Prevalence of flukes ( Fasciola hepatica and paramphistomids) in cattle in south-eastern Mexico

Abstract

The objective of this study was to determine the risk factors and prevalence of trematodes in south-eastern Mexico. The prevalence of trematodes was determined in 1010 bovines. The study was carried out from October 2018 (n=291) to December 2019 (n=719). Only in 2019 rumen and liver fluke eggs were differentiated. Faecal samples (n=311) were obtained from farms in southeast Mexico located in Tabasco, Chiapas and Campeche. In addition, the presence of flukes in liver and rumen from slaughtered cattle in abattoirs was recorded with a total of 408 samples. A logistic procedure was used to obtain the prevalence and the effect of main risk factors such as land physiography (flooded areas and hills), year, sex, animals’ age and type of sample obtained (eggs in faeces and flukes). The general prevalence of flukes in cattle was 32.3 % in 2018 and 41.7 % in 2019. Prevalence of F. hepatica (liver fluke) was 18.6 % (134/719) and that of paramphistomids (rumen fluke) was 33.4 % (240/719). The infected cattle from the slaughterhouse indicated a lower prevalence of F. hepatica (1 %) and rumen fluke (26.7 %) than in farms detected by egg in faeces (41.8 % and 42.1 %, respectively). The physiographic zone was decisive in the presence of F. hepatica and rumen fluke, while sex did not represent a risk factor (P > 0.05). The environmental conditions of the Mexican southeast favour the presence of both liver and rumen fluke.

Full text

DOI 10.2478/helm-2023-0017
141
HELMINTHOLOGIA, 60, 2: 141 – 151, 2023
Prevalence of  ukes (Fasciola hepatica and paramphistomids) in cattle
in south-eastern Mexico
J. C. HERNÁNDEZ-HERNÁNDEZ1, R. GONZÁLEZ-GARDUÑO1,*, D. O. ORTIZ-PÉREZ2, A. VILLA-MANCERA3,
M. S. ARIAS-VÁZQUEZ4, A. PAZ-SILVA4
1Unidad Regional Universitaria Sursureste, Universidad Autónoma Chapingo, km 7.5 Carr. Teapa-Vicente Guerrero, Teapa, Tabasco,
México, *E-mail: rgonzalezg@chapingo.mx; 2Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Chiapas,
Campus Pichucalco, México; 3Facultad de Medicina Veterinaria y Zootecnia, Benemérita Universidad Autónoma de Puebla,
Tecamachalco Puebla, Mexico; 4 Facultade de Medicina Veterinaria, Universidade de Santiago de Compostela,
Carvalho Calero sn. 27002, Lugo, España
Article info
Received February 21, 2023
Accepted May 15, 2023
Summary
The objective of this study was to determine the risk factors and prevalence of trematodes in
south-eastern Mexico. The prevalence of trematodes was determined in 1010 bovines. The study
was carried out from October 2018 (n=291) to December 2019 (n=719). Only in 2019 rumen and
liver  uke eggs were differentiated. Faecal samples (n=311) were obtained from farms in southeast
Mexico located in Tabasco, Chiapas and Campeche. In addition, the presence of  ukes in liver and
rumen from slaughtered cattle in abattoirs was recorded with a total of 408 samples. A logistic proce-
dure was used to obtain the prevalence and the effect of main risk factors such as land physiography
( ooded areas and hills), year, sex, animals’ age and type of sample obtained (eggs in faeces and
 ukes). The general prevalence of  ukes in cattle was 32.3 % in 2018 and 41.7 % in 2019. Preva-
lence of F. hepatica (liver  uke) was 18.6 % (134/719) and that of paramphistomids (rumen  uke)
was 33.4 % (240/719). The infected cattle from the slaughterhouse indicated a lower prevalence of
F. hepatica (1 %) and rumen  uke (26.7 %) than in farms detected by egg in faeces (41.8 % and
42.1 %, respectively). The physiographic zone was decisive in the presence of F. hepatica and ru-
men  uke, while sex did not represent a risk factor (P > 0.05). The environmental conditions of the
Mexican southeast favour the presence of both liver and rumen  uke.
Keywords: Fasciola hepatica; paramphistomids; prevalence; trematodes; tropics
Introduction
In addition to the nutritional, reproductive and management as-
pects that limit the productivity of cattle (Vite et al., 2015), parasite
damage represents an economic problem in livestock as they af-
fect animal health and can even cause death of susceptible ani-
mals (Delafosse, 2022; Sargison et al., 2016). The adverse effects
of Fasciola hepatica on milk production have been estimated at
an approximate reduction of 1.37 – 1.78 kg of milk per cow per
day, with losses between US$5,974.1 – 8,660.0 (Villa-Mancera &
Reynoso-Palomar, 2019). In addition, in meat cattle production,
the losses have been estimated at US$1.41 billion in Mexico, due
to low weight gain and condemnation of livestock by-products
(Rodríguez-Vivas et al., 2017). The negative effects derived from
liver  uke infection affect daily weight gain, live weight and carcass
weight with reductions of 9 %, 6 % and 0.6 %, respectively, al-
though no changes have been observed in the total weight or milk
production (Hayward et al., 2021).
* – corresponding author

