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Revista

de la

Universidad

del Zulia

Fundada en 1947

por el Dr. Jesús Enrique Lossada

Ciencias

Exactas

Naturales

y de la Salud

Año 12 N° 33

Mayo - Agosto 2021

Tercera Época

Maracaibo-Venezuela

REVISTA DE LA UNIVERSIDAD DEL ZULIA. 3ª época. Año 12 N° 33, 2021

Felix P. Ferro M. et al.// Evaluation of the behavior of rabies main indicators …227-246

DOI: http://dx.doi.org/10.46925//rdluz.33.16

Evaluation of the behavior of rabies main indicators in the province

of Chucuito, Puno, Peru

Felix Pompeyo Ferro Mayhua *

Polan Franbalt Ferro-Gonzales**

Luis Jhordan Rossel Bernedo ***

Lucio Ticona Carrizales ****

Victor Meliton Zanabria Huisa*****

ABSTRACT

Rabies, by definition, is an acute and fatal encephalomyelitis that affects man and a large number

of domestic and wild animals. The present research aims to evaluate the main rabies indicators

in Chucuito, a province of the Puno-Peru Region; the analysis of the data registered in the forms

of the zoonosis sanitary strategy has been carried out in the Environmental Health Unit of the

Health network, Chucuito. It is concluded that, during the evaluated years, there was only one

outbreak of human rabies in 2010, coinciding with a low coverage of canine rabies vaccination

(

53%), and with a case of canine rabies in the same year. On the other hand, three cases of canine

rabies were reported in unvaccinated dogs, the bitten people were treated for the most part,

along with adequate control of the dogs.

KEYWORDS: Bitten people; canine bite; indicators of rabies; rabies; vaccination.

*

Ministerio de Salud, Region de Salud Puno. Red de Salud Chucuito. Unidad de Salud Ambiental.

E-mail: poferro@yahoo.com ORCID: http://orcid.org/0000-0003-2986-2774

*

* Profesor auxiliar del Departamento Académico de la Facultad de Ingenieria Económica,

Universidad Nacional del Altiplano. E-mail: polanf@unap.edu.pe ORCID: http://orcid.org/0000-

003-4766-4982

0

*

** Laboratorios ORCID:

http://orcid.org/0000-0002-5800-7104

*** Profesor principal de la Facultad de Gestión Publica y Desarrollo Social, Universidad Nacional

de Juliaca. E-mail: l.ticonac@unaj.edu.pe ORCID: http://orcid.org/0000-0003-2073-8857

**** Profesor principal del Departamento Académico de la Facultad de Medicina Veterinaria y

Bioproyect

S.A.C.

E-mail:

jhordanrossel@gmail.com

*

Zootecnia, Universidad Nacional del Altiplano. E-mail: vzanabria@unap.edu.pe ORCID:

http://orcid.org/0000-0002-2678-5366

Recibido: 25/02/2021

Aceptado: 20/04/2021

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DOI: http://dx.doi.org/10.46925//rdluz.33.16

Evaluación del comportamiento de los principales indicadores de la

rabia en la provincia de Chucuito, Puno, Perú

RESUMEN

La rabia, por definición, es una encefalomielitis aguda y mortal que afecta al hombre y a un gran

número de animales domésticos y salvajes. La presente investigación tiene como objetivo evaluar

los principales indicadores de rabia en Chucuito, una provincia de la Región de Puno-Perú; se ha

realizado el análisis de los datos registrados en los formularios de la estrategia sanitaria de

zoonosis en la Unidad de Salud Ambiental de la red de Salud, Chucuito. Se concluye que, durante

los años evaluados, solo se produjo un brote de rabia humana en 2010, coincidiendo con una baja

cobertura de vacunación antirrábica canina (53%), y con un caso de rabia canina el mismo año.

Por otro lado, se reportaron tres casos de rabia canina en perros no vacunados, las personas

mordidas fueron atendidas en su mayor parte, junto con un adecuado control de los perros.

PALABRAS CLAVE: Personas mordidas; mordedura canina; indicadores de rabia; rabia;

vacunación.

Introduction

Rabies, is considered a zoonotic disease by definition (Wilkins & Del Piero, 2013), is an

acute and fatal encephalomyelitis that affects man and a large number of both domestic and wild

animals caused by rabies virus, which is usually transmitted by an animal bite (Hemachudha et

al., 2002; Jackson, 2014), being transmitted by a transdermal bite or scratch, or salivary

contamination of mucosa or skin wounds andit kills 30 000 to people a year, mainly in

developing countries and especially where unvaccinated stray dogs are common (Morgan &

Palmer, 2007; Pounder, 2005).

