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Revista U.D.C.A Actualidad & Divulgación Científica

Print version ISSN 0123-4226

rev.udcaactual.divulg.cient. vol.25 no.1 Bogotá Jan./June 2022  Epub Feb 25, 2022

https://doi.org/10.31910/rudca.v25.n1.2022.1850 

Agricultural Sciences

Prevalence of rickettsias in ticks (Acari: Ixodidae) collected in domestic animals of the northern region of Caldas department, Colombia

Prevalencia de rickettsias en garrapatas (Acari: Ixodidae) colectadas en animales domésticos del norte del departamento de Caldas, Colombia

Yuliana Zapata-Serna1 
http://orcid.org/0000-0002-7771-7179

Ana Elisa Rojas-Rodríguez2 
http://orcid.org/0000-0002-8421-633X

Jorge Enrique Pérez-Cárdenas3  * 
http://orcid.org/0000-0002-7829-6505

Héctor Jaime Aricapa-Giraldo4 
http://orcid.org/0000-0001-6376-2262

Marylin Hidalgo-Diaz5 
http://orcid.org/0000-0001-8960-0616

Fredy A. Rivera-Páez6 
http://orcid.org/0000-0001-8048-5818

1Universidad Católica de Manizales. Manizales - Caldas, Colombia; e-mail: yzapata@ucm.edu.co

2Universidad Católica de Manizales. Manizales - Caldas, Colombia; e-mail: arojas@ucm.edu.co

3Universidad de Caldas. Manizales - Caldas, Colombia; e-mail: labmicro@ucaldas.edu.co

4Universidad de Caldas. Manizales - Caldas, Colombia; e-mail: hjaricapa@ucaldas.edu.co

5Pontificia Universidad Javeriana. Bogotá, D.C., Colombia; e-mail: hidalgo.m@javeriana.edu.co

6Universidad de Caldas. Manizales - Caldas, Colombia; e-mail: fredy.rivera@ucaldas.edu.co


ABSTRACT

The northern region of the Caldas department in Colombia is considered an endemic area for murine typhus. Recent studies in patients with acute febrile disease demonstrated infection with the spotted fever group's rickettsiae due to an increase in the IgG titer by indirect immunofluorescence in paired sera obtained from these patients. The objective of the current research was to identify the species of ticks present in domestic animals in the northern region of Caldas and establish the presence of rickettsial genomic material in the collected ticks. Ticks were obtained from bovines, horses, and dogs in seven municipalities in the north of Caldas. Ticks were stored in 90 % ethanol until processing and were identified using taxonomic keys, DNA was extracted using commercial techniques, and the gltA gene was amplified by conventional chain reaction polymerase (PCR). Seven hundred thirteen ticks were obtained from 593 domestic animals. The highest infestation occurred in cattle, followed by canines and horses. Ticks found corresponded to the species Riphicephalus microplus, Dermacentor nitens, Amblyomma sp., and Riphicephalus sanguineus s.l. In none of the tick samples, Rickettsia-specific gltA gene DNA was found. It can be inferred that the ticks obtained are not a source of rickettsial infection for people in this department region, despite finding different species associated with the transmission of this disease.

Keywords: Domestic animals; Hard ticks; Murine typhus; Prevalence; Rickettsiaceae; Rickettsial infection

RESUMEN

La región norte del departamento de Caldas, Colombia es considerada como una zona endémica de tifo murino. Estudios recientes realizados en pacientes con enfermedad febril aguda, demostraron la infección con rickettsias, del grupo de las fiebres manchadas, debido al aumento en el título de IgG, por inmunofluorescencia indirecta (IFI), en sueros pareados, obtenidos de dichos pacientes. El objetivo de la investigación fue el de identificar las especies de garrapatas presentes en animales domésticos, de la región norte de Caldas y establecer la presencia de material genómico de rickettsias, en las garrapatas recolectadas. En siete municipios, se recolectaron garrapatas de bovinos, de equinos y de caninos. Las garrapatas, se almacenaron en etanol al 90 %, hasta su identificación taxonómica. Se extrajo el ADN, utilizando técnicas comerciales y se amplificó por reacción de cadena de la polimerasa (PCR) convencional el gen gltA. Se obtuvieron 713 garrapatas de 593 animales domésticos. La más alta infestación se presentó en bovinos, seguido de los caninos y equinos. Las garrapatas encontradas correspondieron a las especies Riphicephalus microplus, Dermacentor nitens, Amblyomma sp. y Riphicephalus sanguineus s.l. En ninguna de las muestras, se comprobó la presencia de ADN del gen gltA específico de Rickettsia. Se puede inferir que las garrapatas obtenidas no serían una fuente de infección rickettsial para las personas, en esta región del departamento; sin embargo, su presencia es un factor de riesgo para la adquisición de rickettsiosis asociadas con las fiebres manchadas.

