Capybara Ticks and the Urban Context of Spotted Fever in Brazil: An Overview

Abstract

Spotted fever is caused by Rickettsia rickettsii and is transmitted through tick’s saliva. Humans, ticks, and capybaras (Hydrochoerus hydrochaeris) are often coexisting in environments that favor the spread of Brazilian spotted fever (BSF). Although capybaras do not transmit R. rickettsii, they can amplify these bacteria among tick vector populations, playing a significant role in the one health approach and epidemiology of the disease. Urban populations of capybaras have increased, especially in Southeast Brazil, as well as the number of cases and lethality of BSF have increased in the country since the 1980s. This expansion is mainly determined by the availability of food and the absence of predators. Thus, urban areas, including parks and university campuses, provide an abundance of food and protection against predators, ensuring the multiplication of the species and increasing the risk of transmission to humans due to the proximity of man with animals in the urban environment. Therefore, this chapter aims to address aspects of spotted fever, considering the many dimensions of the species involved, contributing to public strategies and policies.

1. Introduction

Brazilian Spotted Fever (BSF) also known as New World Spotted Fever or São Paulo Exanthematic Typhus [1] is becoming increasingly widespread among regions of Brazil. Since 2001, Brazil has reported the urbanization of BMF, particularly in the states of São Paulo and Minas Gerais where the disease is already considered endemic in many areas [2].

BSF is an infectious, multisystemic, and febrile disease caused by the species Rickettsia rickettsii and R. parkeri, which are the first responsible for the most serious manifestations, whose lethality can reach 80%, in situations of late diagnosis or lack of access to health services, common in developing countries. Although the expansion of occurrence spaces can have many causes, a commonly associated ecological element is the presence of capybaras, currently found in water bodies and lawns in urban areas [3]. They participate in the transmission cycle, being considered important amplifiers of vector ticks [4], affecting the endemicity and zoonotic aspects [5] of the occurrences. In fact, these rodents are spreading far beyond rural areas, forming clusters in leisure spaces, parks, and lakes present in highly urbanized cities, making infestation by ticks common in people who visit these places [6, 7].

Vector-borne diseases are relevant to human, animal, and environmental health, as pathogens, vectors, and hosts interact through pathologies and can change their epidemiology over time [8]. When considering the changes promoted by the exploitation of natural resources that result in the fragmentation of habitats and changes in ecosystems, it is possible to assume that there is a greater interaction between humans and arthropod-borne pathogens.

In this context, the global strategic framework for health, created to mitigate the risk and minimize the impact of emerging infectious diseases at the animal-human-ecosystem interface and socio-economy, highlights the need for action in One Health Perspective that fits perfectly with the approaches relating to the BSF. Based on the principles of “one world,” “one health,” the referred framework resulted from an action between specialized agencies, such as the World Health Organization (WHO), the United Nations (UN) Food and Agriculture Organization (FAO), and the International Organization for Animal Health (OIE), which jointly recognized the link between human welfare, animals, and the environment [9]. Diseases involving humans and animals (domestic and wild) should be addressed as a priority in an interdisciplinary manner to combat threats and promote the health of life on Earth [10]. The approach must be holistic for disease prevention and for the integrity of the ecosystem that sustains all forms of life.

Due to the complexity of the parasitic cycle involving different hosts (wild animals, arthropod vectors, and humans), the conditions and variables that affect interactions are not completely understood, particularly when related to vector diseases. Therefore, the present narrative intends to provide some clues for a better understanding of some of the main characteristics associated with the occurrence of BSF.

2. Vector-borne diseases in the urban environment

In 1950, only 30% of the world’s population lived in urban areas. World’s population is increasingly urban with more than half living in urban areas. This number continues to increase, and by 2050, two-thirds are expected to be living in newly urbanized areas [11]. However, the size and density of human populations are creating challenges for many dimensions of human health, including the (re)emergence of zoonotic diseases, particularly those transmitted by vectors [12].

