Epidemiology of zoonotic tick-borne diseases in Latin America: Are we just seeing the tip of the iceberg?

Abstract

Ticks are responsible for transmission of multiple bacterial, parasitic and viral diseases. Tick-borne diseases (TBDs) occur particularly in tropical and also subtropical areas. The frequency of these TBDs has been increasing and extending to new territories in a significant way, partly since ticks’ populations are highly favored by prevailing factors such as change in land use patterns, and climate change. Therefore, in order to obtain accurate estimates of mortality, premature mortality, and disability associated about TBDs, more molecular and epidemiological studies in different regions of the world, including Latin America, are required. In the case of this region, there is still a limited number of published studies. In addition, there is recently the emergence and discovering of pathogens not reported previously in this region but present in other areas of the world. In this article we discuss some studies and implications about TBDs in Latin America, most of them, zoonotic and with evolving taxonomical issues.

Over the past decades there have been significant achievements in the understanding of tick borne diseases (TBDs), which are mostly zoonoses and classed as neglected diseases ^{1– 5}. Their occurrence is significant in tropical and subtropical areas, leading to an important impact on public health as well as the economy, as they affect humans, domestic animals and livestock, among others ⁶. Knowledge of the occurrence of these diseases in animal species is of utmost importance for the understanding of the risk for human infection ⁷. Ticks, and animals, including human beings, interact with nature, and their environmental and ecological interactions regulate the populations of ticks and vertebrates, determining their contact rates and the circulation of the diseases ⁸. Moreover, although most TBDs are tick-borne, other ways of transmission can occur. For instance, bovine anaplasmosis, caused by Anaplasma marginale, can be spread through mechanical means, e.g. biting arthropods or by contaminated fomites, like needles, ear tagging, dehorning and castration equipment ⁹. A. marginale can be also transmitted transplacentally, which has contributed to the occurrence of bovine anaplasmosis in some areas ¹⁰.

In Latin America, there is a lack of studies about TBDs. However, data from Panama, Brazil, Mexico, Peru, Colombia, and Venezuela clearly show that these pathogens are prevalent when they are assessed. Recently, two lethal cases of rickettsiosis caused by Rickettsia rickettsii were reported in rural and urban of Panama, probably transmitted by the tick Rhipicephalus sanguineus s.l., accounting for the first molecular detection of this bacteria in this tick in Panama and Central America ¹¹. TBDs caused by rickettsial species are life-threatening infections that in the tropical Americas have an emerging and reemerging trend. Until some years ago, R. rickettsia was the only tick-borne species of rickettsia present in Latin America. Nowadays, multiple other species, such as R. parkeri and R. massiliae, are causing infections in humans in this region. In Peru, different ectoparasite samples have tested positive for a Rickettsia genus-specific qPCR, with strong evidence that active searching of TBDs etiological agents is required in order to improve reporting and detection ¹². Additional, new species are being reported; although their pathogenicity has not been definitely confirmed, they should be considered as potential pathogens ¹³.

Ehrlichiosis is another TBD caused by rickettsial organisms of the genus Ehrlichia ^{14, 15}. Canine monocytic ehrlichiosis caused by Ehrlichia canis apparently is highly endemic in Brazil and has been also detected in Mexico, where it is closely related to strains from the USA ¹⁴. In Brazil, E. canis is the principal Ehrlichia specie found in canines and has been also detected in felines, although the prevalence has not been estimated yet. In addition, in Brazil, E. ewingii has been recently detected, as well as E. chaffeensis in marsh deers, and there is immune-epidemiological evidence that suggests the occurrence of ehrlichiosis in humans ^{16, 17}, but its etiologic agent has not yet been established. Improved molecular diagnostic resources for laboratory testing will allow better identification and characterization of ehrlichial organisms associated with human ehrlichiosis in Brazil ¹⁶.

In Colombia, three outbreaks of human rickettsiosis have been reported in the Northwestern region during 2006–2008, with a lethality up to 54% ¹⁸. And later, in 2010–2011 a cross-sectional study revealed the presence of three different Rickettsia species: R. felis in fleas, and R. bellii and Rickettsia sp. strain Atlantic rainforest, both in Amblyomma ovale ticks ¹⁸. Additionally, in Venezuela, detection of Anaplasma platys has been described in humans. Those patients were bitten by Rhipicephalus sanguineus and suffered chronic non-specific clinical signs, including headaches and muscle pains, supporting A. platys as a zoonotic tick-borne pathogen ¹⁹. Other studies from Venezuela have found a high proportion of positivity of antibodies against Babesia caballi and Theileria equi in horses and other animals ²⁰, suggesting that probably the real frequency and importance of these hemoparasites are overlooked.