The Greeks called this disease "lyssa" (madness) and the Romans "rabere" (rage), from

which the current terminology derives. The Lyssavirus genus is one of six genera in the family

Rhabdoviridae [Greek: Rhabdos (rod)], a family of elongated bullet-shaped viruses within the

order Mononegavirales. Different members of the Rhabdoviridae family, apart from sharing

similar morphology, structure, and replication mechanisms, infect a wide range of hosts varying

from mammals, birds, fish, plants, arthropods, and other invertebrates (Tordo et al., 2005).

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DOI: http://dx.doi.org/10.46925//rdluz.33.16

Lyssaviruses are the etiological agents of rabies, one of the oldest viral diseases known to man

and a disease that has persisted over many centuries (Nel & Markotter, 2007).

Within the group of the main zoonoses in our country; It is rabies, who constitutes one

of the most serious problems in Public Health, whether due to its magnitude and importance,

seriousness and social impact since it leads to death for people exposed to the rabies virus,

mainly due to the lack of post-exposure prophylaxis translating directly into human deaths

(

Devaux et al., 2019; WHO et al., 2004). Epidemiological surveillance of rabies is totally

insufficient (mainly due to economic limitations in the Chucuito-Puno Region) in many

developing countries (as is the case in our country and mainly in our region) and the reporting

of cases is incomplete and underreported (Taylor et al., 2017; World Health Organization, 2013).

The importance of rabies for Public Health does not lie in the relatively small number of

cases, as can be seen in the data presented in rabies control programs by the ministries of health

of countries, but in the high case fatality rate that reaches almost 100% of sick with human

rabies, since there is no cure at present. On the other hand, no less important is the psychological

and emotional impact, suffering and anxiety of people bitten in fear of contracting the disease.

The economic damage due to the man/hours lost in the anti-rabies preventive treatment must

also be considered, therefore It has an effect on the local and national economies directly or

indirectly (Regea, 2017).

Rabies transmitted by dogs is still a public health problem in the least developed

countries in the world (Hampson et al., 2015), is a fatal viral infection that can infect all

mammals, but domestic dogs cause over 99% of all human deaths from rabies (World Health

Organization, 2013), however, most industrialized countries have eliminated rabies from

domestic dog populations, but, in most developing countries, rabies remains endemic in

domestic dog populations and poorly controlled (Coleman et al., 2004), however, four countries

in Latin America and the Caribbean are the only ones in the region where canine rabies is still

active today (Sánchez et al., 2019; Vigilato et al., 2013); as it is, in this case, Puno, one of the

poorest and least developed regions of Peru, despite the greats efforts made by all the countries

of Latin America and the Caribbean (LAC), to decrease in canine and human rabies made in the

last three decades to interrupt of the circulation of the rabies virus among dogs and,

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DOI: http://dx.doi.org/10.46925//rdluz.33.16

consequently, dog-mediated transmission to humans (Schneider et al., 2011; Vigilato et al., 2013).

Animal bites to people include dogs, constitute a serious global public health problem, affecting

children and adults of all ages and socio-economic levels in a transversal way. These bites for

human health depend on factors related to the characteristics of the biting animal and the bitten

person being able causes a large number of wounds that require medical attention and/or

surgical plus preventive rabies therapy such as vaccination (Morgan & Palmer, 2007; Palacio et

al., 2005). On the other hand, how rabies is almost always fatal, even, apparently minor bites in

high-risk countries should be taken seriously (Morgan & Palmer, 2007; Pounder, 2005), and all

the more so in endemic countries and regions such as Puno and its provinces. Therefore, it must

attend to all the people who suffer bite accidents, since they present a high risk of contracting

rabies.

Faced with the constant and recurrent cases of rabies in the country, the Ministry of

Health has a national strategy to control zoonoses and within it rabies, for which there is the

technical health standard No. 131-MINSA for surveillance, prevention, and control of human

rabies in Peru (MINSA, 2017).

Peru is one of the few countries in Latin America, where canine rabies is actually active

and Puno is a Region with permanent reports of rabies cases, so it is extremely important to

carry out an evaluation of the behavior of rabies main indicators in the Chucuito province of the

Puno Region.

1

. Materials and methods

Information from the Environmental Health Unit of the Chucuito Health Network, Puno

Health Region of the Ministry of Health of Peru has been reviewed, specifically from the

zoonosis health strategy, from 2003 to 2019.

The Chucuito health network has as its center of operations the city of Juli, district

capital of the Chucuito province, its jurisdiction being the entire province that encompasses Juli,

Pomata, Zepita, Desaguadero, Kelluyo, Pizacoma and Huacullani districts. It is located in the

south of the Puno Region; it shares border with the Republic of Bolivia (figure 1).

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DOI: http://dx.doi.org/10.46925//rdluz.33.16

Figure 1. Geographical location of the Chucuito province in Puno, Peru.

