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Revista chilena de infectología

versión impresa ISSN 0716-1018

Rev. chil. infectol. vol.36 no.2 Santiago abr. 2019

http://dx.doi.org/10.4067/S0716-10182019000200195 

Infectología al Día

Knowledge about bacterial and viral pathogens present in wild mammals in Chile: a systematic review

Sebastián Llanos-Soto1 

Daniel González-Acuña2 

1Laboratorio de Enfermedades y Parásitos de Fauna Silvestre. Departamento de Ciencia Animal. Facultad de Ciencias Veterinarias, Universidad de Concepción, Chile.

2Laboratorio de Vida Silvestre. Departamento de Ciencia Animal. Facultad de Ciencias Veterinarias, Universidad de Concepción, Chile.

ABSTRACT

This study organizes all available information about viral and bacterial pathogens of wild mammals in Chile. This was done in order to identify pathogens that have been well-documented and recognize those that have not been properly studied, determine the number of articles that have been published annually about this topic and identify regions in Chile that concentrate the highest and lowest number of studies concerning viral and bacterial pathogens. A total of 67 scientific articles published in peer-reviewed journals from 1951 to 2018 were selected for revision. Results indicate that the number of publications has increased per decade but there are years in which no articles were published. Most studies addressed Leptospira, rabies, hantavirus, Mycobacterium avium paratuberculosis (MAP) and distemper. Rodentia, Carnivora, Chiroptera and Cetartiodactyla were the most studied mammal orders. Information about presence/absence of pathogens was found for 44 wild mammal species. Research was mainly carried out in central and southern Chile and the most commonly employed methods for pathogen diagnosis were serology and molecular techniques. Overall, research in wild mammals has been directed towards the evaluation of zoonotic diseases, while vector-borne and non-zoonotic diseases have been mostly neglected by the scientific community over the years.

Keywords: Bacteria; Chile; mammals; virus; zoonoses

Introduction

Knowledge about the presence of infectious diseases in wildlife is pivotal to understand the potential consequences that they might have on species conservation and their threat to human health1. Anthropogenic factors, such as the introduction of alien species, climate change, habitat loss and fragmentation and human encroachment in natural areas might increase the risk of disease transmission from wild reservoirs to domestic animals and humans2,3.

Diseases that are transmitted between animals and humans are called zoonoses and cause both economical and social losses, especially in underdeveloped and developing countries3. Zoonotic pathogens, such as rabies and hantavirus, have their origin in mammal reservoirs and are considered extremely important for public health systems because of their consequences on human health4,5. In this context, affected individuals may have their health compromised by zoonotic diseases, and in many cases, they might be wrongly characterized as common infections or even go unnoticed to health care institutions6. Urbanization and industrial activities, such as agriculture and forestry, have intensified in Chile during recent years and they will probably continue to do so in the future7. These factors may lead to habitat fragmentation, ecosystem disruption and over-exploitation of species, which added to the expansion of human and domestic animal populations in areas close to natural habitats, might contribute to the transmission of infectious diseases from free-living wild animals to domestic animals and humans811.

The objectives of this review were to (1) gather and organize all the information available in articles published in peer-reviewed journals involving the assessment of viral and bacterial infections in Chilean wild mammals, (2) identify which pathogens have been prioritized by the local scientific community and which have received little to no attention, (3) evaluate the number of articles published annually about the prevalence of viral and bacterial pathogens in wild mammal hosts and (4) recognize the number of studies developed in this topic in the different regions of Chile.

Materials and Methods

Peer-reviewed scientific publications evaluating the prevalence of viral and bacterial pathogens in Chilean wild mammals were searched and listed following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) declaration guidelines12. Articles published in Spanish or English from January 1950 through July 2018 were selected for revision. Data from unpublished literature (grey literature) was excluded from this study (i.e., abstracts, books, local bulletins and presentations at scientific conferences) based on the fact that these types of scientific documents do not often undergo a rigorous peer-review process prior to publication. This means that the accuracy, reliability and quality of the findings being presented in these documents cannot be ensured. Viral and bacterial agents were considered pathogenic when there was information available in the literature indicating their ability to cause disease in animals, humans or both. The revision considered pathogens present in free-living native and introduced mammalian species, with the exception of domestic animals and individuals maintained in captivity in zoos, farms and exhibition centers. Publications about pathogens found in mammals from the Chilean Antarctic Territory were also excluded from the review, as they have been already reviewed in another scientific article13.

Google Scholar (https://scholar.google.cl/), Scielo Scientific Library (http://www.scielo.cl/) and PubMed (https://www.ncbi.nlm.nih.gov/pubmed/) databases were used to conduct an extensive search for publications. Keywords “bacteria”, “bacterial”, “Brucella”, “coronavirus”, “Corynebacterium”, “distemper”, “hantavirus”, “herpesvirus”, “infectious disease”, “Leptospira”, “Mycobacterium”, “Mycoplasma”, “parvovirus”, “pathogen”, “picornavirus”, “rabies”, “retrovirus”, “Salmonella”, “vector-borne”, “viral”, “virus”, “zoonosis” AND “Carnivora”, “Cetartiodactyla”, “Chiroptera”, “Didelphimorphia”, “Lagomorpha”, “mammal”, “Microbiotheria”, “Paucituberculata”, “Rodentia”, “wildlife”, “Xenarthra” AND “Chile” were inputed in independent searches. These same keywords were also employed to perform searches in Spanish to account for publications in local journals. Articles that were not available for download online were physically searched in the libraries from Universidad de Chile, Universidad Austral, Pontificia Universidad Católica de Chile and Universidad de Concepción. Information about prevalence for each pathogen was organized and listed in a supplementary table using Microsoft® Excel 2010. The table included data about mammal host, pathogen characterization (e.g., serotype, genetic lineage, class), region in Chile where the study was developed and technique used for diagnosis. Data from selected publications was analyzed using line graphs to evaluate a potential trend in the number of articles published per decade since 1951 and identify the most studied mammal orders in Chile.

Data was searched for a total of 150 mammal species from eight orders: Didelphimorphia (2), Paucituberculata (1), Microbiotheria (1), Chiroptera (11), Xenarthra (3), Rodentia (63), Cetartiodactyla (47), Lagomorpha (2) and Carnivora (20). Three species were excluded from the review because their distribution was restricted to Antarctica (Ommatophoca rossii) or their presence in Chile has yet to be confirmed (Stenella attenuate and Stenella longirostris). Research studies that included previously diagnosed cases of viral and bacterial infections in their analysis (e.g., positive cases of rabies diagnosed by the Chilean National Institute of Public Health, ISP in Spanish) were also included in this review. Pathogens were listed from highest to lowest in the discussion depending on the number of articles available in the literature related to that specific pathogen.

Results

A total of 67 publications about viral and bacterial pathogens in Chilean mammals were included in this review. From the literature assessed, 34 studies evaluated the prevalence of viral pathogens and 35 studies concerned bacteria. Information about presence/absence of pathogens was found for 44 species from the Rodentia (15), Carnivora (10), Chiroptera (9), Cetartiodactyla (8), Didelphimorphia (1) and Lagomorpha (1) orders (Figure 1). Details about the results of this review are indicated in the Supplementary Table 1.

Figure 1 Number of scientific studies regarding viral or bacterial infections in different mammal orders from 1980 to 2018. 