Palabras clave: Animales domésticos; Garrapatas; Infección rickettsial; Prevalencia; Rickettsiaceae; Tifo murino

INTRODUCTION

Ticks are ectoparasites of great importance in transmitting microorganisms to humans and animals (Parola & Raoult, 2001; Jongejan & Uilenberg, 2004; Labuda & Nuttall, 2004; Dumler & Walker, 2005). Ticks from the family Ixodidae, also known as hard ticks, are obligate ectoparasites of all kinds of terrestrial vertebrates; they can produce anemia and paralysis, but their primary importance is given by the fact that they are vectors of nematodes, viruses, bacteria, and protozoa (Guglielmone & Robbins, 2018). Forty-three species have been reported in Colombia belonging to the genera Amblyomma, Ixodes, Haemaphysalis, Rhipicephalus, and Dermacentor (Guglielmone et al. 2003; Rivera-Páez et al. 2018); these ticks are essential in the transmission of rickettsias of spotted fever group such as Rickettsia rickettsii, R. parkeri, R. massiliae, R. africae and R. conorii in America (Matsumoto et al. 2005; Parola et al. 2005). Ticks can be vectors by transmitting rickettsias across their bite but can also be reservoirs by the transstadial and transovarial passage of these bacteria (Bremer et al. 2005; Parola et al. 2005).

Rickettsiae are gram-negative, obligate intracellular coccobacillus bacteria. The genus Rickettsia has been classified into four groups: The spotted fever group (SFG), the typhoid group (TG) (Hackstadt, 1996), the transitional group (TRG) (Gillespie et al. 2007) and the ancestral group (Stothard & Fuerst, 1995). Phylogenetic relationships in this genus have been established by variability in genes coding for the enzyme citrate synthetase (gltA) and external surface antigens and proteins (sca1, sca2, sca4, ompA, and ompB) (Merhej et al. 2014).

Currently, tick-borne rickettsial diseases are recognized as zoonotic diseases, causing a febrile syndrome that can be present in 1.5-5.6 % of travelers to tropical areas and 2.7 and 48.5 % of residents of such places (Blanton, 2013; Merhej et al. 2014). Rocky Mountain spotted fever (Tobia fever in Colombia, Brazilian spotted fever in Brazil) produced by R. rickettsii can be severe, with case fatality rates between 7.3-100 % (Raoult & Parola, 2007; Nogueira-Angerami et al. 2009; Regan et al. 2015). In Latin America, cases of the disease have been described in Brazil (Labruna, 2009), Colombia (Hidalgo et al. 2007; 2011) and Argentina (Paddock et al. 2008). In Colombia, outbreaks with lethality between 26 to 36 % have occurred in departments such as Cundinamarca, Córdoba and Antioquia (Acosta et al. 2006; Pacheco-García et al. 2008; Hidalgo et al. 2011).

In 2012, in the northern area of Caldas, it was found that 5 out of 27 patients with febrile processes compatible with the rickettsial disease presented antibody titers against R. rickettsii; all patients showed a variation in the titer that ranged between 2 to 3 times its initial value in the samples taken during convalescence, which suggests that they were suffering from an active disease (Hidalgo et al. 2013). Given the findings mentioned above, the objectives of this study were to establish the frequency of vectors associated with rickettsiae of the SFG group and to detect and identify the species of rickettsiae present in ticks found in this region of the department.

MATERIALS AND METHODS

A cross-sectional, observational, and descriptive study was conducted in which convenience sampling was carried out in rural properties and the urban area of each municipality. The study area comprised the northern region of the department of Caldas, Colombia: Neira 5°09'46''N, 75°31'31''W, Aranzazu 5°16'18"N, 75°28'12"W, Salamina 5°23'15"N,75°29'41"W, Pácora 5°31'53"N, 75°27'20"W, Aguadas 5°36'07"N, 75°27'22"W, La Merced 5°23'35"N, 75°32'42"W and Filadelfia 5°17'33"N, 75°34'17"W) (Figure 1).

Figure 1 Map of Caldas department of Colombia with the study area colored and ticks species localization. 

Collection and identification of ticks. Ticks parasitizing equine, bovine, and canine individuals were collected between January and December 2015 in each municipality listed above. Ticks were carefully extracted with entomological tweezers to preserve the capitulum of the specimens. The individuals from each animal were stored in Eppendorf® tubes with 90 % ethanol, duly labeled. Data was obtained for each animal sampled, such as sex, age, breed, presence or absence of ectoparasites, date of tick harvest, municipality, place of sampling (urban or rural), altitude, and specific site of vector extraction. Tick morphological identification was carried out by visualization under a stereomicroscope (Euromex ref: stereoblue) and according to Jones et al. (1972), Barros-Battesti et al. (2006), Mehlhorn (2008), Martins et al. (2010) and Nava et al. (2014; 2017).

