Fasciolosis by Fasciola hepatica in creole cattle
Fasciolosis effects on the metabolic profile in Creole cattle in México
Ricardo E. Caicedo Rivas
1
, Mariana Paz-Calderón Nieto
2
, José Alfonso Benavides
Bañales
3
and Alejandra Leal Pérez
4
Laboratorio de Endocrinología de la Reproducción y Malacología, Facultad de Ciencias
Biológicas; Benemérita Universidad Autónoma de Puebla. Puebla. México
Abstract. Diseases caused by parasites reduce productive and reproductive activities in
native animals and even more so in animals destined for human consumption, such as
cattle, one of these diseases is fasciolosis, caused by Fasciola hepatica, whose prevalence
is estimated between 23,5 to 33 % in very humid areas with temperatures that vary between
15.5 ± 1.1 to 34.1 ± 2.1 ., At altitudes that fluctuated between 300 and 2400 masl. The
objective of this study was to determine the pathophysiological changes (histological
analysis and obtain the number of flukes in liver parenchyma, metabolic and enzymatic
profile and differential leukocyte count) in creole cattle in different zoogeographic areas in
México; blood and liver tissue samples were taken from 7,892 Creole animals. Results: the
prevalence of fasciolosis was 48.9 %; in macro histopathology: hepatic obstructions were
detected, an increase in the diameter and thickening of the bile ducts (cholangiohepatitis), a
decrease in the thickness of the left and ventral hepatic lobes, and in chronic cases, liver
cirrhosis was observed; at the histological level: loss of cell morphology and the presence
of F. hepatica eggs were observed, deposited in the liver parenchyma and in the blood and
bile ducts. It was found that liver damage was directly proportional to the number of flukes
found and that these also caused alterations in blood biochemical components. The
biochemical parameters in blood were altered in a very significant way (P <0.05 and P
<0.01), these altered parameters were: Urea / BUN, cholesterol and total proteins; enzymes
such as: γ-GT, ALT / GPT, AST / GOT, LHD and alkaline phosphatase, detected in
females and males; It is concluded that liver damage is directly proportional to the number
of flukes present, and when compared with the metabolic profile, these are significantly
altered.
Key words: Fasciola hepatica, pathophysiology, liver damage, parenchyma, biochemical
parameters.
Resumen. Las enfermedades causadas por parasitos disminuyen las actividades productivas
y reproductivas en los animales nativos y más aún en los animales destinados al consumo
humano, como el ganado bovino, una de estas enfermedades es la fasciolosis, causada por
Fasciola hepatica, cuya prevalencia se estima entre 23.5 a 33 % en áreas muy húmedas con
temperaturas que varían entre 15.5 ± 1.1 a 34.1 ± 2.1 ., a altitudes que fluctuaron entre
300 y 2400 msnm. El objetivo de este estudio fue determinar los cambios fisiopatológicos
Recibido: 2020-08-01. Aceptado: 2020-12-07
1
Corresponding author: ricaido@yahoo.com ; https://orcid.org/0000-0003-4726-5359
2
Complejo Regional Mixteca, (Sede Izucar de Matamoros), Benemérita Universidad Autónoma de Puebla,
Boulevard Valsequillo and San Claudio Ave. Building Bio-1, Lab.347, C.P. 72570. Email:
morella.paz.mp@gmail.com ; https://orcid.org/0000-0002-3023-2465
3
ESVIC-Corporativo México, Puebla. México. Email: mvz_benavides@hotmail.com
4
E mail: aleeleap@gmail.com
Fasciolosis by Fasciola hepatica in creole cattle
(análisis histológico y obtener el número de duelas en parénquima hepático, perfil
metabólico y enzimático y conteo diferencial de leucocitos) en bovinos criollos en
diferentes áreas zoogeográficas en México; se tomaron muestras de sangre y tejido hepático
de 7 892 animales criollos. La prevalencia de fasciolosis fue de 48.9 %; en macro
histopatología: se detectaron obstrucciones hepáticas, un aumento en el diámetro y
engrosamiento de los conductos biliares (colangiohepatitis), una disminución en el grosor
de los lóbulos hepáticos izquierdo y ventral, y en casos crónicos, se observó cirrosis
hepática; a nivel histológico: se observó pérdida de la morfología celular y presencia de
huevos de F. hepatica, depositados en el parénquima hepático y en los conductos
sanguíneos y biliares. Se detectó que el daño hepático era directamente proporcional al
número de trematodos encontrados y que estos también causaron alteraciones en los
componentes bioquímicos sanguíneos. Los parámetros bioquímicos en sangre estuvieron
alterados de manera muy significativa (P<0.05 y P<0.01), estos parámetros alterados
fueron: Urea / BUN, colesterol y proteínas totales; enzimas tales como: γ- GT, ALT / GPT,
AST / GOT, LHD y fosfatasa alcalina, detectada en hembras y machos; se concluye que el
daño hepático es directamente proporcional al número de distomas presentes, y al
compararlo con el perfil metabólico, estos se alteran significativamente.
