.
WitterR, Nunes-VecchiS, dos Anjos-PachecoT, LimaA, et al.Prevalence of canine monocitic ehrlichiosis and canine thrombocytic anaplasmosis in dogs suspected of hemoparasitosis in Cuiabá Mato Grosso. Semina: Cienc Agrar, 2013; 34:3811–3822.