Molecular detection of Rickettsia spp. in ticks. Groups of eight ticks were formed, selecting the arthropods by species and municipality of origin. DNA extraction was performed using the commercial kit Ultraclean Tissue & Cells DNA Isolation Kit sample Cat. 12334-S (MO BIO laboratories) (MO BIO Laboratories, 2019). DNA was stored at -80 °C until amplification by conventional polymerase chain reaction (PCR).

The citrate synthetase enzyme gene (gltA), common in all members of the genus Rickettsia, was amplified using primers CS78 and CS323, which amplify a fragment of 440 bp (Labruna et al. 2004). In the case of the presence of this gene, the ompA, ompB, and 17kD genes of this microorganism would be amplified to establish the Rickettsia species by sequence comparison. To verify the integrity of the DNA obtained, the primers of the tick mitochondrial 16 S rDNA gene (16S+1: CTG CTC AAT GAT TTT TTA AAT TGC TGT GG; 16S-1: CCG GTC TGA ACT CAG ATC AAG T) that amplify a fragment of approximately 463 bp (Black & Piesman, 1994) were used. Rickettsia parkeri DNA was used as a positive control, and ultrapure water was used as a negative control.

Amplification was performed using the Dream Taq Green DNA polymerase kit (Thermo Scientific®) according to the following protocols. For the gltA gene, denaturation at 95 °C for three minutes, followed by 35 amplification cycles with the following temperatures 98 °C for 20 sec, 56 °C for 15 sec and 72 °C for 60 sec, and a final extension at 72 °C for 60 sec (Labruna et al. 2004). Amplification of the 16S rDNA gene, was carried out with an initial denaturation at 95 °C for 3 sec; 10 cycles with the following temperatures 98 °C for 30 sec, 48 °C for 30 sec, 72 °C for 40 sec; 15 cycles of 98 °C for 30 sec, 50 °C for 40 sec and 72 °C for 30 sec; 10 cycles at 98 °C for 30 sec, 55 °C for 30 sec, 72 °C for 40 sec and a final extension at 72 °C for seven minutes (Black & Piesman, 1994).

Statistical analysis. A descriptive study of tick infestation in the animals sampled was performed. To establish possible relationships between infestation, type of domestic animal, area of origin, and municipality, Pearson's Chi-square test was used, using Excel (Microsoft) and Epi-info (CDC).

Ethical aspects. To obtain the sample, the owner of the animal or the administrator of the farm was asked to sign an informed consent form; a survey was filled out with each animal sampled in which the demographic data mentioned above were obtained. The research project was submitted for review by the Bioethics Committee of the Universidad de Caldas, with the approval for the development of the project, by means of act 006 of 2014. The researchers involved in the development of the project are aware of the universal declaration of animal rights proclaimed by the International League for Animal Rights, Geneva, Switzerland, the guide for the care and use of laboratory animals (NRC, 1996) and the ethical principles of animal experimentation enunciated by ICLAS, International Council for Laboratory Animal Science.

RESULTS AND DISCUSSION

A total of 593 domestic animals were examined, collecting 713 adult ticks in the seven municipalities sampled (Table 1). According to the animal-tested, 40 % corresponded to bovines (Bos taurus), 33 % to equines (Equus caballus), and 27 % to canines (Canis lupus familiaris) (Table 2). Most of the animals were females (71 %) and came from rural areas (567 animals, 96 %). Of the total bovines, 92 % were infested, with high statistical significance (Table 2). The most frequently found tick species was R. microplus, followed by Amblyomma sp. and R. sanguineus (Table 3). The number of infested equines was low, corresponding to 12.3 % of the total number of animals in this group (Table 2). Unlike bovines, the most frequent tick species was Dermacentor nitens, found in 10.7 % of this group of animals (Table 3). Four of the seven municipalities had no infested equines, while Filadelfia and La Merced had the highest percentages of infestation, 25 and 44 %, respectively (Table 1).

Table 1 Distribution of ticks by group of domestic animals and municipalities in the northern region of Caldas-Colombia department. 

NI: Not infested; TI: Total infested; TNIN: Total not infested; TM: Total of animals sampled; Pv: P value; OR: odds ratio; IC: confidence interval

Table 2 Frequency and statistical analysis of tick infestation in bovines, equines, and canines in the northern region of Caldas-Colombia department. 

P: P-value; OR: odds ratio; IC: confidence interval.

Table 3 Frequency and statistical analysis of tick species found in cattle, equines and canines in the northern region of Caldas-Colombia department. 

P: P-value; OR: odds ratio; IC: confidence interval.

The percentage of infestation of canines was 13 % (Table 2); the most frequent species was R. sanguineus s.l. (57.1 % of the infested animals); the presence of Amblyomma sp. in this group is highlighted, finding high statistical significance for this type of tick (Table 3).