For the determination of indicators and the way of calculation (see Table 1), they have

been carried out based on the technical health standard (NTS) for the surveillance, prevention,

and control of human rabies in Peru: NTS No 131-MINSA/2017/DGIESP. V. 01. Approved with

Ministerial Resolution (RM) 024-2017/MINSA (MINSA, 2017).

1

.1. Statistical analyses

The main indicators of the behavior of rabies were compared based on the parametric test

T-student or the non-parametric tests Kolmogorov-Smirnov, depending on if the results

followed or not a normal distribution. All the statistical analyses were performed with the SPSS

software package, version 25.0 (IBM SPSS software, Chicago, IL).

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Table 1. Indicators

Indicator Description

This is an

Formula

indicator

of

structure

of human

Bitten

people

treated

푁푢푚푏푒푟 표푓 푏ꢀ푡푡푒푛 푝푒표푝푙푒 푡푟푒푎푡푒푑

푇표푡푎푙 ℎ푢푚푎푛 푝표푝푢푙푎푡ꢀ표푛

∗ 100

rabies.

This

also

indicator

of

structure

of human

rabies.

is

an

Reported

outbreaks

of human

rabies

푁푢푚푏푒푟 표푓 푟푒푝표푟푡푒푑 표푢푡푏푟푒푎푘푠

푇표푡푎푙 푒푥푝푒푐푡푒푑 표푢푡푏푟푒푎푘푠

∗

100

This is an

indicator

of process

of human

rabies.

People

bitten

controlled

푁푢푚푏푒푟 표푓 푝푒표푝푙푒 푏ꢀ푡푡푒푛 푐표푛푡푟표푙푙푒푑

푇표푡푎푙 표푓 푝푒표푝푙푒 푏ꢀ푡푡푒푛 푡푟푒푎푡푒푑

∗ 100

This, like

the

indicator

People who

start rabies

vaccination

푁푢푚푏푒푟 표푓 푝푒표푝푙푒 푤ℎ표 푠푡푎푟푡 푣푎푐푐ꢀ푛푎푡ꢀ표푛

∗ 100

푁푢푚푏푒푟 표푓 푝푒표푝푙푒 푏ꢀ푡푡푒푛 푡푟푒푎푡푒푑 푡ℎ푎푡 푟푒푞푢ꢀ푟푒 푣푎푐푐ꢀ푛푎푡ꢀ표푛

of

the

process of

human

rabies.

This

is

a

People who

did

complete

the

vaccination

scheme

also

not

process

indicator

푁푢푚푏푒푟 표푓 푝푒표푝푙푒 푤ℎ표 푑ꢀ푑 푛표푡 푐표푚푝푙푒푡푒 푡ℎ푒 푣푎푐푐ꢀ푛푎푡ꢀ표푛 푠푐ℎ푒푚푒

푁푢푚푏푒푟 표푓 푝푒표푝푙푒 푠푡푎푟푡ꢀ푛푔 푡ℎ푒 푠푐ℎ푒푚푒

∗

100

of human

rabies.

This is an

indicator

of

outcome

of human

rabies.

Urban

human

rabies

푁푢푚푏푒푟 표푓 푢푟푏푎푛 푟푎푏ꢀ푒푠 푐푎푠푒푠

∗ 100

푇표푡푎푙 ℎ푢푚푎푛 푝표푝푢푙푎푡ꢀ표푛

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This is an

indicator

of

structure

of rabies in

animals.

Samples

sent to the

laboratory

푁푢푚푏푒푟 표푓 푐푎푛ꢀ푛푒 푠푎푚푝푙푒푠 푠푒푛푡 푡표 푡ℎ푒 푙푎푏표푟푎푡표푟푦

퐸푠푡ꢀ푚푎푡푒푑 푐푎푛ꢀ푛푒 푝표푝푢푙푎푡ꢀ표푛

∗ 100

As in the

푁푢푚푏푒푟 표푓 푣푎푐푐ꢀ푛푎푡푒푑 푑표푔푠

∗

100

퐸푠푡ꢀ푚푎푡푒푑 푐푎푛ꢀ푛푒 푝표푝푢푙푎푡ꢀ표푛

Dogs

is

an

vaccinated

against

rabies

indicator

of

structure

of rabies in

animals.

*

The dog population was estimated using the ratio man 10: dog 01

This

also

is

an

indicator

푁푢푚푏푒푟 표푓 푏ꢀ푡ꢀ푛푔 푑표푔푠 푛표푡ꢀ푓ꢀ푒푑

Notified

biting dogs

of

the

∗

100

푁푢푚푏푒푟 표푓 푏ꢀ푡ꢀ푛푔 푑표푔푠 푒푥푝푒푐푡푒푑

structure

of rabies in

animals.

This is an

indicator

of rabies

process in

animals.

