Abstract
Rabies remains a public health problem in the Americas because of the great diversity of wild reservoirs that maintain the virus in nature. Here we report the antigenic characterization of 254 rabies viruses isolated from 148 nonreservoir and 106 reservoir hosts collected in 27 states of Mexico. Nine out of 11 antigenic variants previously reported in the United States were detected in Mexico by using the limited panel of monoclonal antibodies donated by the Centers for Disease Control and Prevention. Some rabies virus variants were isolated from their natural reservoirs, which were also taxonomically identified. Terrestrial reservoirs included stray dogs with V1, Urocyon cineroargenteus (gray foxes) with V7, and two subspecies of Spilogale putorius (spotted skunks) with different viral variants (V8 and V10). Aerial hosts included Tadarida brasiliensis mexicana and Desmodus rotundus, which harbored V9 and V4 and harbored V11, respectively. All variants, with the exception of V9, were isolated from nonreservoir hosts, while V3, V4, and V5 were not isolated from their natural reservoirs but only from livestock. Rabies virus antigenic typing allowed us to determine rabies reservoirs and their distribution in Mexico, data which will probably improve prevention and control of the illness in humans and in the reservoir hosts.
Rabies virus belongs to the Rhabdoviridae family and is the prototype member of the Lyssavirus genus. The latter comprises six genotypes and the Australian strains that have not yet been formally classified (3, 6, 16). Genotype 1 or classical rabies virus is the most widely distributed throughout the world and has the greatest epidemiological importance because of its association with a higher number of rabies cases than those for the other genotypes (31). This genotype has been the only one detected in the Americas so far (29, 30). All mammals infected with rabies virus develop encephalomyelitis, but only reservoir hosts are naturally able to maintain the virus (31). Epizootiological data for rabies and the molecular typing of the virus have shown that there are several reservoirs for genotype 1 whose variants remain in nature by independent cycles (15, 26, 31, 33). Within every cycle, a different reservoir plays a central role in the specific maintenance of each viral variant, whereby there are enzootic cycles of rabies in dogs, called urban rabies, and in wild species such as raccoons, skunks, foxes, vampire bats, insectivorous bats, and fruit bats (1, 14, 16, 23, 25, 27, 29). Rabies is disseminated by intraspecific but also by interspecific transmission (rabid reservoir to any other mammal); however, the latter is not a successful way to maintain rabies enzootically (26, 29). Disease spread can also occur by migration or translocation of reservoir populations infected with rabies virus (26, 29). The occurrence of the illness in any ecosystem strictly depends upon the coexistence of reservoir species and their specific rabies virus variants. Rabies-free areas can be both natural (because the virus has never been there) and human-made (by vaccination) despite the natural presence of reservoir species (26, 31).
In spite of the continuous development of rabies vaccine since 1884, the illness remains a public health concern in both developed and developing countries, due to the great diversity of rabies reservoirs, which has made prevention and control quite complex (6, 29, 31, 33). While autochthonous dog rabies has been eradicated in developed and some developing countries, the health problem continues with respect to bat transmission and remains latent in terrestrial wild reservoirs (26, 29). Human rabies has been substantially reduced in Mexico within the last decade: in 1990, 60 human deaths (60 of 69) involving dog transmission were reported, contrasting with only 1 human death due to this cause reported in 2000 (24). This reduction is the consequence of a significant decrease in dog rabies, from 8,706 cases in 1990 to 261 cases in 2000, as the result of massive dog vaccination campaigns in which the number of doses applied reached 14 million in 2000. On the other hand, the rate of human rabies cases detected in association with wild reservoirs has increased from 6% (4 of 69 plus 5 due to unidentified reservoirs) in 1990 to 80% (4 of 5) in 2000 (Programa de Zoonosis, Subsecretaría de Prevención y Protección de la Salud, Secretaría de Salud, unpublished data). Furthermore, in areas within Mexico where hematophagous bats are endemic the economic losses provoked by rabies in bovines have reached several million U.S. dollars (2). However, the extent of involvement of vampire bats has not been accurately determined. In some regions within Mexico and other Latin American countries, rabies transmission cycles overlap, as suggested by epidemiological and epizootiological data (10, 18, 20). This implies the simultaneous presence of more than one reservoir and more than one rabies virus variant. The scant information on rabies diagnosis in wild reservoir species severely hampers identification in the regions affected (F. Vargas-Pino et al., Abstr. XI Int. Meet. Res. Adv. Rabies Control. Americas, abstr. 67, p. 63-64, 2000). The retrospective and prospective analysis of viral isolates from humans and wild and domestic animals with specific monoclonal antibodies (MAbs) provides data regarding the most likely reservoir species involved in rabies transmission and dissemination (12, 15, 23, 28). Here we report the results for 254 viral isolates that were characterized with a panel of eight MAbs in order to determine the reservoirs and their distribution in Mexico.