142
The importance of endoparasites has been highlighted for a long
time (Sardar et al., 2006) and it has been reported that gastroin-
testinal nematodes (GIN) have a high prevalence, especially in
calves (Stromberg et al., 2015), while in adult cattle the trema-
todes are highly prevalent as indicated in Colombia (Pinilla et al.,
2020). Of the ukes of veterinary importance, Fasciola hepatica
is a cosmopolitan species with a wide presence on all continents
(Jones et al., 2022; Nyirenda et al., 2019). The disease fasciolosis
is caused by F. hepatica or Fasciola gigantica and together have
an extensive geographic range, with a major impact on livestock
(Elelu & Eisler, 2018; Naranjo-Lucena et al., 2018). In Mexico, the
presence of F. hepatica in cattle has been reported for both the
northeast (Munguía-Xóchihua et al., 2007) and southeast (Oje-
da-Robertos et al., 2014), with highly variable prevalence reaching
up to 50 % in some cases. Fasciolosis is considered an important
disease because it constitutes a zoonosis and its presence has
been indicated in around 70 countries with reported cases in both
animals and humans (Torgerson, 2013). However, human fascio-
losis has rarely been diagnosed in Mexico but a clinical report on
this disease in the acute phase was reported in Puebla (Cruz y
López et al., 2016).
In the trematode class, there is another group belonging to the
Paramphistomidae family, which is composed of several genera
that cause the disease called paramphistomidosis. These para-
sites affect the gastrointestinal tract, causing haemorrhagic in-
ammation of the intestines after excystation and subsequent
migration of the juvenile uke to the target organ. In acute cas-
es the thickness of mucosa and submucosa of intestines occur
(Atcheson et al., 2020). The presence of both species has been
observed in Mexico, mainly in the tropics, where climatic condi-
tions favour the development of gastrointestinal parasites, so the
prevalence of F. hepatica and the existence of Paramphistomum
cervi has been reported in Tabasco since 1989 (Rangel-Ruiz et al.,
2003, 1999) and to date there are studies in the southern region
of Mexico (González-Garduño et al., 2019; Ojeda-Robertos et al.,
2020, 2014). However, the importance and high prevalence of ru-
men uke have been indicated recently, a situation similar to that
of many other countries that have evaluated the prevalence of this
group of trematodes (Huson et al., 2018; Ojeda-Robertos et al.,
2014; Ploeger et al., 2017).
Due to the importance of ukes in cattle health, the objective of
this study was to study the risk factors and prevalence of the ukes
F. hepatica and paramphistomids in cattle in south-eastern Mexico.
Materials and Methods
Location
The samplings were carried out on 20 cattle farms located in the
municipalities of Teapa, Jalapa, Huimanguillo and Tacotalpa cor-
responding to the southern region of Tabasco state and in the mu-
Fig. 1. Map of the study area to determine the prevalence of trematodes in southeastern Mexico.