Overall, the number of studies addressing the infection or exposure to viral or bacterial pathogens in wild mammals has increased per decade (Figure 2), however, during the last decade there are years in which the number of articles published ranges from 0 to 2 (i.e., 2010, 2012 and 2016). Publications dedicated to each pathogen varied in number, most studies were related to Leptospira (16 studies), rabies virus (12 studies), hantavirus (10 studies), Mycobacterium avium paratuberculosis (8 studies) and canine distemper virus (6 studies).

Figure 2 Number of scientific studies assessing the prevalence of viral or bacterial infections in wild mammals in Chile from 1951 to 2018. 

The first study to record the presence of pathogens in wild mammals in Chile was performed by Neghme et al. in 1951 and involved the evaluation of Leptospira in brown rats (Rattus norvegicus) captured in a slaughterhouse from the Metropolitana region14. Rodentia was the most studied mammal order with 27 publications assessing the presence of viral and bacterial pathogens. A high number of articles were dedicated to investigate the long-tailed pygmy rice rat (Oligoryzomys longicaudatus), with 19 scientific publications involving the evaluation of Leptospira and hantavirus in this species. Order Carnivora (16), Chiroptera (12) and Cetartiodactyla (12) have also received attention from the scientific community. Only two studies involved a lagomorph species and a single article concerned a member of the Didelphimorphia order. No study determined infection with viral or bacterial pathogens in members of the orders Paucituberculata, Microbiotheria and Xenarthra.

A high number of studies of viral and bacterial infections were focused in southern and central Chile, particularly from the Coquimbo to the Los Lagos regions. The most studied regions were the Los Ríos region with 24 studies, the Metropolitana region with 14 studies and the Los Lagos region with 13 studies. Only three studies in rabies and a single one in hantavirus were carried out in the Maule Region. Research studies including mammal species from the northern regions of Chile are lacking, with two studies in the Antofagasta region and a sigle one in the Tarapacá and the Atacama regions. Research has not been carried out in the Arica y Parinacota region. A total of 7 and 4 studies have been developed in the regions of Aysén and Magallanes, respectively.

Most studies applied serological methods for pathogen diagnosis in mammal hosts, such is the case of the distemper virus and parvovirus and the bacterium Brucella, which have been only assessed using serology. These methods were also commonly applied in research studies involving hantavirus in wild rodents. The application of molecular methods to detect pathogens in wild mammals has raised in the last two decades in Chile, which has been reflected in an increase in the use of these type of techniques for diagnosing viruses and bacteria in wild mammals. The use of other methods, such as direct immunofluresence, bacterial culture and histopathology has been mostly restricted for the specific diagnosis of certain pathogens.

Discussion

Wild mammals have played a crucial role as reservoirs of infectious diseases in developing countries and have been involved in the occurrence of spill-over epizootic events in human populations3. These events negatively impact public health systems in these countries and result in important economic losses3,4. In Chile, most scientists and governamental institutions have destined their efforts in studying those zoonotic agents considered as a serious threat to human health, such as Leptospira, rabies virus and hantavirus. Pathogens restricted to animal hosts and which do not represent a threat to humans (e.g., canine distemper virus) have only recently began to receive scientific attention and, in consequence, information available about them is much more limited.

Leptospira

Leptospirosis is a cosmopolitan zoonotic disease of great relevance for human health, particularly in developing and low-income countries, where sanitary conditions and resources destined for disease diagnosis and prevention are limited15. The agent responsible for causing this disease is Leptospira, a bacterial pathogen capable of infecting a variety of mammal hosts and survive for several months in the environment in areas with warm and humid climate conditions16.

Rodents play an important role in the maintenance and dissemination of pathogenic and non-pathogenic Leptospira to other mammal species in urban and rural areas of Chile, including humans and domestic animals17,18. To this date, evidence of infection by this pathogen have been shown in nine rodent species present in the country; the degu (Octodon degus), olive-colored akodont (Abrothrix olivaceus), long-haired akodont (Abrothrix longipilis), Darwin's leaf-eared mouse (Phyllothis darwini), long-tailed pygmy rice rat (O. longicaudatus), black rat (Rattus rattus), brown rat (R. norvergicus), house mouse (Mus musculus) and long-clawed mole mouse (Geoxus valdivianus)1727. Rattus norvegicus and R. rattus are particularly relevant reservoirs due to the high prevalence of Leptospira documented in these species in rural areas of the country18,27. This bacterium has been described in wild mammals in south-central areas of Chile, and more specifically in the Metropolitana, Los Ríos, Los Lagos and Aysén regions.

Reports indicating the presence of Leptospira in other mammal orders are scarce in comparison to the information available for rodents. This bacterium has been documented in only two carnivore species; the South American sea lion (Otaria flavescens) and the American mink (Neovison vison)9,28. The interaction between wild animals and domestic reservoirs (i.e., dogs and livestock) can act as an important mechanism for the ocurrence of leptospirosis cases in human inhabited environments29. Future studies dedicated to evaluate the role of wild species in the maintainance and transmission of Leptospira will make an important contribution to the understanding about the dynamics of this pathogens in natural and urban areas of the country.

Rabies virus

Rabies is a cosmopolitan zoonotic disease of great importance for public health worldwide30. All mammals are susceptible to rabies virus but only chiropterans and carnivores are capable of successfully maintain and transmit the infection in the long-term30. In Chile, confirmed cases of rabies are characterized by the ISP in different antigenic variants using specific monoclonal antibodies. Each variant represents an assemblage of viruses within a serotype that possesses defined antigenic properties31. This method of antigenic characterization of rabies has been widely applied in the country to study the geographical and temporal distribution of the virus32,33.

The first case of human rabies in Chile was reported in 1879 and surveillance in domestic and wild species has been performed since 1929 by the ISP (at the time called “Instituto Bacteriológico de Chile”)34,35. The efforts of the ISP allowed to identify wildlife and domestic species prevalent to the virus, amongst them livestock, lagomorphs, rodents, carnivores and chiropterans33,34. However, active surveillance of rabies began following the first oubreak of this disease in bats, more specifically, in the brazilian free-tailed bat (Tadarida brasiliensis) in 198533. After this event, rabies cases have been mainly reported in bats33,36.

To this date, five antigenic variants have been identified in Chile, including the canine antigenic variant AgV2 and four variants associated with insectivorous bats; the antigenic variant AgV4 Tadarida, antigenic variant AgV6 Lasiurus, antigenic variant AgV3 Myotis chiloensis and an antigenic variant AgV not typed for Histiotus33,37,38. The most common variant registered in Chile from 2008 to 2013 has been AgV439. Antigenic variants are described to be host-specific 38,40, but recent studies suggest that there could be cross-species spillover transmission of rabies variants in bats32,38,41,42.

Six of the eleven species of bats distributed in the country have been described to be infected with the virus; the big-eared brown bat (Histiotus macrotus), small big-eared brown bat (Histiotus montanus), mouse-eared bat (M. chiloensis), eastern red bat (Lasiurus borealis), hoary bat (Lasiurus cinereus) and Brazilian free-tailed bat (T. brasiliensis)32,33,37,43. Considering the available scientific information, T. brasiliensis and L. cinereus remain the most relevant reservoirs of bat rabies in Chile32,36,37,41,43,44. Escobar et al. (2013) indicate that both T. brasiliensis and L. cinereus, and their respective antigenic variants of rabies (AgV4 and AgV6), share similar ecological niches in Chile and their distribution is limited by the presence of natural ecological barriers, such as the Andes Mountains to the east and the Pacific Ocean to the west32. Bat rabies seems to follow a seasonal pattern with peaks of positivity during hot season (October-March) and decrease in colder months33,39. This could be related to a reduction in bat activity during winter in the Southern hemisphere and therefore less chance of rabies transmission among bats and from bats to other susceptible species33,39,45.