MATERIALS AND METHODS
Samples.
We studied brain samples that were positive by the fluorescent antibody test used for routine diagnosis (9), which came from the following animals: 85 cows, 79 dogs, 40 humans, 15 skunks, 7 cats, 6 insectivorous bats, 5 pigs, 4 horses, 3 foxes, 2 bobcats, 2 coyotes, 2 goats, 2 sheep, 1 donkey, and 1 vampire bat. Samples were collected between 1993 and 2000 from 27 out of the 32 Mexican states, mostly during implementation of rabies focus control measures. Mammalogists identified the species of wild animals (foxes, skunks, and bats). The specimens were incorporated into the mammal collection of the Laboratorio de Cordados Terrestres under the direction of Ticul Alvares-Solorzano.
Viral propagation.
A 20% brain suspension was made from brain samples and was inoculated into the brains of 3-day-old suckling mice (19). On average four mice were used per sample. Mice died from rabies in an average time of 3 weeks, and brain samples were subjected to a semiquantitative fluorescent antibody test. Samples for which 85 to 100% (score, 3+ to 4+) of the microscopic fields had fluorescent foci were suitable for antigenic characterization with MAbs. The remaining samples were subjected to subsequent passages in mouse brain until reaching the level of antigen focus formation mentioned above (12, 23). Instead of prototype strains, previously identified V1 and V10 rabies viruses were used as reactivity controls for MAbs. In some assays, an anti-mouse immunoglobulin G (IgG) was added to positive impressions to rule out cross-reactions with this reagent.
Antigenic characterization of rabies virus.
An indirect fluorescence assay with a set of eight MAbs (donated by the Centers for Disease Control and Prevention, Atlanta, Ga.) (12) and with anti-mouse IgG (whole molecule) conjugated to fluorescein (Sigma, St. Louis, Mo.) was performed. Eight fresh brain tissue impressions per sample were made on eight-well polytetrafluoroethylene-coated microscope slides (bioMérieux, Marcy l'Etoile, France). Impressions were fixed with cold acetone at −20°C for 4 h and dried at room temperature. Twenty microliters of each MAb (C1, C4, C9, C10, C12, C15, C18, and C19), previously diluted 1:1,000, was added and incubated at 37°C for 30 min. Slides were rinsed carefully, impression by impression, with alternating phosphate-buffered saline (0.01 M, pH 7.6) and distilled water for four changes. Slides were dried at room temperature, and 20 μl of anti-mouse IgG conjugated with fluorescein (diluted 1:100) was added and incubated at 37°C for 30 min. The slides were rinsed again with phosphate-buffered saline and water as indicated above. Then 2 ml of a 2% solution of Evans blue dye was added and removed after 5 min. The slides were finally rinsed with water and dried at room temperature. A drop of buffered glycerol was added on each tissue impression. Slides were observed in an epifluorescence microscope at an ×400 magnification. Brain tissues in which V1 and V10 were previously propagated were mixed homogeneously and used as a positive control for the MAbs in each assay. A positive reaction for the MAb on each sample tested was defined as more than 50% of the foci fluorescing brilliant apple green. With this panel it is possible to define 11 reaction patterns, each of which is strongly associated with a different reservoir species (12); nevertheless, the V1 pattern, specific for dogs and mongooses, has also been reported for isolates from coyotes, foxes, and skunks, variants which are not closely related, by genetic studies, to that of dogs (11, 12, 23, 27).