143
nicipalities of Pichucalco, Juarez and Salto de Agua corresponding
to the north of the Chiapas state. Samples were also taken in Es-
carcega, Campeche. In addition, 14 samplings were carried out
in three slaughterhouses, one located in Jalapa, Tabasco 17° 38’
N and 92° 50’ W, another in Juarez Chiapas located at 17° 41’ N
and 93° 13’ W and another in Escarcega, Campeche 18° 33’ N
90° 32’ W (Fig. 1).
The area has a warm humid climate with rain all year round, with
a precipitation range of 2000 – 2500 mm and a temperature range
of 24 – 26 °C, which corresponds to a hot and humid climate with
rains in summer (warm wet, Af; warm sub-humid, Am), equivalent
to equatorial rainforest fully humid (Af), equatorial monsoon (Am)
and equatorial savannah (warm-dry, As) (Kottek et al., 2006).
Cattle management
The livestock production systems were mostly for beef produc-
tion and only two units were dedicated to both milk and beef pro-
duction. In all farms, cattle were raised on native and introduced
pastures, without supplementation, except for dairy cattle that re-
ceived some type of commercial supplement. The breeds in the
region are mostly crossbreeds of Bos taurus with Bos indicus and
in dairy breeds, the synthetic Holstein-Friesian-Zebu breed (5/8
HF × 3/8 Zebu) was found.
Sampling
The study was carried out from August to December 2018 and
in this year only the presence of ukes was determined because
staining with iodine-Lugol was used to differentiate the groups,
which caused an error in the differentiation and the total count was
taken. In 2019 liver and rumen uke eggs were differentiated only
by the coloration of the egg. The number of samples obtained by
locations are indicated in Table 1.
The farms were selected for convenience with producers, who par-
ticipated as volunteers, contacted through the Livestock Produc-
ers Association. To obtain the faeces, always during the morning
before 8:00 am, the cattle from each farm were moved to a han-
dling cage where 20 – 50 g of faeces were obtained directly from
the rectum of the animals in plastic gloves by veterinarians and
students. Then the samples were transported to the animal health
laboratory of the university for coproparasitoscopic analysis. In ad-
dition, other method to determine the prevalence was observing
adult ukes, for which three slaughterhouses were visited as rou-
tine academic activities of parasitological inspection.
To report prevalence of liver and rumen uke eggs, the sedimenta-
tion technique was used. Briey, 10 grams of faeces were weighed
and diluted in 250 ml of running water. Larger particles were re-
moved washings the faeces through a #30 mesh sieve (0.59 mm,
mont-inox) and the collected liquid was allowed to settle in beakers
with 250 ml of water, then the supernatant was removed and wa-
ter was added again, this procedure was carried out three times.
Finally, the sediment was left in 100 ml of water and two drops
of concentrated methylene blue were added. Later, the sediment
from the bottom of the beaker was extracted with a pipette and the
content placed in a Petri dish. The content was reviewed under a
microscope (Iroscope) at 10× to watch for uke eggs, which dif-
fered by colouring; the golden eggs corresponded to liver uke and
the transparent ones to rumen uke (Sanabria & Romero, 2008).
In addition to prevalence, the number of eggs per gram of faeces
was counted in only 140 animals.
To determine the prevalence of adult trematodes, the liver, rumen
and reticulum of slaughtered cattle were inspected. In addition, the
liver and rumen uke specimens were counted and the average
was obtained in the positive animals. Rumen ukes were collected
for their subsequent identication based on their morphology
(Eduardo, 1982), for which the specimens were xed in formalin
and dehydrated. Ten specimens of each isolate were measured
to discriminate species by size. Other specimens were hydrated
and stained with haematoxylin-eosin and mounted on slides to dif-
ferentiate them by their species characteristics (Nikander & Saari,
2007).
Statistical analysis
Two methods of prevalence were used, one with the differentia-
tion of eggs and the other with the presence of adult ukes. The
descriptive statistics using the SAS program (SAS, 2017) allowed
calculating the prevalence as the number of positive cases among
Year Type of sample State Number of samples
2018 Faeces for determination of trematode eggs Tabasco 193
Chiapas 98
2019 Faeces for determination of liver and rumen
uke eggs
Tabasco 227
Chiapas 34
Campeche 50
Presence of liver and rumen ukes in
slaughtered cattle
Tabasco 83
Chiapas 325
Total 1010
Table 1. Number of bovines sampled per year, type of sampling and state of origin of the animals.