푁푢푚푏푒푟 표푓 푏ꢀ푡ꢀ푛푔 푑표푔푠 푐표푛푡푟표푙푙푒푑

푁푢푚푏푒푟 표푓 푎푡푡푒푛푑푒푑 푑표푔푠

∗

Controlled

biting dogs

*Dogs with 03 observation

This,

also

indicator

of rabies

process in

animals.

is

an

Rabies in

vaccinated

dogs

푁푢푚푏푒푟 표푓 푟푎푏ꢀ푒푠 푐푎푠푒푠 ꢀ푛 푣푎푐푐ꢀ푛푎푡푒푑 푑표푔푠

푇표푡푎푙 푣푎푐푐ꢀ푛푎푡푒푑 푑표푔푠

∗ 100

This is an

indicator

of animal

rabies

푁푢푚푏푒푟 표푓 푐푎푠푒푠 표푓 푐푎푛ꢀ푛푒푠 푟푎푏ꢀ푒푠

Canine

rabies

∗

100

퐸푠푡ꢀ푚푎푡푒푑 푐푎푛ꢀ푛푒 푝표푝푢푙푎푡ꢀ표푛

outcome.

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2

. Results

Table 2. Parameters evaluated

People

who did

not

Reported

outbreaks

of human

rabies*

People

who start

rabies

Dogs

Notified Controlled

vaccinated Canine

against rabies*

Bitten

Year people

treated**

People

bitten

controlled

Urban

Samples

complete human sent to the

biting

dogs**

biting

dogs

the

vaccination

scheme*

rabies* laboratory**

vaccination

rabies**

2

003

0.0908

0.0799

0.0785

0.0884

0.1228

0.0293

0.0532

0.1396

0.1097

0.1303

0.1288

0.1129

0.0972

0.1015

0.1094

0.1281

0.1298

0.0000 100.0000

4.4444

2.6786

0.9709

0.0000

1.3793

25.0000 0.0000

33.3333 0.0000

0.1311

0.1141

0.1296

0.0758

0.1101

0.1378

0.0933

0.1981

0.1717

0.1962

86.1753 60.0000

95.1658 80.0000

80.5930 73.5714

59.6008 75.0000

62.9975 103.5714

56.4491 34.0000

67.0866 63.3333

60.5772 53.2374

93.7148 41.5162

76.3927 56.8807

98.8889 0.0000

95.3704 0.0000

95.2830 0.0000

99.0476 0.0000

97.5758 0.0000

94.1176 0.0000

94.7368 0.0000

97.9021 0.0094

97.3913 0.0000

97.3118 0.0000

88.6486 0.0000

86.8263 0.0000

87.6712 0.0133

89.6104 0.0000

89.2216 0.0000

97.7528 0.0000

93.8547 0.0000

2004

0.0000

99.1071

99.0291

2

005

006

100.0000 0.0000

0.0000 0.0000

20.0000 0.0009

0.0000 0.0000

25.0000 0.0000

28.0000 0.0000

14.2857 0.0000

15.6250 0.0000

13.7931 0.0000

16.6667 0.0000

12.5000 0.0000

2

0.0000 100.0000

2

007

2

008

009

8.8235

1.7544

3.3784

2.6087

6.4516

13.3690

16.7665

21.9178

18.8312

21.5569

16.8539

35.7542

2

010

50.0000

99.3243

2

011

0.0000 100.0000

2

012

0.0000

98.3871

96.2567

97.6048

96.5753

97.4026

96.4072

97.1910

93.8547

2

013

0.1446 102.6450 66.7857

2

014

0.1893

0.2130

0.2044

0.2097

0.2950

0.1305

101.0819 55.6667

84.8223 45.6250

82.3553 45.2941

85.2883 46.3889

75.7608 49.4444

70.4995 49.7222

2

015

016

2

017

018

019

2

*

Significant diferences, non-parametric tests Kolmogorov-Smirnov.

* Significant diferences, parametric tests T-student.

2.1. Bitten people treated

Throughout the seventeen years evaluated, it is observed that this indicator has been

increasing each year, with very significant differences (p < 0.05), especially during the years 2010

to 2013 (table 2 and figure 2).

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0.16

0.14

0.12

0.10

0.08

0.06

0.04

0.02

0.00

Bitten people treated

Figure 2. Bitten people treated.

2.2. Reported outbreaks of human rabies

Only in 2010 a case of human rabies was presented, differing significantly (p<0.05) from

the rest of the years evaluated, in which no case of human rabies was reported (table 2 and figure

).

3

60

50

40

30

20

10

0

Reported outbreaks of human rabies

Figure 3. Reported outbreaks of human rabies

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2.3. People bitten controlled

Most of the people bitten were attended in the health establishment, since this indicator

mostly reached 100%, with very few people who stopped being treated, with no differences

between the years evaluated (table 2 and figure 4).

