Murcielagos reservorios del virus de la Rabia y epidemiologia de la Rabia en Colombia: una revision.
Reservatorios de morcegos do virus da raiva e epidemiologia da raiva na Colombia: uma revisao
The rabies virus (RABV) is an RNA virus that belongs to the order Mononegavirales 1 genus Lyssavirus, and in the family Rhabdoviridae (2). The virus particles are bullet shaped and measure 75 nm in diameter with a length of 200 nm (3). The genus Lyssavirus includes fourteen species which are classified by their genomic sequence; they are the RABV Lagos bat virus (LBV), Mokola virus (MOKV), Duvenhage virus (DUVV), European bat lyssavirus type 1 (EBLV1), European bat lyssavirus type 2 (EBLV2), Australian bat lyssavirus (ABLV), Aravan virus (ARAV) and Khujand virus (KHUV), Irkut virus (IRKV), West Caucasian bat virus (WCBV), Bokeloh bat lyssavirus (BBLV), Ikoma Lyssavirus (IKOV) and Shimoni bat virus (SHIBV). Nine of the fourteen species of lyssavirus (DUVV EBLV1, EBLV2, ABLV ARAV KHUV IRKV WCBV and BBLV) have been isolated from insectivorous bats. Additionally, the members of the genus Lyssavirus were subdivided into three phylogroups (I, II and III). Phylogroup I includes RABV DUVV EBLV1, EBLV2, ABLV ARAV KHUV, IRKV and BBLV (2,4). Phylogroup II includes LBV and MOKV and a new lyssavirus named "Shimoni bat virus" (SHIBV), which was isolated from a freshly dead insectivorous bat (Hipposideros commersoni) in the coastal region of Kenya in 2009 and was found to belong to the Phylogroup II lyssaviruses (5). Phylogroup III is compounded by the WCBV and one currently unclassified lyssaviruses identified as IKOV (2). The RABV genome consists of an approximately 12 kb nonsegmented, single negative strand RNA molecule (6), encoding five structural proteins that are: the nucleocapsid (N) protein, a phosphoprotein (P), matrix (M) protein, glycoprotein (G), and an RNA-dependent RNA polymerase (L) in the order 3'-N-P-M-G-L-5' (7). It is impossible to make a clinical differentiation between the disease caused by any virus species (8).
Rabies, the disease
Rabies is one of the most important zoonotic diseases that is caused by a highly neurotropic Rhabdovirus (9). The disease is reported in domestic and wild animals worldwide and it's estimated to cause up to 70,000 human deaths per year, mostly in rural areas of Asia and Africa (10). Rabies represents a neuroinvasive disease that is characterized by acute encephalitis with two clinical manifestations; the furious (classical or encephalitic) and the paralytic form. Furious rabies is the most common form of human rabies, accounting for approximately 80 % of cases. With the exception of Antarctica, rabies is endemic to all continents. Classical RABVs have a worldwide distribution except for a few island nations such as Great Britain, Ireland, New Zealand, Hawaii, the continents of Australia and Antarctica, and an increasing number of Western European countries (11) The disease affects a broad spectrum of warm blooded animals. ALL mammals are susceptible to varying degrees, especially members of the order Carnivora and Chiroptera (10).
Rabies is an invariable fatal disease, particularly when clinical symptoms have developed. Rabid animals commonly show neurological changes such as paraparesis, aggressiveness, hydrophobia and sialorrhea, agitation, mental confusion, and tetraparesis (12). In Latin America, rabies is classified into two epidemiologic forms; urban rabies and sylvatic rabies. The common vampire bat, Desmodus rotundus, has emerged as the principal RABV reservoir host along the species natural range from Mexico to South America. D. rotundus was correlated with the vampire bat RABV variants which is more prevalent than the dog RABV variants in Peru, however, the prevalence of any RABV variant might be dependent of local or regional RABV vaccination plans (9).