Babesiosis is caused by any of a group of vector-borne, protozoal hemoparasites of the phylum Apicomplexa. There are more than 110 described Babesia spp. worldwide, identified from mammalian and also avian hosts ^{21, 22}. This group of TBDs is transmitted by ixodid ticks and they infect a wide variety of vertebrates that maintain transmission cycles. Till today, there are multiple species of the genus Babesia that can infect people, and the regional distribution of Babesia microti is the most prevalent. In the USA, babesiosis is caused primarily by B. microti, whereas cases in European countries are commonly caused by B. divergens ²². In countries such as the USA its incidence has increased 260% between 2005–2010 ²³, with a proportion of 40% of cases of Lyme disease reporting co-infections with Babesia. In Latin American countries, particularly Colombia, the seroprevalence of Babesia has been reported has high as 30% from people of urban and rural locations ²⁴. Additionally, recently, new Borrelia burgdorferi sensu lato strains or new related species have been described in countries such as Uruguay, Brazil and Chile ²⁵.

In the USA, some authors suggest that approximately 95% of ~50 thousand cases of locally acquired vector-borne diseases in humans reported annually to the Centers for Disease Control and Prevention are caused by organisms that were vectorized by ticks ( Table 1) ^{6, 26}. Beyond the Americas, in other regions of the world, like in Europe, ticks are the main vectors of animal and human organisms. Ticks transmit several viral agents, called tick-borne viruses (TBV), such as tick-borne encephalitis virus and Crimean-Congo hemorrhagic fever virus, which have reemerged in multiple areas of the world ²⁷. TBV have a natural cycle between ticks and wild animals in nature, with humans as accidental hosts ^{27, 28}. Emerging TBVs are continually discovered, probably related to the increase of tick populations in different regions of the planet and invasion of human beings into areas infested by ticks ^{27, 28}.

Table 1. Examples of selected tick-borne diseases in Latin America.

Modified from Eisen et al. ⁶.

Disease	Etiological agent(s)	Primary vector(s)
Anaplasmosis	Anaplasma phagocytophilum	Ixodes scapularis, Ixodes pacificus
	Anaplasma platys	Rhipicephalus sanguineus
Babesiosis	Babesia microti	Ixodes scapularis
	Babesia canis	Rhipicephalus sanguineus
	Babesia bovis	Rhipicephalus microplus
	Babesia bigemina	Rhipicephalus annulatus
Borrelia miyamotoi disease	Borrelia miyamotoi	Ixodes scapularis, Ixodes pacificus
Colorado tick fever	Colorado tick fever virus (coltivirus)	Dermacentor andersoni
Ehrlichiosis	Ehrlichia muris eauclairensis	Ixodes scapularis
	Ehrlichia chaffeensis	Amblyomma americanum
	Ehrlichia ewingii	Amblyomma americanum
Heartland virus disease	Heartland virus (phlebovirus)	Amblyomma americanum
Lyme disease	Borrelia burgdorferi	Ixodes scapularis, Ixodes pacificus
	Borrelia mayonii	Ixodes scapularis
Powassan encephalitis	Powassan virus (flavivirus)	Ixodes scapularis
Rickettsia parkeri rickettsiosis	Rickettsia parkeri	Amblyomma maculatum
Rocky Mountain spotted fever	Rickettsia rickettsii	Dermacentor variabilis, Dermacentor andersoni, Rhipicephalus sanguineus s. l.
Pacific Coast tick fever	Rickettsia philipii	Dermacentor occidentalis
Tularemia	Francisella tularensis	Amblyomma americanum Dermacentor variabilis Dermacentor andersoni

Detection and sentinel surveillance of TBD require molecular tools for diagnosis ²⁹, for example, serological tests have proven to be inconclusive in diagnose Lyme disease ³⁰. The use of molecular biology tests in recent years has increased the sensitivity and specificity of the diagnosis of infections in the group of Rickettsiales. Molecular diagnosis enables the accurate identification not only at genus level, but species, providing additional characterization on the epidemiology and the evolution of clinical disease. Furthermore, PCR as well enzyme restriction tests of the vector blood meal can be employed to analyze their feeding source and possibly identify the ecological reservoir of the organisms ³¹. Etiological agents of the group of Rickettsial, including those in the genuses Anaplasma, Neorickettsia, Ehrlichia, and Rickettsia, are relevant and often vector-borne organisms of canines and felines, but also of bovine, livestock and other animals, which appears to be a wide range of hosts ^{10, 32}.

Conclusions

Besides the limited number of studies in Latin America on TBDs, the prevalence of these diseases is increasing, triggered by globalization, as well the impact climate change and variability. Tick and TBDs investigators, vet doctors, medical and public health practitioners should work to share their expertise on different aspects of TBDs, such as tick ecology, disease transmission, diagnostics, and treatment, in order to face the challenges of scientific, political, and public engagement for TBD research and control in this region ³³. Systematic reviews as well as observational analyses are necessary in order to understand the current situation of TBDs. Molecular tools can provide valuable information for understanding the evolution of their etiological agents, as well as provide insights into host-pathogen-vector-environment interactions. Probably, what we have seen till now is just the tip of an iceberg and there is a need for more studies in Latin America about TBDs.

Data availability

No data is associated with this article.

Funding Statement

The author(s) declared that no grants were involved in supporting this work.