The increase in population size and density of dogs, added to the presence of bat (mainly T. brasiliensis) in urban areas, have raised the risk of rabies transmission events from bats to dogs across the country46,47. This is particularly important for central Chile, which possesses a high number of bat-related antigenic variants and an increased richness of chiropteran species33. Highly populated human settlements, such as the large cities located in the Metropolitana, Maule, Biobío and Valparaíso regions, posses an elevated risk of rabies transmission between animals and humans and concentrate the higher number of human cases33,39,47. Rabies cases have been reported in wild carnivores in Chile in years prior to 199048, however, insectivorous bats are currently considered the most important reservoir of rabies in the country with the 97.31% (1339/1376) of positive cases reported by the ISP from 1985 to 201232. The importance of bats as rabies reservoirs and the increasing population of stray dogs in in urban areas rise concern about the current risk of rabies transmission from bats to dogs and, ultimately, humans beens47.

Hantavirus

Seven rodent species have been found to be exposed or infected with the Andes virus in Chile; the olive-colored akodont (A. olivaceus), long-haired akodont (A. longipilis), Darwin's pericote (P. darwini), Southern big-eared mouse (Loxodontomys micropus), black rat (R. rattus), brown rat (R. norvergicus) and long-tailed pygmy rice rat (O. longicaudatus)4957. Reports of hantavirus belong to areas in south and central Chile, particularly from the Coquimbo to Magallanes regions. To this date, the presence of hantavirus in the country has been restricted solely to rodents and has not been possible to identify the virus in wild species from other orders, such as the case of marsupials and chiropterans54.

Oligoryzomys longicaudatus is the most important reservoir of the Andes virus in Chile, being responsible of disseminating the hantavirus to humans along its distributional ranged from the Copiapó to the Magallanes regions54,5759. Oligoryzomys longicaudatus has been characterized as a high mobility species, which increases the risk of encountering humans throughout its wide home range (320-4800m2)60. This species can be found in close proximity to urban areas, inhabiting humid environments and areas covered by bushes near water sources60. Increase in wild rodent population density in peri-urban areas has been linked to an elevation in the number of cases of hantavirus cardiopulmonary syndrome (HCPS) in humans51. It has been suggested that the explosive increase in the number of rodents during years of synchronized flowering of native bamboo, particularly Chusquea quila, might be implicated in the occurrence of hantavirus outbreaks in humans due to an increased available of food provided by these plants51,52. Most cases of hantavirus infection in Chile occur near towns in rural and peri-urban areas where O. longicaudatus is present and people are constantly exposed to become infected with the virus55,61,62.

Mycobacterium

Mycobacterium avium subp. paratuberculosis (MAP) is an important pathogen of cattle and small ruminants, responsible for causing important economic losses in animal production worldwide63. In Chile, native ungulates are at continuous risk of becoming infected with MAP due to the high prevalence of this pathogen reported in livestock, particularly in southern areas of the country64. The guanaco (Lama guanicoe), the Southern pudu (Pudu puda), the Chilean Huemul (Hippocamelus bisulcus) and the European hare (Lepus europaeus) have been reported to carry this bacterium in Chile6569. MAP-infected guanacos did not display any health-related issues and European hares did not present microscopic or macroscopic lesions associated with the infection65,68. In the case of the huemul, the bacterium presented similar molecular characteristics to MAP isolates commonly reported in livestock in Chile, suggesting that the latter are spreading the infection to huemul populations70. The situation is concerning for this endangered deer species, particularly in central Chile, where the population of huemuls is facing severe conservation issues and its habitat is being disturbed by the presence of domestic animals71. Similarly, MAP infections were documented in three Southern pudus found in areas commonly occupied by dairy cattle67. Currently, there is no information about pathological findings of MAP infection in free-ranging pudúes, however, this bacterium was indicated as the cause of death for an individual maintained in captive settings66.

Infections with MAP have also been reported in introduced deer species in southern Chile, such as the red deer (Cervus elaphus) and fallow deer (Dama dama), which could be transmitting the pathogen to livestock and vice versa72,73. The European wild boar (Sus scrofa) is currently distributed in rural and protected areas of south-central Chile and is considered as a carrier of MAP in Europe74,75. Currently, there have not been reports of MAP infection in this species in the country. The role that introduced ungulates species are playing in the transmission of MAP and other pathogens to native wildlife and livestock is a topic that still needs to be explored in Chile.

Canine distemper virus

Distemper is a viral disease prevalent in dogs all over the world and capable causing severe illness in wild carnivores76. A wide range of species from different families, such as the Canidae, Felidae, Hyaenidae, Mustelidae, Ursidae, Vivirridae and Procyonidae have been reported to be exposed or infected to canine distemper virus (CDV), in some cases, with major population declines76,77. CDV currently possesses an endemic status in urban and rural populations of dogs in Chile, with seroprevalences that range from 51 to 73%10,78. Dogs have been indicated as the source of CDV outbreaks in populations of the South American gray fox (Lycalopex griseus) in central Chile10,79,81 and may be a threat to populations of the endangered Darwin's fox (Lycalopex fulvipes) in south-central Chile82.

To this date, there are no study that applied methods to directly detect distemper virus in Chilean wildlife, however, serological surveys have found exposure to the virus in the American mink (N. vison), South American sea lion (O. flavescens), South American gray fox (L. griseus) and Andean fox (Lycalopex culpaeus)8,9,79,80,81. There is no information about infection or exposure to CDV in wild felids and indigenous mustelids in the country.

Neglected pathogens and wild mammal species

This section includes pathogens that have received little attention from the scientific community in Chile and information about their presence in natural hosts is currently lacking or inexistent.

Parvoviruses have been detected in a wide range of wild carnivores around the world, belonging to the Canidae, Felidae and Mustelidae families83. In Chile, canine (CPV) and feline parvoviruses (FPV) are recognized affections of dogs and cats, respectively84. Serological assessments of CPV in L. culpaeus, L. griseus and O. flavescens have found past exposure to this virus9,10,80, meanwhile, there is no information about the exposure or infection with FPV in wild species. Both CPV and FPV, have shown to cause gastrointestinal affections in carnivores elsewhere83, but infections and potential pathological consequences of these viruses on Chilean species are still undetermined.

Like parvoviruses, information about retroviruses in Chilean wildlife is lacking. Mora et al. (2015) found that guignas in Chiloé were infected with feline leukemia (FeLV) and feline immunodeficiency viruses (FIV) with no apparent clinical signs85. Nucleotide sequences obtained from FeLV and FIV in guignas were almost identical to those found in domestic cats, suggesting that cats may be playing an important role in the transmission of retroviruses to wild felids. Some feline species, such as the guigna, inhabit in areas close to human settlements and they ocassionally predate on poultry86, which increases the risk of interacting with infected domestic cats. Retroviruses have been detected in the cougar and other large felids in North America87, however, the presence of these viral agents in populations of cougars and most of the native wild felids species in Chile still needs to be addressed.

