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The New Face of Human Rabies in Mexico, What's Next After Eradicating Rabies
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DOI: 10.1089/vbz.2021.0051

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The New Face of Human Rabies in Mexico, What’s Next

After Eradicating Rabies in Dogs

Nidia Aréchiga Ceballos,1 Paola Puebla Rodrı́guez,1 and Álvaro Aguilar Setién2,*
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Abstract

In pre-Hispanic Mexico, dogs were not identified as an important source of rabies. We know from codexes and
chronicles of the conquerors that at that time, rabies cases in humans and domestic animals were caused by local
wildlife species such as bats. Canine-rabies virus variant seems to have arrived with Europeans. The first
documented case of canine rabies in the Americas is found in Mexico in the Annals of the Holy Inquisition (16th
century). During Mexico’s independence, cases were frequently reported. In the 19th century the first attempts
to control human rabies were made through sanitary measures such as elimination of rabid dogs and applying
postexposure vaccination. During the first half of the 20th century, the efficacy of canine vaccination to prevent
human rabies was established. However, in Mexico, despite reports of numerous human cases (>70/year),
canine vaccination did not have enough coverage. It was only during the 1990s that Mexico made a serious
commitment to eliminate dog-transmitted human rabies. Since the beginning, vaccination campaigns have been
free and massive. Coverage increased from 7,100,000 doses in 1990 to more than 18,000,000 since 2017. This
culminated in the elimination of dog-mediated human rabies cases since 2006. Subsequently, the epidemiology
of rabies had changed. Nowadays, it is wildlife species (mainly bats and skunks) that are the source of human
rabies. As a mega-biodiverse country Mexico has numerous wildlife species with potential to transmit rabies
virus. Thus it is paramount to remain vigilant with respect to canine vaccination campaigns and to promote
rabies research in wildlife.

Keywords: Canine rabies elimination, Mexico, wildlife rabies

Introduction in Latin America, Mexico made tangible the possibility of

being free of human rabies transmitted by dogs (by elimi-

O n November 11, 2019, Mexico was recognized by the

World Health Organization (WHO) and the Pan
American Health Organization (PAHO) for being the first
nating the canine rabies virus variant [RVV], natural reser-
voirs of which are dogs).
Canine rabies is a disease known by the humankind since
country to have fulfilled the requirements to be validated as a ancient times. There is a record of documents that testify the
country free of human rabies transmitted by dogs. This was presence of rabies in ancient civilizations, including the
thanks to sustained canine vaccination campaigns and the Egyptian, Mesopotamian, Greek, and Roman empires (Steele
epidemiological surveillance system. and Fernandez 2017). By the 15th century, canine rabies was
This event marks a milestone in national public health. a frequent disease in the Old World (Flamand 1985, Pradilla
After many years of having one of the highest rates of rabies Ardila 2010, Steele and Fernandez 2017).

1
Laboratorio de Rabia, Departamento de Virologı́a, Instituto de Diagnóstico y Referencia Epidemiológicos, Secretarı́a de Salud, Álvaro
Obregón, Ciudad de México, México.
2
Unidad de Investigación en Inmunologı́a, Hospital de Pediatrı́a, Centro Médico Nacional Siglo XXI, Cuauhtémoc, Ciudad de
México, México.
*OIE-Rabies expert for Mexico CENASA.

69
 70 ARÉCHIGA CEBALLOS ET AL.