The frequency found of Amblyomma sp. in this research is very low compared to other studies conducted in Colombia. In a survey conducted in ten Colombia departments, Rivera-Páez et al. (2018) found a high frequency of Amblyomma. Eleven percent of the ticks were infected with different species of rickettsiae; none of them corresponded to R. rickettsii (Rivera-Páez et al. 2018). In the study conducted by Faccini-Martínez et al. (2017) in the municipality of Villeta (Cundinamarca), a high frequency of different species of the genus Amblyomma was also found; 1.7 % of the ticks had rickettsiae, identifying R. rickettsii in adults of D. nitens, in nymphs and larvae of A. cajennense s.l. and Amblyomma spp. In adults of A. cajennese s.l. and R. microplus, the rickettsia species could not be identified (Faccini-Martínez et al. 2017). Several factors could explain the low frequency of Amblyomma in our study: much of the sampling was conducted at altitudes above 1,000 m a.s.l.; Amblyomma cajennense prefers lower altitudes (average 472.9 m a.s.l.), although they have been found at altitudes of 1,100 m a.s.l.; additionally, it prefers dry climates, with minimum temperatures of 20.9 °C and maximum temperatures of 31 °C and is not very resistant to sudden temperature changes (Acevedo-Gutiérrez et al. 2018); the factors mentioned above are not found in the geographic areas sampled.

The predominant tick species in this study was R. microplus. This finding is compatible with authors who state that this species is the most frequent in Colombia and Latin America, in cattle and other domestic and wild animals that are in contact with their habitats (Benavides & Romero, 2001; Estrada-Peña et al. 2006; Rodríguez-Vivas et al. 2016). Cortés Vecino et al. (2010) described R. microplus as the most frequent tick in regions such as Caldas, Antioquia and Meta and geographical areas with altitudes ranging from 2,000 to 2,903 m a.s.l. Its role in rickettsial transmission is controversial (Bermúdez et al. 2009; Oteo et al. 2014; Pesquera et al. 2015; Monje et al. 2016; Faccini-Martínez et al. 2017; Quintero V. et al. 2017); co-infestation with infected ticks or ingestion of blood from a carrier host may be factors for this tick to present in its DNA the presence of rickettsial genome (Beeler et al. 2011; Merhej et al. 2014). It has also been demonstrated in vitro that infection with R. parkeri generates a negative effect on oviposition; in addition, this tick loses the ability to transmit this rickettsia to experimental animals (Cordeiro et al. 2018). The above evidence could explain the absence of rickettsiae in this species in the present study since no multiple infestation was found in the animals studied, which is also associated with the possible harmful effect of rickettsiae on this particular species.

The percentage of infestation in the municipalities ranged from 27.5 to 69 %, with a higher frequency found in the municipality of La Merced (55 of the 80 infested animals); when analyzing the frequency of infestation against the municipalities sampled, it was found that La Merced and Neira presented high statistical significance (Table 1). In a study of the frequency of active rickettsial disease in 2012 in municipalities in the northern part of the department, it was found that of 26 people with acute febrile illness, five presented an increase of 4-fold or greater in IgG titer against R. rickettsii in the sample taken at convalescence; this finding is compatible with a rickettsial disease of the spotted fever group; the vast majority of these patients came from the municipality of Salamina (Hidalgo et al. 2013). A high proportion of ticks associated with rickettsial transmission (19 of 21 D. nitens, 12 of 13 R. sanguineus s.l., and 6 of 17 Amblyomma sp.) came from Salamina or nearby municipalities (Filadelfia, La Merced and Pácora). Amblyomma samples from the municipality of La Merced were obtained from dogs, an animal group that has more significant contact with humans. Therefore, there is a greater probability of infestation. This is evidence that these municipalities could have a higher risk of rickettsial disease; therefore, future studies could be focused on this area of the region to clarify the type or types of rickettsiae circulating not only in vectors but also in people, domestic and wild animals.

When molecular tests for the detection of the gltA gene were performed, it was found that none of the DNA samples obtained was positive for this gene; this result demonstrates the absence of rickettsial genetic material in the ticks collected. With the results obtained, it is concluded that there are ticks associated with the transmission of rickettsiae; however, for the period in which this sampling was done, the role of ticks obtained from domestic animals in the transmission of these diseases is not evident and, therefore, further studies are required to clarify how rickettsiae of the SFG group are acquired in the region.

Acknowledgments.

To the directors and administrative staff of the Universidad Católica de Manizales, Pontificia Universidad Javeriana and Universidad de Caldas, for contributing with the human, technical and financial resources necessary for the execution of this research project. To the veterinarians of the UMATAS of the seven municipalities, to the owners and administrators of the farms sampled for their support in the collection of samples for this study and to all the support personnel of the BIOSALUD laboratory of the Universidad de Caldas for their collaboration in the preparation of reagents and working supplies.