144
the total number of animals sampled. For the analysis of the risk
factors, the logistic process was used, which was carried out after
the organisation of a database in Excel. The study variables were
coded to adjust the response to a binomial model with two possible
results: presence (1) and absence of ukes (0).
For the terrain physiography variable, two options were recorded:
ood-prone areas, which were at or slightly at sites with clayey
soils, generally ood-prone, and hillocks, which were hills or hills
with slopes that did not allow water pooling (Zavala Cruz et al.,
2016). For the sex variable, females and males were considered.
For the age variable, four categories were made (calves less than
one-year-old, steers from 1 to 3 years-old, young cows from 3 to
7 years-old and old cows over 7 years-old). The type of sampling
consisted of evaluating the presence of uke eggs in faeces and
the presence of adult specimens in slaughtered cattle.
Fig. 2. Morphological identication of Cotylophoron cotylophorum and Paramphistomum cervi.

145
Ethical Approval and/or Informed Consent
All applicable international, national and institutional guidelines
for the care and use of animals were followed. The procedures
were in accordance with the Ofcial Mexican Standard NOM-033-
SAG/ZOO-2014 on methods to kill domestic and wild animals,
and NOM-051-Z00-1995 on humane treatment in the movement
of animals.
Results
The rumen uke species identied by morphology correspond-
ed to Cotylophoron cotylophorum and to Paramphistomum cervi
(Fig. 2). In the case of P. cervi, the size was 7.75 ± 0.96 long
and 2.75 ± 0.65 wide. Surface without papillae. Genital pore of
gracile type with an absent genital sphincter and sphincter papilla.
Acetabulum subterminal, from paramphistomum type. While in the
case of C. cotylophorum the size was 6.02 ± 1.24 long and 3.40 ±
0.54 width; surface with papillae. Acetabulum subterminal, of the
cotylophoron type and the terminal genitalium of cotylophoron type
according to Eduardo (1985).
Faecal uke egg counts
The faecal uke egg counts were very low, as shown in Table 2.
The highest trematode egg counts were 13.7 eggs per gram of
faeces (epg) in Tabasco state. The steers under three years of
age had the lowest egg counts of both liver and rumen uke. The
average of trematode eggs was 11.1 ± 14.0 epg and only 3.02 ±
4.4 epg for rumen uke and 8.48 ± 11.04 epg for liver uke.
Rumen uke counts
The highest counts of adult rumen ukes corresponded to 434
specimens located in cattle in Chiapas state and only 108 in
Tabasco state. The average values were 41 ± 51 specimens in the
positive cattle and the values broken down by sex, age and state
of origin are indicated in Figure 3.
Fluke prevalence
The prevalence of trematodes (liver and rumen uke globally) in
cattle by year was 32.3 % (94/291) to 41.7 % (300/719) in 2018
and 2019 respectively. Only in 2019 was possible to perform the
differentiation of uke eggs, obtaining a prevalence of liver uke
of 18.6 % (134/719) and of rumen uke was 33.4 % (240/719).
Variable N Mean SE Q1 Median Q3
Fasciola hepatica egg per gram of faeces (epg)
Male 11 0.2 0.2 0.0 0.0 0.7
Female 129 8.7 1.0 2.0 4.0 12.0
Steers (< 3 years) 11 0.2 0.1 0.0 0.0 0.7
Cows (> 3 years) 129 9.2 1.1 2.0 4.0 14.0
Tabasco 107 10.3 1.2 2.0 4.0 16.0
Chiapas 33 2.7 0.9 0.0 0.7 4.0
Rumen uke egg per gram of faeces (epg)
Male 11 0.7 0.4 0.0 0.7 1.3
Female 130 3.1 0.4 0.0 2.0 4.0
Steers (< 3 years) 11 0.3 0.1 0.0 0.0 0.7
Cows (> 3 years) 130 3.3 0.4 0.0 2.0 4.0
Tabasco 107 3.4 0.5 0.0 2.0 4.0
Chiapas 34 1.9 0.4 0.0 0.7 2.0
Trematode egg per gram of faeces (epg)
Male 11 0.9 0.4 0.0 1.3 1.3
Female 136 11.4 1.2 2.0 4.0 15.0
Steers (< 3 years) 11 0.5 0.2 0.0 0.7 1.3
Cows (> 3 years) 136 12.0 1.3 2.0 6.0 16.0
Tabasco 107 13.7 1.5 2.0 8.0 18.0
Chiapas 40 4.5 0.9 1.3 2.0 6.5
N number of samples. SE Standard error. Q1 First quartile. Q3 Third quartile.
Table 2. Average faecal uke egg (liver and rumen ukes) counts in cattle in southeastern Mexico according to sex, age and origin.