Information about viral and bacterial pathogens in native ruminants is very scarce. Bovine viral diarrhea virus (BVDV) was detected in the southern pudu and two Chilean huemuls were found to be exposed to the virus88,89. Similar to MAP, BVDV isolates from the southern pudu share molecular characteristics with viruses circulating in cattle, suggesting that livestock are acting as disseminators of pathogens to native wildlife in Chile70,88. Other pathogens present in livestock, such as bovine rhinotracheitis virus (BoHV-1) and Brucella spp., were assessed in the Chilean huemul using serological methods, but no individual were found to be exposed89.

There is no information about infections with viral or bacterial pathogens in aquatic carnivores, such as members of the Otariidae, Phocidae and Mustelidae families, except for the South American sea lion (O. flavescens) and the invasive American mink (N. vison). Furthermore, cetaceans have been mostly overlooked by the local scientific community, with only one viral disease being identified in Chile90,91. The Chilean dolphin (Cephalorhynchus eutropia), black porpoise (Phocoena spinipinnis), bottle-nosed dolphin (Tursiops truncatus) were found to present marks on their bodies typical of tattoo skin disease, an affection that might lead to neonatal mortality and have negative consequences on host population dynamics90,91. No other pathogens have been reported in cetaceans distributed in Chile, despite the fact that exposure to cetacean morbillivirus and Brucella sp. was described in species living along the Peruvian section of the Pacific Ocean9294.

Tick-borne pathogens

Ticks are hematophagous ectoparasites of almost every terrestrial vertebrate and play an important role as vector of pathogens95. In Chile, viral and bacterial tick-borne pathogenic agents have been neglected and information available about the presence of Anaplasma platys96, Ehrlichia canis97, “Candidatus Rickettsia andeanae”98 and Rickettsia felis99 is restricted to domestic mammals. However, a recent study identified “Candidatus Neoehrlichia chilensis” in wild rodent species from southern Chile using molecular methods100.

Recently, Borrelia burgdorferi was reported in Brazil, Mexico, Canada, Chile, Costa Rica, Colombia and Venezuela101, however, most cases have been diagnosed based only on clinical and serological evidence, without a molecular characterization and isolation of the agent101. This has only been done by Ivanova et al. (2014), who reported Borrelia chilensis VA1, a new spirochete species from the Lyme group102. Additionally, Verdugo et al. (2017), found infection with B. chilensis in Ixodes stilesi ticks collected from the native southern pudu deer and suggests that I. stilesi may be playing a role in the maintainance of the spiroquete103. Further studies are necessary to properly understand the mechanisms of natural transmission of this bacterium and the risks of infection for domestic animals and humans.

Pathogen transmission between wildlife and domestic animals

Pathogen transmission between wild species and livestock is bidirectional and affect both animal production and species conservation all over the world104. Factors, such as human encroachment into wildlife inhabited areas and the expansion and intensification of animal production systems to natural areas, can increase the risk for contact and pathogen transmission at the livestock-wildlife interface105. The interaction among livestock and wild species not only occurs in anthropogenically disturbed zones, but also in protected natural areas of Chile71,106. Pathogens, such as MAP, BVDV and Corynebacterium pseudotuberculosis, are being transmitted from farm animals to wild ungulates facing conservation issues70,88,107. For this reason, it is extremely relevant to understand the consequences that these infectious agents might have on the health of the affected species and the existent mechanisms for the transmission of diseases between livestock animals and wildlife.

Dogs are another threat for Chilean wildlife due to their predatory behaviour over native species and for their role as carriers of infectious pathogens108. Dogs inhabiting natural areas have been linked with outbreaks of viral diseases in carnivore populations that have resulted in mass mortality events of wild animals in the past109. Dogs populations have increased in size and density over the years in urban and rural areas of Chile, which might increase the possibility of encounters between wildlife and domestic dogs and the transmission of pathogenic organisms10,46,78,79,110.

Conclusions

To date, most publications have involved the study of zoonotic viral and bacterial pathogens in Chilean wild mammals. Non-zoonotic and vector-borne pathogens have been neglected by the local scientific community, despite their importance for wildlife conservation and public health, respectively. It is also concerning that a large number of studies have been performed in southern and central regions of Chile, while the development of research studies in the northern areas of the country have been limited. Research about viral and bacterial pathogens in Chilean wild mammals is still very scarce and further studies are necessary in order to properly understand the role that certain species might be playing as reservoir of infectious agents. The information gathered in future investigations dedicated to evaluate the presence of infection in wild mammals will establish the basis for more complex studies destined to understand the epidemiology and ecology of zoonotic and non-zoonotic infectious diseases in the country.

Annexed Summary of peer-reviewed studies published from 1951 to 2017 evaluating the prevalence of bacterial and viral infections in Chilean wildlife 

