ORIGINAL ARTICLE/ ARTÍCULO ORIGINAL
Biotempo (Lima)
17
ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697
Biotempo, 2017, 14(1), jan-jun: 17-25.
IMPACT OF TEMPERATURE IN THE PRESENCE OF RESPIRATORY
INFECTIONS OF BIRDS IN A TROPICAL COUNTRY
IMPACTO DE LA TEMPERATURA EN LA PRESENCIA DE INFECCIO-
NES RESPIRATORIAS DE AVES EN UN PAÍS TROPICAL
Ricardo Osés Rodríguez1; Rigoberto Fimia Duarte2; José Iannacone3,4;
George Argota Pérez5; Lisvette Cruz Camacho2 & Ismabel Domínguez Hurtado1.
1 Provincial Meteorological Center (CMP). Villa Clara, Cuba.
ricardo.oses@vcl.insmet.cu
2 Faculty of Health Care Technology “Julio Trigo López”. University of Medical Sciences Dr. Serafín Ruiz de Zárate Ruiz de Villa
Clara, Cuba. rigobertofd@fts.vcl.sld.cu
3 Faculty of Biological Sciences. University Ricardo Palma (URP). Lima, Peru.
4 Laboratory of Animal Ecology and Biodiversity. National University Federico Villarreal (UNFV).
joseiannacone@gmail.com
5 Center of Advanced Investigations and Formation in Education, Health and Environment “AMTAWI”. Peru.
george.argota@gmail.com
ORIGINAL ARTICLE/ ARTÍCULO ORIGINAL
ABSTRACT
Retrospective data were used to obtain statistical data on the epizootics of the susceptible and dead due to avian u in the
province of Villa Clara, Cuba in the period 2005-2007. These data were correlated with the average temperatures correspon-
ding to this period in this county. Total deaths were correlated with the total of susceptibles; the latter were correlated in turn
with the provincial temperatures. To analyze the data, the Autoregressive Integrated Moving Averages (ARIMA) model of the
Box-Jenkins Methodology was used. Techniques of multivariate regression for modeling the total number of poultry deaths
were also applied. The nal ARIMA model showed that an increase of 1 degree of temperature meant an increase of 53.37
deaths using a 95 % probability value. This work enables corroborating and quantifying the impact of mean temperature on
the susceptibility and death in poultry in the study area. With an increase of 1ºC of average monthly temperature can be ex-
pected an increase of 8894 susceptible cases, and as the susceptible ones increase by 1000, deaths are increased in 6 birds, so
that for the susceptible ones for 0.06 will be approximately the same to the total of deaths.
Keywords: Climatic impact –avian u infections – Cuba – temperature
RESUMEN
En el trabajo se utilizó la información retrospectiva para obtener los datos estadísticos de la epizootiología de los susceptibles y
de las muertes de las infecciones por gripe aviar, de la provincia Villa Clara, Cuba en el período 2005-2007. Estos datos fueron
correlacionados con el promedio de temperaturas correspondiente a este período en esta provincia. El total de muertes fue co-
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Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 Osés Rodríguez et al.
rrelacionado con el total de las susceptibles; estas últimas se correlacionaron a cambio con las temperaturas provinciales. Para
el procesamiento de la información, se utilizó el modelo de Promedios Autoregresivos Integrados (ARIMA) de la Metodología
Box-Jenkins. Se emplearon también las técnicas de regresión multivariada para modelar el total de muertes de las aves. El mo-
delo nal ARIMA expresó un incremento de 1°C de temperatura, lo cual signicó un incremento de 53,37 muertes. También
se utilizó un 95 % de valor de probabilidad. Este trabajo permite corroborar y cuanticar el impacto de la temperatura media
en las susceptibles y en las muertes de las aves en el área de estudio. Se obtuvo que con 1ºC de temperatura media mensual, se
pueda esperar un incremento de 8894 casos susceptibles y como estos incrementan en 1000 las muertes, se incrementan en 6
aves, por lo que las susceptibles para 0,06 serán las mismas aproximadamente al total de muertes.