Pathogenesis of rabies
Paralytic rabies is characterized by flaccid paralysis in the bitten limb, which ascends symmetrically or asymmetrically, whereas the furious rabies manifests hyper-excitability, autonomic dysfunction, hydrophobia, and aerophobia (13,14).
RABV may enter the organism by different transmission routes such as animal bites or scratches, and the virus can remain latent close to the inoculation site for long periods of time. The virus replicates slowly within muscle cells until it arrives to the neuromuscular junction (14). The viral glycoprotein is essential for transsynaptic spreading by using cell nicotinic acetylcholine receptors at the neuromuscular junctions (15). The virus migrates along peripheral nerves to the central nervous system via retrograde fast axonal transport, a process that is facilitated by the viral P protein (17), at a rate of 12 to 100 mm/d (16). In the CNS, RABV replicates in neurons and induces necrosis and inflammation18. Then, the virus spread to other organs of the body, reaching the salivary gland where high viral concentrations of virus could be found in the saliva, peripheral nerves and other organs (7) (Figure 1).
RABV might be present in different tissues of bats: particularly the buccal cavity, saliva, and brown fat. The distribution of RABV in tissues was evaluated in 26 bat species from Brazil. The species Artibeus lituratus (13), Myotis nigricans (4), Eptesicus furinalis (5), Eptesicus diminutus (1), Lasiurus blossevillii (1), and Lasiurus ega (2) were tested by using hnRT-PCR. The virus was detected in tongue (92 % and 85 %), brown fat (82 % and 77 %), lung (62 % and 77 %), heart (42 % and 77%), stomach (92 % and 64 %), liver (38 % and 67 %), spleen (43 % and 27 %), bladder (73 % and 88 %), kidney (77 % and 38 %), intestine tissues (77 % and 38 %), and feces (38 % and 42 %) from frugivorous and insectivorous bats. It was noted that the virus was higher in stomachs of frugivorous bats than from insectivorous bats (19). A possible reason for those findings could be that infected bats defecate on the fruits that are eaten later by frugivorous bats, which ingest the virus. Contrary, insectivorous bats, due to their eating habits, may have lower viral loads, However, additional studies are necessary to determine the relationship between feeding habits of the non-hematophagous bats and the rabies virus.
Rabies virus transmission
The RABV is usually transmitted from an infected animal to one that's susceptible 1 The virus is usually present in the saliva of rabid animals, and it enters the body via infiltration of virus-laden saliva into a wound or by the exposure of mucosal surfaces to saliva from an infected animal (bites) (20). Additionally, a rare form of transmission may be by the inhalation of aerosols with RABV present. This would most likely occur in caves with dense populations of bats in which the virus is present (21).
The RABV and the majority of lyssaviruses, are found in natural bat reservoirs. These animals are unique among mammals due to having exceptional sociality and longevity. Given these features and the recognized status of bats as reservoirs for RABVs in the Americas, individual bats may experience repeated exposure to RABV during their lifetime (22). Hematophagous, frugivorous, and insectivorous bats can transmit the RABV23, and phylogenetic analysis using nucleotide sequences of N or G genes revealed that RABV is grouped into clusters according to the bat species that support the existence of species-specific variants or lineages of the virus (19, 24).
Main species of Bats reservoirs for rabies virus in the world
The class Mammalia has 5,416 species and the order Chiroptera comprises of the second largest group of mammals in number, with 1,120 species (23) Bats have a worldwide distribution, absent only in the Polar Regions and some oceanic islands. Most of these animals live in tropical and subtropical regions, but can be found in temperate regions (25). A number of bats reservoirs for RABV has been described, including hematophagous, insectivorous and frugivorous bats (Table 1), although the RABV has been detected mainly in insectivorous bat species (Figure 2).
Insectivorous bat species have worldwide distribution and can be found in almost all ecosystems, together with others frugivorous bats species, whereas all the three species of hematophagous bats are only found in Latin America, with the common vampire (Desmodus rotundus) being the only well-known RABV reservoir --.
