Housing Conditions Linked to Tick (Ixodida: Ixodidae) Infestation in Rural Areas of Colombia: A Potential Risk for Rickettsial Transmission

Abstract

This cross-sectional study explores the different conditions related to the infestation of ticks in households and the potential risks for rickettsial transmission in Urabá, Colombia. The main outcome of interest was villagers’ perception of tick infestation. The data were analyzed using a clog-log mixed regression model. Ticks were collected from infested humans to diagnose infection by spotted fever group rickettsiae (SFGR). In addition, a thematic analysis of qualitative data from key informants concerning knowledge about ticks was conducted. The prevalence of infestation of ticks in households was estimated at 60.99% (95% CI: 51.58–93.51). The multivariate model suggested that households with palm leaf roofs (PR = 1.95; 95% CI: 1.19–2.95), canines (PR = 1.76; 95% CI: 1.21–2.46), rats (PR = 2.19; 95% CI: 1.45–3.08), and with the presence of opossums in areas surrounding the households (PR = 1.51; 95% CI: 1.05–2.10) had a higher prevalence of tick infestation. Two samples of the tick species Amblyomma patinoi were found infected with Rickettsia amblyommatis and Candidatus Rickettsia colombianensi. A thematic analysis provided the names that local community members give to ticks, areas where ticks are common, and the individuals at risk of infestation. The presence of domestic, synanthropic, and wild animals suggests a high risk of the dissemination of ticks inside dwellings and close to them in these rural areas.

Urabá, Antioquia, is one of the regions of Colombia with the highest indicators of unmet basic needs. These unmet needs are mostly observed in rural communities where basic resources, such as clean drinking water and sanitary sewage systems, are precarious. The dwellings are frequently built with thatched or wood roofs and dirt floors. Areas surrounding the houses are characterized by the cultivation of rice, yucca, cocoa, and tomato, for the purposes of household consumption and/or sale. The economy in the region is based on agricultural products, including crops of rice, corn, cacao, yucca, and yam, as well as livestock products. In addition, the cultivation of teca trees (Tectona grandis) is replacing areas previously used for crops or livestock.

Urabá is one of the regions of Colombia with the highest indices of vector transmitted diseases, such as malaria and dengue (Arroyave et al. 2013), and of the main emergent and re-emergent diseases in the country (Cardona-Ospina et al. 2015). Tick-borne rickettsiosis or Spotted Fever Rickettsiosis (SFR) is one of the diseases that produced deadly outbreaks in rural regions of Urabá, Colombia, in 2006 and 2008 (Acosta et al. 2006, García Pacheco et al. 2008). These outbreaks were caused by Rickettsia rickettsii, which is transmitted to humans by tick bites.

Ticks, being some of the most versatile vectors in the transmission of pathogenic agents such as bacteria, viruses, and protozoans, are ectoparasites that (unlike mosquitos) are necessarily hematophagous in all their stages and both sexes (Guglielmone et al. 2014). In total, 283 hard tick species have been found infesting humans worldwide (Guglielmone and Robbins 2018), specifically the genus Amblyomma is among the most important in the America region due to its capacity to infest a large variety of hosts, including humans, domestic, and wild animals (Labruna 2009, Souza et al. 2009). Furthermore, it is a genus of tick that is infected by a diversity of species of rickettsiae, such as R. rickettsii, Rickettsia parkeri, and Rickettsia amblyommatis (Nava et al. 2008, Labruna et al. 2011).

The complex Amblyomma cajennense has been one of the most studied and referenced vectors of R. rickettsii in the Neotropics (Horta et al. 2009). Additional species, such as Dermacentor andersoni, Dermacentor variabilis, and Rhipicephalus sanguineus sensu lato are recognized vectors of rickettsioses in North and Central America (Biggs et al. 2016, Dahlgren et al. 2016, Álvarez-Hernández et al. 2017). In Colombia, there have been reports of a diversity of ticks species infected with rickettsiae, especially of Amblyomma genus. Nonetheless, its role as a vector for rickettsioses has not been fully established (Quintero et al. 2013, Faccini-martínez et al. 2015). The objective of this study was to explore conditions of tick infestation in households and to explore the potential risk of transmission of spotted fever group rickettsiae (SFGR) agents in rural areas of Urabá, Antioquia, where there have been deadly outbreaks of SFR.

