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Journal of Helminthology
cambridge.org/jhl
Research Paper
Cite this article: Hernández-Guzmán K,
Molina-Mendoza P, Olivares-Pérez J, Alcalá-
Canto Y, Olmedo-Juárez A, Córdova-Izquierdo
A, Villa-Mancera A (2021). Prevalence and
seasonal variation of Fasciola hepatica in
slaughtered cattle: the role of climate and
environmental factors in Mexico. Journal of
Helminthology 95,e46,1–8. https://doi.org/
10.1017/S0022149X21000444
Received: 10 June 2021
Revised: 26 July 2021
Accepted: 28 July 2021
Keywords:
Fasciola hepatica; fasciolosis; prevalence;
epidemiology; seasonality; geographic
information system; cattle; slaughterhouse;
Mexico
Author for correspondence:
A. Villa-Mancera, E-mail: abel.villa@gmail.com
© The Author(s), 2021. Published by
Cambridge University Press
Prevalence and seasonal variation of Fasciola
hepatica in slaughtered cattle: the role of
climate and environmental factors in Mexico
K. Hernández-Guzmán1, P. Molina-Mendoza1, J. Olivares-Pérez2, Y. Alcalá-Canto3,
A. Olmedo-Juárez4, A. Córdova-Izquierdo5and A. Villa-Mancera6
1
Ingeniería en Agronomía y Zootecnia, División de Ciencias Naturales, Universidad Intercultural del Estado de
Puebla, Puebla, Mexico;
2
Unidad Académica de Medicina Veterinaria y Zootecnia, Universidad Autónoma de
Guerrero, Ciudad Altamirano, Guerrero, Mexico;
3
Departamento de Parasitología, Facultad de Medicina Veterinaria
y Zootecnia, Universidad Nacional Autónoma de Mexico, CP 04510, CDMX, Mexico;
4
Centro Nacional de
Investigación Disciplinaria en Salud Animal e Inocuidad (CENID SAI-INIFAP), Jiutepec, Morelos, Mexico;
5
Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana, CP 04960, Unidad
Xochimilco, CDMX, Mexico and
6
Facultad de Medicina Veterinaria y Zootecnia, Benemérita Universidad Autónoma
de Puebla, Tecamachalco, CP 75482, Tecamachalco Puebla, Mexico
Abstract
The objective of this study is to determine the prevalence of Fasciola hepatica infection in
cattle slaughterhouses, as well as its association with climatic/environmental factors (derived
from satellite data), seasonality and climate regions in two states in Mexico. Condemned livers
from slaughtered animals were obtained from three abattoirs in the states of Puebla and
Veracruz. The overall prevalence of the parasite in cattle between January and December of
2017 was 20.6% (1407 out of 6834); the highest rate of condemnation was observed in
Veracruz (26.3%; tropical climate), and the lowest rate was found in Puebla (15.5%; temperate
climate). The seasonal prevalence of fluke infection was 18.6%, 14.8% and 28.4% during the
wet season, and 17.1%, 12.4% and 22.8% during the dry season in the three abattoir sites,
located in the districts of Zacatlán, Teziutlán and Ciudad Alemán, respectively. Liver condem-
nations due to bovine fasciolosis were prevalent in the Zacatlán, Teziutlán and Ciudad Alemán
districts during summer, autumn and summer, respectively. Using generalized estimating
equations analysis, we determined six variables –rainfall (wet/dry), land surface temperature
day, land surface temperature night, normalized difference vegetation index, seasonality and
climate regions (temperate/tropical) –to be significantly associated with the prevalence of
condemned livers. Climate region was the variable most strongly associated with F.hepatica
infection (odds ratio (OR) 266.59; 95% confidence interval (CI): 241.90–353.34), followed
by wet and dry seasons (OR 25.56; 95% CI: 20.56–55.67).