Palabras clave: Fasciola hepatica, fisiopatología, daño hepático, parénquima, parámetros
bioquímicos
Introduction
Mexico is one of the countries in Latin America with the highest number of ruminants
(cattle and sheep, mainly), however, the ruminant population is affected by a parasitic
disease called fasciolosis and which affects herbivorous animals, this parasitosis is caused
by the parasite of the class Trematoda, family Fasciolidae: Fasciola hepatica (Dalton,
1999). This disease is emerging or re-emerging in many countries, and its prevalence,
intensity, and geographic distribution are increasing (Mas-Coma, 2004). Fasciolosis is
currently the vector-borne disease with the widest known latitudinal, longitudinal, and
altitudinal distribution (Mas-Coma et al., 2003). This parasitosis affects many regions of
Mexico, with a prevalence of 33.3 % in cattle in very humid areas (tropical and subtropical)
and 13.3 % in sheep, and in buffaloes by 65 % (Rangel y Martínez, 1994; Ortega et al.,
2007; Caicedo et al., 2010); Nowadays this parasitosis has decreased its prevalence, in
approximately 10 years, this decrease is due to the use of food additives mainly such as
beta-adrenergic agonists (β2-AA), it is now re-emerging and has been detected in animals
with high levels of serum concentrations of β2-AA (Clenbuterol-Clb) in blood from 1253.5
± 87.5 to 1850 ± 123.4 ng / ml (Caicedo et al., 2009; Paz-Calderón et al., 2011; Caicedo et
al., 2011, Saavedra et al., 2019); while in sheep its prevalence is lower because there are no
definitive diagnostic studies of this disease in this species ruminant. Recently, in Mexico
diagnostic and control techniques of this parasitosis were implemented, however these
programs established by higher education entities have not encouraged government
authorities to incorporate more resources for the study of this parasitosis and have not
persisted its scope and repercussions in damage to national economic productivity. The
purpose of this study was to evaluate the pathophysiological effects caused by F. hepatica
in native or creole cattle in different zoogeographic zones of Mexico.
Fasciolosis by Fasciola hepatica in creole cattle
Materials and Methods
Blood samples and livers: Clinically healthy cattle (animals without flukes and without
abnormalities at the liver level) and animals with fasciolosis slaughtered in different
municipal slaughterhouses and private farms in Mexico were collected, for two years the
population of sampled animals was 7892 cattle.
Histological analysis: The number of trematodes (flukes) in the liver parenchyma was
determined by examining the affected livers. To observe the damage of liver parenchyma,
liver tissue samples were taken and subjected to a histological process and stained with
H&E.
Blood samples: were taken to count white blood cells (differential count). The analysis of
the metabolic profile was carried out in blood serum samples, macro minerals were
measured as; Calcium/Ca and phosphorus/P, metabolites such as: Urea/BUN, total
Cholesterol (TC) and total Proteins (TP) and various enzymes were measured (gamma
glutamyl transferase-γGT; alanine amino-transferase-ALT/GPT; aspartate amino-
transferase-AST/GOT; lactic dehydrogenase-LDH; Alkaline phosphatase-ALP) and these
metabolites were detected with different diagnostic kits (Bio-System-USA).