146
The prevalence by origin of sample (faeces or adult trematode in
slaughterhouse), physiographic zone, locality, sex and age of cat-
tle only for differentiated eggs in 2019 are presented in Table 3.
The prevalence of F. hepatica calculated from the slaughterhouse
was lower than obtained by the presence of eggs in faeces. Fe-
males presented higher prevalence than males and the age also
inuences the prevalence with higher prevalence in cows than
steers.
Of the risk factors analysed, the type of sample was decisive in
the diagnosis of trematodes and a small number of cases were
observed at the slaughterhouse respect to prevalence by egg in
faeces. In addition, physiographic conditions and the origin of the
animal were conclusive in the presence of this parasite. Sex and
age were factors that did not affect the presence of ukes (Table 4).
In the case of rumen uke, no differences were observed in the
type of sample, so the diagnosis by eggs in faeces and ukes in
rumen showed similar prevalence. No differences were found in
sex (Table 5) and there were also no differences in liver ukes in
relation to age.
Discussion
In the present study, the prevalence of trematodes in Tabasco,
Chiapas and Campeche states in Mexico reached 36 – 41 %, while
for F. hepatica it was only 18.6 % and for rumen ukes 33.4 %.
These values are at the same level as those indicated in previous
studies in this area in which a prevalence of 29 % is reported for
liver uke and 27.6 % for paramphistomids, the latter with a range
of 27 to 50 % (González-Garduño et al., 2020; Ico-Gómez et al.,
2021). The studies with liver uke in other countries of the Ameri-
can continent such as Colombia indicated 20.5 % of coprological
prevalence and 41.5 % of seroprevalence (Pinilla et al., 2020) and
in Peru a prevalence of 59 % was reported (Julon et al., 2020). In
addition, in Argentina, a prevalence range of 40 – 80 % has been
documented (Kleiman et al., 2007), while in Brazil, the rumen uke
prevalence of 26 % was indicated in a study from 1982 (Mattos &
Ueno, 1996) and a similar prevalence was indicated in Venezuela
(Gauta et al., 2011).
Paramphistomids also have a wide dispersion and in the last two
decades reports have increased in various countries (Sanabria &
Romero, 2008) even in Europe, where it is considered an emerg-
ing disease (Huson et al., 2017). Generally, high importance has
been attributed to liver uke due to its ability to infect different
species of mammals, including humans, and there are generally
more studies than those of rumen uke, although the coexistence
of both ukes is the result population dynamics of hosts inuenced
by environmental factors (Dreyfuss et al., 2014; Naranjo-Lucena
et al., 2018).
Of the two rumen uke species found in the region, P. cervi has
been cited in previous studies in the same region, while C. cot-
ylophorum has been described morphologically and recently in
Camagüey, Cuba, was identied molecularly (León Companioni
et al., 2020). In Mexico, is important that subsequent studies per-
form molecular analysis because is necessary to discriminate be-
Fig 3. Fluke counts after cattle slaughter in southeastern Mexico by origin, sex and age.