Rabies cases and virus variants in Colombia
RABV in Colombia have been grouped into three variants, Colombian genetic variant I viruses (isolated in Arauca and the Central Region of the country), Colombian genetic variant II viruses (isolated in the Caribbean Region) and the third group that consists of viruses isolated from two insectivorous bats (Eptesicus brasiliensis and Molossus molossus), three domestic dogs and a human. The genetic sequence analysis indicated that the virus isolates belonging to the third group were variants of bat RABV, the first finding that associated bats to rabies in dogs and humans in Colombia (49) Rabies in Colombia and other Latin American countries are an important public health and economic problem, and the disease is categorized as urban rabies and sylvatic rabies, which have distinct epidemiological cycles (50, 51) Urban rabies is usually transmitted by the domestic dog and this animal is the main transmitter and reservoir of the virus, whereas sylvatic rabies is transmitted principally by bats the main reservoirs of the disease that is transmitted to domestic animals such as cows and horses, however, mongooses and coyotes can share the Variant Kurban rabies) with domestics dogs in less proportion (49, 56)
Wild RABV variants identified in Colombia are V3 (hematophagous bats), V4 (insectivorous bats), V5 (hematophagous bats) and V8 (skunk) (52). A study that analyzed a total of 124 samples obtained from human cases of rabies and 8 from other mammal species within the period 1 994-2005, identified eight genetic lineages (GL1- GL8), of RABV. Phylogenetic analyses of the partial nucleoprotein gene sequence determined specific variants within those genotypes. The GL4 comprised of Variant V3 and V8 and a variant no determined (ND), which were associated with hematophagous bats, the GL5 and GL6 consisted of V4 viruses associated with Tadarida brasiliensis bats, the GL5 grouped independently. The GL7 and GL8 segregated independently within clades associated with colonial insectivorous and solitary bats, both of these were no determined variants. RABVs isolated from humans grouped within GL2, GL3 and GL4, which corresponded to V1, V3, V8 and ND. Dogs and Desmodus rotundus are the two major RABV reservoirs and vectors in Colombia, although insectivorous bats may also be involved (53).
RABV variants V3 and V4 are the most prevalent in Colombia, and this situation seems to be influenced by increased deforestation and urban architecture that provides shelter, causing more frequent interactions between humans and bats 44. The variant V4, that is associated with frugivorous and insectivorous bats, was isolated from a dog and a human in the northern of Colombia (54).
RABV was isolated for the first time from bats in Colombia by Alarcon in 1968, who reported the isolation of two strain of RABV from insectivorous and frugivorous bats (Myotis nigricans, Lasiurus ega and Carollia perspicillata) captured from areas of the departments of Guajira, Santander and Antioquia. Other bat species such as Glossophaga longirostris, Artibeus lituratus palmarum, Platyrrhinus Helleri (Vampyrops Helleri), Trachops Cirrhosus cirrhosus, Peroptexys kappleri, Phyllostomus Hastatus, Saccopteryx bilineata, and Molossus molossus were negative to the virus (42). In the urban zone of Cali, the species Carollia perspicillata, Artibeus lituratus, Eptesicus brasiliensis, Myotis nigricans, Molossus molossus, and Tadarida brasiliensis were also reported as transmitters of RABV in the period December 2000 to June 2002 (55).
The National Institute of Health of Colombia has reported a considerable number of cases of sylvatic rabies transmitted by bats since 2000. A total of thirty-five cases of human rabies, twenty-two of those cases were transmitted by bats, eight by cats, and five by dogs. Regarding the virus variants, two were variant VA (atypical), five-Variant V1 (domestic and wild dogs, mongooses and coyotes), twenty-four-variant V3 (hematophagous bat), three-Variant V4 (insectivorous bat), and one of those cases was variant V8 (skunk) (56). Outbreaks of rabies disease have been recorded in high magnitude in Bajo Baudo, Choco, where hematophagous bats represent the major threat for sylvatic rabies transmission (51, 57). Outbreaks of rabies caused by variants V3 have also been recorded in San Luis de Palenque in Casanare and Floridablanca in Santander (56) and Santander de Quilichao in Cauca, where a cat was the transmitter to humans, linking sylvatic rabies and the urban ecosystem (27) In Encino and Piedecuesta in Santander, other two human rabies cases were reported to be caused by the variant V3 transmitted by cat and a hematophagous bat, respectively. Cats usually get infected by contact with bats during their predatory behavior (50).