RESULTS
We analyzed 254 specimens, which comprised 148 samples from nine species belonging to nonreservoir hosts and 106 samples from six species of reservoir hosts. Nine out of 11 antigenic variants were identified in brain specimens of mammals collected in 27 states throughout Mexico (Tables 1 and 2). Figures 1 to 3 depict the geographic location and respective host of each variant. The number of variants found per species was higher in nonreservoir hosts than in reservoir hosts. Additionally, in nonreservoir specimens, the higher the number of samples and the wider the territory that they encompassed, the higher the number of variants that were found. The same trend could not be inferred for reservoir hosts (Tables 1 and 2).
TABLE 1.
Rabies variants isolated in Mexico from nonreservoir and reservoir hosts
| Host type and species | No. of samples analyzed | Viral variant(s) | % Variants (respectively) |
|---|---|---|---|
| Nonreservoir | |||
| Human | 40 | V1, V10, V3, V8, V11 | 80, 8, 6, 3, 3 |
| Cow | 85 | V11, V1, V3, V8, V10 | 70, 16, 7, 5, 2 |
| Cat | 7 | V8, V1 | 57, 43 |
| Pig | 5 | V1, V5, V8 | 60, 20, 20 |
| Horse | 4 | V1, V3, V8 | 25, 50, 25 |
| Bobcat | 2 | V7, V10 | 50, 50 |
| Goat | 2 | V1, V11 | 50, 50 |
| Sheep | 2 | V3, V11 | 50, 50 |
| Donkey | 1 | V1 | 100 |
| Reservoir | |||
| Dog | 79 | V1, V5 | 99, 1 |
| Skunk | 15 | V8, V10, V1 | 60, 33, 7 |
| Fox | 3 | V7, V1 | 67, 33 |
| Coyote | 2 | V1, V7 | 50, 50 |
| Insectivorous bat | 6 | V9, V4 | 83, 17 |
| Hematophagous bat | 1 | V11 | 100 |
| Total | 254 |
TABLE 2.
Distribution of rabies variants in Mexico by state and year
| State | Species involved | Viral variant(s) (no. of cases) | Yr of occurrence (respectively) |
|---|---|---|---|
| Baja California Sur | Human | V10 (1, 1, 1) | 1995, 1999, 2000 |
| Spilogale putorius lucasana | V10 (4, 1) | 1998, 1999 | |
| Cow | V10 (1), V1 (1) | 1998; 1999 | |
| Bobcat (Lynx rufus) | V10 (1) | 2000 | |
| Horse | V1 (1) | 1999 | |
| Chiapas | Cow | V11 (1, 9), V3 (1) | 1997, 2000; 2000 |
| Dog | V1 (1) | 1999 | |
| Bat | V11 (1) | 2000 | |
| Chihuahua | Human | V1 (1, 1, 1) | 1994, 1996, 1997 |
| Tadarida brasiliensis mexicana | V9 (1, 1) | 1998, 1999 | |
| Coahuila | Coyote | V1 (1) | 2000 |
| Distrito Federal | Human | V1 (1, 1) | 1993, 1994 |
| Durango | Skunk | V1 (1) | 2000 |
| Dog | V1 (1, 2) | 1999, 2000 | |
| Estado de México | Human | V1 (2, 3), V3 (1) | 1993, 1994; 1999 |
| Cow | V1 (1, 2, 1) | 1996, 1997, 2000 | |
| Dog | V1 (10, 1) | 1998, 1999 | |
| Guanajuato | Tadarida brasiliensis mexicana | V9 (1) | 1998 |
| Spilogale putorius leucoparia | V8 (1) | 1999 | |
| Dog | V1 (1) | 1998 | |
| Cat | V8 (1) | 1997 | |
| Guerrero | Human | V1 (1) | 1999 |
| Dog | V1 (5, 3, 2) | 1998, 1999, 2000 | |
| Donkey | V1 (1) | 1999 | |
| Hidalgo | Human | V1 (1, 1) | 1996, 1997 |
| Cow | V11 (2, 31) | 1999, 2000 | |
| Goat | V11 (1) | 1999 | |
| Horse | V8 (1) | 1999 | |
| Sheep | V11 (1) | 2000 | |
| Dog | V1 (1, 1) | 1996, 1998 | |
| Jalisco | Cow | V8 (2, 1) | 1996, 2000 |