Materials and Methods

Site and Study Design

An exploratory cross-sectional study was conducted in rural areas of Urabá, Antioquia, Colombia, specifically in two localities: Alto de Mulatos in the municipality of Turbo (8°08′12.5″N 76°33′01.7″W) and Las Changas in the municipality of Necoclí (8°32′52.5″N 76°34′23.7″W) (Fig. 1). The inclusion criteria to answer survey questions were heads of family that could understand and sign the informed consent. Due to safety concerns, individuals suspected of being affiliated to illegal armed groups were excluded from the study.

Sample Size

Nine hamlets were selected from the study area, five from Alto de Mulatos and four from Las Changas. These hamlets were selected based on ease of access, safety (i.e., minimal presence of armed groups) and ecological characteristics influencing the presence of ectoparasites and SFGR transmission (the presence of domestic, wild and synanthropic animals, as well as forest fragmentation and deforestation). A census of households was performed in each of the nine hamlets to obtain a sample frame. In total, 461 households were registered in the census, of which 225 were located in areas with a higher concentration of households connected by sidewalks and located close to the health center, and 236 were located at the periphery in areas with a lower density of households spread along access routes. A random finite proportional sampling was designed and a sample size of 208 households was estimated, with a 5% error, 95% confidence level, and 50% household tick infestation, considering that the actual proportion of infestation was unknown (Fig. 1).

Outcome and Exposures

The main outcome data were obtained with the administration of a 51-item survey of heads of households (male or female). Trained personnel conducted the survey between November 2015 and January 2016. The main outcome variable was a history of the presence or absence of ticks inside households according to Campbell-Lendrum et al. (2007). Exposure variables were the materials of the dwellings, such as types of roofs, walls, and floors. Other exposure variables were types of crops, trees, and bushes; the presence of domestic animals such as equines, pigs, poultry, felines, and canines; the presence of synanthropic rodents and opossums in dwellings and in areas close to the dwellings; the agricultural practices of household members, such as deforestation and forest fragmentation for crop use; outdoor work (ranchers, farmers, and day laborers); the use of white clothes and long sleeve shirts for working outdoors; personal cleaning of tick infestation after working outdoors; and the measures taken to control rodents in dwellings. In addition, household location and density were included as exposure variables.

Semi-Structured Interviews

A thematic analysis of qualitative data was performed. Semi-structured interviews with four key informants were conducted by a research assistant to gain an understanding of the type of knowledge about ticks in Alto de Mulatos. The interviews sought to learn the common names used for ticks in the region, measures taken to eliminate tick infestation, risk perception of ticks, locations at higher risk of tick infestation, and knowledge about main tick hosts. Interviews were not performed in Las Changas because of the armed conflict between the Colombian National Army and illegal armed groups operating in the region.

Key informants were chosen using a purposeful sampling method. Two interviews were conducted with individuals whose relatives had died in the SFR outbreak that occurred in 2008, and two were conducted with agricultural workers who are at risk of tick infestation. The interviewees resided in Alto de Mulatos, three were males of 54, 63, and 64 yr of age and were involved in agricultural work. The fourth participant was a 28-yr-old college student woman. The interviews were done face-to-face at the households of the participants in mid-2016.

The interviews were digitally audio-recorded and transcribed verbatim. The interviewer also kept a field journal, where direct observations of the study region were documented. The transcriptions were coded to relevant accounts. Codes related to the common names of ticks used by the participants, methods used by participants for tick extraction when they were infested, measures used for controlling pruritus after tick bites, tick hosts, places of higher risk, and people at risk of tick infestation.