Statistical analysis of data obtained: An analysis of variance (ANOVA) with the statistical
program Stat-2 was used (Olivares, 1994) and to determinate the significance between
averages was used Duncan’s new multiple range test.
Results and Discussion
A) Number of flukes in the liver parenchyma: In the hepatic ducts of the livers confiscated
in the municipal slaughterhouses, flukes were found in a variable number, with a minimum
of 1 fluke and a maximum of 273 flukes per liver, in females the highest number of flukes
collected was 54, while in males it was 273. This variation is due to the number of
metacercariae ingested by each animal (reinfestation, possibly, animals with a high number
of worms), which was impossible to detect in this study due to the animals analyzed were
naturally infected with F. hepatica.
Most of the confiscated livers showed a significant increase in the diameter of the hepatic
ducts (Figure 1a); in addition, its color was whitish-yellowish, due to the obstruction of
these ducts by the parasite (Figure 1b), as well as the decrease in the thickness of the
affected lobes (left and ventral) of approximately 30 mm (in normal livers this decrease
does not occur, however, there is no history of this anomaly), since when the parasitic
disease progresses there are losses in the consistency of the liver, caused by fibrosis and
finally cirrhosis in very chronic cases (Figure 1b, c). As a result, the liver loses its
metabolic faculties and allows the accumulation of substances rich in salt, which
crystallizes, causing obstruction of the ducts (Figure 1c), however, these ducts were
obstructed by the presence of flukes within them, bringing favorable conditions for the
reproduction of bacteria such as Clostridium spp (Robles, 1998), Escherichia coli,
Enterococcus faecalis, and Klebsiella pneumoniae (Valero et al., 2006). All the previous
characteristics and based on the literature (Guy et al., 2001; Mas-Coma, 2005 and Caicedo
et al., 2009) indicate that the majority of the animals with F. hepatica were with a chronic
parasitic disease.
Fasciolosis by Fasciola hepatica in creole cattle
Figure 1. a) Opening of a hepatic duct where crystallized bile and flukes of F. hepatica
are observed, b) change of the liver coloration (fibrosis-cirrhosis), and c)
crystallization of bile fluid within liver ducts, this is cholangiohepatitis.
At the cellular level, compared to with clinically healthy liver tissue (Figure 2a), we could
observe loss of the morphology, chronic hepatitis, inflammation forming micro-abscesses,
proliferation of bile ducts, intracytoplasmic cholestasis, chronic inflammatory infiltrate
based of lymphocytes, dilation of the sinusoids (Figure 2b), thickening of the Glisson´s
capsule by a chronic process, presence of fibroblasts, fibrosis, cirrhosis, and eggs of F.
hepatica in the ducts and in the hepatic parenchyma (Figure 2c and d).
a
b
c
Fasciolosis by Fasciola hepatica in creole cattle
Figure 2: a) Section of clinically healthy creole bovine liver (animals without worms and
without abnormalities at the liver level), showing hepatocytes (H), sinusoidal ducts (S), bile
ducts (BD), hepatic portal vein (HPV), terminal hepatic vein (THV). b) Section of the
Creole bovine liver with fascioliasis, showing the presence of an inflammatory infiltrate
with a predominance of lymphocytes (IIPL), proliferation of capillaries, hepatic fibrosis
(F), hepatocyte cords with degenerative changes (HC). c) Replacement of the liver
parenchyma by fibrosis and thickening of the capillary wall with an inflammatory infiltrate
(F/C), d) Accumulation of F. hepatica (Fh) eggs surrounded by tissue necrosis (TN) and
cellular detritus (CD), delimited by fibrous liver tissue (FT) with an inflammatory infiltrate
B) Differential recount: About the counting of white blood cells, we found significant
differences (P<0.01) in eosinophils values in the analyzed groups, also in monocytes in
males (Table 1). According to the number of flukes, there were significant differences in
males who presented a decrease of neutrophils, an increase of lymphocytes; and in both
groups (males and females) there was a decrease of monocytes and an increase of
eosinophils, (Table 2).