147
Risk factor
Fasciola hepatica Rumen uke Trematodes
N Positives (%) Positives (%) NPositives (%)
Year
2018* 291 - - 291 94 (32.3)
2019 719 134 (18.6) 240 (33.4) 719 300 (41.7)
Type of sample
Eggs in faeces 311 130 (41.8) 131 (42.1) 602 281 (46.7)
Flukes 408 4 (1.0) 109 (26.7) 408 113 (27.7)
Physiographic zone
Flood-prone areas 278 117 (42.1) 138 (49.6) 321 216 (67.3)
Hillocks 441 17 (3.9) 102 (23.1) 689 178 (25.8)
Sex
Male 204 1 (0.5) 52 (25.5) 212 52 (24.5)
Female 515 133 (25.8) 188 (36.5) 798 342 (42.9)
Age
Steers >1<3 years 187 1 (0.5) 45 (24.1) 254 57 (22.4)
Young cows (<7) 424 131 (30.9) 160 (37.7) 623 289 (46.4)
Old cows (> 7y) 108 2 (1.8) 35 (32.4) 133 48 (36.1)
State
Tabasco 310 109 (35.2) 119 (38.4) 503 207 (41.2)
Chiapas 359 25 (7.0) 102 (28.4) 457 168 (36.8)
Campeche 50 0 (0.0) 19 (38.0) 50 19 (38.0)
N. Total number of animals sampled. * In 2018 the prevalence was only for trematodes eggs.
Table 3. Prevalence of ukes in cattle in a humid warm climate of Mexico by study variable.
tween the different species that have been reported in the region
(González-Garduño et al., 2020).
The average counts of rumen ukes obtained in Mexico were
lower (41 adult specimens) than those indicated in Iran (100 – 200
adult ukes) in slaughterhouse studies (Khedri et al., 2015). Addi-
tionally, in Spain, highest values were recorded (165 – 300 adult
specimens) (González-Warleta et al., 2013). In the case of faecal
egg counts, in France was observed that 19 % of bovines excreted
more than 200 epg of rumen uke (Delafosse, 2022), values higher
than the average count obtained in the present study. In Spain, the
mean values in excretion are close to 20 epg (González-Warleta
et al., 2013). However, for F. hepatica in cattle from Argentina (Mo-
riena et al., 2004), a small number of trematode eggs with values
very similar to those indicated in the present study was reported.
The prevalence of both ukes (liver and rumen ukes) depended
on the type of diagnostic test performed and with sedimentation
technique the highest prevalence was observed. Although it was
not possible to perform diagnostic tests in blood, seroprevalence
is more sensitive and therefore, of a higher value than the detec-
tion of eggs in faeces (40 % vs 20 %), as indicated by a study
on F. hepatica in cattle in Colombia (Pinilla et al., 2020). The re-
sults of the faecal egg count in the region showed that 18.6 %
of the adult animals were infected. However, it could be a higher
percentage since some were not detected with this technique,
which can have 59 to 68 % sensitivity (Carneiro et al., 2018). In
slaughterhouse studies show a higher prevalence for F. hepatica
due to the presen ce of eggs in the bile content (39.4 %) and lower
prevalence due to the presence of adult parasites in the bile ducts
(32.4 %) and the egg count (15.5 %) in faeces (Giraldo Forero
et al., 2016). However, studies in slaughterhouses show a great
variability in results with values as low as 12 % and up to 30 %
with the condemnation of livers due to the presence of F. hepat-
ica (Hernández-Guzmán et al., 2021). The low prevalence of F.
hepatica (1 %) in the slaughterhouses of the present study can
be associated with the fact that they were the result of samplings
carried out at xed times and not of the systematic registration of
all animals that entered the slaughterhouses. In addition, many of
the animals destined for slaughter have come from feedlots where
they were previously dewormed and therefore, less likely to carry
adult parasites. In the case of rumen uke, the diagnosis in faeces
(42 %) was higher than prevalence of adult parasites in the rumen
of sacriced animals (26.7 %), as previously indicated.