Introduction
Fasciolosis, a widespread foodborne zoonotic disease that affects a wide range of mammals –
particularly grazing animals –is caused by infection with Fasciola hepatica. Over 180 million
people are at risk of infection globally. Furthermore, approximately 2.4 to 17 million indivi-
duals are thought to be infected with liver fluke, and this number is likely increasing
(Sabourin et al., 2018). Economic losses in the livestock industry exceed USD 3 billion world-
wide, including USD 119 million per year in the Mexican cattle industry (Mehmood et al.,
2017; Villa-Mancera & Reynoso-Palomar, 2019b). Infected animals show reduced weight
gain, fertility and meat and milk production, as well as liver condemnation in abattoirs,
although this condition rarely causes mortality in cattle (Torgerson & Claxton, 1999;
Sanchez-Vazquez & Lewis, 2013; Qin et al., 2016). In Mexico, several recent studies using bulk-
tank milk enzyme-linked immune sorbent assay (ELISA) in cattle herds have indicated that the
F.hepatica prevalence in three climate regions ranged from 62.76% to 63.56% (Villa-Mancera
& Reynoso-Palomar, 2019a,b). A high prevalence of parasite infection in cattle has been found
in north-west Mexico using the indirect ELISA test (24.4%) and sedimentation faecal examin-
ation (11.4%) (Munguía-Xóchihua et al., 2007). In addition, dairy cattle herds in the tropical
climate had milk production losses of 1.50 kg per day, while dairy cow herds in the temperate
climate showed losses of 1.29 kg per day (Villa-Mancera & Reynoso-Palomar, 2019b).
Geographic information systems (GIS) and remote sensing technologies have been
useful for extracting data on environmental features to investigate their relationships with
disease at known sites, as well as to areas where disease does not exist (Dutra et al., 2010;
Charlier et al., 2014). The susceptibility of cattle to the effects of climate change is not
restricted to tropical, arid or temperate zones, and recent environmental and climate changes
due to global warming may alter the epidemiology, seasonality and geographical distribution
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of the free-living stages of this parasite, thereby increasing the
risk of livestock populations to the disease (Villa-Mancera
et al., 2015;Charlieret al., 2016; Villa-Mancera & Reynoso-
Palomar, 2019b).
Although the existing data on liver condemnation in cattle
slaughterhouses are not representative of the true infection status,
they are useful for enabling herd tracking of regional parasite con-
trol programs. The aim of this study is to determine the seasonal
prevalence of F.hepatica among slaughtered cattle in two climate
regions in Mexico, using data collected by the inspection of livers.
We also investigate the relationship between climatic and environ-
mental factors and parasite status.
Materials and methods
Study area and geographic information systems
The study was conducted at three abattoir sites in the states of
Puebla (Zacatlán and Teziutlán districts, east-central Mexico) and
Veracruz (Ciudad Alemán district, eastern Mexico) from January
through December of 2017. The states of Puebla and Veracruz
cover areas of 33,919 km
2
and 71,826 km
2
, respectively. After
slaughter, with the presence of veterinary inspectors, the livers of
6834 cattle were inspected by visual examination, palpation and
incision. The latitude and longitude of each abattoir were identified
using a global positioning system (GPS, Garmin eTrex
Vista, Olathe, KS, USA), and the coordinates were georeferenced
using ArcGIS 10.1 (ESRI, Redlands, California, USA) and
Köppen climate classification maps modified by García (1988)
(fig. 1). In addition, we obtained information on elevation data
provided by the Shuttle Radar Topography Mission, with a
resolution of 1 km (http://srtm.csi.cgiar.org/). This study was
approved by the local Animal Care and Ethics Committee of the
Meritorious Autonomous University of Puebla, and all procedures
complied with the National Legislation Pertaining to Animal
Health Research.
Remotely sensed climatic data
Satellite-based precipitation data were averaged to obtain a mean
monthly rainfall dataset for January through December, covering
a radius of about 50 km around each abattoir site; these data
were extracted from the Tropical Rainfall Measuring Mission
(TRMM) 3B42 version 7 and TRMM 3B43 (http://disc2.gesdisc.
eosdis.nasa.gov). Furthermore, we obtained monthly land surface
temperatures (LSTs) and the normalized difference vegetation
index (NDVI) from the Moderate Resolution Imaging
Spectroradiometer sensor aboard the Terra satellite (https://
lpdaac.usgs.gov/)–products MOD11C3 and MOD13C2.005 –
with 0.05° spatial resolution. LST data were used as a proxy for
day and night temperature, while the NDVI was used as a proxy
for soil moisture (Sandholt et al., 2002). Finally, LST and NDVI
values were log-transformed to improve normality and to stabilize
the variance (Sokal & Rohlf, 1995).