REFERENCES

1. ACEVEDO-GUTIÉRREZ, L.Y.; PATERNINA, L.E.; LONDOÑO, A.F.; PARRA-HENAO, G.; RODAS, J.D. 2018. Modelos potenciales de distribución geográfica y climática del complejo Amblyomma cajennense (Acari: Ixodidae); potencial vector de Rickettsia rickettsii en Colombia. Biomédica. 38(4):534-544. 10.7705/biomedica.v38i4.3916 [ Links ]

2. ACOSTA, J.; URQUIJO, L.; DIAZ, A.; SEPULVEDA, M.; MANTILLA, G.; HEREDIA, D.; ACOSTA, J. DE S.J.; DE LA ROCHA QUEVEDO, A.; SEPÚLVEDA, M.S.; HEREDIA, D.J.; ACOSTA-CABRONERO, J.; HARRERA-ESTRELLA, A. 2006. Brote de rickettsiosis en Necoclí, Antioquia, febrero-marzo de 2006. Inf Quinc Epidemiol Nac. 11(12):177-192. [ Links ]

3. BARROS-BATTESTI, D.; ARZUA, M.; BECHARA, G.H. 2006. Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies. Instituto Butantan (Brasil). 233p. [ Links ]

4. BEELER, E.; ABRAMOWICZ, K.F.; ZAMBRANO, M.L.; STURGEON, M.M.; KHALAF, N.; HU, R.; DASH, G.A.; EREMEEVA, M.E. 2011. A focus of dogs and Rickettsia massiliae-infected Rhipicephalus sanguineus in California. Am J Trop Med Hyg. 84(2):244-249. 10.4269/ajtmh.2011.10-0355 [ Links ]

5. BENAVIDES, E.; ROMERO, A. 2001. Consideraciones para el control integral de parásitos externos del ganado. En: Federación Colombiana de Ganaderos-FEDEGAN. (ed). Manejo integrado de plagas y enfermedades en explotaciones ganaderas 7. Anexo Coleccionable. Carta Fedegan. p.64-86. [ Links ]

6. BERMÚDEZ, S.E.; EREMEEVA, M.E.; KARPATHY, S.E.; SAMUDIO, F.; ZAMBRANO, M.L.; ZALDIVAR, Y.; MOTTA, J.A.; DASCH, G.A. 2009. Detection and identification of rickettsial agents in ticks from domestic mammals in eastern Panama. J. Med. Entomol. (Estados Unidos) 46(4):856-861. 10.1603/033.046.0417 [ Links ]

7. BLACK, W.C.; PIESMAN, J. 1994. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc. Natl. Acad. Sci. 91(21):10034-10038. 10.1073/pnas.91.21.10034 [ Links ]

8. BLANTON, L.S. 2013. Rickettsial infections in the tropics and in the traveler. Curr Opin Infect Dis. 26(5):435-440. 10.1097/QCO.0b013e328363811b [ Links ]

9. BREMER, W.G.; SCHAEFER, J.J.; WAGNER, E.R.; EWING, S.A.; RIKIHISA, Y.; NEEDHAM, G.R.; JITTAPALAPONG, S.; MOORE, D.L.; STICH, R.W. 2005. Transstadial and intrastadial experimental transmission of Ehrlichia canis by male Rhipicephalus sanguineus. Vet. Parasitol. 131:95-105. 10.1016/j.vetpar.2005.04.030 [ Links ]

10. CORDEIRO, M.D.; DE AZEVEDO BAÊTA, B.; CEPEDA, P.B.; TEIXEIRA, R.C.; RIBEIRO, C.C.D.U.; DE ALMEIDA VALIM, J.R.; PINTER, A.; DA FONSECA, A.H. 2018. Experimental infection of Rickettsia parkeri in the Rhipicephalus microplus tick. Ticks Tick Borne Dis. (Holanda). 9(1):93-96. 10.1016/j.ttbdis.2017.10.003 [ Links ]

11. CORTÉS VECINO, J.; BETANCOURT ECHEVERRI, J.A.; CÁRDENAS, J.; PULIDO HERRERA, L. 2010. Distribución de garrapatas Rhipicephalus (Boophilus) microplus en bovinos y fincas del Altiplano cundiboyacense (Colombia). Corpoica Cienc. Tecnol. Agropecu. 11(1):73-84. 10.21930/rcta.vol11_num1_art:197 [ Links ]

12. DUMLER, J.S.; WALKER, D.H. 2005. Rocky Mountain spotted fever--changing ecology and persisting virulence. N Engl. J. Med. 353(6):551-553. 10.1056/NEJMp058138 [ Links ]