1

01.00

00.00

99.00

98.00

97.00

96.00

95.00

94.00

93.00

92.00

91.00

90.00

People bitten controlled

Figure 4. People bitten controlled

2.4. People who start rabies vaccination

The percentage of people who start vaccination is increasing over the years during the years

evaluated, without differences significant, being a minimum percentage with respect to the

number of people bitten attended (table 2 and figure 5).

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40.00

35.00

30.00

25.00

20.00

15.00

10.00

5

0

.00

People who start rabies vaccination

Figure 5. People who start rabies vaccination

.5. People who did not complete the vaccination scheme

2

As in the previous case, of all the people who start rabies vaccination, a majority percentage

do not complete the vaccination schedule, there are significant differences (p<0.05) between

each year, given that in some years no person bitten with started vaccination completes rabies

treatment (table 2 and figure 6).

1

20.00

00.00

80.00

60.00

40.00

20.00

0

.00

People who did not complete the vaccination scheme

Figure 6. People who did not complete the vaccination scheme

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2

.6. Urban human rabies

There was only one case of human rabies in 2010, very significantly different (<0.05) from

the rest of the years evaluated (table 2 and figure 7).

0

.001

0.0009

0.0008

0.0007

0.0006

0.0005

0.0004

0.0003

0.0002

0.0001

0

Urban human rabies

Figure 7. Urban human rabies

.7. Samples sent to the laboratory

2

The sending of samples to the laboratory for epidemiological surveillance for the diagnosis of

rabies increased mostly significantly irregularly (<0.05) each year, with the exception of 2019,

which decreased markedly (table 2 and figure 8).

0.35

0.30

0.25

0.20

0.15

0.10

0.05

0.00

Samples sent to the laboratory

Figure 8. Samples sent to the laboratory

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2.8. Dogs vaccinated against rabies

The percentage of dogs vaccinated against rabies is between 60-102%, with very significant

differences (p<0.05) between each year evaluated (table 2 and figure 9).

1

20.00

00.00

8

6

4

2

0.00

0

.00

Dogs vaccinated against rabies

Figure 9. Dogs vaccinated against rabies

.9. Notified biting dogs

2

The percentage of reported biting dogs are between 34 and 103%, with marked differences

p<0.05), of the total number of expected bites (table 2 and figure 10).

(

1

20.00

00.00

80.00

60.00

40.00

20.00

0

.00

Notified biting dogs

Figure 10. Notified biting dogs

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2.10. Controlled biting dogs

Almost 100% of biting dogs were controlled, maintaining it during the evaluated years

without statistical differences between each year (table 2 and figure 11).

1

00.00

9

8

8.00

6.00

4.00

2.00

0.00

8.00

6.00

4.00

2.00

0.00

Controlled biting dogs

Figure 11. Controlled biting dogs

.11. Rabies in vaccinated dogs

2

No case of rabies was reported in dogs vaccinated against rabies (table 2 and figure 12).

1

0

.9

.8

.7

.6

.5

.4

.3

.2

.1

0

Rabies in vaccinated dogs

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Figure 12. Rabies in vaccinated dogs

2.12. Canine rabies

During the years evaluated, only in the years 2010 and 2015 were laboratory confirmed cases

of canine rabies, one and two cases respectively very different (p<0.05) from the rest of the years

in which no cases of canine rabies were reported (table 2 and figure 13).

0

.01

.00

Canine rabies

Figure 13. Canine rabies

3. Discussion

The percentage of people bitten increased over the years similar to that reported by

Fontes-Pereira et al., (2012), the majority of which were controlled in almost 100% (table 1,

figures 1 and 3) as recommended, providing care to 100% of the exposed population at risk with

postexposure (Schneider et al., 2011), above that reported by Hampson et al., (2008), who point

out that at least 20% of all rabies exposures do not seek medical attention, which undoubtedly

contributes to reducing cases of human rabies and/or eradicating them. This is the main

objective of rabies control programs both in Peru and in the rest of the world.

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People who started rabies vaccination due to the severity of the injuries were increasing,

due to the availability of rabies vaccines for human use, however, very few people did not

complete the complete vaccination schedule, for reasons of treatment suspension due to

adequate control of biting animal (table 2 and figures 5 and 6), however, this finding is

compatible with what was stated by Hemachudha et al., (2002).

The only reported case of human rabies was in 2010, caused by a dog bite and reported

too late to the health establishment, it was considered the only epidemic outbreak, caused by an

unvaccinated dog since during the time evaluated the only three cases of canine rabies occurred

in unvaccinated dogs, Coinciding in that the cases of human and canine rabies have been reduced

by nearly 90% over the past 20 years since the inception of a Regional elimination program

(

Schneider et al., 2011).