Pathogen Host Order Host Pathogen characterization Prevalence/Number of positives (percentage) Location Diagnostic technique Reference
Rabies (Rhabdoviridae) Chiroptera Brazilian free-tailed bat
Tadarida brasiliensis
Not determinded 12/73 (14.1%) Metropolitana (9), Valparaíso (2), O'Higgins region (1) Direct immunofluorescence and mouse inoculation tests 36
Not determined 3/3 (100%) Metropolitana region Direct immunofluorescence and mouse inoculation test 111
Not determined 1/619 (0.16%) Metropolitana region Direct immunofluorescence 36
Antigenic variant 4 (AgV4) 104 positives Metropolitana (60), Valparaíso (13), O'Higgins (13), Maule (8), Biobío (7), Coquimbo (4), Araucanía (2) and Los Lagos (1) regions Mouse inoculation test and indirect immunofluorescence 112
Genetic lineage B 1 positive Not specified Mouse inoculation test and RT/PCR 41
Genetic lineage C 2 positives Metropolitana and Valparaíso regions Mouse inoculation test and RT/PCR 41
Genetic lineage D 82 positives Coquimbo to Los Lagos regionsa Mouse inoculation test and RT/PCR 41
Genetic lineage E 3 positives Metropolitana region Mouse inoculation test and RT/PCR 41
Genetic lineage A Antigenic variant 4 (AgV4) 2 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Genetic lineage B Antigenic variant 4 (AgV4) 4 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Genetic lineage C Antigenic variant 4 (AgV4) 27 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Antigenic variant 4 (AgV4) 672 positives Metropolitana (260), Biobío (158), Valparaíso (88), O'Higgins (48), Maule (45), Los Lagos (44), Coquimbo (17), Araucanía (10) and Atacama regions (2) Direct immunofluorescence 37
Not determined 297 positives Metropolitana region Direct immunofluorescence 43
Antigenic variant 4 (AgV4) 568 positives Not specified Mouse inoculation test and Direct immunofluorescence 38
Antigenic variant 9 (AgV9) 4 positives Not specified Mouse inoculation test and Direct immunofluorescence 38
Cluster I 64 positives Not specified RT/PCR and DNA sequencing 38
Cluster III 1 positive Not specified RT/PCR and DNA sequencing 38
Cluster IV 1 positive Not specified RT/PCR and DNA sequencing 38
Antigenic variant 4 (AgV4) 910 positives From Coquimbo to Los Ríos regions Direct immunofluorescence 32
Not determined 1243/23868 (4.95%) Not specified Direct immunofluorescence 33
Not determined 856 positives Not specified Direct immunofluorescence 39
Chiroptera Histiotus sp. Antigenic variant not typed 13 positives Metropolitana (3), Valparaíso (3), Biobío (3) and Magallanes regions (4) Direct immunofluorescence 37
Chiroptera Big-eared brown bat
Histiotus macrotus
0/4 Not specified Direct immunofluorescence and mouse inoculation test 36
Genetic lineage A Antigenic variant 4 (AgV 4) 1 positive Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Genetic lineage A Antigenic variant not typed 9 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Not determined 3 positives Metropolitana region Direct immunofluorescence 43
Cluster III 9 positives Not specified RT/PCR and DNA sequencing 38
Not determined 24/188 (11.32%) Not specified Direct immunofluorescence 33
Not determined 14 positives Not specified Direct immunofluorescence 39
Chiroptera Small big-eared brown bat
Histiotus montanus
Not determined 1/7 (12.50%) Not specified Direct immunofluorescence 33
Chiroptera Lasiurus sp. Genetic lineage E 1 positive Biobío region Mouse inoculation test and RT/PCR 41
Genetic lineage B Antigenic variant 4 (AgV4) 5 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Antigenic variant 6 (AgV6) 27 positives Metropolitana (19), Valparaíso (1), O'Higgins (2) and Biobío regions (5) Direct immunofluorescence 37
Chiroptera Eastern Red Bat
Lasiurus borealis
0/8 Not specified Direct immunofluorescence and mouse inoculation test 36
Not specified 4 positives Metropolitana region Direct immunofluorescence 43
Antigenic variant 6 (AgV6) 4 positives Not specified Direct immunofluorescence and mouse inoculation tests 38
Cluster IV 4 positives Not specified RT/PCR and DNA sequencing 38
Not determined 14/81 (14.74%) Not specified Direct immunofluorescence 33
Not determined 9 positives Not specified Direct immunofluorescence 39
Chiroptera Hoary bat
Lasiurus cinereus
Not determined 19 positives Metropolitana region Direct immunofluorescence 43
Antigenic variant 6 (AgV6) 14 positives Not specified Direct immunofluorescence and mouse inoculation tests 38
Cluster IV 11 positives Not specified RT/PCR and DNA sequencing 38
Antigenic variant 6 (AgV6) 52 positives From Metropolitana to Los Ríos regions Direct immunofluorescence 32
Not determined 44/131 (25.14%) Not specified Direct immunofluorescence 33
Not determined 37 positives Not specified Direct immunofluorescence 39
Chiroptera Southern Red Bat
Lasiurus blossevillii
0/1 Not specified Direct immunofluorescence 33
Chiroptera Myotis sp. Genetic lineage D Antigenic variant 3 (AgV3) 2 positives Not specified Mouse inoculation test, indirect immunofluorescence and RT/PCR 113
Chiroptera Mouse-eared bat
Myotis chiloensis
Genetic lineage A 1 positive Valparaíso region Mouse inoculation test and RT/PCR 41
Antigenic variant 3 (AgV3) 7 positives Metropolitana (2), Atacama (1), Valparaíso (1), Araucanía (1) and Los Lagos (2) regions Direct immunofluorescence 37
Not determined 2 positives Metropolitana region Direct immunofluorescence 43
Antigenic variant 4 (AgV4) 2 positives Not specified Direct immunofluorescence and mouse inoculation tests 38
Antigenic variant 3 (AgV3) 5 positives Not specified Direct immunofluorescence and mouse inoculation tests 38
Antigenic variant 8 (AgV8) 2 positives Not specified Direct immunofluorescence and mouse inoculation tests 38
Cluster II 6 positives Not specified RT/PCR and DNA sequencing 38
Not determined 13/1210 (1.06%) Not specified Direct immunofluorescence 33
Not determined 9 positives Not specified Direct immunofluorescence 39
Chiroptera Vampire bat
Desmodus rotundus
0/3 Not specified Direct immunofluorescence 33
Chiroptera Kalinowski's Mastiff Bat
Mormopterus kalinowskii
0/8 Not specified Direct immunofluorescence 33
Carnivora South American gray fox
Lycalopex griseus
Not determined 5/58 (8.62%) Magallanes region: Bernardo O'Higgins (1), San Gregorio (1), Morro Chico (1), Porvenir(2) Direct immunofluorescence and mouse inoculation tests 48
Carnivora Lycalopex sp. 0/120 Not specified Direct immunofluorescence 33
Carnivora Molina's Hog-nosed skunk
Conepatus chinga
0/5 Not specified Direct immunofluorescence 33
Carnivora Lesser grison
Galictis cuja
0/4 Not specified Direct immunofluorescence 33
Carnivora South American sea lion
Otaria byronia
0/3 Not specified Direct immunofluorescence 33
Carnivora Guiña
Leopardus guigna
0/3 Not specified Direct immunofluorescence 33
Carnivora Pampas cat
Leopardus colocolo
0/1 Not specified Direct immunofluorescence 33
Rodentia Coypu
Myocastor coypus
0/2 Not specified Direct immunofluorescence 33
Carnivora Mountain lion
Puma concolor
0/1 Not specified Direct immunofluorescence 33
Distemper (CDV) Carnivora Lycalopex spp. Not determined 14/33 (42%) Coquimbo region Microneutralization assay 10
Carnivora South American gray fox
Lycalopex griseus
Not determined 1 positive Biobío region ELISA 83
Not determined 13/28 (46.4%) Coquimbo region Microneutralization test and Cytopathic effect in cell culture 79
Carnivora Andean fox
Lycalopex culpaeus
Not determined 1/5 (20%) Coquimbo region Microneutralization test and Cytopathic effect in cell culture 79
Not determined 8/16 (50%) Metropolitana (7) and O'Higgins region (1) Indirect ELISA and seroneutralization test 80
Carnivora South American Sea Lion
Otaria byronia
Not determined 2/3 (66.7%) Los Ríos region Seroneutralization test 9
Carnivora American mink
Neovison vison
Not determined 9/23 (39.1%) or 5/23 (21.7%)b Los Ríos region Microneutralization test 10
Hantavirus-Andes Rodentia Long-tailed Pygmy Rice Rat
Oligoryzomys longicaudatus
Not determined 13/102 (12.74%) Aysén region ELISA 49
Not determined 1 2.7%c Aysén region Serologyd 50
Not determined 24 positives Aysén (11), O'Higgins (5), Biobío (2), Araucanía (3), Los Ríos (1), Los Lagos (1) and Metropolitana regions (1) Serologyd 51
Not determined 18/59 (13.51%)e Los Ríos (10) and Los Lagos regions (4) ELISA 52
Not determined 2 positives Biobío region ELISA 53
Not determined 20/209 (9.57%) Los Lagos region ELISA 59
Not determined 5/48 (10.4%) Biobío (2), Valparaíso (1), O'Higgins (1), Maule (1), Araucanía, Los Ríos and Los Lagos regions Strip immunoblot assay (SIA) 54
Not determined 1/69 (1.44%) Magallanes region Strip immunoblot assay (SIA) and RT-PCR 57
0/3 Metropolitana region ELISA 56
Rodentia Olive-colored akodont
Abrothrix olivaceus
Not determined 6/80 (7.5%) Aysén region ELISA 49
Not determined 7.50%c Aysén region Serologyd 50
Not determined 4/547 (0,73%) Metropolitana, Biobío, O'Higgins, Araucanía, Los Lagos and Aysén (4) regions Serologyd 51
No positivesf Los Lagos and Los Ríos regions ELISA 52
0/98 Los Lagos region ELISA 59