Fasciolosis by Fasciola hepatica in creole cattle
Table 1. Values of the counting of white blood cells of clinically healthy bovines (animals
without flukes and without abnormalities at the liver level) and bovines with F. hepatica.
Neutrophils
%
Lymphocytes
%
Eosinophils
%
Monocytes
%
Basophills
%
Males
Healthy
54.9 ± 1.6
38.7 ± 1.5
2.0 ± 0.3a
3.8 ± 0.4
a
0.6 ± 0.1
a
F. hepatica
47.8 ± 3.0
45.7 ± 2.9
4,3 ± 1,1
a
1.8 ± 0.4
b
0.3 ± 0.1
b
Females
Healthy
50.7 ± 2.2
43.8 ± 2.0
2.9 ± 0.4
b
2.4 ± 0.4
0.2 ± 0.1
a
F. hepatica
45.9 ± 4.1
42.1 ± 3.8
8.4 ± 2.3
a
2.3 ± 0.4
0.8 ± 0.4
b
a, b
Different letters show significant differences (P< 0.05 and P< 0.01)
Table 2. Values of the counting of white blood cells of bovines with F. hepatica according
to the number of flukes into the liver and healthy bovine: animals without flukes and
without abnormalities at the liver level.
No. of
flukes
n
Neutrophils
%
Lymphocytes
%
Eosinophils
%
Monocytes
%
Basophils
%
Males
Healthy
992
54.9 ± 1.6
a
38.7 ± 1.5
b
2.0 ± 0.3
3.8 ± 0.4
a
0.6 ± 0.1
a
1-10
249
50.4 ± 5.3
ab
42.2 ± 4.0
b
4.8 ± 0.26
b
2.6 ± 0.7
0.0 ± 0.0
11-25
301
49.8 ± 2.8
ab
43.0 ± 3.7
ab
5.5 ± 0.17
b
1.3 ± 0.6
c
0.5 ± 0.3
26-50
154
54.5 ± 0.5
ab
41.5 ± 1.5
b
6.5 ± 0.5
b
1.5 ± 1.5
b
0.0 ± 0.0
>51
292
31.0 ± 1.0
b
64.0 ± 1.0
a
6.5 ± 0.4
b
1.5 ± 0.5
b
1.0 ± 0.0
Fema
les
Healthy
956
50.7 ± 2.2
43.8 ± 2.0
2.9 ± 0.4
b
2.4 ± 0.4
a
0.2 ± 0.1
1-10
436
50.5 ± 6.9
44.4 ± 6.0
3.0 ± 0.7
b
1.9 ± 0.6
b
0.3 ± 0.2
11-25
478
45.0 ± 2.0
45.5 ± 5.5
8.0 ± 0.8
c
1.5 ± 0.5
c
0.0 ± 0.0
a, b, c
Different letters show significant differences (P< 0.05 and P< 0.01)
The increase in the number of eosinophils in animals with F. hepatica (Table 1 and 2) is
consistent with the diagnostic characteristics of the disease (Guy et al., 2001; Mas-Coma,
2005); however, this increase is more evident during the parenchymal phase and these
leukocyte blood cells tend to increase when the parasite enters the bile ducts and initiates
rupture of the parenchyma, invading both the hepatic canaliculi and hepatic arterioles and
venules over time, producing obstruction of these structures, resulting in cell death,
apoptosis, fibrosis occurs, leukocyte inflammatory processes, there is a degeneration of
liver tissue, loss of much of the metabolic functionality, the liver falls into cirrhosis, finally,
liver dysfunction (Poitou et al., 1992, 1993; Jemli et al., 1993, Caicedo et al., 2009). It is
also observed that among the white-leukocyte cells: lymphocytes and eosinophils both
increase their number in animals with Fasciola hepatica: males and females; the same
happens when the values of animals with different numbers of flukes detected at the level
of the hepatic parenchyma are analyzed (P< 0.05).