Fasciola hepatica risk index
The calculation of fluke infection risk was carried out using the
index developed by Malone et al.(1998), based on growing
degree-day (GDD) and using climatic factors that impact the
F.hepatica life cycle:
Index =[GDD ×days in the month,IF R–PET ×0:8()
.0+GDD ×RD()
R–PET()
25
,IFR–PET .0]
where GDD is the average monthly mean temperature –10°C
(MOD11C3); Ris the total monthly rainfall (mm/month,
TRMM 3B43); PET is the potential evapotranspiration as calcu-
lated by the Penman method (mm/month); and RD is the number
of rain days per month with more than 1 mm of rainfall
(GPM_3IMERG-Day 0.1° × 0.1°). Four risk categories were
described by Yilma & Malone (1998) to classify the calculated
risk index values: (1) no-risk: ≤600; (2) low risk: 601–1500; (3)
moderate risk: 1501–3000; and (4) high risk: >3000.
Statistical analysis
Data were analysed using the software IBM SPSS 25 for
Windows (SPSS Inc., Chicago, IL, USA). To complete the
most comprehensive study of the variability in exposure to
F.hepatica over time, we compiled datasets for both wet/dry sea-
sons and temperate-climate seasons (spring, summer, autumn
and winter). A chi-square test was used for comparison of the
prevalence between seasons, and a univariable generalized esti-
mating equation (GEE) analysis was used to identify variables
with significant associations between seasonal prevalence of
positive cattle for F.hepatica. Abattoir data on liver inspection
as a repeated measure, a binomial distribution and logit as the
link function was specified. Furthermore, a multivariable GEE
model was constructed using parasite infection as a dependent
variable and monthly rainfall (wet/dry), LST day, LST night,
NDVI, season (spring, summer, autumn and winter) and
climate region (temperate/tropical) data as independent vari-
ables. The results are expressed as odds ratios (ORs), with 95%
confidence intervals (95% CIs).
Results
Prevalence of condemned livers
In total, we inspected the livers of 6834 cattle –1861 from
Zacatlán district, 1735 from Teziutlán district and 3238 from
Ciudad Alemán district (table 1). The overall prevalence of F.hep-
atica infection was 20.6% (n= 1407); the highest rate of condem-
nations was found in animals from Ciudad Alemán (26.0%; CI:
24.09–27.86), followed by Zacatlán (17.5%; CI: 14.78–20.29) and
Teziutlán (13.2%; CI: 12.27–14.07).
Climate and environmental data
The elevation above sea level, Köppen climate classification and
the risk index of the abattoir for each site were as follows:
Zacatlán district: 2028 m, temperate climate and 632; Teziutlán
district: 1890 m, temperate climate and 440; and Ciudad
Alemán district: 24 m, tropical climate and 1082. A graphical
representation of the prevalence of F.hepatica in slaughtered cat-
tle compared to climate and environmental factors is shown in
supplementary fig. S1.
2 K. Hernández‐Guzmán et al.
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Fig. 1. Map of Mexico in the Köppen climate classification system showing the slaughterhouse locations in the districts of Zacatlán, Teziutlán and Ciudad Alemán.
Journal of Helminthology 3
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Seasonal prevalence of F. hepatica
To investigate the seasonality of F.hepatica during the wet and
dry seasons for each slaughterhouse, we tabulated the percentage
of condemned livers (table 2). The highest average prevalence for
all abattoirs was detected in the wet season (24.1%), whereas the
lowest prevalence was observed in the dry season (17.6%). Overall,
there was a significant difference between the wet and dry seasons
(P= 0.019). The wet season in Zacatlán and Teziutlán is the four-
month period from June through September, while the dry season
lasts from October through May. For the tropical climate in the
Ciudad Alemán district, the wet season extends from May to
November and the dry season stretches from December to
April. The highest percentages of prevalence during the study per-
iod were found in the wet (28.4%) and dry (22.8%, P= 0.022) sea-
sons from Ciudad Alemán district, with a tropical climate, low
altitude and low risk category. The lowest estimated prevalence
of condemned livers was observed in Teziutlán district, which
has a temperate climate, high altitude and a no-risk classification.
The lowest percentage of livers condemned for liver flukes
occurred in winter (16.8%), while the highest percentage was
found in summer (23.7%, table 3). A significant difference
between seasons and districts was also observed (P< 0.05). The
greatest numbers of condemned livers were reported from
Ciudad Alemán district, which showed the highest prevalence
(29.9%) in the study. Statistically significant differences were
found in Zacatlán and Ciudad Alemán districts between seasons
(P< 0.05).