On the contrary, in the Americas the recovered evidence ‘‘Escuela de Agricultura y Veterinaria’’), in <3 months,
indicates that canine RVV, as we now know it today, did not managed to obtain the first national anti-rabies vaccine. Thus,
exist. The dogs of the pre-Columbian villages were apparently on April 23, 1888, the child Isidro Delgadillo received the
not identified as important carriers or transmitters of rabies. first rabies vaccination in the country (Liceaga 1888).
One possible explanation for this phenomenon is the fact that Shortly after, during the first half of the 20th century, the
dog populations at that time were low, which is demonstrated vaccination of dogs was shown to be an effective measure to
by the restricted diversity of haplotypes, which is found in reduce cases of human rabies. In this way, already in the
ancient New World’s dog breeds. In the Americas, the first dog 60s canine rabies in Western Europe had been controlled
rabies cases were described after the arrival of the Europeans, through the vaccination of dogs, which drastically changed
and it is likely that the canine RVV was introduced by the dogs the epidemiology of the disease. With the majority of dogs
that arrived from Europe. Later, during the colonization, canine vaccinated, the risk of this domestic species as a transmitter
RVV spread throughout the continent. of rabies to humans was reduced; leaving only some wild-
The oldest record of canine rabies in the American Con- living animals such as the red fox (Vulpes vulpes) as the few
tinent is registered in Mexico in the Annals of the Holy In- transmitting reservoirs of the disease (Aguilar Setién and
quisition (1709); progressively, other records were found in Garza Ramos 1988).
Barbados in 1719 and in the United States in 1753 (Lucas Contrary to what happened in Western European countries,
et al. 2008, Vos et al. 2011, Steele and Fernandez 2017). at that time in Mexico, dog rabies represented a serious public
In Mexico, before the arrival of the European conquer- health problem with record numbers of human deaths. The fight
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ors, rabies virus circulated mainly in wild reservoirs in- against this disease had been inefficient owing to the lack of
cluding members of the order Chiroptera. There are vaccines, means of diagnosis, and financial and human re-
inklings of rabies being transmitted by vampire bats in pre- sources. In Mexico, canine vaccination as a control measure for
Columbian documents: graphic representations of the God rabies began to be determinant in the second half of the 20th
Zotz in the Mayan codexes, and in the chronicles of Eu- century. Sustained dog vaccination and biannual campaigns
ropean pioneers, that is, Descubrimiento y Conquista de starting in the 1990s to the present culminated on November 11,
Yucatán by Solı́s (1896). Nevertheless, the type of rabies 2019 with the recognition of Mexico by the WHO/PAHO as a
transmitted by Chiroptera, did not become manifest until country free of human rabies transmitted by dogs.
the introduction of cattle by Europeans, which led to an However, it should be noted that the risk is latent, although
increase of the hematophagous bat population (Desmodus the canine RVV that emerged and developed after the conquest
rotundus). As a consequence, the number of rabies cases has been controlled, the Pre-Columbian RVVs continues in
increased as well. wild mammals. This source of rabies hangs like the sword of
In the beginning, it was not recognized and related with as Damocles over canine populations, which forces us to maintain
the well-known rabies in Europe, transmitted mainly by ca- sufficient herd immunity in this species over time.
nids. The disease transmitted by vampire bats in Latin In a mega-biodiverse country like Mexico, rabies in
America was known by different names, for instance, in wildlife is difficult to control not only because of the diversity
Mexico derriengue, güila, and tronchado; in Brazil peste das of species that can act as reservoirs/vectors, but also because
cadeiras, and so on, and different causes were attributed to it. of the different behavior of each species in their habitats.
It was in the 20th century that the Brazilian researcher This review describes Mexico’s efforts to eradicate canine
Queiros Lima (Lima 1934) linked this condition with the RVV and some of the peculiarities of rabies that remains well
rabies known ancestrally in the Old World. In fact, recent established in wild-living mammals and that can be the
phylogenetic studies demonstrate that Lyssaviruses have source of virus reintroduction into dogs if vaccination pro-
circulated in the Chiroptera order before terrestrial carnivores grams of these domestic animals are relaxed.
and it is highly probable that in remote times, they were
transmitted from bats to carnivores such as dogs, foxes,
Canine Vaccination in Mexico
wolves, and so on (Badrane and Tordo 2001, Vos et al. 2011).
During the Colonial Period and in the early years of In 1954, the Chilean veterinarian Eduardo Fuenzalida and
Mexico‘s independence, until the 19th century, dog rabies the physician Raul Palacios made possible the production
was already a frequently observed and well-known disease. of low-cost vaccines in Latin America that were used for
The only effective control measure that was applied in that postexposure treatment in humans and vaccination of dogs.
time was the slaughter of sick dogs. Eventually, some tradi- This inactivated vaccine was produced in lactating mice
tional herbal medicine was also applied to people who had (Fuenzalida and Palacios 1955).
been bitten, the disease was supposedly controlled through The Olympic Games of 1968, which were held in Mexico,
the utilization of a plant called ‘‘Trompetilla’’ (Bouvardia prompted a large-scale dog vaccination campaign in Latin
ternifolia) (Flores 1888). America for the first time. This was carried out owing to the
Regarding measures to treat rabies in humans, Mexico has large number of human rabies cases that were reported at the
the distinction of having been one of the first countries in the time, under the fear that those attending the sporting event
world implementing the postexposure rabies vaccination could be affected by the virus. For this campaign, mainly the
devised by Louis Pasteur at the end of the 19th century. The Fuenzalida vaccine was used (Steele 1988, Lucas et al. 2008).
Mexican physician Eduardo Liceaga, during a trip to Europe In 1970, Mexico vaccinated >200,000 dogs and in the 1980s
in 1887, visited Louis Pasteur and obtained the brain of a more than a million doses per year were applied (Fig. 1). De-
rabbit inoculated with virus to produce a vaccine against spite these efforts, the cases of rabies in dogs and humans did
rabies. In 1888, Dr. Liceaga arrived with the virus in Mexico not decline. Between 1970 and 1989 Mexico reported a total of
where the veterinarian José de la Luz Gómez (Principal of the 1430 cases in humans and almost 76,000 cases in dogs.
 ELIMINATON OF DOG RABIES IN MEXICO 71
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FIG. 1. Rabies cases in humans transmit-