C) Metabolic profile: In relation to the metabolic profile, there were significant differences
(P <0.05 and 0.01, respectively), in the values of Urea / BUN and phosphorus between the
two groups of males, while the females only in Urea / BUN (Table 3). The data obtained
show that there were differences in the parameters between males and females and more
when the data were correlated with the number of trematodes, as seen in table 3, there were
more males with a greater number of trematodes in the liver than in females, Possibly here
the immunological characteristics of the females play an important role, which is less
Fasciolosis by Fasciola hepatica in creole cattle
susceptible to this parasitic infection, the values and metabolic differences are clearly
observed. in Table 3 and 4. These data agree with Caicedo et al., 2009.
Fasciolosis by Fasciola hepatica in creole cattle
Table 3. Values of the metabolic profile of clinically healthy bovines (animals without flukes and without abnormalities at the liver
level and bovines with F. hepatica.
n
Calcium
mg/dL
Phosphorus
mg/dL
Urea/BUN
mg/dL
Bilirubin
mg/dL
Cholesterol
mg/dL
Total
Proteins
g/L
ᵧGT (U/I)
GPT (U/I)
GOT (U/I)
LHD (U/I)
Alkaline
Phosphatase
(U/I)
Males
Healthy
992
8.4 ± 0.5
5.2 ± 0.01
a
26.4 ± 1.5
a
0.2 ± 0.01
182.9 ± 19.4
a
49.8 ± 1.9
28.5 ± 4.7
258.1 ± 66.6
131.8 ± 39.5
a
1 838 ± 88.4
a
375.8 ± 39.3
a
F. hepatica
996
8.8 ± 0.4
5.5 ± 0.1
b
13.9 ± 1.9
b
0.3 ± 0.02
163.8 ± 22.6
b
47.1 ± 1.7
29.3 ± 5.1
259.7 ± 51.6
51.9 ± 20.4
b
1 338 ± 227.4
b
431.3 ± 41.5
b
Female
s
Healthy
956
8.2 ± 0.5
5.3 ± 0.1
22.8 ± 2.6
a
0.4 ± 0.08
161.3 ± 28.5
52.5 ± 1.8
26.4 ± 6.3
258.3 ± 44.3
68.2 ± 28.9
1 980 ± 155.1
250.9 ± 48.1
a
F. hepatica
914
8.1 ± 0.3
5.3 ± 0.1
14.9 ± 1.6
b
0.3 ± 0.02
162.7 ± 16.4
47.4 ± 2.9
22.9 ± 2.3
b
245.5 ± 44.9
67.7 ± 17.4
1 500 ± 192.9
b
404.8 ± 59.9
c
a, b, c
Different letters show significant differences (P<0.05 and P<0.01)
Fasciolosis by Fasciola hepatica in creole cattle
From the metabolic profile of the animals studied with fasciolosis grouped by the number
of flukes located in the liver parenchyma (Table 4), it was detected that in males and
females the bilirubin values decrease when the number of trematodes in the liver
parenchyma increases. This agrees with Ortega et al., (2007); Torres, 2010 and Caicedo et
al., (2010); this decrease in bilirubin concentrations in the blood is due to the accumulation
of bile due to obstruction of the bile ducts, preventing it from entering the bloodstream due
to the lack of biliary communication that is lost, in addition to the absence of hepatocytes
due to the development of a fibrosis [begins with leukocyte inflammatory processes, cell
death-apoptosis and finally there is growth of bacteria of the genus Clostridium spp,
(Robles, 1998) and also in animals that are re-infested by Fasciola hepatica, this re-
infestation does not lead to liver regeneration, developing cirrhosis itself with possible
development of hepatitis, thus preventing the formation of bile at the level of the
hepatocytes and the bile that forms tends to accumulate in the different structures of the