Collection of Ticks Infesting People

Surveyed heads of households were asked to collect infesting ticks in tubes containing 70% alcohol that were provided to each household. They were instructed to not collect ticks from domestic animals. A careful visual inspection of ticks was done to detect if there were traces of animal hair (i.e., suggesting that the ticks had been collected from animals). Hard ticks were identified using the morphological keys of adult and immature stages (Barros-Battesti et al. 2006, Martins et al. 2010). Argasids were identified according to morphological descriptions of Ornithodoros genus (Acari: Argasidae) (Endris et al. 1989, Venzal et al. 2008). Adults of the Amblyomma cajenense complex were identified using the morphological characteristics previously reported (Nava et al. 2014). In addition, sequencing of 12S mtDNA was used to confirm the morphological identification of a random selection of specimens of the Amblyomma cajenense complex (n = 10), A. sabanerae (n = 1), and all tick specimens positive to SFGR (two pools). The tubes were both distributed and collected between December 2015 and May 2016 (Quintero et al. 2017), and between November 2016 and May 2017. The samples were sent to the laboratory of Ciencias Veterinarias—Centauro of the Universidad de Antioquia for identification of tick species, sex, and stages.

Molecular Diagnosis of Rickettsial Infection in Ticks

DNA extraction of ticks was performed using a Thermo GeneJet DNA Purification kit. Some samples were prepared in pools according to the same stage, sex, or household (77 pools). Pools were compound by a maximum of eight individuals for larvae stage, seven for nymph stage, and three for adults (engorged ticks [>10 mg] were cut in sterile Petri dishes using a sterile scalpel blade). To evaluate the presence of DNA inhibitors in the sample, the 12S mtDNA was amplified by a conventional polymerase chain reaction (PCR) in all collected ticks (Beati and Keirans 2001).

To detect SFGR, a real-time PCR of gltA amplifying a fragment of 146 bp was used. Primer and probe sequences were gltA-F 5′-GCTCTTCTCATCCTATGGCT-3′, gltA-R5′-AGACATTGCAGCGATGGTAG-3′ and 5′-56FAM-TGCGGCTGTCGGTTCTCTTGCGGCA-3BHQ_1-3′ (Quintero et al. 2017). The amplification was performed in a LightCycler 96 Real-time-PCR System using the FastStart Universal Probe Master Mix Roche. A larger DNA fragment of gltA (401 bp) (Guedes et al. 2005) and ompA (631 bp) (Fournier et al. 1998) was amplified and sequenced in positive samples detected by real-time PCR. Positive control was DNA from Rickettsia rhipicephali donated by Laboratório de Doenças Parasitárias of Universidade de São Paulo, Brazil.

Phylogenetic Analysis

Sequences of gltA and ompA from SFGR agents and 12S mt DNA from ticks were edited in Geneious. Consensus sequences were aligned to reference sequences obtained from GenBank. Bayesian phylogenetic analysis was performed using Markov Chain Monte Carlo (MCMC) sampling implemented in MrBayes 3.2.6, under the best model selected according to the Bayesian Information Criteria in jModeltest2. The MCMC search was run for 1 × 10⁶ generations with trees sampled every 200th generations and a burn-in length of 100.000.

Statistical Analysis

Relative and absolute frequencies were reported for dichotomous and polychotomous variables. A complementary log–log mixed regression was used for bivariate and multivariate analyses. The random effect of the model was hamlets with a variance component correlation matrix, and variables with P ≤ 0.25 in the bivariate analysis were included in multivariate analysis. The final multivariate model was built using the stepwise method according to researcher’s criteria. Prevalence ratio estimates were calculated according to Penman and Johnson (2009). Confounder effect was assessed in the model and the best model explaining the outcome was selected according to AIC (Akaike’s Information Criteria) and BIC (Bayesian Information Criteria). Prevalence ratios and their 95% CIs adjusted by random effects (hamlets) and P-values are presented. All statistical procedures were conducted in PROC GLIMMIX of SAS version 14.2.