The outbreak of human rabies coincides with the low coverage of canine rabies

vaccination obtained and with the report of a case of canine rabies the same year in the entire

province of Chucuito (Table 2, figures 3, 9 and 12), this being the cause probable of the presence

of human rabies since as do not have protection coverage (between 70 and 80%) the risk of cases

of human rabies is high (Bourhy et al., 2008; Kuzmin et al., 2012; MINSA, 2006, 2017; OIE, 2015;

Sánchez-Soriano et al., 2020; Schneider et al., 2011; World Health Organization, 2013; Zinsstag

et al., 2009), this association has already been reported by Cediel et al., (2010), besides we are

also an endemic region for rabies, this result coincides with that indicated by several authors

that the dog is the main transmitter of human rabies (Fontes-Pereira et al., 2012; World Health

Organization, 2013), for example, 90% of the cases of human rabies in the world are due to the

bite of sick dogs, although infection can also occur through contact of the saliva with the mucosa

and by injuries caused by scratches (Galán Torres, 2012).

Taking into account that the annual canine rabies vaccination campaigns confer

extraordinary value and dramatically reduce the health burden of rabies (Fitzpatrick et al., 2014;

Hampson et al., 2009), vaccination is carried out annually in the province of Chucuito, the

percentage of dogs vaccinated during the years evaluated varied greatly based on the estimated

dog population, coinciding with that reported by Freire de Carvalho et al., (2018), keeping in the

sustained safety range of 70-80% (Bourhy et al., 2008; Kuzmin et al., 2012; MINSA, 2006, 2017;

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OIE, 2015; Sánchez-Soriano et al., 2020; Schneider et al., 2011; World Health Organization, 2013;

Zinsstag et al., 2009), with the exception of the years 2007 to 2010, with the lowest coverage

(

table 2 and figure 9), but still well above the vaccination coverage reported by Kallo et al.,

2020); coinciding with the efforts of LAC countries to maintain sustained efforts in the area of

dog vaccination by providing an understanding of the baseline effort required to reduce the

incidence of dog-mediated rabies (Freire de Carvalho et al., 2018), considering, that infection can

be eliminated at source through sustained mass vaccination of reservoir populations (Hampson

et al., 2009), doing mass vaccination should aim for coverage as high as possible (Zinsstag et al.,

2009).

Galán Torres (2012) recommends that the vaccination schedule should be unique, such

recommendation in the country and the Puno region should be adopted in order to achieve more

adequate coverage. However, the registration and/or notification of biting dogs it was quite

irregular (figure 10), being controlled almost 100% (figure 11), contrary to what was reported in

Haiti, where 50% of the dogs involved in a bite event are unknown (Ma et al., 2020); in addition,

was reinforced with the sending of samples for the diagnosis of canine rabies as epidemiological

surveillance, reaching an adequate percentage (Cediel et al., 2010; MINSA, 2006, 2017; Schneider

et al., 1996) with the exception of the year 2019 where it declined a little (table 2 and figure 8),

considering that adequate and fair investment in dog vaccination (despite the fact that in this

case, the investment has been scarce) could bring down costs in medical treatment

demonstrating the need for intersectoral coordination (Fitzpatrick et al., 2014; Hampson et al.,

2015; Zinsstag et al., 2009).

Conclusions

During the years evaluated, only one outbreak of human rabies occurred in 2010,

coinciding with low coverage of canine rabies vaccination and a case of canine rabies the same

year. Three cases of canine rabies were reported in unvaccinated dogs. The most of the bitten

people were controlled. There was an adequate control of the biting dogs with a minimum of

three controls. Sending samples to the laboratory for rabies diagnosis as epidemiologic.

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References

Bourhy, H., Reynes, J.-M., Dunham, E. J., Dacheux, L., Larrous, F., Huong, V. T. Q., Xu, G., Yan, J.,

Miranda, M. E. G., & Holmes, E. C. (2008). The origin and phylogeography of dog rabies virus.

Journal of General Virology, 89(11), 2673–2681. https://doi.org/10.1099/vir.0.2008/003913-0

Cediel, N., de la Hoz, F., Villamil, L. C., Romero, J., & Díaz, A. (2010). Epidemiología de la rabia

canina en Colombia. Revista de Salud Publica, 12(3), 368–379. https://doi.org/10.1590/S0124-

0

0642010000300003

Coleman, P. G., Fèvre, E. M., & Cleaveland, S. (2004). Estimating the Public Health Impact of

Rabies. Emerging Infectious Diseases, 10(1), 140–142. https://doi.org/10.3201/eid1001.020774

Devaux, C. A., Mediannikov, O., Medkour, H., & Raoult, D. (2019). Infectious Disease Risk Across

the Growing Human-Non Human Primate Interfaceꢀ: A Review of the Evidence. Frontiers in Public

Health, 7(November), 1–22. https://doi.org/10.3389/fpubh.2019.00305

Fitzpatrick, M. C., Hampson, K., Cleaveland, S., Mzimbiri, I., Lankester, F., Lembo, T., Meyers, L. A.,

Paltiel, A. D., Galvani, A. P., & Haven, N. (2014). Cost-effectiveness of canine vaccination to prevent

human rabies in rural Tanzania Meagan. Ann Inter Med, 160(2), 91–100.