0/127 From Valparaíso to Los Lagos regions including the Metropolitana region Strip immunoblot assay (SIA) 54
Rodentia Long-haired akodont
Abrothrix longipilis
Not determined 1/36 (2.78%) Aysén region ELISA 49
Not determined 2.70% Aysén region Serologyd 50
Not determined 12/300 (4%) Los Ríos (3), Biobío (2), Araucanía and Aysén regions (2) Serologyd 51
Not determined 4/43 (9.3%) Los Ríos (4) and Los Lagos regions ELISA 52
Not determined 2/44 (4.6%) Biobío region ELISA 53
Not determined 3/163 (1.84%) Los Lagos region ELISA 59
No positives9 Valparaíso, O'Higgins, Maule, Biobío, Los Ríos and Los Lagos regions Strip immunoblot assay (SIA) 54
0/29 Metropolitana region ELISA 56
Rodentia Sanborn's akodont
Abrothrix sanborni
No positives9 Los Ríos region Strip immunoblot assay (SIA) 54
Rodentia Darwin's leaf-eared mouse
Phyllotis darwini
Not determined 2/61 (3.3%) Metropolitan region Serologyd 51
No positives9 O'Higgins region Strip immunoblot assay (SIA) 54
Rodentia Southern big-eared mouse
Loxodontomys micropus
Not determined 1 positive Biobío region Serologyd 51
0/8 Los Lagos region ELISA 59
Not determined 1/19 (5.3%) Biobío region ELISA 53
No positives9 Los Lagos region Strip immunoblot assay (SIA) 54
Rodentia House mouse
Mus musculus
No positives9 Valparaíso, Araucanía and Metropolitana regions Strip immunoblot assay (SIA) 54
0/24 Antofagasta and Metropolitana regions ELISA and PCR 55
Rodentia Black rat
Rattus rattus
No positives9 Valparaíso, Maule, Biobío and Los Lagos regions Strip immunoblot assay (SIA) 54
Not determined 1/57 (1.75%) Coquimbo (1), Valparaíso, Metropolitana, Araucanía and Los Lagos regions ELISA and PCR 55
0/2 Metropolitana region ELISA 56
Rodentia Brown rat
Rattus norvegicus
No positives9 Valparaíso, O'Higgins, Maule, Biobío and Metropolitana regions Strip immunoblot assay (SIA) 54
Not determined 2/80 (2.5%) Metropolitana region ELISA and PCR 55
Not determined 1/6 (16.66%) Metropolitana region ELISA, RT-PCR and sequencing 56
Didelphimorphia Elegant Fat-tailed opossum
Thylamys elegans
No positives9 Valparaíso and O'Higgins regions Strip immunoblot assay (SIA) 54
Rodentia Degu
Octodon degus
0/25 Metropolitana region Serologyd 51
Rodentia Chilean climbing mouse
Irenomys tarsalis
0/2 Los Ríos region ELISA 59
Rodentia Pearson's long-clawed mouse
Geoxus annectens
0/1 Los Ríos region ELISA 59
Hantavirus -Seoul Rodentia Brown rat
Rattus norvegicus
Not determined 2 positives Not specified Not specified 55
Canine parvovirus (CPV) Carnivora Lycalopex spp. Not determined 16/33 (49%) Coquimbo region Haemagglutination inhibition test (HAI) 10
Carnivora Andean fox
Lycalopex culpaeus
Not determined 1/16 (6.25%) Los Cipreses National Reserve (O'Higgins region) ELISA and haemagglutination inhibition test (HAI) 80
Carnivora South American Sea Lion
Otaria byronia
Not determined 3/3 (100%) Los Ríos region Hemagglutination inhibition test (HAI) 9
Feline leukemia virus (FeLV) Carnivora Guigna
Leopardus guigna
Not determined 3/15 (20%) Chiloé Island (Los Lagos region) PCR amplification and sequencing 85
Feline immunodeficiency virus (FIV) Carnivora Guigna
Leopardus guigna
Not determined 2/15 (13.3%) Chiloé Island (Los Lagos region) PCR amplification and sequencing 85
Herpesvirus (Gammaherpesvirus) Carnivora Darwin's fox
Lycalopex fulvipes
Not determined 4/28 (14.29%) Chiloé Island (Los Lagos region) PCR 114
Bovine rhinotracheitis (BoHV-1) Cetartiodactyla Chilean Huemul
Hippocamelus bisulcus
0/18 Aysén region Serological neutralization test 89
Foot-and-mouth disease virus Cetartiodactyla Southern Pudu
Pudu puda
Not determined 1 negative Biobío region Serological neutralization test 88
Bovine viral diarrhea virus (BVDV) Cetartiodactyla Chilean Huemul
Hippocamelus bisulcus
Not determined 2/18 (11.1%) Aysén region Serological neutralization test 89
Cetartiodactyla Southern Pudu
Pudu puda
1 positive Biobío region Serological neutralization test, reverse-transcriptase PCR and DNA sequencing 88
Tattoo skin virus (Poxvirus) Cetartiodactyla Chilean Dolphin
Cephalorhynchus eutropia
Not determined 4/13 (30.8%) Chilean Northern Patagonia Visual inspection of lesions 90
Cetartiodactyla Black Porpoise
Phocoena spinipinnis
Not determined 3/3 (100%) Punta de Choros (Coquimbo region) Visual inspection of lesions 90
Not determined 3/4 (75%) Punta de Choros (Coquimbo region) Visual inspection of lesions 91
Cetartiodactyla Bottle-nosed Dolphin
Tursiops truncatus
Not determined 1/1 (100%) Isla de Choros (Coquimbo region) Visual inspection of lesions 90
Leptospira spp. Carnivora American mink
Neovison vison
Not determined 31/57 (55.6%) Los Ríos (5), Los Lagos (10) and Aysén regions (16) PCR 28
Rodentia Degu
Octodon degus
Not determined 26/260 (10%) Metropolitana region PCR 27
Not determined 7/144 (4.86%) Metropolitana region Nested PCR 18
Rodentia Olive-colored akodont
Abrothrix olivaceus
Not determined 3 positives Los Ríos region Renal biopsy 19
Serovar Poi (3) Hardjo (3), Pomona (3), Copenhageni (2), Medanensis (1), Icterohaemorrhagiae (1), Icterohaemorrhagiae- Medanensis (1), Sejroe 19/41 (46.3%) Los Ríos region Microscopic agglutination test (MAT) and renal biopsy 20
Not determined 8/14 (57.1%) Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
Not determined 35/83 (42.2%) Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 91/206 (44.2%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
Not determined 6/53 (11.3%) Los Ríos region Bacterial culture, dark-field microscopy and endonuclease restriction enzyme 25
Serovar Icterohaemorrhagiae 1/10 (10%) Metropolitana region Microscopic agglutination test (MAT) 26
Not determined 21/187 (11.23%) Metropolitana region Nested PCR 18
Rodentia Long-haired akodont
Abrothrix longipilis
Serovar Sejroe (5), Poi (2) Copenhageni (1), Medanensis (1), Hardjo (1), Copenhageni, Pomona, Icterohaemorrhagiae 13/22 (59.09%) Los Ríos region Microscopic agglutination test (MAT) and renal biopsy 20
Not determined 9/16 (56.3%) Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
Not determined 62/126 (49.2%) Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 87/175 (49,7%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
0/9 Los Ríos region Bacterial culture and dark-field microscopy 25
Rodentia Darwin's pericote
Phyllotis darwini
Not determined 4/68 (5.9%) Metropolitana region PCR 27
Not determined 3/62 (4.8%) Metropolitana region Nested PCR 18
Rodentia Long-tailed Pygmy Rice Rat
Oligoryzomys longicaudatus
Not determined 2 positives Los Ríos region Renal biopsy 19
Serovar Copenhageni (2), Poi (3), Pomona (3), Icterohaemorrhagiae-Copenhageni (1), Copenhageni-Poi (1), Sejroe, Medanensis, Hardjo 15/36 (41.7%) Los Ríos region Microscopic agglutination test (MAT) and renal biopsy 20
Not determined 15/36 (41.7%) Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
Not determined 25/89 (28.1%) Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 77/191 (40.3%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
Not determined 16/76 (21.1%) Los Ríos region Bacterial culture, dark field microscopy and endonuclease restriction enzyme 25
Not determined 2/45 (4.44%) Metropolitana region Nested PCR 18
Rodentia Rattus sp. Serovar Icterohaemorrhagiae 2 positives Metropolitana region Guineae pig inoculation 115
Rodentia Black rat
Rattus rattus
Serovar Copenhageni (1), Medanensis (1), Sejroe, Hardjo, Pomona, Poi, Icterohaemorrhagiae 3/5 (60%) Los Ríos region Microscopic agglutination test (MAT) and renal biopsy 20
Not determined 7/17 (41.8%) Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
Not determined 9/34 (26.5%) Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 18/85 (21.2%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
0/15 Los Ríos region Bacterial culture and dark-field microscopy 25
Serovar Icterohaemorrhagiae 1/3 (33.33%) Metropolitana region Microscopic agglutination test (MAT) 26
Not determined 51/246 (20.7%) Los Ríos region PCR 116
Not determined 5/84 (5.95%) Metropolitana region Nested PCR 18
Rodentia Brown rat
Rattus norvegicus
Not determined 63/100 (63%) Metropolitan region Direct observation with ultramicroscope 14
0/2 Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
0/8 Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 2/27 (7.4%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
Not determined 2/14 (14.3%) Los Ríos region Bacterial culture, dark-field microscopy and endonuclease restriction enzyme 25
Serovar Icterohaemorrhagiae 3/9 (33.3%) Metropolitana region Microscopic agglutination test (MAT) 26
Not determined 3/29 (10.3%) Los Ríos region PCR 116
Not determined 24/63 (38.1%) Metropolitana region Nested PCR 18
Rodentia House mouse
Mus musculus
0/2 Los Ríos region Microscopic agglutination test (MAT) and renal biopsy 20
Not determined 1/8 (12.5%) Los Ríos region Indirect immunofluorescence, immunoperoxidase, dark-field microscopy and Levaditi's staining 23
Not determined 2/26 (7.7%) Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 20/97 (20.6%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