Results

Prevalence of Tick Infestation in Households

About 246 households were surveyed, 103 in Alto de Mulatos, and 143 in Las Changas. Outcome data from five households was lost, two from Alto de Mulatos and three from Las Changas. A prevalence of infestation of ticks in households was estimated at 60.99% (95% CI: 51.58–93.51). In Alto de Mulatos, 80.20% of households were infested and 47.14% of households were infested in Las Changas.

Characterization of Households Infested With Ticks

Of the households with tick infestation, 51.70% had thatched roofs (partially or entirely), 0.41% of the households had cement roofs, 3.40% tile floors, and 74.15% had dirt floors (partially or entirely). About 25.17% of the infested dwellings had brick and cement walls, and 95.52% wooden walls (Supp Table 1 [online only]).

Characteristics of Areas Around Households

Of the households infested with ticks, 93.20% had trees nearby (10 m from the households), 61.22% had grass, and very few households (between 2.04 and 8.16%) grew crops nearby (e.g., rice, yam, yucca, tomato, corn, and cocoa). Furthermore, 86.39% of the households reported synanthropic rodents, 54.55% reported the presence of opossums in areas near the house, and 63.27% reported canines inside and outside of the houses. Additional characteristics of areas surrounding the households of infested and noninfested houses are described in Supp Table 1 (online only).

Tick Identification Collected From People and Analysis of Rickettsial Infection

In total, 380 ticks were collected from 40 households, 14 from Las Changas, and 26 from Alto de Mulatos. Most of the ticks infesting humans belonged to the genus Amblyomma (n = 323/380, 85%). We identified by morphology species of Amblyomma patinoi from A. cajennense complex (n = 45 adults), Amblyomma ovale (n = 1 adult), Amblyomma sabanerae (n = 1 nymph), and Amblyomma spp. (n = 181 nymphs and n = 94 larvae). The stage of Amblyomma genus most frequent found infesting human was the nymph (181/323, 56.05%). Identification of A. patinoi (10 specimens randomly selected) and A. sabanerae (nymph) were confirmed by 12 mt DNA (Fig. 1 and Supp Fig. 2 [online only]).

Other tick species identified by morphology was Rhipicephalus microplus and Dermacentor nitens. Besides, we identified two females of Ornithodoros (Alecterobius) puertoricensis of the family Argasidae infesting humans (Table 1).

Two tick pools (one pool of six nymphs and the other of five nymphs) were infected with SFGR. The ompA sequences from the pool of six nymphs was closely related to R. amblyommatis in the Bayesian phylogenetic analysis (92% posterior probability support; Fig. 3). However, the gltA sequences from these individuals were closely related to Rickettsia honei (98% posterior probability support; Fig. 4). The pool of six nymphs was identified as A. patinoi by phylogenetic analysis of 12S mtDNA (99% probability support; Fig. 2).

The pool of five nymphs was infected with Candidatus R. colombianensi according to Bayesian phylogenetic analysis of ompA and gltA (100 and 95% posterior probability support, respectively; Figs. 3 and 4). This pool of five nymphs was identified as A. patinoi of A. cajennense complex by Bayesian phylogenetic analysis (Supp Fig. 3 [online only]).

Bivariate and Multivariate Analyses

For multivariate analyses, characteristics of dwellings, their surroundings, and the presence of animals were included (Supp Table 1 [online only]). The analysis showed that dwellings with roofs partially or fully built with vegetation material had 1.95 (95% CI: 1.19–2.95) times the prevalence of tick infestation compared to the dwellings with roofs without this type of material. The presence of domestic animals such as canines in the households increased 1.76-fold (95% CI 1.21–2.46) the prevalence of tick infestation. Similar results were found in relation to the presence of synanthropic rodents (PR = 2.03, 95% CI 1.45–3.08) and opossums (PR = 1.52, 95% CI: 1.05–2.10; Model 5, Table 2).

