Wild and domestic animals likely involved in rickettsial endemic zones of Northwestern Colombia

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Abstract

Between 2006 and 2008, three outbreaks of human rickettsiosis occurred in Northwestern Colombia (municipalities of Necoclí, Los Córdobas and Turbo), with case fatality rates between 27% and 54%. The aim of this study was to determine previous exposure of wild and domestic animals to spotted fever group (SFG) rickettsiae through serological tests, to detect rickettsial evidence in their ectoparasites, and to analyze their possible role in the epidemiology of rickettsial diseases in this zone of the country. A cross-sectional association study was performed from 2010 to 2011. Blood and ectoparasite samples were collected from domestic animals and small mammals. A statistically significant association (p < 0.05) between seropositive animals and the study zones was observed. A total of 2937 ticks, 672 fleas and 74 lice were collected and tested in pools by PCR. The minimum infection rate (MIR) of the positive pools was 5% in ticks, 4% in fleas, and 0% in lice. Phylogenetic analyses showed circulation of three 4.Rickettsia species: R. felis in fleas, and R. bellii and Rickettsia sp. strain Atlantic rainforest, both in Amblyomma ovale ticks. In conclusion, this study demonstrated the occurrence of SFG rickettsiae in domestic, synanthropic and wild animals, and suggests the use of equines and canines as good sentinels of infection, in the study zone. We speculate that a transmission cycle exist involving rodents in the areas where these outbreaks have occurred. Tomes' spiny rats (Proechimys semispinosus) and common opossums (Didelphis marsupialis) could be good candidates as amplifier hosts for SFG rickettsiae in enzootic/endemic zones.

Introduction

Rickettsia spp. are obligate intracellular bacteria transmitted by hematophagous arthropods such as fleas, mites, ticks and lice (Fournier and Raoult, 2007). Most of these arthropods are thought to be vectors, but some may also act as reservoirs for some rickettsial human pathogens (Fournier and Raoult, 2007). The genus Rickettsia has been divided into four groups (Typhus, TG; Spotted Fever, SFG; Transitional, TRG; and Ancestral, AG) (Gillespie et al., 2008), from which the SFG and TG have the most important public health concern (Fournier and Raoult, 2007).

The first reported outbreak of a tick-borne rickettsiosis in Colombia occurred in 1934 in the town of Tobia (Department of Cundinamarca), when the disease was named “Tobia spotted fever”. This episode was caused by Rickettsia rickettsii, and produced 62 deaths from 65 cases (95% fatality rate) (Patiño, 1941; Patiño et al., 1937). In February 2006, an outbreak of human rickettsiosis occurred in the municipality of Necoclí Colombia, five of the 14 individuals who fulfilled the case definition died (Acosta et al., 2006). This episode was followed by two more in the municipalities Los Córdobas where six of the 11 confirmed patients died (Hidalgo et al., 2007), and Turbo with four of the 15 individuals who fitted the case definition died (Giraldo et al., 2008). All of these outbreaks occurred in neighboring towns in northwest Caribbean coast of Colombia and all of them were confirmed as caused by R. rickettsii.

Different studies have been performed in Colombia to establish the rickettsial transmission cycle involving humans and animals. In 2013, an eco-epidemiological study in Urabá (Antioquia) reported 6 patients (3%) with active infection for SFG rickettsiosis shown by seroconversion. Researchers also found wild and synanthropic SFG-seropositive rodents and obtained a sequence of Rickettsia (gltA gene) from an Amblyomma sp. larva, which showed an identity of 99% with Rickettsia tamurae in a Bayesian analysis (Quintero et al., 2013). Furthermore, a new species found in Colombia has been preliminarily called Rickettsia sp. strain colombianensi, and the circulation of R. bellii in ticks and of R. felis in fleas has also been described (Miranda et al., 2012, Miranda and Mattar, 2014, Ramirez-Hernandez et al., 2013).

The goal of this study was to assess rickettsial infection in wild and domestic animals and their ectoparasites in the three zones of Colombia where the last outbreaks occurred. Specifically, we show the presence of distinct species of Rickettsia and their possible reservoirs, likely amplifiers and vectors involved in the enzootic/endemic condition found in this region of the country.

Section snippets

Study area

The study areas correspond to the villages of Alto de Mulatos (Municipality of Turbo, 08°08.272′N, 076°33.009′W) and Las Changas (Municipality of Necoclí, 08°32.892′N, 076°34.429′W); located in the Urabá region (Deparment of Antioquia) and the Contrapunto and Corea districts (Los Córdobas municipality 08°50.813′N, 076°20.294′W) in the Department of Córdoba. Hereafter we will call each sampling zone using the municipality name as either Turbo, Necoclí or Los Córdobas. These three sites comprise

Results

The period for the fieldwork in the two regions did not coincide because of safety concerns. Consequently, there was a one-year disagreement between the schedules of Antioquia, September 2010 and October 2011, and Córdoba, June 2011 and June 2012.

A total of 656 specimens were included in the study: 52% (n = 340) from domestic animals, 36% (n = 236) from synanthropic rodents (Rattus rattus and Mus musculus) and 12% (n = 80) from wild small mammals (marsupials and rodents). The animals were distributed

Discussion

The serological results from domestic animals showed high percentages of seropositivity (between 40 and 60%). The frequency of seropositivity in domestic animals varied significantly according to the sampling study area, with the highest positivity in Necoclí with an OR of 5.16 (95% CI: 2.83–9.41). The positivity was similarly associated with the animal species, with equines having a 46% seroreactivity (horses n = 47, donkeys n = 47 and mules n = 33) and canines having 41% (n = 135) IFA seropositivity.

Funding

We thank Colciencias for their financial support through project No. 111549326228 [Ecological study of Rickettsia endemicity in Colombia] “Estudio ecologico de endemicidad por Rickettsia en Colombia”. We are also grateful with the 2013/2014 University of Antioquia sustainability program for their financial support.

Conflict of interest

The authors have no conflict of interest to declare for the publication of the results presented in the manuscript.

Acknowledgements

We would like to acknowledge the community leaders and health workers of Las Changas, Alto de Mulatos and Los Córdobas for their cooperation and help in obtaining the samples. We would also like to thank Daisy Gómez, Edwin Osorio and Laura Vargas from the Mammalogy Group at the University of Antioquia (Grupo de Mastozoología y Colección Teriológica de la Universidad de Antioquia, CTUA) for their assistance in the identification of rodents; Luis Enrique Paternina from CENTAURO Group at the

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