GEEs
The univariable GEE analysis of condemned livers at slaughter
over time is outlined in supplementary table S1. Supplementary
table S2 presents the significant differences between seasons
(spring, summer, autumn and winter) and between the wet and
dry seasons. The results of the multivariable GEE analyses are pre-
sented in table 4. Among confirmed fasciolosis cases in the abat-
toirs, temperate vs. tropical climate regions (OR 266.59; 95% CI:
241.90–353.34) and wet vs. dry season (OR 25.56; 95% CI: 20.56–
55.67) were all strongly associated with increased odds of con-
demned livers.
Discussion
The present study is the first to determine the seasonal prevalence
of bovine fasciolosis with different climate regions, elevations and
risk factors in Mexico through the inspection of livers, as well as
the first study to link the presence of this disease to climate and
environmental factors. The percentages of prevalence of con-
demned livers in Zacatlán and Teziutlán districts with temperate
climate ranged from 13.2% to 17.5%, similar to the range in
prevalence reported in Brazil (10.14–18.66%) (Dutra et al.,
2010) but higher than those observed in Portugal (2.2%)
(Barbosa et al., 2019) and lower than those reported in Brazil
(37.6%), Algeria (26.7%), Portugal and Spain (28%), Uruguay
(33.9%) and Peru (55.72%) (Arias et al., 2011; Ouchene-Khelifi
et al., 2018; Quevedo et al., 2018; da Costa et al., 2019;
Arias-Pacheco et al., 2020). This study shows that the prevalence
of F.hepatica in the tropical climate was 26.0%, which is consist-
ent with the prevalence (25.8%) reported in cross-sectional sur-
veys in tropical climates in Mexico (Ojeda-Robertos et al.,
2020), although it is higher than the prevalence found in Costa
Table 1. Monthly prevalence of Fasciola in the livers of slaughtered cattle during the year 2017 in three abattoirs in the states of Puebla and Veracruz.
Month
Puebla state Veracruz state
Zacatlán district Teziutlán district Ciudad Alemán district
No. of animals
slaughtered
No. of livers
condemned
Prevalence
(%)
No. of animals
slaughtered
No. of livers
condemned
Prevalence
(%)
No. of animals
slaughtered
No. of livers
condemned
Prevalence
(%)
Jan 148 17 11.5 135 14 10.4 212 48 22.6
Feb 149 18 12.1 137 15 10.9 239 55 23.0
Mar 162 24 14.8 139 17 12.2 243 55 22.6
Apr 152 18 11.8 140 17 12.1 195 42 21.5
May 154 22 14.3 141 18 12.8 241 63 26.1
Jun 155 26 16.8 142 21 14.8 256 73 28.5
Jul 148 31 20.9 135 20 14.8 274 76 27.7
Aug 154 28 18.2 132 19 14.4 320 97 30.3
Sep 156 29 18.6 144 22 15.3 315 99 31.4
Oct 160 37 23.1 160 21 13.1 248 68 27.4
Nov 165 40 24.2 162 22 13.6 340 90 26.5
Dec 158 38 24.1 168 23 13.7 355 84 23.7
Total 1861 328 17.5 1735 229 13.2 3238 850 26.0
4 K. Hernández‐Guzmán et al.
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Rica (1.83%) (Rojas & Cartín, 2016). Therefore, climate and
environmental variables, the livestock system and general man-
agement factors –such as the length of the grazing season and
the proportion of grazed grass in the diet –are important consid-
erations in the prevalence of condemned livers and for comparing
results across studies and countries. For instance, in Switzerland,
Rapsch et al.(2006) estimate the true prevalence of F.hepatica in
slaughtered cattle at 18.0%; the high diagnostic sensitivity was
found using coproscopy, bile examination and antibody ELISA
rather than condemned livers, resulting in a lower prevalence.
One of the limitations of the present study was the failure to
obtain faeces and serum samples due to financial, technical and
political reasons.
This study shows that the prevalence of F.hepatica at altitudes
higher than 1800 m above sea level in Puebla (which has a tem-
perate climate) ranges from 13.2% to 17.5%, which is lower
than the prevalence in Peru (55.4% and 55.72% at 3300 m and
3350 m above sea level, respectively) (Arias-Pacheco et al., 2020;
Caravedo et al., 2021). Our survey also shows that the prevalence
of this parasite in the tropical climate (24 m above sea level) was
26.0% –higher than that reported in Cuba (18.27%) –with an
altitude of 122 m above sea level (Palacio Collado et al., 2017).
In addition, Malone et al.(1998) report that the optimum thermal
conditions in tropical sites for the development of F.hepatica are
found in lower-elevation areas, providing an example of previous
studies that have reported a significant relationship between eleva-
tion and parasite infection risk (Dutra et al., 2010; Martins et al.,
2012; Villa-Mancera & Reynoso-Palomar, 2019a,b).