According to the AIC and BIC criteria, the model that best explains tick infestation is Model 5, which takes into account the characteristics of the materials of the dwellings (roofs of vegetable material), and the presence of domestic animals (canines), synanthropic rodents, and opossums. The variability across the nine hamlets did not significantly explain the variability found for tick infestation among households (Table 2).

Knowledge and Practice Related to Ticks

Key informants described ticks as a bothersome problem which is more frequent at certain times of the year, especially in the summer, and which affects canines, horses, and people. According to the interviewees, constant contact with this arthropod is quite common. They stated that the individuals most at risk of being bitten by ticks are men that work in the fields and children that play in areas with lots of grass (Fig. 5).

“I think you can’t imagine how many ticks there are here in the summer…say you are just walking and one tiny leaf can be full (of ticks), so if you have a white skirt you can see it coffee coloured from ticks…people say “I won’t get close to the horse because ticks will stick to me…but they get to you easier when you go walking and from one little plant, one little leaf, one tree…they just stick to you, it’s amazing…there are lots of ticks.”

(Interview. 28-year-old women. Alto de Mulatos, Turbo, 2016)

Measures taken to get rid of ticks are essentially the task of the female partner of the individual affected. They put pressure on the tick with their fingers or nails, consequently increasing the risk of secondary infections by leaving parts of the hypostome of the tick under their skin.

During the visits to the study area, we observed one person with scar as consequence of tick bite, with fever and regional lymphadenopathies, signs that are compatible with R. parkeri rickettsiosis (Fig. 6). None of these cases had been diagnosed in the Urabá region. This case was discarded after negative results in serological tests performed in both acute and convalescence phases of disease. It is likely that these lesions could be the result of incorrect extraction of ticks from the skin.

“Q: How do you remove the ticks?

A: I scratch it and take it out, pull it out.

Q: With the nail?

A: Yes, entirely.”

(Interview. 64-year-old male. Alto de Mulatos, Turbo, 2016)

“Sometimes a little piece still remains.”

(Interview. 63-year-old male. Alto de Mulatos, Turbo, 2016)

The interviews suggested that although it is mostly men that bring them in, women groom the men thus also become a source of dispersion of ticks within the household because ticks could get attached to their clothes. In that sense, they would be an accidental source of infestation. Furthermore, men seem to see ticks as a routine matter with low-risk perception, given that they expect their partners to remove the ticks from their body.

“Q: When was the last time you had a tick stuck on you?

A: When was the last time? Ask my wife, she is the one that removes them.”

(Interview. 63-year-old male. Alto de Mulatos, Turbo, 2016)

Interviewees reported that they use common alcohol, menthol, or mentholin to decrease the itch and hives from tick bites. They also reported applying a substance called ‘contra’, which is hard liquor mixed with certain roots. Interviewees believe that ‘contra’ has medicinal properties and that it is useful for lesions from tick bites.

Q: What do you take when the tick leaves a hive?

A: I don’t take anything, I spread alcohol or menthicol or hard liquor if I have nearby, I rub with hard liquor that you prepare with “contra”.

(Interview. 64-year-old male. Alto de Mulatos, Turbo, 2016)

It was valuable to learn the actual names used in the hamlets to refer to the different stages and species of ticks. The different names are partially related to the size, color, or animal on which they are found. For instance, names such as ‘Cuscua’ or ‘Naiví’ for small ticks, ‘Pancha’ for medium sized ticks, and ‘Rolera’ for large and red ticks. A name by species that seems to be considered distinct from the others is the ‘common’ tick of dogs. A common and bothersome tick is known as ‘Rolera’ that according to the interviewees causes the majority of incidents. The name ‘Rolera’ is probably given to the species A. cajennense as these were recognized by some villagers in images of ticks shown to them.