13. ESTRADA-PEÑA, A.; BOUATTOUR, A.; CAMICAS, J.L.; GUGLIELMONE, A.; HORAK, I.; JONGEJAN, F.; LATIF, A.; PEGRAM, R.; WALKER, A.R. 2006. The known distribution and ecological preferences of the tick subgenus Boophilus (Acari: Ixodidae) in Africa and Latin America. Exp Appl Acarol. 38:219-235. 10.1007/s10493-006-0003-5 [ Links ]

14. FACCINI-MARTÍNEZ, Á.; RAMÍREZ-HERNÁNDEZ, A.; BARRETO, C.; FORERO-BECERRA, E.; MILLÁN, D.; VALBUENA, E.; SÁNCHEZ-ALFONSO, A.C.; IMBACUÁN-PANTOJA, W.O.; CORTÉS-VECINO, J.A.; POLO-TERÁN, L.J.; YAYA-LANCHEROS, N.; JÁCOME, J.; PALOMAR, A.M.; SANTIBÁÑEZ, S.; PORTILLO, A.; OTEO, J.A.; HIDALGO, M. 2017. Epidemiology of Spotted Fever Group Rickettsioses and Acute Undifferentiated Febrile Illness in Villeta, Colombia. Am J Trop Med Hyg. 97(3):782-788. 10.4269/ajtmh.16-0442 [ Links ]

15. GILLESPIE, J.J.; BEIER, M.S.; RAHMAN, M.S.; AMMERMAN, N.C.; SHALLOM, J.M.; PURKAYASTHA, A.; SOBRAL, B.S.; AZAD, A.F. 2007. Plasmids and rickettsial evolution: insight from Rickettsia felis. PLoS One. 2(3):e266. 10.1371/journal.pone.0000266 [ Links ]

16. GUGLIELMONE, A.; ESTRADA-PEÑA, A.; KEIRANS, J.; ROBBINS, R. 2003. Ticks (Acari: Ixodida) of the Neotropical Zoogeographic Region. International Consortium on Ticks and Tick-borne Diseases (ICTTD-2). (Holanda). 173p. [ Links ]

17. GUGLIELMONE, A.A.; ROBBINS, R.G. 2018. Hard ticks (Acari: Ixodida: Ixodidae) parasitizing humans: a global overview. Springer. 331p. [ Links ]

18. HACKSTADT, T. 1996. The biology of rickettsiae. Infect Agents Dis. 5(3):127-143. [ Links ]

19. HIDALGO, M.; MIRANDA, J.; HEREDIA, D.; ZAMBRANO, P.; VESGA, J.F.; LIZARAZO, D.; MATTAR, S.; VALBUENA, G. 2011. Outbreak of Rocky Mountain spotted fever in Córdoba, Colombia. Mem Inst Oswaldo Cruz. 106(1):117-118. 10.1590/s0074-02762011000100019 [ Links ]

20. HIDALGO, M.; MONTOYA, V.; MARTÍNEZ, A.; MERCADO, M.; DE LA OSSA, A.; VÉLEZ, C.; ESTRADA, G.; PÉREZ, J.E.; FACCINI-MARTÍNEZ, A.A.; LABRUNA, M.B.; VALBUENA, G. 2013. Flea-borne rickettsioses in the north of Caldas province, Colombia. Vector Borne Zoonotic Dis. 13(5):289-294. 10.1089/vbz.2012.1173 [ Links ]

21. HIDALGO, M.; OREJUELA, L.; FUYA, P.; CARRILLO, P.; HERNANDEZ, J.; PARRA, E.; KENG, C.; SMALL, M.; OLANO, J.P.; BOUYER, D.H.; CASTANEDA, E.; WALKER, D.; VALBUENA, G. 2007. Rocky Mountain spotted fever, Colombia. Emerg. Infect. Dis. 13:1058-1060. 10.3201/eid1307.060537 [ Links ]

22. JONES, E.K.; CLIFFORD, C.M.; KEIRANS, J.E.; KOHLS, G.M. 1972. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the western hemisfere. Brigham Young Univ. Sci. Bull. Biol. Ser. 17(4):1-47. [ Links ]

23. JONGEJAN, F.; UILENBERG, G. 2004. The global importance of ticks. Parasitology. 129(Suppl):S3-14. 10.1017/s0031182004005967 [ Links ]

24. LABRUNA, M.B. 2009. Ecology of Rickettsia in South America. Ann NY Acad Sci. 1166:156-166. 10.1111/j.1749-6632.2009.04516.x [ Links ]

25. LABRUNA, M.B.; WHITWORTH, T.; HORTA, M.C.; BOUYER, D.H.; MCBRIDE, J.W.; PINTER, A.; POPOV, V.; GENNARI, S.M.; WALKER, D.H. 2004. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 42(1):90-98. 10.1128/jcm.42.1.90-98.2004 [ Links ]