Not determined 7/31 (22.58%) Los Ríos region Bacterial culture, dark-field microscopy and endonuclease restriction enzyme 25
0/13 Metropolitan region region Microscopic agglutination test (MAT) 26
Not determined 18/80 (22.5%) Los Ríos region PCR 116
Not determined 6/47 (12.8%) Metropolitana region Nested PCR 18
Rodentia Long-clawed mole mouse
Geoxus valdivianus
0/1 Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
Not determined 1/2 (50%) Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 17
Rodentia Southern big-eared mouse
Loxodontomys micropus
0/1 Los Ríos region Indirect immunofluorescence and immunoperoxidase 24
0/1 Los Ríos region Serology, immunochemical diagnostic and microscopic agglutination test (MAT)h 25
Leptospira interrogans Carnivora American mink
Neovison vison
Not determined 5 positivesi Aysén region Ribosomal RNA gene sequencing 28
Carnivora South American Sea Lion
Otaria byronia
Serovar Bratislava and Pomona (1), Hardjo, Icterohaemorrhagiae, Copenhageni, Canicola 1/3 (33.33%) Los Ríos region Immunohistochemestry (IHC) 9
Rodentia Degu
Octodon degus
Serovar Bratislava (2) 26/260 (10%) Metropolitana region Microscopic agglutination test (MAT) and PCR 27
Not determined 7/144 (4.9%) Metropolitan region Nested PCR 18
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Olive-colored akodont
Abrothrix olivaceus
Serovar Hardjo (1), Javanica (5), Icterohaemorrageae (1), Pomona 8/31 (25.8%)i Los Ríos region Microscopic agglutination test (MAT) 21
Not determined 12/33 (36.4%) Los Ríos region Serology, microscopy or bacterial culture4 22
Rodentia Long-haired akodont
Abrothrix longipilis
Serovar Pomona (7), Hardjo (2), Canicola (1), Hardjo-Pomona (2), Icterohaemorrhageae 12/53 (22.6%) Los Ríos region Microscopic agglutination test (MAT) 21
Not determined 29/60 (48.3%) Los Ríos region Serology, microscopy or bacterial cultured 22
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Long-tailed Pygmy Rice Rat
Oligoryzomys longicaudatus
0/8 Los Ríos region Microscopic agglutination test (MAT) 21
0/9 Los Ríos region Serology, microscopy or bacterial cultured 22
Rodentia Brown rat
Rattus norvegicus
Serovar Icterohaemorrhageae-Javanica (1), Pomona, Hardjo, Canicola 1/4 (25%) Los Ríos region Microscopic agglutination test (MAT) 21
0/4 Los Ríos region Serology, microscopy or bacterial cultured 22
Rodentia Black rat
Rattus rattus
Serovar Pomona (3), Hardjo (2), Javanica, Canicola, Icterohaemorrhageae 5/7 (71.4%) Los Ríos region Microscopic agglutination test (MAT) 21
Not determined 4/7 (57.1%) Los Ríos region Serology, microscopy or bacterial cultured 22
Rodentia House mouse
Mus musculus
0/2 Los Ríos region Microscopic agglutination test (MAT) 21
0/7 Los Ríos region Serology, microscopy or bacterial cultured 22
Rodentia Long-clawed mole mouse
Geoxus valdivianus
0/1 Los Ríos region Microscopic agglutination test (MAT) 21
Not determined 1/1 (100%) Los Ríos region Serology, microscopy or bacterial cultured 22
Leptospira borgpetersenii Rodentia Degu
Octodon degus
Serovar Ballum 2/260 (0.77%) Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Carnivora American mink Neovison vison Not determined 4 positivesi Los Ríos (2), Los Lagos (1) and Aysén regions (1) Ribosomal RNA gene sequencing 28
Leptospira kirschneri Rodentia Degu
Octodon degus
0/260 Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Carnivora South American Sea Lion
Otaria byronia
Serovar Grippotyphosa 0/3 Los Ríos region Immunohistochemestry (IHC) 9
Leptospira biflexa Rodentia Degu
Octodon degus
0/260 Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Carnivora South American Sea Lion
Otaria byronia
Serovar Patoc 2/3 (66.67%) Los Ríos region Immunohistochemestry (IHC) 9
Leptospira santarosai Rodentia Degu
Octodon degus
0/260 Metropolitana region Microscopic agglutination test (MAT) 27
Rodentia Darwin's pericote
Phyllotis darwini
0/68 Metropolitana region Microscopic agglutination test (MAT) 27
Yersinia enterocolitica Rodentia Olive-colored akodont
Abrothrix olivaceus
Not determined 2/117 (1.7%) Los Ríos region Bacterial culture 117
Rodentia Long-haired akodont
Abrothrix longipilis
Not determined 5/32 (15.6%) Los Ríos region Bacterial culture 117
Rodentia Long-tailed Pygmy Rice Rat
Oligoryzomys longicaudatus
Not determined 2/106 (1.9%) Los Ríos region Bacterial culture 117
Rodentia Brown rat
Rattus norvegicus
Not determined 3/1 5 (20%) Los Ríos region Bacterial culture 117
Mycobacterium avium para-tuberculosis Lagomorpha European hare
Lepus europaeus
Not determined 48/380 (12.6%) Los Ríos region Mycobacteria growth indicator tube (MGIT) and Real-time PCR 68
Not determined 62/92 (67.4%) Los Ríos region Bacterial culture and Real-time PCR 69
Cetartiodactyla Southern Pudu
Pudu puda
Not determined 1/1 (100%) Biobío region Histopathology 66
Not determined 3/3 (100%) Los Ríos region Mycobacteria detection system and real-time PCR 67
Cetartiodactyla Guanaco
Lama guanicoe
Not determined 21/501 (4.2%) Magallanes region Bacterial culture and PCR 65
Cetartiodactyla Red deer
Cervus elaphus
Not determined 4/4 (100%) Los Lagos region Histopathology, bacterial culture and PCR 72
Not determined 14/14 (100%) Los Ríos and Los Lagos regions Histopathology 73
Cetartiodactyla Fallow deer
(Dama dama)
Not determined 9/9 (100%) Los Ríos and Los Lagos regions Histopathology 73
Cetartiodactyla Chilean huemul
(Hippocamelus bisulcus)
Not determined 6/14 (42.8%) Aysén and Magallanes regions (Bernardo O'Higgins National Park) Mycobacteria detection system and PCR 70
Mycoplasma sp. Carnivora Darwin's fox
Lycalopex fulvipes
Not determined 17/30 (56.67%) Chiloé Island (Los Lagos region) Real-time PCR and DNA sequencing 118
Mycoplasma haemocanis Carnivora Darwin's fox
Lycalopex fulvipes
Not determined 8 positivesi Chiloé Island (Los Lagos region) DNA sequencing 118
Mycoplasma haemofelis Carnivora Darwin's fox
Lycalopex fulvipes
Not determined 1 positivei Chiloé Island (Los Lagos region) DNA sequencing 118
Coxiella burnetti Carnivora Darwin's fox
Lycalopex fulvipes
0/30 Chiloé Island (Los Lagos region) RReal-time PCR 118
Borrelia sp. Carnivora Darwin's fox
Lycalopex fulvipes
0/30 Chiloé Island (Los Lagos region) RReal-time PCR 118
Cetartiodactyla Southern Pudu
Pudu puda
0/2 Los Ríos region PPCR and DNA sequencing 103
Bartonella sp. Carnivora Darwin's fox
Lycalopex fulvipes
0/30 Chiloé Island (Los Lagos region) RReal-time PCR 118
Rickettsia sp. Carnivora Darwin's fox
Lycalopex fulvipes
Not determined 1/30 (3.3%) Chiloé Island (Los Lagos region) Real-time PCR and DNA sequencing 118
Candidatus Neoehrlichia chilensis Rodentia Abrothrix sp. 4/5 (80%) Los Ríos region cPCR and DNA sequencing 100
Rodentia House Mouse
Mus musculus
1/5 (20%) Los Ríos region cPCR and DNA sequencing 100
Salmonella enterica Carnivora South American Sea Lion
Otaria byronia
Serovar Havana (1), Newport (1) 2/13 (15.38%) Antofagasta region Bacterial culture and invA gene detection by PCR 119
Brucella sp. Carnivora South American Sea Lion
Otaria byronia
0/3 Los Ríos region Plaque agglutination 9
Brucella canis Carnivora South American Sea Lion
Otaria byronia
0/3 Los Ríos region Plaque agglutination 9
Brucella abortus Carnivora South American Sea Lion
Otaria byronia
0/3 Los Ríos region Bengal rose 9
Cetartiodactyla Chilean Huemul
Hippocamelus bisulcus
0/18 Aysén region Rose Bengal test 89
Escherichia coli Carnivora South American Sea Lion
Otaria byronia
DAEC (Diffusely-adherent
Escherichia coli) (1), EPEC (Enteropathogenic E. coli)
1/15k (6.7%) Tarapacá region Bacterial culture and PCR 120
Campylobacter insulaenigrae Carnivora South American Sea Lion
Otaria byronia
Strain OFI 1/5k(6.7%) Los Ríos region Bacterial culture and amplified fragment length polymorphism analysis 121
Edwarsiella tarda Carnivora South American Sea Lion
Otaria byronia
Not determined 22/301 (73.3%) Los Ríos region Bacterial culture 122
Klebsiella pneumoniae Rodentia Long-tailed chinchilla
Chinchilla lanigera
Not determined 13/53 (24.5%) Coquimbo region Bacterial culture 123
Carnivora South American Sea Lion
Otaria byronia
Not determined 1/30 (3.3%) Los Ríos region Bacterial culture 137
Proteus mirabilis Carnivora South American Sea Lion
Otaria byronia
Not determined 2/30 (6.7%) Los Ríos region Bacterial culture 137
Rodentia Long-tailed chinchilla
Chinchilla lanigera
Not determined 1/53 (1.9%) Coquimbo region Bacterial culture 138
Corynebacterium pseudotuberculosis Cetartiodactyla Chilean Huemul
Hippocamelus bisulcus
Ovine genotype 2/2 (100%) Aysén region Bacterial culture and PCR 107
Morganella morganii Carnivora South American Sea Lion
Otaria byronia
Not determined 2/30 (6.7%) Los Ríos region Bacterial culture 137
Rodentia Long-tailed chinchilla
Chinchilla lanigera
Not determined 1/53 (1.9%) Coquimbo region Bacterial culture 138
Staphylococcus aureus Rodentia Long-tailed chinchilla
Chinchilla lanigera
Not determined 4/53 (7.5%) Coquimbo region Bacterial culture 138
Pseudomona auriginosa Rodentia Long-tailed chinchilla
Chinchilla lanigera
Not determined 2/53 (3.8%) Coquimbo region Bacterial culture 138