Given that incidents of tick infestation seem to be a matter of everyday life, the interviews suggested that ticks are not perceived as a risk. While growing up, these individuals felt that these annoyances were part of their everyday life being in and out of farm fields and areas of outdoor recreation.

Afterward you just get used to ticks, because in reality you get used to them, I see a tick walking up and I shake myself, just normal, I do not get alarmed.

(Interview. 28-year-old woman. Alto de Mulatos, Turbo, 2016)

Observations in the area showed that in the more concentrated areas of the hamlets, dogs are not treated as pets and are considered street animals. For the most part, these dogs gather around households or public institutions. Prevention measures to avoid tick infestation in canines (e.g., frequent bathing with organophosphates or other products) seemed to be inadequate, since this study showed that ticks were infesting a large number of canines in the region. More so, study participants thought that canines self-removed ticks while bathing in rivers or other water sources.

Discussion

In Latin America, there have been reports of ticks in dwellings (particularly of the Argasidade family) that pose potential risks of infestation in humans. These reports show dwelling characteristics similar to those of the majority of dwellings in the Urabá region, including wood and cement walls, and dirt floors. In addition, in the surroundings of the residences with tick infestations, domestic and wild animals such as pigs, poultry, agouties, opossums, and squirrels were observed (Kohls and Hoogstraal 1961, Nava et al. 2013, Labruna et al. 2014, Bermúdez et al. 2017).

The majority of epidemiological studies that explore dwelling conditions related to the presence of arthropods find a strongly linked to infectious diseases (Malaviya et al. 2014). For instance, Chagas disease is strongly associated with certain characteristics of the dwelling due to the presence of insects of family Reduviidae, which are the insects that transmit the parasites that cause the disease. In the Mexican peninsula of Yucatan, it was found that dwellings that had certain characteristics such as the presence of poultry, dogs, piles of rocks that provide cover for arthropods, and proximity to vegetation were favorable to the presence of Triatoma dimidiata, the vector for Chagas in that area (Dumonteil et al. 2013). In Latin America there are few studies that seek to determine or describe the relationships between dwelling characteristics and tick infestation. This is because most reports focus essentially on the ecological conditions of the different tick species (Cabrera and Labruna 2009, Nava et al. 2009).

Unlike reports in other countries of tick infestation in people, in Colombia, there are few studies aimed at reporting these incidents of infestation. For instance, in Argentina, there have been studies of several species of ticks that infest humans, such as Amblyomma neumanni, Amblyomma parvum, and Amblyomma tigrinum, that have been reported to be linked to incident cases (Nava et al. 2006a,b, 2009). The risk due to infestation is also known for ticks of the other families, like the species Otobius megnini (Nava et al. 2006a). Similar findings to those of our study have been reported in the northern province of Misiones, Argentina, where several human-infesting species of ticks have been found among them, A. ovale and R. microplus (Lamattina and Nava 2016).

Rhipicephalus microplus and D. nitens, tick species strongly associated with bovines and equines (Nava et al. 2017), were found infesting humans in the rural areas of Urabá, indicating close contact between humans, bovines, and equines. In fact, dwellings that submitted samples of ticks identified as R. microplus and D. nitens had bovines and equines near the household or were in constant contact with these animals.

Furthermore, in Brazil, as in other Latin American countries, reports of tick infestation are mostly associated with the genus Amblyomma. Species such as Amblyomma sculptum, A. dubitatum, and Amblyomma aureolatum are of high relevance for the transmission of disease in areas where the interception between agents, vectors, and amplified hosts is present (Szabó et al. 2013). Colombia is no different from these other countries. The genus Amblyomma has been reported as a potential vector of disease in the center and north of the country (Londoño et al. 2014, Faccini-Martínez et al. 2016). In the Municipality of Villeta, Cundinamarca, the species A. patinoi with the potential risk of infestation and transmission of R. rickettsii that can cause the most lethal form of rickettsioses has been reported (Faccini-martínez et al. 2015).