In this study, the wet and dry seasons had a significant influ-
ence on the bovine fasciolosis occurrence in the tropical climate
(in Veracruz); the prevalence rate was greater during the wet sea-
son (28.4%) than in the dry season (22.8%). These results align
with those of a study by Bernardo et al.(2011), who report a
higher rate of fasciolosis cases in cattle slaughtered during the
dry season (25.79%) and a lower rate in the wet season
(23.87%) in Brazil. Again, this is consistent with previous reports
from Tabasco, Mexico indicating a prevalence of between 9.36%
and 8.34% during the wet and dry seasons, respectively
(Ojeda-Robertos et al., 2020). A high condemnation rate in the
wet season is likely due to increased populations of infected snails
in grazing pastures and humid microhabitats that enhance the
survival of the infective metacercariae, as well as the lack of meta-
cercariae exposure during the dry season. Villa-Mancera et al.
(2019b) propose seven specific factors that serve as significant
predictors of parasite infection, based on the detection of F.
hepatica-specific antibody levels in bulk-tank milk samples: rain-
fall, elevation, the proportion of grazed grass in the diet, contact
with other herds, herd size, parasite control use and education
levels.
No significant difference in the prevalence of condemned
livers was found between the wet and dry seasons in a temperate
climate at altitudes of 1890 m and 2028 m. Consequently, the
findings in this study are similar to those of another study con-
ducted in Peru, in which prevalence rates of 56.3% and 53.9%
in the wet and dry seasons were found, at 3300 m above sea
level (Arias-Pacheco et al., 2020). Persistent infection throughout
the year may result from continued exposure of the cattle to
encysted metacercariae in grazing pastures.
In our study, the highest seasonal prevalence of Fasciola infec-
tion in the tropical climate was observed in summer (29.9%), fol-
lowed by autumn (25.7%), spring (25.7%) and winter (22.8%).
These results are similar to those reported in Brazil (Bernardo
et al., 2011) and show significant seasonal pattern for fasciolosis
infection in livers in Zacatlán district, which have temperate cli-
mates. Furthermore, these results are similar to those reported
in Algeria, where the prevalence was significantly different for
all seasons (Ouchene-Khelifi et al., 2018). However, this finding
contrasts with that of a study in Greece reporting that infection
prevalence was not significantly different for all seasons
(Theodoropoulos et al., 2002).
We used a GEE approach to construct a multivariable model,
showing that six variables were significantly associated with para-
site infection: rainfall (wet/dry), LST day, LST night, NDVI, sea-
son and climate region (temperate/tropical) (table 4). Climate
region was clearly one of the most significant factors in F.hepatica
infection in cattle; tropical climates present a 266.59-times higher
risk of infection in slaughtered animals than a temperate climate
(95% CI: 241.90–353.34). Similar odds were observed with LST
day (OR 11.18; 95% CI: 10.98–42.09) and LST night (OR 11.20;
95% CI: 11.00–42.11). Our results are reinforced by the fact that
several researchers have found that temperature is a positive pre-
dictor of infection in Ireland, England and Wales, and Mexico
(McCann et al., 2010; Selemetas & de Waal, 2015;
Villa-Mancera & Reynoso-Palomar, 2019b). However, this
finding contrasts with previous studies in Brazil that have
reported no significant differences in prevalence based on tem-
perature (Dutra et al., 2010). Cattle slaughtered in the wet season
had 25.56-times higher liver fluke infection rates than those
Table 2. Significant differences between the wet and dry seasons in the number and prevalence of condemned livers due to F.hepatica infections at three Mexican
abattoirs.
State/district
Wet season Dry season
No. of animals
slaughtered
No. of livers
condemned
Prevalence
(%)
No. of animals
slaughtered
No. of livers
condemned
Prevalence
(%) P
Puebla
Zacatlán 613 114 18.6
a
1248 214 17.1
c
0.739
Teziutlán 553 82 14.8
a
1182 147 12.4
c
0.250
Veracruz
Ciudad Alemán 1994 566 28.4
b
1244 284 22.8
d
0.022
Total 3160 762 24.1 3674 645 17.6 0.019
Rainy season:
a
June–September,
b
May–November; dry season:
c
October–May,
d
December–April.
Journal of Helminthology 5
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slaughtered in the dry season (95% CI: 20.56–55.67).