ted by dogs and wild animals after mas-
sive dog vaccination campaigns in Mexico
1990–2015. (A) Rabies cases in humans
and number of vaccinated dogs. (B) Cases
of canine rabies and number of vaccinated
dogs. (C) Human cases caused per dog and
other wild species from (the main wild
species involved were bats and skunks).

In 1966, the Mexican-American film ‘‘El Mal’’ gave testi- The rabies epidemic was serious, in 1974 the Federal
mony of the suffering that this disease can infringe upon the Government included within the National Health Plan to
infected people. This film and others from the same period (i.e., achieve control of human rabies. This objective was not
Seis dı́as para morir) are proof of the effort that was made to reached at that time because other public health programs
motivate people to acquire the habit of vaccinating pets. such as those directed at influenza, pneumonia, enteritis, and
 72 ARÉCHIGA CEBALLOS ET AL.

different diarrheal diseases that were the main causes of death already much weakened when other animals approach at-
in the population were given priority (Gutierrez Cedillo tracted as possible food or out of curiosity, exchanging bites
2017). Since 1976, throughout Latin America the concern and aggressions. Such type of transmission is called passive.
had arisen to control this zoonosis, but it was not until 1983 Needless to say, active transmission is the most effective. In
that the members of PAHO requested support for the devel- the case of chiropterans, it is the vampire bat, the only ones
opment of a program that would allow the control of canine that have the ability to actively transmit rabies. The other
rabies in this region. species (frugivores, polynivores, and insectivorous) can
Mexico assumed the commitment in an exemplary man- transmit rabies less frequently, although sometimes some
ner, between 1983 and 1988, 426 cases of human rabies were sick animals with erratic behavior approach humans, or are
registered with an average of 71 cases per year (rate 0.095 per found active during the daylight.
100,000 habitants). We have witnessed a group of children in a nursery in
The majority of these cases were men between 14 and 40 Mexico City who played with an insectivorous bat (Tadarida
years who lived in populations that had fewer than 10,000 brasiliensis) unable to fly owing to being ill with rabies virus
habitants. In 87.5% of these cases, the aggressor species was (Loza-Rubio et al. 2000). Fortunately, the children were
the dog. treated promptly through postexposure vaccination, with no
The political will to control cases of human and canine accidents to regret.
rabies was reflected in the National Health Program from The Mexican territory is home of carnivores that have been
1990 to 1994. It was during this period that Mexico per- identified as active transmitters of rabies in the North of the
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formed the transition from Fuenzalida-type vaccines pro- American Continent (the United States and Canada) such as:
duced in lactating mice to inactivated rabies vaccines raccoons (Procyon lotor), striped skunk (Mephitis mephitis),
produced in cell cultures, which as a rule must have a mini- spotted skunk (Spilogale putorius), hooded skunk (Mephitis
mum of 2 international units (IU/mL) of potency. macroura), American hog-nosed skunk (Conepatus leuco-
Starting in 1990, canine vaccination became a massive, notus), gray fox (Urocyon cinereoargenteus), coyote (Canis
intensive, and free of charge activity, with the establishment latrans), and bobcats (Linx rufus).
of the campaign named: ‘‘National Canine Rabies Vaccina- In addition to these characteristic animals of North
tion Week.’’ Thanks to these actions, a large number of dogs America in Mexico, there are other species, typical of the