26. LABUDA, M.; NUTTALL, P.A. 2004. Tick-borne viruses. Parasitology. 129(Suppl 1):S221-245. 10.1017/s0031182004005220 [ Links ]

27. MARTINS, T.F.; ONOFRIO, V.C.; BARROS-BATTESTI, D.M.; LABRUNA, M.B. 2010. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis. 1(2):75-99. 10.1016/j.ttbdis.2010.03.002 [ Links ]

28. MATSUMOTO, K.; BROUQUI, P.; RAOULT, D.; PAROLA, P. 2005. Experimental infection models of ticks of the Rhipicephalus sanguineus group with Rickettsia conorii. Vector Borne Zoonotic Dis. 5(4):363-372. 10.1089/vbz.2005.5.363 [ Links ]

29. MEHLHORN, H. 2008. Tick Genus Diagnosis. In: Mehlhorn, H. (Ed). Encyclopedia of Parasitology. Springer (Berlin). p.1383-1383. [ Links ]

30. MERHEJ, V.; ANGELAKIS, E.; SOCOLOVSCHI, C.; RAOULT, D. 2014. Genotyping, evolution and epidemiological findings of Rickettsia species. Infect Genet Evol. 25:122-137. 10.1016/j.meegid.2014.03.014 [ Links ]

31. MO BIO LABORATORIES. 2019. UltraClean® Tissue & Cells DNA Isolation Kit Sample. Instruction Manual. [ Links ]

32. MONJE, L.D.; COSTA, F.B.; COLOMBO, V.C.; LABRUNA, M.B.; ANTONIAZZI, L.R.; GAMIETEA, I.; NAVA; S.; BELDOMENICO, P.M. 2016. Dynamics of Exposure to Rickettsia parkeri in Cattle in the Paraná River Delta, Argentina. J Med Entomol. 53(3):660-665. 10.1093/jme/tjv250 [ Links ]

33. NATIONAL RESEARCH COUNCIL, NRC. 1996. Guide for the Care and Use of Laboratory Animals. The National Academies Press (Washington, DC). p.124. 10.17226/5140 [ Links ]

34. NAVA, S.; BEATI, L.; LABRUNA, M.B.; CÁCERES, A.G.; MANGOLD, A.J.; GUGLIELMONE, A.A. 2014. Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum, Typhus and Amblyomma sculptum (Ixodida: Ixodidae). Ticks Tick Borne Dis. 5(3):252-276. 10.1016/j.ttbdis.2013.11.004 [ Links ]

35. NAVA, S.; VENZAL, J.M.; GONZÁLEZ-ACUÑA, D.; MARTINS, T.F.; GUGLIELMONE, A.A. 2017. Morphological Keys for Genera and Species of Ixodidae and Argasidae. In: Nava, S.; Venzal, J.; González-Acuña, M.D.; Martins, T.F.; Guglielmone, A.A. (Eds). Ticks of the Southern Cone of America. Academic Press (New York). p.323-336. [ Links ]

36. NOGUEIRA-ANGERAMI, R.; NUNES, E.M.; MENDES NASCIMENTO, E.M.; RIBAS FREITAS, A.; KEMP, B.; FELTRIN, A.F.C.; PACOLA, M.R.; PERECIN, G.E.C.; SINKOC, V.; RIBEIRO RESENDE, M.; KATZ, G.; JACINTHO DA SILVA, L. 2009. Clusters of Brazilian spotted fever in São Paulo State, southeastern Brazil. A review of official reports and the scientific literature. Clin Microbiol Infect. 15(Suppl 2):202-204. 10.1111/j.1469-0691.2008.02637.x [ Links ]

37. OTEO, J.A.; NAVA, S.; DE SOUSA, R.; MATTAR, S.; VENZAL, J.M.; ABARCA, K.; LABRUNA, M.B.; ZAVALA-CASTRO, J. 2014. Guías Latinoamericanas de la RIICER para el diagnóstico de las rickettsiosis transmitidas por garrapatas. Rev. chil. Infectol. 31(1):54-65. 10.4067/S0716-10182014000100009 [ Links ]

38. PACHECO-GARCÍA, O.; GIRALDO, M.; HIDALGO, M.; GALEANO, A.; ECHEVERRI, I.; ECHAVARRÍA-RODRÍGUEZ, L.; PARRA, E.; REY, G. 2008. Estudio de brote febril hemorrágico en el corregimiento de Alto de Mulatos - Distrito Especial Portuario de Turbo, Antioquia, enero de 2008. Inf Quinc Epidemiol Nac. (Colombia). 13(10):145-160. [ Links ]

39. PADDOCK, C.D.; FERNÁNDEZ, S.; ECHENIQUE, G.A.; SUMNER, J.W.; REEVES, W.K.; ZAKI, S.R.; REMONDEGUI, C.E. 2008. Rocky Mountain spotted fever in Argentina. Am J Trop Med Hyg. 78(4):687-692. [ Links ]