Palabras clave: Impacto climático – infección de gripe aviar – Cuba – temperatura
INTRODUCTION
The cold avian infections stands for a very contagious
viral disease caused by the strains type A of the cold
virus that can affect to all birds species (Godoy, 2006;
Juckett, 2006; Causey & Edwards, 2008; Fuller et al.,
2010); although it has enough potential so as to infect
to different species of mammals, included the human
being, the pig and the cat. In addition to biological and
ecological factors, climate factors inuence the emer-
gence of infectious diseases (Patz et al., 1996; Sehgal
2010; Si et al., 2010; Herrick et al., 2013; Si et al., 2013).
The highly pathogenic cold avian or the originally na-
med “ow plague” is initially described in Italy in 1878.
It was also known as the Lombardy disease. Although
Centanni and Savonuzzi in 1901 identied a causing
agent of the disease, it was no longer in 1955 when it is
described as a virus of the Cold A family, as responsi-
ble (Juckett, 2006). The rst time the virus was isolated
in tern birds in South Africa, in 1961 (Juckett, 2006).
It was traditionally thought the human cold by avian
virus was an exceptional fact, but such opinion chan-
ged when the outbreaks occurred in the last years; the
rst one, called “chicken cold”, occurred in 1997 in
Hong Kong and it was produced by a virus A (H5N1).
Subsequently, there were more outbreaks, once more
in Hong Kong in 2002, also by A (H5N1) and in Ho-
lland in 2003, by A (H7N7), but among them it is no-
ticeable the present succession of outbreaks by virus
A (H5N1) that started in 2003 in the Asian southeast;
and now, has the greatest sanitarian interest related to
worldwide cold avian (Di Trani et al., 2006; Si et al.,
2010; Tsuchihashi et al., 2011; Herrick et al., 2013;
Zhang et al., 2014).
The breathing dysfunctions cause a decrease of the
production in birds, mainly in those that are conned
and subjected to high productive rhythms. Cold avian
infections are among the frequent illnesses (Jaakkola et
al., 2014).
One of the interactions among the components of the
productive system that most inuence is the relations-
hip between the environment and the animal. The en-
vironment in which the animal acts is compound pri-
marily of the environmental or climatic factors, which
should be structured to offer well-being. The climatic
changes and especially the waves of heat, so frequent
in the tropic, cause damages so abrupt and sudden,
capable to ruin the most enviable productive indexes
possible to obtain after an efcient productive task
(Zhang et al., 2014).
The modern poultry keeping, as any other industry,
has as north of its activity the protability, and in such
a concerned market the producers don’t have a diffe-
rent option for the maximum of efciency; therefo-
re, as the hens express to the maximum the potential
productive content in their genetics, it is indispensable
to manage an appropriate environment that provides
them the appropriate environmental conditions (Gil-
bert et al., 2008). The temperature, humidity, quality of
the air, they are some of the environmental factors to
keep in mind during the productive period of the do-
mestic birds (North & Bell, 1990; Causey & Edwards,
2008; Tsuchihashi et al., 2011; Herrick et al., 2013; Si et
al., 2013; Jaakkola et al., 2014).
The high temperatures make susceptible of breathing
illnesses to the birds, among those the cold avian infec-
tions (Gilbert et al., 2008). This is a breathing illness of
the domestic hens caused by the bacteria Haemophilus.
The illness is spread worldwide and causes important
economic losses (Blackall, 1999; Shaman et al., 2010).
The susceptible birds generally develop the symptoms
in the 3 days after the exhibition to the infection. Those
19
Cold avian infections
that are recovered pretend to be normal but they stay as
bearer for long periods. Once the lot is infected all the
birds they should be considered bearer (Agrobit, 2000).
Before the scenario of the climatic change, the increa-
se of the frequency of climatic events ends and certain
pollutants of the air, especially the ozone, will increase
the chronic breathing illnesses (Anonymous, 2009).