were vaccinated in a short time and the confirmed cases in Neotropical areas such as the white-nosed coati (Nasua
these animals presented a downward trend from >2500 cases narica), which are potential transmitters of the disease
before 1990 (Fig. 1), to 244 in 2000, which represented a (Aréchiga-Ceballos et al. 2010, Fehlner-Gardiner 2018).
90.24% reduction. Furthermore, rabies control in humans and If this was not enough, the tropical and subtropical areas
animals was strengthened as well as prevented through the of the national territory have large populations of the
implementation of a national and massive plan that included common vampire bat that, owing to its hematophagous
radio, television, posters, and so on, to reach the largest habits, has become one of the most effective and active
number of habitants. transmitters of the rabies virus, both to domestic animals
Between 1995 and 2000, human rabies transmitted by dogs and to humans.
remained present in the country; however, the last three cases As canine RVV is controlled in Mexico, human rabies
of human rabies transmitted by dogs were one diagnosed in transmitted by wild-living species becomes important. From
2003, in the State of Chiapas, and two others cases in the State 2000 to 2019, 46 cases of human rabies transmitted by wild
of México in 2005. Since 2006, no human rabies cases have animals have been confirmed; of these, 90% of the attacks
been registered by canine transmission (Fig. 1). were made by bats or skunks (Fig. 2).
Between 2007 and 2020 the samples of wildlife animals
analyzed for rabies diagnosis at the Laboratory Network and
Transformation of Epidemiological
the National Reference laboratory of the Mexican Ministry of
Presentation of Rabies in Mexico
Health (Instituto de Diagnóstico y Referencia Epidemioló-
The geographical location of Mexico makes it a confluence gicos, InDRE) related to human exposures were 407. Bats
zone between the Nearctic and the Neotropic, in such a way represented 63% (257/407) and skunks 28% (114/407). The
that there are a great variety of wild animal species that can remaining 9% was represented by foxes, coatis, wildcats,
act as reservoirs/vectors of rabies virus. Having controlled pumas, coyotes, deer, and opossums (Fig. 2).
canine RVV in the main does not include other RVVs from At the beginning of the 21st century, cases of rabies in
wild-living mammals in which, as we have mentioned, the dogs were lower; with a decrease of 81.6% (244 cases
virus has circulated since ancient times. These species are between 2000 and 2003 in 11 states, to only 45 in 2004
capable of infecting humans although to a lesser degree than in 10 states). This decrease was interrupted in 2005,
dogs do. The wild species in which the rabies virus circulates when an outbreak occurred in the State of Mexico that
are capable of transmitting the disease to humans and do- registered 125 cases, which represented 79.2% of the
mestic animals in two different ways. Animals that have a total for that year. This outbreak occurred owing to the
hunting instinct (carnivores), such as canids, procyonids, and conjunction of several factors in an area where urban and
mephitidae (skunks), when they are sick with rabies, are rural populations overlap and where there is human
prone to move, attack, and bite other animals of their species overpopulation and consequently with a canine over-
or from different species, including humans. This type of population with a human–dog ratio of 1:3. In addition, it
transmission is called active. This behavior is different in was detected that there was limited coverage of rabies
those animals that are not hunters. These generally do not vaccination and the presence of a high density of free
move to attack; it is in the last stages of the disease, being roaming dogs or ownerless stray dogs.
 ELIMINATON OF DOG RABIES IN MEXICO 73