liver parenchyma, hence the yellowing of the liver. On the other hand, the most important
liver enzymes detected, were the values of alkaline phosphatase (ALP), alanine amino-
transferase (ALT / GPT), Aspartate amino-transferase (AST / GOT), they showed
decreasing values compared to clinically healthy animals (animals without flukes and
without abnormalities at the liver level); while total cholesterol (TC) in males and AST /
GOT in females showed a decreasing trend as well, when the number of trematodes in the
liver increases; while lactic dehydrogenase (LHD) in males and females tends to decrease
significantly (P <0.05 and P <0.05), these data coincide with those of Caicedo et al.,
(2010); This decrease is due to the increase in flukes in the liver parenchyma, increasing the
obstructions in the different structures, inhibiting the hepatic homeostatic activity of the
animals, significantly affecting weight gain (Loyacano et al., 2002 and Caicedo et al.,
2010); It is added that the increase in liver flukes also produces a decrease in reproductive
and productive parameters, however, it does not cause the death of animals with a high
degree of infestation and they become reservoirs for the transmission of Fasciola hepatica;
finally the values obtained in this study are significant (P <0.05 and P <0.05) (see Table 4).
Fasciolosis by Fasciola hepatica in creole cattle
Table 4. Values of the metabolic profile of bovines with F. hepatica according to the number of flukes into the liver.
n
Calcium
mg/dL
Phosphor
us mg/dL
Urea/BUN
mg/dL
Bilirubin
mg/dL
Cholesterol
mg/dL
Total
Proteins g/L
ᵧGT (U/I)
GPT (U/I)
GOT (U/I)
LHD (U/I)
Alkaline
Phosphatase
(U/I)
Males
Healthy
992
8.4 ± 0.5
5.2 ± 0.01
26.4 ± 1.5
a
0.25 ± 0.01
182.9 ± 19.4
a
49.8 ± 1.9
a
28.5 ± 4.7
a
258.1 ± 66.6
a
131.8 ± 39.5
a
1838 ± 88.4
a
375.8 ± 39.3
a
1-10
249
8.8 ± 0.6
5.4 ± 0.2
17.4 ± 3.2
ab
0.29 ± 0.02
193.6 ± 38.5
a
42.8 ± 1.2
b
17.4 ± 2.9
b
239.1 ± 41.2
77.5 ± 56.1
b
1048.3 ±498.8
a
490.9 ± 69.5
b
11-25
301
9.2 ± 0.2
5.4 ± 0.1
18.7 ± 1.2
ab
0.28 ± 0.01
199.2 ± 21.6
b
50.7 ± 0.5
a
23.2 ± 2.9
151.7 ± 11.7
b
59.4 ± 13.1
b
1740.4 ± 129.5
490.6 ± 20.2
b
26-50
154
10.9 ± 0.4
5.8 ± 0.02
13.5 ± 1.1
ab
0.28 ± 0.01
143.2 ± 12.4
b
45.4 ± 3.6
b
29.9 ± 1.6
155.1 ± 7.8
b
60.2 ± 3.5
c
2064.2 ± 324.1
b
371.2 ± 24.5
a
>51
292
8.9 ± 0.5
5.4 ± 0.02
9.2 ± 1.4
b
0.24 ± 0.01
97.8 ± 8.9
c
39.6 ± 3.8
c
29.6 ± 0.9
60.2 ± 5.3
11.3 ± 2.1
d
1440.9 ± 232.2
c
151.8 ± 13.4
c
Females
Healthy
956
8.2 ± 0.5
5.3 ± 0.1
22.8 ± 8.2
a
0.37 ± 0.08
a
161 ± 28.5
a
52.5 ± 1.8
26.4 ± 6.3
258.3 ± 44.3
a
68.2 ± 28.9
a
1980.4 ± 155.1
a
250.9 ± 48.1
b
1-10
436
7.6 ± 0.4
5.2 ± 0.1
16.9 ± 2.4
b
0.27 ± 0.03
b
171.7 ± 31.3
b
49.2 ± 3.3
22.4 ± 2.6
230.6 ± 77.1
ab
73.9 ± 36.4
1455.5 ± 152.6
b
505.4 ± 88.8
a
11-25
478
8.2 ± 0.6
5.4 ± 0.2
18.2 ± 3.2
0.31 ± 0.02
163.5 ± 7.9
58.9 ± 4.9
29.7 ± 8.4
300 ± 114.8
b
47.8 ± 16.3
b
1413.6 ± 458.4
b
357.4 ± 26.1
ab
a, b, c
Different letters show significant differences (P<0.05 and P<0.01)
Fasciolosis by Fasciola hepatica in creole cattle
As a result of the damage caused by fasciolosis in creole cattle in the studied areas, The