As it is known, the heat can affect the animals in two
ways: chronic or acute. In the chronic form, caused by at-
mosphere temperatures (TA) superior to 32°C, the con-
sumption of water is duplicated, it diminishes the food
consumption and the gain of weight is affected. While
with TA among 38 to 40ºC and relative humidity between
50 and 55%, the corporal temperature can reach from
45 to 48°C and cause the death for sharp stress, with the
consequent decrease of the productive efciency and of
the economic earnings (De Basilio et al., 2008).
In Villa Clara province, Cuba there have been modelling
works, among them the methodology ROR, widely used
(Osés & Grau, 2011), another important methodology
is the Box et al. (1994). Methodology ROR has been also
used for the prognosis of great intensity earthquakes in
Cuba (Osés et al., 2012a), besides it is implemented in
mosquitoes control (Fimia et al., 2012a), the results have
been used in the study of climatic change and health in
Villa Clara, Cuba (Osés et al., 2012b), these mathematic
models were applied in the Malaria (Fimia et al., 2012b).
Methodology ROR was also applied in meteorological
investigations, specically in the modeling of cold fronts
and the impact of sun spots (Osés et al., 2012c). Metho-
dology ROR has been used for long term prediction of
larvarial density of Anopheles mosquitoes (Osés et al.,
2012d); besides in Osés et al. (2014) it was carried out a
long term prognosis with one year in advance, for me-
teorological variables; however, the methodology Box et
al. (1994), will be used, since it is a very important tool
for climatic modeling, this also presents good results in
modeling and has the limits of condence of modeling
parameters well established.
For all before exposed, the objective of this research
was to investigate the impact of climate of the tempe-
rature in the presence of the avian cold infections of
a tropical country.
MATERIALS AND METHODS
Study Area
The study was carried out in Villa Clara province,
which is located in the center part of Cuba; such pro-
vince limits to the west, with Cienfuegos and Matanzas
provinces and to the east, with Sancti Spíritus; such
province is composed of 13 municipalities politically
and administratively, Santa Clara is the capital (Fig. 1).
infections are among the frequent illnesses (Jaakkola et
al., 2014).
One of the interactions among the components of the
productive system that most inuence is the relations-
hip between the environment and the animal. The en-
vironment in which the animal acts is compound pri-
marily of the environmental or climatic factors, which
should be structured to offer well-being. The climatic
changes and especially the waves of heat, so frequent
in the tropic, cause damages so abrupt and sudden,
capable to ruin the most enviable productive indexes
possible to obtain after an efcient productive task
(Zhang et al., 2014).
The modern poultry keeping, as any other industry,
has as north of its activity the protability, and in such
a concerned market the producers don’t have a diffe-
rent option for the maximum of efciency; therefo-
re, as the hens express to the maximum the potential
productive content in their genetics, it is indispensable
to manage an appropriate environment that provides
them the appropriate environmental conditions (Gil-
bert et al., 2008). The temperature, humidity, quality of
the air, they are some of the environmental factors to
keep in mind during the productive period of the do-
mestic birds (North & Bell, 1990; Causey & Edwards,
2008; Tsuchihashi et al., 2011; Herrick et al., 2013; Si et
al., 2013; Jaakkola et al., 2014).
The high temperatures make susceptible of breathing
illnesses to the birds, among those the cold avian infec-
tions (Gilbert et al., 2008). This is a breathing illness of
the domestic hens caused by the bacteria Haemophilus.
The illness is spread worldwide and causes important
economic losses (Blackall, 1999; Shaman et al., 2010).
The susceptible birds generally develop the symptoms
in the 3 days after the exhibition to the infection. Those
Figure 1. Political and administrative map of Cuba and Villa Clara province.
The present work was carried out in the Provincial Me-
teorological Center; as well as in the Provincial Poultry
Company of Villa Clara. The retrospective data were
used to ask for the statistical information of the epi-
zootiologics of the susceptible and dead due to cold
avian infections, to prepare the specialized units of
20
Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 Osés Rodríguez et al.