Changes in landscape structure stimulate the loss, rotation, or homogenization of biodiversity, increasing the contact between humans and animals, which can influence the dynamics of transmissions in communities of reservoir hosts and vectors, contributing to modulations in epidemiological processes and the expansion of pathogens that reach the humans [13, 14]. The beginning of the 2020s was marked by a serious pandemic that initially presented itself with zoonotic characteristics, whose cause corroborates the new thinking that as humans spread, pathogens also spread, representing an even greater problem in countries with a large number of poor people and in emerging economies. This is because, in such locations, in addition to much nature being transformed into agricultural or urban areas, health systems are usually underfunded and have difficulties in dealing with possible outbreaks [15].

Cities, as densely populated areas, have always been habitats for domestic animals. For some time, however, they are increasingly housing “wild” animals as they present themselves as safe and well-supplied places where these animals have chosen to survive and raise their descendants. This is because, in their decisions, when choosing a residence, food and security are more attractive than other aspects of the landscape [16]. As a result, a park close to busy streets, with noisy children, has been more attractive to these animals than the curious quietness of rural landscapes, “drenched in chemicals” [17].

Of course, given the complexities of ecosystems and rapid global changes, the effects of land use on the ecological factors that sustain zoonotic occurrences cannot be hastily judged [18]. Although there is evidence that the diversity of local species affects the transmission of pathogens [19], this result is not generic, with the greatest risks for diseases caused by pathogens transmitted by arthropod vectors being proven [20, 21], as in the BSF cycle.

The reason why such pathogens spread after environmental changes is not that we suddenly come into contact with wild animals, such as jaguars and wolves. This hypothesis does not answer the modern questions that involve the maintenance, for decades, of these zoonotic cycles in the most anthropized environments. On the contrary, researchers reveal that most common wild animals, particularly those known to carry pathogens threatening to humans, are more prolific in these areas [15]. However, the biases that cooperate for the intense multiplication of these vectors after the urbanization process are not yet fully clarified. Surprisingly, animals that generally carry many viruses or bacteria seem to better tolerate the destruction of nature, when compared with those that carry fewer pathogens [22]. One reason for this could be that these animals are usually quite small and short-lived or have adaptive immune strategies that do not let them get sick from the pathogens they host.

The tendency for hosts and non-hosts to respond differently to human-induced changes in their habitats has been observed in some specific disease systems, but may contribute to the documented links between anthropogenic ecosystems and emerging zoonoses [21, 23] and for BSF, transmitted in an urban cycle that involves ticks, capybaras, and humans. Hosts with an accelerated life cycle contribute to an increase in their abundance, virtually due to life history trade-offs—between reproductive rate and investment— [24], associated with the ability to be resilient in the face of anthropic pressures [25]. In addition, characteristics such as host status, human tolerance [26], as well as the challenge load and co-evolution of shared pathogens [13] contribute to the clarification of such interactions.

3. Species involved in the transmission of spotted fever in Brazil

BSF is caused by Gram-negative bacteria of the genus Rickettsia (Rickettsiales: Rickettsiaceae), transmitted by vectors that use different vertebrate hosts, altering the endemicity and zoonotic aspects of their occurrence. Due to their strictly intracellular survival, these bacteria are classically transmitted to humans by arthropods, which include ticks, mites, fleas, and lice. However, many non-pathogenic human species have been described, of which the true roles in the ecological relationships with the vectors and with the pathogenic rickettsiae have not yet been fully clarified [27].

Since 2001, Brazil has reported an expansion of transmission areas, which is seriously integrated with the increase in the number of reported cases and in their lethality. The bioagent R. rickettsii is the main species causing BSF, being restricted to the Americas with confirmations, in addition to Brazil, Canada, United States, Mexico, Costa Rica, Panama, Colombia, and Argentina. However, in the country, other rickettsiosis from the spotted fever group has already been isolated, such as Rickettsia parkeri cepa Mata Atlântica and R. parkeri stricto sensu, whose notifications are associated with less severe and, as a rule, non-lethal clinical conditions [28, 29]. Added to this diversity of infectious agents, there is a variety of potential vectors that make the enzootic and epidemic cycle of BMF in Brazil quite complex, as a result of possible eco-epidemiological variations.

Ticks can act as vectors and reservoirs in the transmission dynamics of pathogens from the spotted fever group. Several species of Rickettsia can coexist in the same environment, so that different species of ticks that parasitize different mammals can also become infected. The main ticks implicated in the transmission of R. rickettsii in the United States are Dermacentor andersoni and D. variablilis; in some areas in Mexico and in the state of Arizona in the United States, Rhipicephalus sanguineus has been indicted as the vector; in South America, the tick species Amblyomma cajennense is the most commonly incriminated vector.