Fontes-Pereira, A., Morais, J., Abeledo, M., Roque, E., álvarez, J., José, A., Canele, B., & Monteiro

Noel, K. (2012). Rabia Urbana En Huambo, Angola, 2007-2009. Revista de Salud Animal, 34(1), 25–30.

Freire de Carvalho, M., Vigilato, M. A. N., Pompei, J. A., Rocha, F., Vokaty, A., Molina-Flores, B.,

Cosivi, O., & Del Rio Vilas, V. J. (2018). Rabies in the Americas: 1998-2014. PLoS Neglected Tropical

Diseases, 12(3), 1–16. https://doi.org/10.1371/journal.pntd.0006271

Galán Torres, J. (2012). La rabia: perspectiva actual. Sanidad Militar: Revista de Sanidad de Las Fuerzas

Armadas de España, 68(4), 201–202.

Hampson, K., Coudeville, L., Lembo, T., Sambo, M., Kieffer, A., Attlan, M., Barrat, J., Blanton, J. D.,

Briggs, D. J., Cleaveland, S., Costa, P., Freuling, C. M., Hiby, E., Knopf, L., Leanes, F., Meslin, F. X.,

Metlin, A., Miranda, M. E., Müller, T., … Dushoff, J. (2015). Estimating the Global Burden of Endemic

Canine

Rabies.

PLoS

Neglected

Tropical

Diseases,

9(4),

1–20.

https://doi.org/10.1371/journal.pntd.0003709

Hampson, K., Dobson, A., Kaare, M., Dushoff, J., Magoto, M., Sindoya, E., & Cleaveland, S. (2008).

Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies. PLoS

Neglected Tropical Diseases, 2(11), 1–9. https://doi.org/10.1371/journal.pntd.0000339

Hampson, K., Dushoff, J., Cleaveland, S., Haydon, D. T., Kaare, M., Packer, C., & Dobson, A. (2009).

Transmission dynamics and prospects for the elimination of canine Rabies. PLoS Biology, 7(3), 0462–

0

471. https://doi.org/10.1371/journal.pbio.1000053

Hemachudha, T., Laothamatas, J., & Rupprecht, C. E. (2002). Human rabies: a disease of complex

244

REVISTA DE LA UNIVERSIDAD DEL ZULIA. 3ª época. Año 12 N° 33, 2021

Felix P. Ferro M. et al.// Evaluation of the behavior of rabies main indicators …227-246

DOI: http://dx.doi.org/10.46925//rdluz.33.16

neuropathogenetic mechanisms and diagnostic challenges. The Lancet Neurology, 1(June), 101–109.

Jackson, A. C. (2014). Rabies. In Handbook of Clinical Neurology (Vol. 123, pp. 601–618).

https://doi.org/10.1016/B978-0-444-53488-0.00029-8

Kallo, V., Sanogo, M., Boka, M., Dagnogo, K., Tetchi, M., Traoré, S., Lechenne, M., Gerber, F.,

Hattendorf, J., Zinsstag, J., & Bonfoh, B. (2020). Estimation of dog population and dog bite risk

factors in departments of San Pedro and Bouake in Côte d’Ivoire. Acta Tropica, 105447.

https://doi.org/10.1016/j.actatropica.2020.105447

Kuzmin, I., Shi, M., Orciari, L. A., Yager, P. A., Velasco-Villa, A., Kuzmina, N. A., Streicker, D. G.,

Bergman, D. L., & Rupprecht, C. E. (2012). Molecular inferences suggest multiple host shifts of

rabies viruses from bats to mesocarnivores in Arizona during 2001-2009. PLoS Pathogens, 8(6), 1–11.

https://doi.org/10.1371/journal.ppat.1002786

Ma, X., Blanton, J. D., Millien, M. F., Medley, A. M., Etheart, M. D., Fénelon, N., & Wallace, R. M.

(

2020). Quantifying the risk of rabies in biting dogs in Haiti. Scientific Reports Nature Research, 10(1),

1

–10. https://doi.org/10.1038/s41598-020-57908-9

MINSA. (2006). Norma Tecnica de salud para la prevencion y control de rabia humana en el Peru (I. del M. de

Salud (ed.); 1ra edicio).

MINSA. (2017). Norma tecnica de salud para la vigilancia, prevencion y control de la rabia humana en el Peru (p.

9

2 pag).