| Cat | V8 (1) | 2000 | |
| Michoacan | Dog | V1 (1), V5 (1) | 2000; 1999 |
| Morelos | Dog | V1 (1) | 2000 |
| Nayarit | Human | V8 (1) | 2000 |
| Nuevo León | Coyote (Canis latrans) | V1 (1) | 1998 |
| Oaxaca | Human | V1 (1, 1) | 1997, 1999 |
| Puebla | Human | V1 (1, 3, 1) | 1996, 1997, 2000 |
| Tadarida brasiliensis mexicana | V9 (1) | 1998 | |
| Tadarida brasiliensis mexicana | V4 (1) | 1997 | |
| Cow | V1 (2, 5, 1), V3 (1), V10 (1), V11 (4, 3) | 1996, 1997, 2000; 1996; 1996; 1996, 1998 | |
| Pig | V1 (2, 1) | 1998, 2000 | |
| Goat | V1 (1) | 1998 | |
| Cat | V1 (1, 1) | 1996, 2000 | |
| Dog | V1 (15, 12, 1) | 1996, 1998, 2000 | |
| Queretaro | Pig | V5 (1) | 1999 |
| San Luis Potosí | Human | V1 (3) | 1996 |
| Spilogale putorius leucoparia | V8 (1, 4, 1) | 1994, 1997, 2000 | |
| Conepatus mesoleucus | V8 (1) | 1998 | |
| Cow | V1 (1), V8 (1) | 1996; 1996 | |
| Pig | V8 (1) | 1999 | |
| Cat | V8 (2) | 1997 | |
| Tadarida brasiliensis mexicana | V9 (1) | 1999 | |
| Sinaloa | Bobcat (Lynx rufus) | V7 (1) | 2000/PICK>{tt} |
| Sonora | Coyote | V7 (1) | 1999 |
| Urocyon cineroargenteus | V1 (1), V7 (1) | 2000; 2000 | |
| Tabasco | Cow | V3 (1), V11 (2) | 2000; 2000 |
| Human | V4 (1) | 2000 | |
| Tamaulipas | Cow | V3 (1, 1) | 1999, 2000 |
| Dog | V1 (1) | 1997 | |
| Horse | V3 (2) | 2000 | |
| Tlaxcala | Human | V1 (1, 3, 1) | 1993, 1994, 1995 |
| Cat | V1 (1) | 1996 | |
| Dog | V1 (6, 3, 3, 1, 4) | 1996, 1997, 1998, 1999, 2000 | |
| Veracruz | Human | V1 (5), V11 (1) | 1997; 2000 |
| Cow | V11 (7, 1) | 1996, 1997 | |
| Yucatan | Cow | V3 (1) | 2000 |
| Sheep | V3 (1) | 2000 | |
| Zacatecas | Urocyon cineroargenteus | V7 (1) | 1999 |
| Spilogale putorius leucoparia | V8 (1) | 1998 | |
| Cow | V1 (1) | 2000 |
FIG. 1.
(a) Geographic location of the antigenic pattern V1 detected in reservoir and nonreservoir hosts; (b) magnification of the states with higher numbers of V1 cases, shaded in panel a. Symbols indicate species from which rabies virus was isolated as follows: human figure, humans; club, dogs; pen point, foxes; six-pointed asterisk, skunks; cross with rounded tips, coyotes; horned circle, cows; teardrop, cats; heart, pigs; star inside circle, humans, cows, and dogs; ship's wheel, humans and pigs; yin-yang symbol, humans, dogs, and cats; lightning bolt, humans and cows. Larger symbols represent higher numbers of cases.
FIG. 3.
Distribution of rabies virus variants V11, V3, V5, V9, and V4 isolated from bats and other species. Symbols represent isolation of rabies virus variants from different hosts as follows: flower, V11 isolated from Desmodus rotundus; eight-pointed star, V9 isolated from T. brasiliensis mexicana; cross with diamond tips, V4 isolated from T. brasiliensis mexicana; star inside circle, V11 isolated from humans; shaded triangle, V11 isolated from cows, goats, and sheep; circle inside star, V3 isolated from humans; diamond with concave sides, V3 isolated from cows, sheep, or horses; solid circle, V5 isolated from one dog and one pig. Larger symbols represent higher numbers of cases.