However, in the context of the BSF, the following interactions are currently described: [i] R. rickettsii transmitted by the tick Amblyomma sculptum and Amblyomma aureolatum in the Southeast and parts of the South region; [ii] R. parkeri Atlantic Forest strain vectored by Amblyomma ovale in Atlantic Forest fragments in the South, Southeast, and Northeast of the country; and [iii] Amblyomma tigrinum infected with R. parkeri is in the Pampa biome in the South region, distinguishing these Brazilian areas from others in Latin America [28, 30, 31].

Below, images of the two main tick species associated with the transmission of the bacterium R. rickettsii, which causes Brazilian spotted fever (Figure 1).

Figure 1.

Adult male ticks of the species (A) A. sculptum and (B) A. aureolatum. Source: [32].

Bacterial infection in arthropods occurs during hematophagy performed on a rickettsemic, vertebrate host; being favored by transovarian and/or transstadial transmission, which balances part of the damage caused by infection in vector ticks [33]. In turn, the transfer of the pathogen to another vertebrate occurs when the infected ectoparasite takes a new blood meal, after the changes in phases. Thus, the occurrence of Rickettsia in a given space is based on the coexistence of ixodid species susceptible to infection and on vertebrates capable of sustaining this tick’s population. Both can vary over time and space, influencing the epidemic cycle by overlapping human activities with the proximity of other vertebrate hosts and the seasonality of the tick [30, 34].

In this aspect, some key factors in the epidemiology of BSF, particularly the occurrence of R. rickettsii in southeastern Brazil, are already partially clarified and point to the need for amplifying hosts to maintain transmission. Larvae, nymphs, and adults of A. sculptum are partially refractory to rickettsia and less than half of infected females are able to promote transovarian transfer (transmission to offspring) effectively. In addition, higher mortality and lower reproductive performance are observed when the tick is infected, compared with those free from the pathogen [35]. Given this finding, mathematical models indicated that A. sculptum cannot sustain R. rickettsii for successive generations without the genesis of new cohorts of infected ticks, via horizontal transmission, made possible by vertebrate amplifying hosts, during rickettsemia.

Horses are primary hosts of the Amblyoma sculptum tick. They act in the maintenance of these arthropods and in the movement of rickettsiae between environments. Even though they are not susceptible to infection, horses serve as sentinels in epidemiological studies, showing the distribution of the disease and predicting human cases [36]. However, in the contexts of the occurrences, the capybara (Hydrochoerus hydrochaeris) appears as the largest amplifying host of R. rickettsii for A. sculptum in BSF endemic areas in southeastern Brazil [7, 37, 38, 39]. In the state of São Paulo, some areas became endemic for BSF after the detection of an increase in the number of individuals in free-ranging capybara clusters [40].

Thus, the sanitary monitoring of capybara populations is essential for the control and conservation of public health. For the record, it is worth mentioning that the tick Amblyomma dubitatum has also been frequently discovered infesting capybaras in southeastern Brazil, despite not playing an essential role in the epidemiology of BSF [41, 42, 43].

4. Aspects of the epidemiological scenario

The first report of spotted fever in Brazil occurred in São Paulo, in 1929 [1], and R. rickettsii transmitted by the tick A. cajennense was indicated as the causal agent. In the report, the similarities with Rocky Mountain spotted fever were already highlighted. In the following two decades, new occurrences were described in the state of Minas Gerais [44] and in São Paulo, where the species Rickettsia typhi was isolated for the first time [45]. After this period, BSF remained for several years as a silent disease, subordinated to existing flaws in medical care, diagnosis, and information processes.

Between the 1980s and 2000s, case reports are seen in scientific journals, indicating infections that occurred in southeastern Brazilian states, after four cases in Rio de Janeiro [46] and in the state of Espírito Santo, which came to be considered as an endemic region for BSF [47]. The states of Minas Gerais and São Paulo showed a serious reemergence, in whose epidemic outbreaks occurred in 1984, 1992, 1995, and the lethality reached about 50% of diagnosed patients [48, 49, 50]. Despite this, it was only in 2001 that the BSF notification became mandatory and, in 2014, it was determined that, in addition to being mandatory, it must be immediate, taking place within a maximum period of 24 hours, in order to improve surveillance, diagnosis, and treatment [51].