Villa Clara province, in the period 2005 - 2007. These
data were correlated with the temperatures stockings
average corresponding to this period in this provin-
ce, contributed by the database of Provincial Center
of Meteorology, particularly those of the Department
of Applied Meteorology. The total of deaths was co-
rrelated with the total of susceptible; these last ones
correlated in turn with the temperatures provincial
stockings.
About data processing
For the information processing, the model Autore-
gressive Integrated Moving Averages (ARIMA) was
used of Box-Jenkins Methodology through the sta-
tistical package SPSS Version 13. Techniques of mul-
tivariate regression for modeling the total of poultry
deaths were also applied.
RESULTS AND DISCUSSION
In Fig. 2, the behavior of the susceptibility of birds
is observed for the province, seemingly a marked sea-
sonality is not observed, seeming an aleatory event at
rst sight with big picks of more than 500 000 birds
and a half value 200 000. The biggest value takes place
in August 2007, where a near pick is reaching the 600
000 birds in the whole territory. These results coincide
with the obtained by Nicholson et al. (2003).
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Años/Mes
600000.00
500000.00
400000.00
300000.00
200000.00
100000.00
0.00
TOTALSUSCEPTIBLES
Comportamiento de la susceptibilidad de las aves
Figure 2. Behavior of susceptibility of birds to the cold avian infections in a tropical country, period 2005-2007.
16151413121110987654321
Lag Number
1.0
0.5
0.0
-0.5
-1.0
ACF
Lower Confidence
Limit
Upper Confidence Limit
Coefficient
TOTALSUSCEPTIBLES
A process order autoregressive was shown with a spi-
ke very different in the autocorrelation of rst order
the mobile stocking of order 1 was discarded to be a
model but expensive and less probable, in gs. 3 and
4 the total and partial autocorrelations are presented.
A marked seasonality is not evidenced since it can be
only found a spike or column which means a move-
ment order autoregressive.
Figure 3. Autocorrelogram Function (ACF) of the series with regression to 1 step of the susceptibility of birds to
the cold avian infections in a tropical country, period 2005-2007. Lag Number = delay.
21
Cold avian infections
When using the model integrated autoregressive of
stockings motives of Box & Jenkins known as mo-
deling ARIMA, the errors of the pattern gave in the
order of 138649 cases, in Table 1 can be appreciated
the pattern obtained after several steps, being eviden-
ced an order autoregressive signicant, and the retur-
ned provincial half temperature of one month was
included that presented correlation with the variable
Susceptibility; being obtained that the parameter is
highly signicant since the P value is similar to 0.014,
smaller than 0.05, therefore it is signicant to 95%,
coinciding with that outlined by Tsuchihashi et al.
16151413121110987654321
Lag Number
1.0
0.5
0.0
-0.5
-1.0
Partial ACF
Lower Confidence
Limit
Upper Confidence Limit
Coefficient
TOTALSUSCEPTIBLES
(2011) and Osés et al. (2012b), who gives a primordial
paper to the high temperatures in the susceptibility
before the caloric stress in the birds and the presen-
tation of breathing illnesses. Thus, it can be afrmed
that with 1ºC of monthly mean temperature can be
expected an increase of 8894 susceptible cases of the
variable temperature for the susceptibility of birds
to breathing infections. This result entirely coincides
with the obtained by Osés et al. (2012b), where a de-
gree of mean temperature means an increase of sus-
ceptible in 8894 cases.
Table 1. ARIMA Model obtained.
Estimates Standard Error t Sig
Non-Seasonal Lags AR1 .429 .165 2.603 .014
Regression Coefcients LAG1TM 8894.290 1674.033 5.313 .000
A Kalman ltering algorithm was used for estimation. AR1 Parameter Autoregressive of order 1. LAG1TM = Mean Temperature.
Figure 4. Partial Autocorrelogram Function (ACF) of the series with regression to 1 step of
the susceptibility of birds to the cold avian Infections in a tropical country, period 2005-2007.
Lag Number = delay.
