Presence of Rickettsia Species in a Marginalized Area of Yucatan, Mexico

In the state of Yucatan, Mexico, rickettsiosis has become a common vector-borne disease in the general population. Ectoparasite species such as Rhipicephalus sanguineus and Amblyomma mixtum have been identified as Rickettsia vectors in Yucatan by studies focused on the wild animal population in rural areas. There have been studies that have tried to determine the presence of Rickettsia species in ectoparasites collected in Yucatan, but these studies did not include marginalized areas, where living in close contact with domestic and peridomestic animals that carry ectoparasites is a high-risk factor for acquiring rickettsial infection or many other vector-borne diseases. We evaluated the vector diversity and the presence of Rickettsia species presence in the ectoparasite population that parasitizes domestic animals in a marginalized rural town of Yucatan, Mexico; we also evaluated the seroprevalence of rickettsial antibodies in the human population of this town in order to determine the prevalence of rickettsial infection. A total of 437 ectoparasites were collected from the study area. The tick specimens collected belonged to the species Rhipicephalus sanguineus (n=380, 49 positive), Amblyomma mixtum (n=3, 0 positive), Ixodes affinis (n=4, 0 positive), Ctenocephalides felis (n=33, 0 positive), and Trichodectes canis (n=17, 0 positive). Conventional polymerase chain reaction and sequencing were used to identify the DNA of Rickettsia. Six out of 354 (1.8%) serum samples were positive for antibody to R. typhi. The combination of low antibody titers and the presence of Rickettsia species infecting ectoparasite species found in the study area requires eco-epidemiological studies and the identification of potentially protective practices or habits.


Introduction
In the state of Yucatan, Mexico, rickettsiosis is the main vector-borne disease due to the high presence of tick and flea species in urban and suburban areas [1]. It is well known that rickettsiosis is commonly associated with poverty and rural areas [2]; however, in the state of Yucatan, most of the patients with rickettsiosis live in urban areas. Because of this, very little is known about the transmission dynamics of Rickettsia species in rural areas of Yucatan. A first approach to the study of these dynamics is to assess the seroprevalence of rickettsial antibodies in the population and to examine locally collected ectoparasites to determine the presence of Rickettsia species. This would help us know if the lower rate of rickettsial infection in the rural population of Yucatan could be due to a lower presence of Rickettsia species in rural areas or to practices and habits of the rural population that inhibit the life cycle of Rickettsia sp.

Study Site.
The study was conducted in the Mayapan municipality (20 ∘ 28 05 N-89 ∘ 12 50 W), located southeast from Merida, the capital of Yucatan. It is considered one of the ten most marginalized municipalities in Yucatan, according to a report by the Consejo Nacional de Población (a government department that estimates the marginalization index in Mexico). The population of Mayapan work mainly in agriculture, hunting, and construction jobs in Merida; 2 Journal of Tropical Medicine

Sera.
Serum was collected from the adult population of Mayapan who signed an informed consent form before collecting blood samples. The collected blood samples were allowed to clot at room temperature and then centrifuged; after separating the serum, it was stored at -20 ∘ C until further analysis.

Indirect
Immunofluorescence. Six out of 354 (1.8%) serum samples were positive for antibody to R. typhi, with titers ranging from 1:64 to 1:256; however, no samples positive for antibodies to R. rickettsii were obtained. All but 1 of the subjects positive to exposure were female, with an age range of 30 to 76 years and an average age of 52 years. Of the positive subjects, five reported cohabiting with domestic animals such as dogs and cats, two reported the presence of rodents or rodent droppings in their houses, and none had been exposed to opossums.

Discussion
Important rickettsial diseases are mainly transmitted by tick species like Rocky Mountain spotted fever in the Americas (RMSF) and boutonneuse fever in the Mediterranean region and Africa [7,9,10]. The seroprevalence of rickettsial agents in the rural population studied here contrasts with previous results reported for Yucatan, in which 5.6% of the tested population had positive reactions to different rickettsial antigens [11]. That study included small towns and cities of Yucatan but no marginalized populations. In the study, it is interesting that this infection is less prevalent in a highly marginalized population. Current practices and habits of the rural population that prevent the transmission of infection from reservoirs of the disease might explain this lower prevalence. Some of these practices may include cohabitation with cats, which control the pests that harbor tick or flea species, or with dogs, which keep opossums away from the houses. Because these practices would not explain the exposure to R. typhi, since the flea vectors responsible for its transmission are harbored mainly by the population which is reduced by those practices, rodents and opossums, one might expect an increase in the risk of exposure to R. felis. Given that cats and dogs are usually infested with cat fleas, it is possible that the antibodies detected using R. typhi antigen are actually a cross-reaction with R. felis, but this requires further investigation. The presence of R. rickettsii in R. sanguineus ticks is very interesting and contrasting. This is not the first report of the presence of this Rickettsia species in Yucatan, Mexico, it increases the possibility that R. rickettsii could have a homogeneous distribution, not only in the state of Yucatan but throughout the entire Yucatan Peninsula, using R. sanguineus and A. mixtum as a vector. In contrast, in Baja California, at the north of Mexico, outbreaks of Rocky Mountain spotted fever were associated with an increase in the presence of both R. sanguineus ticks infected with Rickettsia species and stray dogs [9,12]. Further collaboration studies are required to evaluate and compare biological, ecological, and/or evolution factors that contribute to the increase of the possibility of R. sanguineus biting humans in north and south of Mexico. Other tick species (A. mixtum) infected by Rickettsia species such as Rickettsia amblyommatis have been identified by previous studies in the west coast of Mexico [13]. Amblyomma mixtum is important because it frequently bites humans [14] and is considered as the preferred vector of R. rickettsii in other countries in Latin America, commonly Brazil [15][16][17][18].
Since the Rocky Mountain spotted fever (RMSF) is well known to aggressively affect humans and we found the presence of a tick species that frequently transmits RMSF, it is possible to say that the rural population of Yucatan must be at high risk of acquiring rickettsial infection; however, there must be other biological, ecological, or mainly social factors that decrease this risk and which should be analyzed from an eco-epidemiological point of view [19].

Conflicts of Interest
The authors declare that they have no conflicts of interest.