FIG. 2. Rabies diagnosis

in wildlife between 2007 and
2020 at the National Re-
ference laboratory of the
Mexican Ministry of Health
(InDRE) that were related to
human cases (total N = 407).
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Also, the lack of public services and health centers, as well Importance of Vaccination, Surveillance,
as the incorrect disposal of garbage were factors that favored and Research
the presence of dogs in these conditions and movements of
the canine populations. In Mexico, the Epidemiological Surveillance System for
The implemented measures with the rabies focus control Rabies began in 1970, allowing the definition of the epide-
(Secretarı́a de Salud 2018), allowed to continue its reduction miological characterization for future decision making. The
in subsequent years, registering in 2009 only 12 cases, in the rabies virus diagnostic laboratory began its work in 1979 at
next entities: 1 in Chiapas, Chihuahua, Guerrero, and Hi- the Institute for Health and Tropical Diseases (which years
dalgo, 6 in the State of Mexico, and 2 in Yucatan. Afterward, later would be called the Institute for Diagnosis and Epide-
the number of doses increased until reaching 18.2 million in miological Reference). Diagnostic confirmation of rabies
2012, having accumulated a total of 195.8 million doses cases described up to 1989 was carried out mainly by means
applied to dogs and cats (Figs. 1 and 2). of the fluorescent antibody test. In 1989, the InDRE rabies
These programs have represented the application of vaccines laboratory began its function as a reference laboratory.
in a wide variety of climates, altitudes, and urban conditions. The antigenic characterization of the RVV began in 1993
Mexico has managed to eliminate the rabies virus trans- when the technique for typing the different variants by
mission from dogs to humans since 2006, in addition by monoclonal antibodies was standardized, which is applied to
gradually reducing and eventually eliminating canine RVV samples to determine the most likely reservoir species in each
(Fig. 1). The last cases of rabies in dogs in the country oc- outbreak. At present, techniques such as cell isolation culture
curred in 2017 and 2020. In 2017, three cases were reported and molecular tests such as RT-PCR have been incorporated
in the states of Chiapas, Yucatan, and Sinaloa in dogs who into the diagnostic algorithm, together with nucleotide se-
had no history of rabies vaccination, the analysis of labora- quencing have made possible the establishment of a trustable
tory confirmed that in all the cases, the virus that was causing way to determine relationships between viruses and reservoir
the disease corresponded to variants whose reservoir was species, as well as the epidemiological cycles.
wild species, two of them were from hematophagous bat Earlier in Western European countries, once rabies was
origin and the other was from a skunk. In 2020, in Yucatan, an controlled in dogs by vaccination, it was practically confined
unvaccinated puppy was attacked by a skunk having an RVV to a single wild species: the red fox (V. vulpes) (Aguilar Setién
related to the sylvatic cycle of rabies in this state. These et al. 1998). This has allowed almost total control of rabies
accidents demonstrate the necessity to always maintain herd (urban and wild) in those latitudes, focusing on the application
immunity in domestic dogs and cats. of oral vaccination strategies for the red fox and maintaining
Nowadays, based on the laboratory diagnoses performed vaccination of domestic animals (Müller and Freuling 2018).
in the InDRE of human rabies cases, we can represent a scheme Trying to control wildlife rabies in a country like Mexico is
of the new epidemiological face of the transmission of the more difficult, as mentioned previously, owing to the variety of
rabies to humans in Mexico. In this scheme, it can be seen that species capable of becoming rabies reservoirs.
currently in Mexico vampire bats and the skunks are the most It is difficult to apply a single control strategy for species as
active animals in the transmission of rabies to humans, this dissimilar as hematophagous bats and skunks. The behavior
without ignoring the sporadic aggressions of other sick wild and the baits or attractants vary from one species to another.
carnivores or the accidental spillovers that are caused by han- Despite these difficulties, some proposals for the immuni-
dling infected nonhematophagous chiropteran and cattle. zation of chiropterans (Aguilar-Setién et al. 2002) and skunks
 74 ARÉCHIGA CEBALLOS ET AL.