148
Risk factor B Standard
error
Wald Odds ratio 95% CI
Constant -3.9 0.8 22.45
Type of sample
Fluke Baseline 1.00
Eggs in faeces 1.19 0.49 6.0 3.3* 1.27-8.53
Physiographic zone
Hillocks Baseline 1.00
Flood-prone areas 2.48 0.37 44.7 11.98** 5.78-24.82
Sex
Female Baseline 1.00
Male -0.35 0.49 0.52 0.71ns 0.27-1.83
Age
Old cows (> 7y) Baseline 1.00
Steers >1<3 years -0.81 0.53 2.33 0.44ns 0.16-1.26
Young cows (<7) -0.24 0.42 0.32 0.78ns 0.35-1.79
State
Campeche Baseline 1.00
Tabasco 1.98 0.61 10.46 7.27** 2.19-24.21
Chiapas 3.29 0.75 18.90 26.88** 6.09-118.51
**P-value highly signicant <0.01, *signicant <0.05, nsnot signicant >0.05, CI condence interval
Table 4. Odds ratio of the study variables that affect the presence of trematodes (Fasciola hepatica and rumen uke) in cattle in a hot humid climate.
Of the risk factors, the land physiography (landform including
topography, water and soil) is very important in the presence of
parasitic diseases, both for fasciolosis and for paramphistomosis.
In the farms located in at areas prone to ooding with soils with a
high proportion of clay, the probabilities of occurrence of F. hepat-
ica were 16 times higher than in hilly areas. In the case of rumen
ukes, there was a ve times greater probability of infection in
ood-prone areas than in the hills. Environmental conditions have
been considered as one of the main factors affecting the distribu-
tion of F. hepatica (Hernández-Guzmán et al., 2021), among which
the type of soil, precipitation and altitude stand out (Jiménez-Ro-
cha et al., 2017), as conrmed by a study in Bangladesh (Khan
et al., 2017). These factors affect the distribution of both liver and
rumen ukes and their intermediate host, snails of species as Gal-
ba truncatula (Jones et al., 2022) Lymnaea glabra (Dreyfuss et al.,
2014; Naranjo-Lucena et al., 2018) and in Mexico the presence of
Fossaria humilis and F. bulimoides (Cruz-Mendoza et al., 2004) is
related with the presence of F. hepatica. However, for rumen uke
it is necessary to determine the intermediate host species related
to the highest occurrence. In addition to environmental conditions,
another author attributes the high prevalence of trematodes to a
lack of prevention and control strategies in the bovine population
(Pinedo et al., 2010).
In the place of origin, differences were observed in the prevalence
of both trematodes, which is the result of multiple factors that affect
the presence of the parasite, as suggested by studies that address
the diagnosis of these trematodes (Hernández-Guzmán et al.,
2021; Jiménez-Rocha et al., 2017; Jones et al., 2022; Naranjo-Lu-
cena et al., 2018).
Females presented higher prevalence than males because this
last receive different health and nutritional management that fe-
males, especially when they are destined for slaughter. In relation
to age, the results of this study indicate a higher prevalence in
adult animals, which is consistent with the study carried out by
Moriena et al. (2004) in Argentina, whose results indicate that the
prevalence rate increased in direct proportion to the animals’ age.
Additionally, in Colombia, bovines older than two years of age had
a ve times greater risk of presenting these parasites than younger
animals (Pinilla et al., 2020). The low prevalence found in young
cattle has been associated in principle with the long prepatent pe-
riod of F. hepatica (12 weeks), so the presence of eggs in faeces
could be higher in adult animals, due to the probability of infection
increases in grazing (Livia-Córdova et al., 2021). In addition, in the
case of rumen uke, the effectiveness of anthelmintics is much
lower than in the case of F. hepatica (Ico-Gómez et al., 2021). It
may be one of the reasons why the prevalence results are higher

149
for this group of parasites. In addition, other studies should be con-
ducted to determine the inuence of the host on the prevalence of
paramphistomidosis.
Conict of Interest
Authors state no conict of interest.
Authors Contribution
Study conception and design: RGG, and JHH; sample collection
and analyses: JHH, and DOOP; Data analysis and interpretation
of results: AVM and MSAV; manuscript preparation: RGG and
APS; Final review of the draft: MSAV, APS and RGG.
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Female Baseline 1.0 1.0
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CampecheΩ- - - - - Baseline 1.00
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**P-value highly signicant <0.01, *signicant <0.05, nsnot signicant >0.05, CI condence intervals. Ω Liver uke was not observed in Campeche.
Table 5. Odds ratio of the study variables that affect the presence of liver and rumen uke in cattle in a hot humid climate.

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