The behavior of the real value was analyzed and pre-
dicted (Fig. 5), the pattern showed that the correlation
is of 0.52 and with a value of signicance of 99%.
This is interpreted as the real value and the predicted
either coincides in increase or decrease in 52.4% and
this is evidenced with 99% signicance.
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Revista Biotempo: ISSN Versión Impresa: 1992-2159; ISSN Versión electrónica: 2519-5697 Osés Rodríguez et al.
Correlations between the total of deaths and the to-
tal of susceptible, being observed a positive correla-
tion (r= 0.39, p= 0.02). Total deaths with temperature
mean have not correlation with mean temperature (r=
-0.02, p= 0.87), but total of susceptible with mean
temperature is positive correlated (r = 0.40; p= 0.02).
Thus, it is predicted the total of deaths with regard to
the susceptible ones that in turn depend of tempera-
ture (Tables 2 and 3) (Nicholson et al., 2003; Si et al.,
2013; Jaakkola et al., 2014).
According to the parameters of the pattern, it can be
expressed that as the susceptible ones increase in 1000,
the deaths ascend in 6 birds; thus, the total of suscepti-
ble for 0.06 will be the same approximately to the total
of deaths.
Accordingly to the previous analysis it can be conclu-
ded that the nal pattern has the following form: Total
of deaths t = 0.002574 * Susceptibility -1+53.37 TM-1
+0.006*et. (t = 4.46; p = 0.00). Where: et: it is the
error that is made when predicting the Susceptibility at
one time certain t. Susceptibility -1: it is the Suscepti-
bility in the previous month. TM-1: it is the provincial
medium temperature in the previous month.
Therefore, it can be appreciated that a degree of tem-
perature means an increase of 53.37 deaths, thus,
when temperatures of 30 ºC are presented, it can be
expected an increase of deaths of 1601 birds, this be-
longs together with that outlined in the Anonymous
(2009), where it is expressed the complications and
deaths by breathing dysfunctions in the increments
of temperature. The values averages of the monthly
temperatures were analyzed in the period 2005-2007,
then, it can be appreciated that in the three years the
temperatures stockings of the warm months oscillate
among the 26-27°C and more; as well as the high one
averages yearly of the humidity 81-82%. In this aspect
it coincides with that outlined by North & Bell (1990)
that starting from the 27°C, the birds begin to suffer
of caloric stress, as rising the susceptibility and dea-
ths increase in birds due to the presence of the illness
(Blackall, 1999; WHO, 2002; Shaman et al., 2010).
In our paper no signicant correlation was found with
the relative humidity with the susceptibility, this coinci-
de with Zhang et al. (2015) in which the relative humi-
dity do not inuence in the appearance of the virus on
inuenza A (H7N9), the humidity is usually regarded
as a factor impacting on the transmission of diseases,
that are transmitted by droplets or aerosols according
to Koep et al. (2013) and Jaakkola et al. (2014). Our
results can impact the poultry market reducing the
number of cases of H7N9, this coincide with Xu et al.
(2013) and with Yu et al. (2014). We coincide with Tsu-
chihashi et al. (2011), Herrick et al. (2013), and Zhang
et al. (2015), because temperature inuences the high
risk of infection.
It was obtained that with 1ºC of monthly mean tem-
perature can be expected an increase of 8894 suscepti-
ble cases. As the susceptible ones increase in 1000, the
deaths are increased in 6 birds; thus, the susceptible
ones for 0.06 will be the same approximately to the
total of deaths. The nal ARIMA modeling expressed
that an increase of 1 degree of temperature means an
increase of 53.37 deaths.
N
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Fecha
600,000Casos
500,000Casos
400,000Casos
300,000Casos
200,000Casos
100,000Casos
0Casos
Valor Real
Valor Predicho
Comportamiento de la susceptibilidad en la Provincia
Figure 5. Behavior of the Susceptibility with regard to the Predicted value (=Valor Predicho) and Real in Villa Clara, Cuba.
23
Cold avian infections
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Received April 12, 2016.
Accepted October 21, 2016.