Due to the continuous increase in cases and the expansion of the areas of occurrence, BSF was considered an emerging disease in Brazil, without, however, a significant advance in information and knowledge about the disease, among the scientific, medical classes, and the general population [31]. Even today, there is not enough data to determine the impact of BSF on the Brazilian population, since prospective longitudinal studies documenting the natural course of the disease have not been performed.

In the brief history described above, two important aspects stand out in the epidemiological context. Failures in the diagnosis were confirmed through laboratory documents in the various fatal cases that occurred in Minas Gerais until the early 2000s [52]. Equally important, in 1996, Lemos et al. [53] isolated bacteria from the group of Rickettsia sp. of spotted fever in the tick Amblyomma cooperi, vectors collected from capybaras in São Paulo. It is clear that the impact of the BSF on public health will not be properly evaluated until appropriate methods of diagnosis and epidemiological surveillance are effectively implemented. Recent data bring some clarity about the incidence rates and some aspects (i) of humans affected by the disease; (ii) ticks (maintained by capybaras); and (iii) transmission environments, and need to be analyzed [54, 55]. The transversality between these aspects will be briefly described below.

In the Brazilian occurrences of BSF, white men, aged between 20 and 64 years, coming from rural areas are more commonly infected and report having had contact with ticks during their leisure activities, unlike women who have a domestic and peridomestic environment, as the likely site of infection [56]. Most cases affecting males corroborate the data described in international reports from the Centers for Disease Control and Prevention [57] and the European Center for Disease Prevention and Control [58]. The fact that most cases are represented by white ethnicity may be influenced by the difficulty in observing the rash when in black individuals, and further compromise the diagnosis of BSF in this ethnic group [59].

Studies in endemic areas of BSF have shown that the disease is correlated with environments where there are large populations of the tick A. sculptum, which, in turn, are supported by the presence of capybaras, fundamental hosts for this species, in anthropic environments. On the contrary, landscapes similar to these, where there are low parasite loads or where the tick A. dubitatum is predominant, did not become endemic areas, even with the presence of capybaras [7]. Recently, research conducted by Geraldi et al. [35] revealed that there are other aspects that contribute to the dynamics of transmission by demonstrating that there are variations in the susceptibility of the tick to infection by R. rickettsii, which may explain the different frequencies of BSF in areas where the vector A. sculptum and capybaras cohabit. However, the complete elucidation of the mechanisms that govern this susceptibility and their effects on the risk of the disease in urban environments still need further studies [7].

Historically, BSF notifications predominate in southeastern Brazil, with the percentage of fatal cases ranging from 30–50% [60]. Particularly in the state of São Paulo, there are extensive areas where transmission has been proven, with 978 laboratory confirmed cases between 2001 and 2018 [7]. The disease, however, continues to advance through new territories, reaching the south, northeast, and central-west regions of Brazil [56], varying estimates on the prevalence and incidence (Figure 2).

Figure 2.

Geographical distribution of confirmed cases of spotted fever by federative unit (FU) and average incidence rate in affected municipalities and between 2007. Source: [56].

Some factors seem to influence the lethality percentages. Undeniably, the strain that prevails in Brazil is much more virulent when compared with the R. rickettsii that occurs in North America, responsible for Rocky Mountain spotted fever [61]. However, aspects such as the lack of specificity in its clinical signs and the absence of exanthema (classic marker) in many patients lead to suspicion and make early diagnosis difficult. Diseases such as dengue, viral exanthematous diseases, and leptospirosis present clinical signs similar to those of BSF, requiring specificities in the differential diagnosis and increasing the possibility of the use of inappropriate drugs that prevent therapeutic cure [62]. Furthermore, it should not be forgotten that infections caused by R. parkeri, a strain present in several regions of the Atlantic Forest, present mild clinical signs, with inoculation bedsores and lymphadenopathy, introducing other elements that make adequate medical management difficult [63]. Furthermore, the geographically restricted availability of parenteral doxycycline, the drug of choice for the treatment of severe cases, highlights the neglected status of BSF in Brazil [64, 65]. A review of the treatment protocol for BSF took place in 2013 and doxycycline is now recommended regardless of patient age, being provided by the Ministry of Health for strategic locations in endemic areas. However, in silent areas or with recent introduction of the agent, the difficulty in accessing the drug remains [66].