Outbreaks of rabies caused by variant V4 were reported in Moniquira, Boyaca, where the insectivorous bat Tadarida brasiliensis was identified as the main reservoir (44). The variant V4 was also responsible for an outbreak in Roldanillo, Valle del Cauca in 2012 (56), whereas in Barrancabermeja, Santander an outbreak was caused by the atypical variant VA (56). An atypical RABV variant from sylvatic origin was also responsible for the disease in a child that had contact with a cat in San Luis, Tolima in 2010 (INS, 2014).
Diagnosis of rabies infection
The diagnosis of the virus is conducted by the use of a number of methodologies that include the detection of rabies antigens in tissues, nucleic acids, amplification of rabies particles or serological tests.
Mouse inoculation test
It consist of an intracerebral inoculation of a clarified supernatant of a 10-20 % (w/v) homogenate of brain material including brainstem (cortex, Ammon's horn, thalamus, medulla oblongata) in an isotonic buffered solution with antibiotics, into groups of 3 to 10 mice that should be observed by 28 days to record mortality and detection of RABV. In the case of newborn mouse, they can be evaluated on days 5, 7, 9 and 11 post-inoculation. Any deaths occurring during the first 4 days are regarded as nonspecific (due to stress or bacterial infection) (59).
Fluorescent antibody test (FAT)
It is the most widely used test for rabies diagnosis recommended by WHO and OIE as the gold standard test and it may be used directly on a smear. The test uses purified immunoglobulin previously conjugated with fluorescein isothiocyanate (FITC) that is added onto an acetone-fixed brain tissue smear, preferably made from several parts of the central nervous system. FAT provides a reliable diagnosis in 98--100 % of cases for all RABV strains if a potent conjugate is used. FAT can be applied in fresh or frozen brain tissues sections, with very similar results (99.8% sensitivity and 100 % specificity) when applied to fresh or formalin-fixed tissues (61), however, it should not be used in decomposed tissue samples (60).
Reverse transcription PCR (RT-PCR)
Classical reverse transcription-polymerase chain reaction assay has been reported to be a sensitive and specific tool for routine diagnostic purposes (62). It consist of the use of a reverse transcriptase to synthesize a complementary DNA copy from viral RNA and then, conventional PCR is used to amplify a gene fragment from the virus genome (63). The technique can be used to detect RABV in decomposed samples that often appear due to the warm climate and fluctuations in ambient temperature during sample transport and storage (64). Positive diagnostic results from such samples are reliable but negative results may be invalid (58).
A comparison of RT-PCR and MIT for detection of RABV in 95 positive samples that were stored for 4--13 years at -20 and -80 [degrees]C revealed that only 32 (33,6 %) of the samples were positive with the mouse inoculation test, while RT-PCR detected the viral genome in 62 (65,3 %) samples. Samples that were stored for >10 years gave 59.7 % positivity by RT-PCR and only 22.1 % by MIT (65).
Heminested RT-PCR (HnRT-PCR)
It is one of the most sensitive and rapid technique for rabies diagnosis. The method can be applied to both living animals and post mortem collected samples, when the brain samples are in a decomposed state. The PCR products can be used for DNA sequencing for final identification of virus origin by epidemiological analysis (66). Our group implemented this technique to analyze brain tissues from a number of bats collected in rural areas of the Tolima region (Figure 2). A total of eleven bats species including Artibeus jamaicensis, Artibeus lituratus, Carollia perspicillata, Desmodus rotundus, Molossus molossus, Molussus ater, Myotis nigricans, Phyllostomus hastatus, Platyrrhinus dorsalis, Saccopteryx bilineata and Saccopteryx leptura were analyzed by HnRT-PCR and all samples were negative for the presence of RABV (Figure 2).