data detected by histopathology and the metabolic profile show the great physiological
influence that this parasitosis, fasciolosis, has in directly influencing the homeostatic
mechanism of ruminants, however cattle do not die with a high degree of infestation and
this will depend on the age of the animal, the younger, the more susceptible it is to
irreversible damage to the liver. (Loyacano et al., 2002; Ortega et al., 2007; Caicedo et al.,
2010); therefore, fasciolosis can be considered as a parasitic disease of great
epidemiological importance, since it causes great damage to the animal and important
economic losses to the farmer.
Conclusion
This study shows that fasciolosis is the most important parasitic disease in cattle, since it
affects a digestive gland that is very important in vertebrates, the liver, which performs
many vital functions such as metabolic function, so this research establishes the metabolic
changes that animals experience according to the degree of infestation, and these damages
are more significant in males than in females, in addition, fasciolosis by Fasciola hepatica,
once it infects the liver, triggers a series of pathological diseases and these diseases produce
alterations in the processes productive and reproductive. However, for the early diagnosis
of fasciolosis it will depend on the ecological zone where the livestock system develops, if
it is endemic to Fasciola hepatica and if there are also intermediate hosts of this parasitosis.
For its detection it is necessary to implement diagnosis, prevention and control programs,
avoiding the great economic losses caused by fasciolosis in cattle.
Acknowledgment
This project was financed with the laboratory's own resources through continuing education
courses and with funds from the Office of the Vicerector for Research and Postgraduate
Studies-VIEP-BUAP and with support from the Faculty of Biological Sciences of the
Benemérita Autonomous University of Puebla-Mexico, for allowing us to use its facilities
and in collaboration with livestock producers and municipal traces of various municipalities
at the federal level.
Literature Cited
Caicedo R., R. E., Torres Beltrán A., Hernández, Zepeda J.S., Resendiz Martínez R., Pérez
Y Terrón. R. and Cabrera Bautista E. 2009. Effects of β
2-
agonist-adrenergic in the
diagnosis of fasciolosis in animal ruminant Bos indicus X Bos taurus, in the State of
Puebla, Mexico. In International Symposium on sustainable Improvement of animal
production and health. FAO/IAEA, Vienna, Austria, Vol1: 183-187.
Caicedo Rivas, R.E.; J. Dimas Ríos; A. Torres Beltrán; S.V. Martínez Badillo; R. Pérez
Aviles; J.S. Hernández Zepeda y R. Reséndiz Martínez. 2010. La fasciolosis como
ecopatología que afecta la productividad ganadera en el Estado de Puebla, México.
En XI Symposia Iberoamericano sobre Conservación y Utilización de Recursos
Zoogéneticos. Joao Pessoa-Paraíba, Brasil. ISSN: 2179-1961. Pág.395-399
Caicedo Rivas, R. E.; M. Paz-Calderón Nieto and S. V. Badillo M. 2011. Clenbuterol (β
2
-
agonista adrenérgico), enmascara las patologías hepáticas en bovinos. Revista AICA
(Actas Iberoamericanas de Conservación animal), (1):327-331.