In Brazil, rapid environmental changes, the absence of stable policies for environmental preservation, and the low socioeconomic condition of the population are associated with the high importance of BSF—expressed by the high lethality in outbreaks that predominate in family nuclei—establishing this Rickettsiosis as a relevant public health problem. Therefore, continued studies and solutions to support surveillance strategies will help in future assessments of epidemiological aspects.

5. The growing urbanization of capybaras and Brazilian spotted fever

Mammals represent the most successful evolutionary class among vertebrates. Facilitated by a brain that promotes learning and being capable to maintain a constant body temperature, they developed, throughout evolution, a variety of life strategies that allowed them to colonize the most diverse habitats, establishing themselves on all continents [67].

H. hydrochaeris is among the largest rodents found in the Neotropics. When Iberian settlers arrived in South America at the end of the fifteenth century, they came across a diverse fauna and the species was originally named, after analogies with other European animals known to them. However, the name capybara originates from the indigenous word (Tupi): kapii’gwara, which means grass eater (ka’pii = “grass” + gwara = “eater”) [68]. It had its first detailed description in the mid-seveteenth century, based on observations in the state of Pernambuco, when northeastern Brazil was occupied by the Dutch. Later, in the search to define their origin and their preferred habitats, mistakes were made, but according to [69], the São Francisco River, one of the main Brazilian rivers, should be listed as the typical locality for the species, as mentioned by [70].

In Brazil, capybaras can be found in all 26 states and the Federal District (Figure 3) mainly in agricultural habitats, with a predominance of pastures and sugarcane fields where they can reach high densities. They are considered competitors that cause damage to a variety of crops, including sugarcane, corn, rice, bananas, soybeans, and compete for food with cattle, affecting agricultural production [70, 71]. In addition to these places, they frequent bodies of water (rivers, dams, and reservoirs) within urban limits, in public parks, and residential areas [69], currently causing conflicts, particularly in the Southeast, where they invade properties, eat ornamental plants in gardens, and are involved in traffic accidents on the streets and roads [3].

Figure 3.

Distribution of capybaras (Hydrochoerus hydrochaeris) in Brazil. Black dots show records of the species’ presence. Source: [69].

Recent increases in BSF cases [72] and the probable association with high capybara densities have accentuated considerations about the epidemiological role of this rodent in the urbanization of the disease. The expansion of occupation areas occurs as agricultural deforestation occurs, mainly due to the availability of food and the decline of their natural predators, such as jaguars [48, 49]. Thus, they can form numerous populations in certain environments, coming to be considered urban pests. This is because, in anthropogenic wetlands, where it finds an abundant source of food, H. hydrochaeris can develop with a carrying capacity greater than that observed in untouched environments. These facts raise important points about the roles played and the risk of transmission in important zoonosis, such as BSF [50].

It is also worth emphasizing relevant aspects regarding the presence of animals in urban daily life: the presence of wild animals in human groups can be interpreted as a possibility of greater exposure to nature and a source of benefits for the mental health of individuals [73], and increasing the value of recreational ecosystem services provided by green areas [74]. The relationship with nature offers benefits, even if there is no handling or prolonged intimacy in contact with animals. Simple eye contact, regardless of duration, can have a broad and robust impact on people’s affective and cognitive conditions [73, 75].

According to the biophilia hypothesis [76], as a result of evolution, humans have always sought to connect with other life forms. This hypothesis translated some of the multiple dimensions of humans’ innate relationship with nature, including emotional connections with landscapes and animals. In the last decade, the benefits of this contact have been increasingly studied [77]. Improvements in neuropsychological development and mental health have been reported when experiences occur in early childhood [78, 79], but benefits such as reductions in social and emotional difficulties and even deterioration cognitive impairment can extend into old age [80].

Urbanization, as it threatens to weaken the link between humans and nature [81], converging with Wilson’s proposals relating to biophilia, may favor (or even promote) the acceptance of capybaras in the enclosures of a City. However, it is worth mentioning that as capybaras constitute groups that occupy leisure spaces, parks, and lakes, which, when located in areas with occurrence of BSF, increase the risk of tick infestations among people who visit these places [7, 82].