Real time PCR
It is an alternative test that have been demonstrated to be more sensitive than HnRT-PCR and can be used to further extend the rabies RNA detection limits in decomposed samples (67). This technique allows to assess gene expression analysis, determination of viral load and detection of genetically modified organisms (68) The primers are designed in such a way that a fluorescent signal is generated only when the primers are incorporated into an amplification product. Detection of target sequences occurs by monitoring the fluorescence generated by intercalating dyes or fluorophore labelled primers for sequence-specific probes (69). This assay has high sensitivity and specificity enabling simultaneous amplification and quantification of specific nucleic acid sequences that made it exceptional for diagnosis for this infectious agent (69, 70). Real time PCR was compared to conventional RT-PCR to analyze saliva samples from 21 suspected patients and found that the sensitivity was superior (75% vs. 37%) to that offered by RT-PCR (71).
Enzyme linked immunosorbent assay (ELISA)
The ELISA is the most used diagnostic test for rabies, which measures specific immunoglobulins such as IgM. The test consist in the detection of RABV neutralizing antibody in sera samples taken from the suspected animal (72). The test reduce time, facilitate handling and avoid the use of biosecurity level 2 or 3 laboratories, do not require live RABV or cell culture and can be automated. The test was developed for domestic carnivores and wildlife and is the only one certified and prescribed by the OIE for rabies detection. However, the ELISA test, although it may have 100 % specificity, the sensitivity was around 78.2 % when 593 samples of domestic carnivores were evaluated (73, 74).
Prevention of rabies
Rabies is considered a vaccine-preventable disease and annual vaccination of pets is the recommended strategy to prevent and control rabies (76) However, it has been reported that epizootic areas of the rabies virus are self-limiting and D. rotundus sacrificial campaigns have minimal or no incidence on the rate of presentation of the disease in these areas (77) In the case of an attack by a potentially rabid animal, it must be immediately informed to the competent health authorities to start an appropriate research (study of focus, rabies vaccination of dogs and cats, watching suspected animals, taking and sending samples, and institutional active search) and specific treatment which is contemplated by the INS (52). It is recommended to avoid wild animals as pets and not to handle animals suspected of carrying the disease (dogs, cats, cattle) or handle bats that are on the ground or showing abnormal behavior (75). Competent authorities in each country must have an active surveillance system for the disease and appropriate vaccination programs in areas with high risk of presentation (10). Unfortunately, in Colombia the coverage of vaccination of pets is very limited, the percentage of vaccination coverage of municipalities in Colombia is limited only 59,9 % of municipalities have a % coverage [greater than or equal to] 80 %, 7,96 % of municipalities a % coverage between 70 and 79 %, 6,64 % of the municipalities a % coverage between 60-69 % and 25,5 % of the remaining municipalities a % coverage [less than or equal to] 59 % (78).
Rabies is a zoonotic disease caused by a neurotropic virus that is present in many species of chiropters all over the world. RABV induces an acute encephalitis, clinically manifested as furious and a paralytic form. The virus is classified in Latin countries as urban rabies and sylvatic rabies that are transmitted by domestic animals and bats respectively (Figure 1). Insectivorous and frugivorous bats act predominantly as reservoirs of rabies and transmitters of the disease in many part of the world. In Colombia, variants V3,V4 and VA (variant hematophagous bat, variant insectivorous bat and variant atypical associated with bats), of the virus, are responsible for a significant number of rabies outbreaks in human (52). The disease is mainly linked to felines such as cats that may hunt infected bats, getting infected too, which make a rabid cat that usually contact with humans, transmitting the virus. Thus evaluation of rapid diagnosis techniques such as RT-PCR to detect RABV in bat tissues might be needed to promote active surveillance to bats populations. Rabies is prevented by annual vaccination of pets, however, the coverage of this activity in Colombia is stiff limited, thus much effort is needed to educate and sensitize the people on this fatal disease.