To date, the species of A. cajennense complex reported in Colombia are A. patinoi and Amblyomma mixtum and are located in the center of the country and in the Llanos Orientales (Rivera-Páez et al. 2016). In the present study, it was confirmed the presence of A. patinoi infesting humans in the Urabá region. However, it is also possible that A. mixtum is present in this region.

The number of incidents caused by the nymph stage of the genus Amblyomma is noticeable, and it is highly probable that the main vector of rickettsiae in this area at this stage is due to the aggressive infestation and its infection with the species of the genera Rickettsia (Candidatus R. colombianensi and R. amblyommatis). These species would not be so pathogenic to humans but could play an important role in the epidemiology of SFR (Dahlgren et al. 2016).

In this study, a nymph of A. patinoi infected with R. amblyommatis was infesting one person from Alto de Mulatos. Similarly, R. amblyommatis have also been reported infecting A. sculptum ticks collected in humans in Brazil and infecting A. mixtum ticks collected in equines and vegetation in Panamá and Costa Rica, respectively (Castro et al. 2015, Nunes et al. 2015, Troyo et al. 2016).

Additionally, in this study, it was found that A. patinoi infesting humans in Alto de Mulatos and detected infected with Candidatus R. colombianensi. In another study conducted in the same area, one tick of Amblyomma dissimile attached to the clothes of one person was also infected with Candidatus R. colombianensi (Quintero et al. 2017). This species is commonly found infesting reptiles and amphibians (Nava et al. 2017) and must be considered a potential agents of tick transmitted infections. Whether Candidatus R. colombianensi produces clinical symptoms or is a member of the tick’s microbiota is unknown. In any case, it must be considered a potential agent if it causes febrile syndromes.

Recently in the Urabá area, there were reports of A. ovale collected from canines infected with R. parkeri strain Atlantic rainforest (Quintero et al. 2017). This species of Rickettsia has been documented as causing clinical cases in Brazil (Barbieri et al. 2014). It could have the potential to cause clinical cases in Urabá, Antioquia, as has been demonstrated by cases of infestation with A. ovale, found in humans both in Alto de Mulatos and Las Changas.

Amblyomma ovale in its adult stage is commonly found in canines, but immature stages are found in mammals of the orders Rodentia (Cricetidae, Echimyidae, Muridae, Heteromyidae), Carnivora (Procyonidae), Coraciiformes (Momotidae), and Passeriformes (several families) (Guglielmone et al. 2014). Another important animal in the cycle of infestation of immatures is Didelphis marsupialis (Guglielmone et al. 2014), an opossum species common in the study area that is known as ‘zorra chucha’ (piglet fox) or ‘zorra canguro’ (kangaroo fox).

Another study found A. varium infected with R. amblyommatis infesting humans in the same study area (Quintero et al. 2017). This finding broadens the options of tick species and SFGR that could be involved in the transmission cycle in the study area. The tick species A. varium, in its immature stages, has been found infesting mammals of the family Bradypodidae, commonly known as sloths, albeit without reports of human infestation (Guglielmone et al. 2014).

A nymph of A. sabanerae, infesting one person in Las Changas, was identified using phylogenetic analysis of 12S mtDNA. Frequent hosts for nymphs and adult of this species are Testudines: Emydidae; in addition Didelphimorphia are considered exceptional hosts for this tick species (Guglielmone et al. 2014). In Summit Municipal and Soberanía National Parks, Panama, there were reports of human infestations with A. sabanerae (Bermúdez et al. 2012).