Figure 1a shows the distribution of V1 in Mexico isolated from nonreservoir and reservoir hosts. Figure 1b represents a magnification of the states with a higher density of cases related to V1. Interestingly, there was no evidence of V1 in dogs in the northern states. Nevertheless, samples of V1 were isolated from wild animals, cattle, or humans, with the exception of Tamaulipas and Durango. Figure 2 shows the distribution of variants transmitted by wild terrestrial reservoirs. V8 and V10 were isolated from skunks and nonreservoir hosts. V8 was found in the central states, and the major subspecies of skunk identified was Spilogale putorius leucoparia (1). V10 samples were limited to the south of the Baja California peninsula, with Spilogale putorius lucasana (17) being the only skunk subspecies involved. For both cases there was one striking exception, a V8 sample isolated from Conepatus mesoleucus (hog-nosed skunk [1]) in San Luis Potosí and a V10 sample isolated from a cow in Puebla. No new V8 and V10 rabies cases have been detected so far among hog-nosed-skunks and cows, respectively, but V8 is still being isolated in the region from S. putorius leucoparia. It is important to note that the cow involved in the isolation of V10 was raised in the state of Puebla.
FIG. 2.
Distribution of rabies virus variants V7, V8, and V10 isolated from foxes, skunks, and other species. Symbols: arrowheads pointing up and down, V8 isolated from S. putorius leucoparia; sunburst, V10 isolated from S. putorius lucasana; diagonally aligned squares, V7 isolated from U. cineroargenteus; cross with open center, V8 isolated from cats, horses, or cows; cross with rounded tips, V8 isolated from humans; Latin cross, V10 isolated from humans; flower, V10 isolated from two cows and one bobcat; Greek cross, V7 isolated from one coyote and one bobcat. Larger symbols represent higher numbers of cases.
V7 was isolated from gray foxes (Urocyon cineroargenteus) in Zacatecas and Sonora as well as from other wild species such as coyotes (Canis latrans) and bobcats (Lynx rufus) along the Sierra Madre Occidental within the boundaries of the northern states of Sonora and Sinaloa, respectively. Figure 3 shows the distribution of rabies in hematophagous bats; these were mainly isolated from cows in tropical and subtropical regions of the eastern coast (Tamaulipas) and in the southeastern states of Chiapas and Yucatan. V3 was also found in Estado de Mexico. V5 was found in the center of the country and in Michoacan, a subtropical state of western Mexico. V11 was the only variant that could be isolated from a vampire bat (Desmodus rotundus) in the state of Chiapas. V9 was isolated mainly from Tadarida brasiliensis mexicana (Mexican free-tailed bat) in the states of Chihuahua, San Luis Potosí, Guanajuato, and Puebla. V4 was isolated from one specimen of T. brasiliensis mexicana in Puebla.
DISCUSSION
Nine out of 11 antigenic rabies virus variants previously reported in the United States were found within Mexico (10, 11, 12, 14, 32). V4, V7, V8, V9, V10, and V11 were directly isolated from their natural wild reservoirs; V1 was isolated from dogs; and V3 and V5 were obtained from nonreservoir hosts. More than one antigenic variant was usually observed for nonreservoir hosts, even in species with low numbers of samples, such as pigs and horses. These results support previous findings that show the high susceptibility of mammals to any rabies virus (26, 29, 31). The high number of samples obtained from humans, cows, and dogs underlines the priority that these species have for the national program for the control of rabies. Furthermore, they show the diversity of variants found in nonreservoir species and thus an approximate estimate of the potential risk of humans acquiring rabies from the specific reservoirs of the variants found. The detection of variants transmitted by reservoirs other than dogs allowed for notification of the national program of zoonosis to search for other wild reservoir species. Besides the high number of rabid dogs, we could identify several samples from rabid skunks and insectivorous bats. The geographic distribution of rabies virus variants within Mexico is shown in Fig. 1 to 3. V1 has been concentrated in the central region of the country and correlates with a higher density of human and dog populations; the data also suggest that it is enzootic in the region because of its persistence over time. The presence of V1 in several southern states during 1999 and 2000 could be related either to trade activities or to an undetected region of enzooticity for dogs. In contrast, in the north of the country V1 was isolated mainly from wild species and livestock. This finding could be related to the domestic dog-coyote enzootic cycle identified by sequence analysis of the V1 nucleoprotein gene isolated from samples from coyotes and dogs (22, 27, 29). Alternatively, the presence of V1 in the northern states could be explained by the occurrence of a variant with a phylogenetic relationship with V1 rabies virus isolated from some skunks in California, Arkansas, and Wisconsin and foxes in Texas (11, 27), which is phylogenetically distant from V1 of dogs and coyotes (11).