This study was funded by grants from the Central Research Office of the University of Totima to Noel Verjan Garcia (Project No. 1 2021 4). The study was conceived and accepted by the Consejo Tecnico Seccional para la Vigilancia y Control de las Zoonosis en el Totima and approved by the bioethics committee of the University of Totima. The authors thank to Victoria Rodriguez and Gisella Holguin for technical assistance in RT-PCR and Hector Nieto for the illustration.
Conflicts of interest
The authors declare they have no conflicts of interest with regard to the work presented in this report.
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Jimmy Fernando Cifuentes Jimenez , Est MVZ; Ruben Dario Perez Lopez , MVZ; Noel Verjan Garcia [mail] * MVZ MSc PhD CvLAC
Recibido: 24 de febrero de 2017.
Aceptado: 23 de junio de 2017.
* Corresponding author: Noel Verjan Garcia, Ph.D. Immunobiology and Pathogenesis Research Group. Department of Animal Health, University of Tolima, Faculty of Veterinary Medicine, Santa Helena, Parte Alta, Ibague, Tolima, Colombia, A.A. 546.
 immunobiology and Pathogenesis Research Group, Faculty of Veterinary Medicine and Zootecnia, Universidad del Tolima, Altos de Santa Helena A.A. 546, Ibague, Tolima.
 Instituto Colombiano Agropecuario, ICA, Ibague, Tolima.
Caption: Figure 1. Connection of sylvatic rabies to urban ecosystem. 1. The cat hunts an infected chiropter. 2. The cat is bitten, the virus enter to the body through the wound by infiltrating of saliva, and the virus replicates in the peripheral muscles close to the wound and migrates to CNS. In the CNS, the virus is distributed to other organs, eventually reaching the salivary glands. 3. The rabid animal shows neurological changes. 4. The animal is predisposed to attack humans or other animals. The cycle repeats and causes the death of the infected individual.
Caption: Figure 2. Main bat reservoirs of RABV are represented by a photograph and a schematic diagram. A. Tadarida brasiliensis (insectivoro), B. Desmodus rotundus (hematophagous), C. Artibeus lituratus (frugivorous) and D. Carollia perspicillata (frugivorous).
Caption: Figure 3. HnRT-PCR amplification of 299 bp of RABV N gene from chiropters brain tissues. Total RNA was extracted from bran tissue of six captured bats in the Tolima region and subjected to RT-PCR analysis and the cDNA construction was validated with the amplification of the housekeeping gene b-actin in each sample. M: 100 bp DNA ladder; Positive control RNA from RABV was kindly provided by Dr. Andres Paez from the National Institute of Health of Colombia (INS). F06, H07, H08, H09, I10 and H25 corresponds to brain bats samples.