(Wohlers et al. 2018) have been studied. On the contrary, it white-nosed coatis from the Yucatan Peninsula. Epidemiol
must be added that it is currently known that the rabies virus Infect 2010; 138:1586–1589.
can cause different pathogenesis depending on the species, Badrane H, Tordo N. Host switching in Lyssavirus history from
dose, and variant involved. the Chiroptera to the Carnivora orders. J Virol 2001; 75:
Thus, there are several studies that found a high ser- 8096–8104.
oprevalence of antibodies against rabies in chiropterans Benavides JA, Velasco-Villa A, Godino LC, Satheshkumar PS,
(Salas-Rojas et al. 2004, de Thoisy et al. 2016) and other wild et al. Abortive vampire bat rabies infections in Peruvian peri-
animals (Bigler et al. 1983, Aréchiga-Ceballos et al. 2010, domestic livestock. PLoS Negl Trop Dis 2020; 14:e0008194.
Araujo et al. 2014, Benavides et al. 2020). This presupposes Bigler WJ, Hoff GL, Smith JS, McLean RG, et al. Persistence
that in these animals, owing to various circumstances the of rabies antibody in free-ranging raccoons. J Infect Dis 1983;
148:610.
virus is not 100% lethal and that some individuals and species
de Thoisy B, Bourhy H, Delaval M, Pontier D, et al. Bioeco-
manage to overcome the infection more frequently than it
logical drivers of rabies virus circulation in a neotropical bat
was previously thought, and possibly also spread the virus community. PLoS Negl Trop Dis 2016; 10:e0004378.
over a period of time (Aguilar-Setien et al. 2005, Streicker Fehlner-Gardiner C. Rabies control in North America—past,
et al. 2012). present and future. Rev Sci Tech 2018; 37:421–437.
Given this scenario, it is necessary to maintain three cur- Flamand A. The Rabies virus: Biochemistry and genetics [in
rent activities to keep a country like Mexico free from human French]. In: Rosset R, ed. Pasteur and rabies. Paris: Inst
rabies transmitted by dogs. First of all, it is necessary to Pasteur, 1985:131–137.
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maintain and not lower the vaccination coverage of domestic Flores FA. History of medicine in Mexico from the Indians time
carnivores (canines and felines). Second, it is necessary to to the present [in Spanish]. Ciudad de México: Oficina Ti-
keep the epidemiological surveillance system in force. Fi- pográfica de la Secretarı́a de Fomento, 1988.
nally, it is necessary to promote research on the character- Fuenzalida E, Palacios R. An improved method to prepare the
istics of infection in wildlife, which would open the field to anti-rabies vaccine [in Spanish]. Bol Inst Bact Chile 1955; 8:
new possibilities for the control and elimination of rabies 3–10.
(Fehlner-Gardiner 2018). Gutierrez Cedillo V. Statement and maintenance of free areas:
The current COVID-19 pandemic has caused countries Perspectives and limitations [in Spanish]. 2017. Available at
like Mexico to use most of their health resources to control it. http://panaftosa.org/redipra16/dmdocuments/SEMINARIO_
This can make that neglected diseases, such as rabies, even Redipra16_Veronica_Mexico.pdf.
more neglected, reversing gains. Liceaga E. Rabies preventive inoculations [in Spanish]. Gaceta
Médica de México 1888; 23:229–249.
Acknowledgments Lima EdQ. Bovine rabies transmission by the hematophagous bat
Desmodus rotundus [in Portuguese]. Brasil Med 1934; 48:38.
Authors thank Francisco Aréchiga Ceballos and Sebastian Loza-Rubio E, de Mattos CC, Aguilar-Setién A, de Mattos CA.
Aguilar-Pierlé for his kind review and correction of this Isolation and molecular characterization of a rabies virus
article. obtained from a non hematophagous bat in Mexico City [in
Spanish]. Veterinaria México 2000; 31:147–152.
Author Disclosure Statement Lucas CH, Pino FV, Baer G, Morales PK, et al. Rabies control
in Mexico. Dev Biol (Basel) 2008; 131:167–175.
No conflicting financial interests exist. Müller FT, Freuling CM. Rabies control in Europe: An over-
view of past, current and future strategies. Rev Sci Tech
Funding Information 2018; 37:409–419.
No funding was received for this article. Pradilla Ardila G. Rabies: 4,000 years of validity [in Spanish].
Revista de la Universidad Industrial de Santander. Salud
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