Morgan, M., & Palmer, J. (2007). Dog bites. British Medical Journal, 334(7590), 413–417.

https://doi.org/10.1136/bmj.39105.659919.BE

Nel, L. H., & Markotter, W. (2007). Lyssaviruses. Critical Reviews in Microbiology, 33(4), 301–324.

https://doi.org/10.1080/10408410701647602

OIE. (2015). Global Elimination of Dog-Mediated Human Rabies. In Report of the Rabies Global

Conference.

10-11

december.

http://apps.who.int/iris/bitstream/10665/199176/1/%0A

WHO_HTM_NTD_NZD_2015.11_eng.pdf

Palacio, J., León, M., & García-Belenguer, S. (2005). Aspectos epidemiológicos de las mordeduras

caninas. Gaceta Sanitaria, 19(1), 50–58. https://doi.org/10.1157/13071818

Pounder, D. (2005). Avoiding rabies. Get vaccinated before travel, avoid animals, and get help

urgently if bitten. BMJ, 331, 469–470. https://doi.org/10.1201/b18317

Regea, G. (2017). Review on Economic Importance’s of Rabies in Developing Countries and Its

Controls. Archives of Preventive Medicine, 2(1), 015–021. https://www.peertechz.com/articles/review-

on-economic-importance-s-of-rabies-in-developing-countries-and-its-controls.pdf

Sánchez-Soriano, C., Gibson, A. D., Gamble, L., Bailey, J. L. B., Mayer, D., Lohr, F., Chikungwa, P.,

245

REVISTA DE LA UNIVERSIDAD DEL ZULIA. 3ª época. Año 12 N° 33, 2021

Felix P. Ferro M. et al.// Evaluation of the behavior of rabies main indicators …227-246

DOI: http://dx.doi.org/10.46925//rdluz.33.16

Chulu, J., Handel, I. G., Bronsvoort, B. M. d. C., Mellanby, R. J., & Mazeri, S. (2020). Implementation

of a mass canine rabies vaccination campaign in both rural and urban regions in southern Malawi.

PLoS Neglected Tropical Diseases, 14(1), 1–19. https://doi.org/10.1371/journal.pntd.0008004

Sánchez, P., Alejandro, O., Sanchez, D., Angélica, R., Ramirez, A. A., & Escobar, L. (2019). Rabia en

las Américas , varios desafíos y «ꢀUna Sola Saludꢀ»: artículo de revisión Rabies in the Americas ,

various challenges and «ꢀOne Healthꢀ»: Review article. Rev Inv Vet Peru, 30(4), 1361–1381.

Schneider, M. C., Aguilera, X. P., da Silva Junior, J. B., Ault, S. K., Najera, P., Martinez, J., Requejo,

R., Nicholls, R. S., Yadon, Z., Silva, J. C., Leanes, L. F., & Periago, M. R. (2011). Elimination of

neglected diseases in Latin America and the Caribbean: A mapping of selected diseases. PLoS

Neglected Tropical Diseases, 5(2). https://doi.org/10.1371/journal.pntd.0000964

Schneider, M. C., De Almeida, G. A., Souza, L. M., De Morares, N. B., & Diaz, R. C. (1996). Controle

da raiva no Brasil de 1980

a

1990. Revista de Saude Publica, 30(2), 196–203.

https://doi.org/10.1590/s0034-89101996000200012

Taylor, L. H., Hampson, K., Fahrion, A., Abela-ridder, B., & Nel, L. H. (2017). Difficulties in

estimating the human burden of canine rabies. Acta Tropica, 165, 133–140.

https://doi.org/10.1016/j.actatropica.2015.12.007

Vigilato, M., Clavijo, A., Knobl, T., Silva, H. M. T., Cosivi, O., Schneider, M. C., Leanes, L. F., Belotto,

A. J., & Espinal, M. A. (2013). Progress towards eliminating canine rabies: Policies and perspectives

from Latin America and the Caribbean. Philosophical Transactions of the Royal Society B: Biological Sciences,

3

68(1623). https://doi.org/10.1098/rstb.2012.0143

WHO, FAO, & OIE. (2004). Report of the WHO / FAO / OIE joint consultation on in collaboration with the

Health Council of the Netherlands (Issue May, p. 65).

Wilkins, P. A., & Del Piero, F. (2013). Rabies. In Equine Infectious Diseases: Second Edition (Second Edi,

pp. 203-209.e1). Elsevier Inc. https://doi.org/10.1016/B978-1-4557-0891-8.00019-1

World Health Organization. (2013). WHO Expert Consultation on Rabies. Second report. In World

Health Organization technical report series (Issue 982).

Zinsstag, J., Dürr, S., Penny, M. A., Mindekem, R., Roth, F., Menendez Gonzalez, S., Naissengar, S.,

&

Hattendorf, J. (2009). Transmission dynamics and economics of rabies control in dogs and

humans in an African city. Proceedings of the National Academy of Sciences of the United States of America,

06(35), 14996–15001. https://doi.org/10.1073/pnas.0904740106

1

246