V8 showed a wide distribution in central Mexico and was isolated from S. putorius leucoparia, while V10 was limited to the Baja California peninsula and was present in a different subspecies of spotted skunk (S. putorius lucasana); both were also found in nonreservoir hosts during the study (1994 to 2000). These data indicate that these variants are also enzootic and that their main reservoir is not the striped skunk (Mephitis mephitis), as in the United States (7, 33). V8 and V10 have differences at the genetic level; the phylogenetic tree suggested by other studies (11, 20) grouped both variants in different lineages, implying that they diverged long ago or are only distantly related. Thus, our data, along with those of previous studies (11, 20), show that in Mexico there are at least two independent skunk rabies foci that perhaps diverged long ago (11, 20). V7 was isolated for the first time in Mexico from two gray foxes (U. cineroargenteus), the variant's natural reservoir (5, 12, 22, 27), and from one coyote (C. latrans). V7 was also isolated from one bobcat (L. rufus), suggesting interspecies transmission and a wider distribution (5, 11) that corresponds to the main western mountain chains (Sierra Madre Occidental) and that in Zacatecas (13).
Regarding aerial reservoirs, isolation rates and distribution of the vampire bat-associated rabies virus variants (V11, V3, and V5) found in this study correlate with the relative population densities and distribution of the three vampire bat species found in Mexico (2, 13, 17, 21). It is not clear whether Desmodus rotundus is the major reservoir (14, 32) for the three variants found (V11, V3, and V5) or if Diphylla ecaudata and Diaemus youngi could also be infected and thus also play a role in the enzootic maintenance of the variants. The hypothesis of the involvement of the latter species and of Desmodus rotundus in the enzootic maintenance of rabies virus might not be likely if the feeding behavior of Diphylla ecaudata and Diaemus youngi were considered. However, the lack of data available about feeding preferences in rabid vampire bats strengthens our hypothesis. The fact that V5 was found only in one pig and one dog probably means that the natural reservoir of this variant could have low population densities, low rabies rates, and restricted distribution in the country, data that are in agreement with the ecology of Diaemus youngi (17, 21).
Rabies in the colonial insectivorous bat T. brasiliensis mexicana was first detected in the southern United States in 1953 (4, 8, 29). In Mexico, just one case of V9 rabies attributed to T. brasiliensis was recently reported (11). In the present study six rabid T. brasiliensis mexicana specimens were found and identified taxonomically, and their respective rabies virus isolates were characterized antigenically. Given the migratory behavior of this species, the identification of a rabies virus antigenic variant is not enough to determine whether the rabid T. brasiliensis mexicana bats belong to the same colony (11, 27). A different situation prevailed in the central region in the state of Puebla, where V4 and V9 were almost simultaneously detected. This study globally shows that rabies virus antigenic typing allowed determination of rabid reservoirs and their distribution in Mexico, which will probably enable better prevention and control of the illness in humans and in the reservoir hosts.
Acknowledgments
We acknowledge the following: Charles Rupprecht, Carlos De Mattos, Cecilia De Mattos, and Jean Smith from the Centers for Disease Control and Prevention, Atlanta, Ga., for providing MAbs, training, technical support, and encouragement; Ticul Alvarez and Jorge A. Villalpando for their support in identifying wild animals; our colleagues working at the National Network of Public Health Rabies Laboratories as well as the epidemiologists and personnel of the rabies control program in Mexico for providing all samples; the Ministry of Agriculture, Livestock and Food Protection for providing some specimens from wild animals and cattle; Dolores Correa (InDRE) for encouraging this work; and our collaborators Jorge Romero, Beatriz Escamilla, Juan Manuel Campos, Irma Padilla, Ofelia Hernandez, and Lidia Crecencio for their generous hard work and help.
We also acknowledge Alfonso Ruiz; Primo Arambulo III from the Pan-American Health Organization (PAHO), Washington, D.C.; and Eduardo Alvarez Peralta from PAHO Mexico for giving financial support for training and technology transfer.
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