Aside from hard ticks, in this study several specimens of the species O. puertoricensis were found, a tick species that belongs to the family Argasidae and that is commonly known as soft ticks. This tick species has several hosts, among them synanthropic and wild rodents, particularly in its immature stages (Quintero et al. 2013). This species in its immature stages has also been found in canines on the Atlantic coast of Colombia (Paternina et al. 2009). In La Laja, province of Los Santos, Panama, there were reports of infestation of soft ticks of the genus Ornithodoros in a woman who lived in this area (Rangel and Bermúdez 2013). The possibility that it could be a species (specifically the species O. talaje and O. rudis) that can transmit diseases such as recurrent fevers caused by bacteria of the genus Borrelia cannot be rejected (Dunn 1927).

The reports of risk perception of the inhabitants of the municipality of Villeta, Cundinamarca, are important in relation to the infestation of ticks and the presence of rickettsioses. To some extent, the inhabitants of areas that have been affected by lethal outbreaks of SFR consider tick infestation as a daily occurrence, a consequence of field labor. Suárez et al., 2004 (Suárez et al. 2008), stated that ‘Ticks, although perceived as bothersome and unwanted animals, are not seen as a threat. In this sense, we can state that the population, in particular in rural areas, coexists with the vector in a pacific way. Ticks are not foreign agents, extraneous to everyday life; in fact, they are considered part of life and work in the fields’.

In this sense, in order to manage preventative measures, it is of crucial importance that people living in areas affected by tick-transmitted diseases are aware of the risks. Knowledge of the affected communities’ perception of risk from these diseases will provide us with a better sense of how to confront the issue in these areas. Although this study did not seek in-depth generation of theories of comprehension, it does provide a first approximation to how people from the study area view ticks and their annoyances. These conditions are closely associated to high indices of unsatisfied basic needs, demonstrated in part by the characteristics of the majority of dwellings in these rural areas, the lack of protective measures, and the precarious handling of pets.

One of the main limitations of the study was the subjective outcome measure, given the potential bias in the information, particularly related to recall bias. We decided to obtain subjective outcome data due to the conditions in these rural areas (the constant armed conflict between the Colombian Army and illegal armed groups), the limited number of field researchers to objectively obtain outcome data (i.e., direct collection of ticks in each of the selected dwellings). The subjective outcome measure is related to explanatory variables with biological plausibility. It would be important to validate this information with studies using objective outcome measures to quantify ticks that are collected in dwellings of the study area during a certain time period.

Conclusions

Urabá, Antioquia, is an area in Colombia that has one of the highest indices of social inequity. This has created conditions in dwellings that are favorable to the infestation of ticks. Consequently, it increases the probability of cases of infectious diseases transmitted by ectoparasites. The presence of vegetable material in the roofs of dwellings, and the presence of domestic, synanthropic, and wild animals, are potential risks factors for the infestation of ticks in and around the households. The study provides evidence for the need to develop government initiatives to improve infrastructure conditions of the dwellings, as well as educational programs that may shift perceptions in relation to how to care for domestic animals and to eradicate rodents from dwellings.

Ethics Approval and Consent to Participate

This study was approved by the Committee of Ethics in Research of the Facultad Nacional de Salud Pública (meeting of 22 May 2014) and the Committee of Animal Research of the Universidad de Antioquia (meeting of 10 June 2014). All the study participants signed the informed consent. Participants did not receive monetary compensation for their participation in the study. Participants consent the publication of their images.

Acknowledgments

We are thankful to the Grupo de Investigación en Salud y Ambiente and the Grupo de Epidemiología of the Facultad Nacional de Salud Pública, Universidad de Antioquia (Colombia) for its logistical support. We thank the community of Alto de Mulatos and Las Changas for their participation in this study and Karen Mena, the anthropologist who conducted the interviews in the field. This study was supported by Departamento Administrativo de Ciencia, Tecnología e Innovación (Colciencias) (award: 111565741009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability

Sequence data that support the findings of this study have been deposited in GenBank with the accession codes MF774054, MF774055, MF774056, MF774057, MF774058, and MF774059.

References Cited