Fasciolosis by Fasciola hepatica in creole cattle
Chirinos, A.R. and N.I. DE Chirinos. 1993. Evaluación de los efectos de la distomatosis
hepática bovina sobre la eficiencia reproductiva y producción lechera. Rev. Científ.
FCV-LUZ. III, 35-45.
Dalton, J.P. (editor) 1999. Fasciolosis. Dublin, Irlanda. CABI International Publishing.
Guy, W., V. Rajan, CH. Veetta and K. Rajender. 2001. Laparoscopic appearance of
Fasciola hepatic infection. Gastrointestinal Endoscopy; 53, 668-671.
Jemli, M.H., J.P. Braun, P. Dorchies, S. Romdhane and M. Kilani. 1993. Exploration
biochimique et hématologique chez l’agneau infesté expérimentalement par Fasciola
hepatica. Recueil de Médecine Vétérinaire 169, 241-249.
Loyacano, A.F., J.C. Williams; J. Gurie and A.A. Derosa. 2002. Effect of gastrointestinal
nematode and liver fluke on weight gain and reproductive performance of beef
heifers. Vet. Parasitol. 107, 227-234.
Mas-Coma, S. 2004. Human fascioliasis. In: J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram,
R. Carr, D.O. Cliver, G.F. Craun, R. Fayer, V.P.J. Gannon (Eds.), World Health
Organization (WHO), Waterborne Zoonoses: Identification, Causes and
Control, JIWA Publishing, London, UK, pp. 305-322.
Mas-Coma, S. 2005. Epidemiology of fasciolosis in human endemic areas. J. Helminthol.
79, 207216.
Mas-Coma, S., M. D. Bargues, M.A. Valero and M.V. Fuentes. 2003. Adaptation capacities
of Fasciola hepatica and their relationship with human fascioliasis: from below sea
level up to the very high altitute. pp. 81123 in Combes, C. and Jourdane, J. (Eds.)
Taxonomy, ecology and evolution of metazoan parasites. Vol. II. Perpignan,
Perpignan University Press.
Olivares, E. 1994. Paquete de diseños experimentales FAUANL. Versión 2.5. Facultad de
Agronomía UANL. Marín, N.L.
Ortega, V.; R.E. Caicedo; J.S. Hernández; R. Resendiz and A. Ramírez. 2007.
Fisiopatología hepática en bovinos (Bos taurus X Bos indicus) con fasciolosis en el
Estado de Puebla. Memorias del L Congreso Nacional de Ciencias Fisiológicas,
Puebla, Pue., México.
Paz-Calderón Nieto, M.; R.E. Caicedo Rivas Y B. Hernández Pérez. 2011. Efecto del
clembuterol en los niveles de fosfatasa acida “Fracción Prostática”, en bovinos
machos. Revista AICA (Actas Iberoamericanas de Conservación animal), (1):136-
140.
Poitu, I., E. Baeza and C. Boulard. 1993. Analysis of the results obtained using a technic of
experimental primary infestation with Fasciola hepatica in the rat. International
Journal of Parasitology; 23, 403-406.
Rangel Ruiz, L. J. y E. Martínez Durán. 1994. Pérdidas por decomiso de hígados y
distribución geografica de la fasciolasis bovina en el Estado de Tabasco, México. Vet.
Mex. (25(4), 327-331.
Robles, C. A. 1998. Enfermedades Clostridiales del Ganado. 1a. Edición. Argentina. INTA.
Saavedra Rodríguez, A.; R.E. Caicedo Rivas; Paz-Calderón Nieto, M. y Estrada Poblano,
M. 2019. Physiological effect of β
2
-agonist adrenergic “Clenbuterols”, in cattle Bos
taurus X Bos indicus, in the State of Puebla, México. Agroproductividad: Vol.12,
Num.6, pp. 63-68
Valero, M.A., M. Navarro, M.A. Garcia-Bodelon, A. Marcilla, M. Morales, J.L.
Hernández, P. Mengual and S. Mas-Coma. 2006. High risk of bacterobilia in
advanced experimental chronic fasciolosis. Acta Tropica 100, 1723.