Table.1 Chiroptera species that have been reported positive for the presence of RABV in the world. N Species Location 1 Desmodus rotundus Brazil/Colombia 2 Diphylla ecaudata Brazil 3 Diaemus youngi Brazil 4 Tadarida brasiliensis Chile 5 Lasiurus cinereus Chile 6 Histiotus macrotes Chile 7 Myotis chiloensis Chile 8 Artibeus lituratus Brazil 9 Chrotopterus auritus Brazil 10 Eptesicus fuscus United state 11 Myotis sp United state 12 Lasionycteris noctivagans United states migratory tree-roosting hoary 13 Lasiurus cinereus United states migratory tree-roosting hoary NA 14 Eptesicus spp Brazil 15 Nyctinomops macrotis Brazil 16 Molossus spp Brazil 17 Tadarida spp Brazil 18 Histiotus velatus Brazil 19 Lasiurus spp Brazil 20 Molossus ater Brazil 21 Molossus molossus Brazil 22 Eumops auripendulus Brazil- Ecuador 23 Nyctinomops laticaudatus Brazil- Ecuador 24 Eptesicus furinalis Brazil- Ecuador 25 Lasiurus cinereus United states 26 Lasiurus borealis United states/ Chile 27 Lasionycteris noctivagans United states 28 Dasypterus floridanus Florida/ solitary 29 Phyllostomus supercilliatum United states 30 Myotis evo United states 31 Antrozous pallidus Canada, Mexico and Cuba 32 Macrotus californicus Mexico and the United States 33 Pipistrellus hesperus western United States and Mexico 34 Myotis keenii Canada 35 Euderma maculata Canada 36 Myotis lucifugus Canada 37 Myotis yumanensis Canada 38 Lasiurus intermedius Canada 39 Myotis evotis Canada 40 Myotis nattereri German and France 41 Myotis dasycneme Germany 42 Myotis daubentonii Germany 43 Eptesicus isabellinus Germany 44 Eptesicus serotinus Germany- Spain 45 Pipistrellus nathusii Germany 46 Miniopterus schreibersii Southeastern Europe 47 Hipposideros commersoni Kenya 48 Rousettus aegyptiacus Europe Mediterranean 49 Pipistrellus pipistrellus Spain EBLV1, EBLV2 50 Artibeus jamaicensis Kenia 51 Eidolon helvum Nigeria 52 Rousettus aegyptiacus Kenia 53 Micropteropus pusillus Central African Republic 54 Epomophorus wahlbergi South Africa 55 Nycteris gambiensis Guinea 56 Artibeus obscurus Brazil 57 Phyllostomus hastatus hastatus Brazil 58 Uroderma bilobatum Colombia 59 Phyllostomus hastatus Colombia 60 Eptesicus braziliensis Colombia 61 Carollia perspicillata Colombia 62 Myotis nigricans Colombia 63 Lasiurus ega Colombia 64 Molossus molossus Colombia N Ecology Reference 1 hematophagous 12, 27 2 hematophagous 8, 25 3 hematophagous 25 4 insectivorous 8, 28 5 insectivorous 28 6 insectivorous 28 7 insectivorous 28 8 frugivorous 24 9 omnivorous 25 10 insectivorous 22 11 insectivorous 29 12 insectivorous 30 13 insectivorous 30 14 insectivorous 31 15 insectivorous 25 16 insectivorous 31 17 insectivorous 31 18 insectivorous 25 19 insectivorous 31 20 insectivorous 32 21 insectivorous 33 22 insectivorous 33 23 insectivorous 33 24 insectivorous 33 25 insectivorous 34 26 insectivorous 28, 34 27 insectivorous 35 28 insectivorous 35 29 insectivorous 36 30 insectivorous 35 31 insectivorous 35 32 insectivorous 35 33 insectivorous 35 34 insectivorous 37 35 insectivorous 37 36 insectivorous 37 37 insectivorous 37 38 insectivorous 37 39 insectivorous 37 40 insectivorous 38 41 insectivorous 38 42 insectivorous 38 43 insectivorous 38 44 insectivorous 38, 39 45 insectivorous 38 46 insectivorous 40 47 insectivorous 5 48 frugivorous 5 49 insectivorous 39 50 frugivorous 8 51 frugivorous 41 52 frugivorous 41 53 frugivorous 41 54 frugivorous 41 55 insectivorous 42 56 frugivorous 25 57 insectivorous 25, 43 58 insectivorous 44 59 Frugivoro-insectivorous (45) 44 60 insectivorous 46 61 frugivorous 47 62 insectivorous 47 63 insectivorous 47 64 insectivorous 48
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|Title Annotation:||Articulo de revision|
|Author:||Cifuentes Jimenez, Jimmy Fernando; Perez Lopez, Ruben Dario; Verjan Garcia, Noel|
|Publication:||Revista CES Medicina Veterinaria y Zootecnia|
|Date:||May 1, 2017|
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