aRegions were not specified for each positive sample.

b9 seropositive samples considering a titer cut-off of 1:8 and 5 positives with a titer cut-off of 1:16.

cOnly the prevalence is indicated but there is no information about number of positive cases nor total number of individuals studied.

dThe specific serological method for analysis was not indicated in the study.

eThe study specified the collection site for only 14 positive samples.

fOnly the number of captured individuals is specified not the number of analyzed samples.

gThe total number of individuals examined in the study was not specified in the methodology.

hThe specific serological and immunohistochemical method for analysis were not indicated in the study.

iDNA/RNA sequencing was performed in samples confirmed in the same study.

jThe detail of number of positive samples presented in this study does not match with the total number of positive samples.

kThe study does not indicate if each fecal sample collected was from a unique individual or samples were taken more than one time from the same individual.

1The study does not indicate if each sample was collected from a unique individual.

A Spanish version of this review was published in Rev Chilena Infectol, 2019; 36 February (1).

Acknowledgments

The authors would like to thank Mr. Andrés Felipe Peña for his assistance with the management of literature references. We acknowledge the support of FONDECYT n° 1170972

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Received: June 10, 2018; Accepted: October 25, 2018

Corresponding author: Daniel González Acuña Facultad de Ciencias Veterinarias Universidad de Concepción Av. Vicente Méndez 595 Chillán, Chile. Phone: +56 422208739 Fax: +56 422208739 danigonz@udec.cl

Conflicts of interest. None declared.

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