Furthermore, rainfall has been found to have a consistent relation-
ship with prevalence based on data on fasciolosis in Belgium,
England and Wales, and Mexico (McCann et al., 2010;
Bennema et al., 2011; Villa-Mancera & Reynoso-Palomar,
2019a). In China, temperature, rainfall and elevation have been
associated with F.hepatica infestation (Qin et al., 2016).
Temperatures greater than 10°C are required for the development
of the free-living larval stages and intra-snail stages of the trema-
tode, as well as the development of the parasite’s intermediate
molluscan (Andrews et al., 1999; Torgerson & Claxton, 1999).
In Mexico, for the life cycle to be complete, Lymnaea humilis
and Lymnaea bulimoides must be frequently present, appearing
during or immediately after rainfall peaks (Cruz-Mendoza et al.,
2011). The NDVI includes several factors (land cover, tempera-
ture, rainfall and vapour pressure) that have been identified as
positive predictors of disease in Australia (Durr et al., 2005).
However, there are also negative aspects to our approach. For
example, our study is limited to using data from one or two
slaughterhouses for each climatic region. While our study reports
ranges in prevalence similar to those in other studies, more accur-
ate and robust outputs may be obtained by using existing data on
liver condemnation in slaughterhouses throughout all of Mexico.
In conclusion, this is the first study to provide epidemiological
data on the seasonal prevalence of fasciolosis in cattle slaughter-
houses from different climate regions in two states of Mexico,
demonstrating that the overall prevalence of F.hepatica was
20.6%. Moreover, our study examines and compares seasonal
data with regards to climate and environmental factors, and it
highlights the importance of continuous monitoring programmes
for liver fluke infection. Lastly, we identify some of the factors
associated with the prevalence of condemned livers, including
rainfall, LST, NDVI, season and climate region. Further studies
are necessary to generate more knowledge on shifts in levels of
exposure between years and climatic regions.
Supplementary material. To view supplementary material for this article,
please visit https://doi.org/10.1017/S0022149X21000444
Financial support. This study was supported by Benemérita Universidad
Autónoma de Puebla (VIEP-VIMA-NAT-18-I) and PRODEP (Programa
para el Desarrollo Profesional Docente para el Tipo Superior), Folio
UIEP-CA-6-ID-31483.
Table 3. Seasonal prevalence of bovine fasciolosis in three slaughterhouses in the states of Puebla and Veracruz.
State/district
Spring Summer Autumn Winter
Slaughtered/
condemned Prevalence (%)
Slaughtered/
condemned Prevalence (%)
Slaughtered/
condemned Prevalence (%)
Slaughtered/
condemned Prevalence (%)
Puebla
Zacatlán
a
461/66 14.3 458/88 19.2 483/115 23.8 459/59 12.9
Teziutlán 423/56 13.2 411/61 14.8 490/66 13.5 411/46 11.2
Veracruz
Ciudad Alemán
a
692/178 25.7 909/272 29.9 943/242 25.7 694/158 22.8
Total
a
1576/300 19.0 1778/421 23.7 1916/423 22.1 1564/263 16.8
a
Prevalence of F.hepatica is significantly different (P< 0.05, chi-square test).
Table 4. Significant associations between prevalence of condemned livers at
three Mexican slaughter and seasonal, climate and environmental variables,
using multivariable GEE analysis.
Variable
Odds
ratio
Confidence
interval (95%) P-value
Intercept <0.001
Annual rainfall
Wet vs. dry 25.56 20.56, 55.67 <0.001
LST day 11.18 10.98, 42.09 <0.001
LST night 11.20 11.00, 42.11 <0.001
NDVI 11.54 11.40, 42.50 <0.001
Seasonal 5.86 3.06, 57.43 0.015
Climate regions
Temperate vs. tropical 266.59 241.90, 353.34 <0.001
6 K. Hernández‐Guzmán et al.
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Conflicts of interest. None.
Ethical standards. This study was approved by the local Animal Care and
Ethics Committee of the Meritorious Autonomous University of Puebla, and
all procedures complied with the National Legislation Pertaining to Animal
Health Research.
Author contributions. Conceptualization, methodology, funding acquisi-
tion, project administration, supervision, writing –review and editing: K.H.
and P.M. Investigation, supervision, formal analysis: J.O. Conceptualization,
methodology, writing –review and editing: Y.A. Supervision, data analysis,
writing –original draft: A.O. and A.C. Analysis tools, writing –review and
editing: A.V. All authors read and approved the final manuscript.
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