40. PAROLA, P.; PADDOCK, C.D.; RAOULT, D. 2005. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev. 18(4):719-756. 10.1128/CMR.18.4.719-756.2005 [ Links ]

41. PAROLA, P.; RAOULT, D. 2001. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis. 32(6):897-928. 10.1086/319347 [ Links ]

42. PESQUERA, C.; PORTILLO, A.; PALOMAR, A.M.; OTEO, J.A. 2015. Investigation of tick-borne bacteria (Rickettsia spp., Anaplasma spp., Ehrlichia spp. and Borrelia spp.) in ticks collected from Andean tapirs, cattle and vegetation from a protected area in Ecuador. Parasit Vectors. 8:46. 10.1186/s13071-015-0662-3 [ Links ]

43. QUINTERO V., J.C.; PATERNINA T., L.E.; URIBE Y., A.; MUSKUS, C.; HIDALGO, M.; GIL, J.; CIENFUEGOS G., A.V.; OSORIO Q., L.; ROJAS A., C. 2017. Eco-epidemiological analysis of rickettsial seropositivity in rural areas of Colombia: A multilevel approach. PLoS Negl Trop Dis. 11(9):e0005892. 10.1371/journal.pntd.0005892 [ Links ]

44. RAOULT, D.; PAROLA, P. 2007. Rickettsial diseases. CRC press (Estados Unidos). 400p. [ Links ]

45. REGAN, J.J.; TRAEGER, M.S.; HUMPHERYS, D.; MAHONEY, D.L.; MARTINEZ, M.; EMERSON, G.L.; TACK, D.M.; GEISSLER, A.; YASMIN, S.; LAWSON, R.; WILLIAMS, V.; HAMILTON, C.; LEVY, C.; KOMATSU, K.; YOST, D.A.; MCQUISTON, J.H. 2015. Risk factors for fatal outcome from rocky mountain spotted Fever in a highly endemic area-Arizona, 2002-2011. Clin Infect Dis. 60(11):1659-1666. 10.1093/cid/civ116 [ Links ]

46. RIVERA-PÁEZ, F.A.; LABRUNA, M.B.; MARTINS, T.F.; PEREZ, J.E.; CASTAÑO-VILLA, G.J.; OSSA-LÓPEZ, P.A.; GIL, C.A.; SAMPIERI, B.R.; ARICAPA-GIRALDO, H.J.; CAMARGO-MATHIAS, M.I. 2018. Contributions to the knowledge of hard ticks (Acari: Ixodidae) in Colombia. Ticks Tick Borne Dis. 9(1):57-66. 10.1016/j.ttbdis.2017.10.008 [ Links ]

47. RODRÍGUEZ-VIVAS, R.I.; APANASKEVICH, D.A.; OJEDA-CHI, M.M.; TRINIDAD-MARTÍNEZ, I.; REYES-NOVELO, E.; ESTEVE-GASSENT, M.D.; PÉREZ DE LEÓN, A.A. 2016. Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico. Vet Parasitol. 215:106-113. 10.1016/j.vetpar.2015.11.010 [ Links ]

48. STOTHARD, D.R.; FUERST, P.A. 1995. Evolutionary analysis of the spotted fever and Thyphus groups of Rickettsia using 16S rRNA gene sequences. Systematic and Applied Microbiology. 18(1):52-61. 10.1016/S0723-2020(11)80448-0 [ Links ]

How to cite: Zapata-Serna, Y.; Rojas-Rodríguez, A.E.; Pérez-Cárdenas, J.E.; Aricapa-Giraldo, H.J.; Hidalgo-Diaz, M.; Rivera-Páez, F.A. 2022. Prevalence of rickettsias in ticks (Acari: Ixodidae) collected in domestic animals of the northern region of Caldas department, Colombia. Rev. U.D.C.A Act. & Div. Cient. 25(1):e1850. http://doi.org/10.31910/rudca.v25.n1.2022.1850

Open access article published by Revista U.D.C.A Actualidad & Divulgación Científica, under Creative Commons License CC BY-NC 4.0

Official publication of the Universidad de Ciencias Aplicadas y Ambientales U.D.C.A, University, Accredited as a High-Quality Institution by the Colombian Ministry of Education.

Edited by: Helber Adrián Arévalo Maldonado

Funding: This project was funded by the Catholic University of Manizales, through agreement N°100 of the academic council of December 18, 2014, by the University of Caldas, project code: 0766914 and by Colciencias, project code: 112765740609, contract 684 of 2014.

Received: August 06, 2021; Accepted: February 14, 2022

*correspondence autor: labmicro@ucaldas.edu.co

Conflict of interest:

The manuscript was prepared and reviewed by all authors. The authors declare that there is no conflict of interest for the publication of this manuscript that would jeopardize the validity of the results obtained.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License