Although capybaras cannot transmit R. rickettsii, they play an important role in public health, as they amplify the agent among tick populations [4]. Thus, despite the presence of capybaras increasing biodiversity in cities and reinforcing the biophilia hypothesis, they pose a risk in the transmission of pathogens, requiring interdisciplinary participation and integrated actions to improve disease control. Researchers have already proven that BSF-endemic areas have much higher tick loads both in capybaras and in the environment, when compared with areas where the disease is not frequent [7]. And, to make the scenario even more complex, mathematical models have shown that the introduction of a single capybara infected with R. rickettsii parasitized by at least one infected tick is enough to establish an infection by R. rickettsii in the entire population of A. sculptum hosted by up to 50 capybaras [37]. In maintaining the infection, it is noteworthy that a capybara, during the primary infection, can remain in bacteremia for about 14 days, infecting other ticks that feed on its blood during this period [35].

The tick A. sculptum infected by R. rickettsii remains infected even after ecdysis (changes of stages), being able to transmit the bacteria in the following stages [35]. Thus, even with its preferred hosts in endemic areas, A. sculptum can accidentally parasitize humans in all its active stages [51], completing the zoonotic cycle.

Transmission to humans depends on the duration of contact between the tick and the person, requiring at least 4–6 hours for transmission to occur [5]. However, as very small tick stages can transmit rickettsiae, it is very common for people to remain infested long enough with the ticks without realizing it. Symptoms appear between 2 and 14 days after infection [83] and are mostly nonspecific. Early treatment is essential and mortality is associated with the difficulty in establishing the diagnosis, the delay in starting the specific therapy, and the little knowledge of the medical profession about the disease [84].

Tetracyclines and chloramphenicol are the only drugs with proven efficacy to treat BSF. In adults, treatment requires high dosage and needs to be continued for a few days after the fever subsides. Thus, in Brazil, despite the high prevalence and the fact that many areas are considered endemic for BSF, the lack of knowledge about the disease often leads to a delay in diagnosis, complicating the prognosis [85]. Therefore, it is important to take advantage of every opportunity to disseminate and expand knowledge about this disease.

Finally, it is worth noting that capybaras and ticks are only parts of the BSF cycle, requiring a deeper understanding of the different aspects of ecological relationships and monitoring of environmental conditions to reduce infections in humans [86]. We consider that cities are moldable and serve as a habitat for people and animals, and it is essential to analyze the extent to which urban ecology has been concerned with offering opportunities for new and different forms of interaction in human-animal relationships. According to the French anthropologist Philippe Descola [87], it is becoming increasingly clear that the established concepts—since the Renaissance—about city and countryside; culture and nature or humans and animals are not sustainable and need to be revisited in contemporary times.

6. Final considerations

In terms of future perspectives, given the persistence of the urbanization pattern, it seems clear that the BSF will not disappear easily from Brazil. In view of the above, there is a need for constant and rigorous epidemiological surveillance in urban areas where capybara is present. However, in the management of the conflicts mentioned above, disinformation must be fought [60] and short-term solutions are not inefficient. Public policies must adapt to manage the issue of BSF, in its urban occurrences, taking into account the many dimensions of the relationships between humans, other animal species, and the environment.

In order to reduce the risk of transmission and minimize the impact of BSF, surveillance and response systems should be instituted at national and regional levels, supporting public and animal health services with strategies to protect the health of ecosystems.

In addition, the greater lethality of BSF is also evidenced by its neglected status in Brazil, such as the lack of information in the health and surveillance sectors and the unavailability, in many regions of the country, of first-choice medication for the treatment of severe clinical cases of the disease.

We understand that the issue of the BSF and all aspects that involve its control must be rethought, correcting interventions not directed to health, with the development of feasible and accessible analysis methodologies within an integrative, multidisciplinary, and multisectoral vision with all that, directly or indirectly, have to do with this problem, in an articulation of planning, governance, and public health, in the search for health cities.

Finally, we emphasize the need to change the current emphasis on the short-term response to the disease and to encourage the construction of more sustainable systems capable of responding effectively to future events that involve the various nuances of the BSF that arise from the environment-animal-human interface.