eISSN: 2256-2958 Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):113–121
https://doi.org/10.17533/udea.rccp.v37n3a1
© 2024 Universidad de Antioquia. Publicado por Universidad de Antioquia, Colombia.
SHORT COMMUNICATION
Relationship between number of adult rumen fluke (Calicophoron
microbothrioides) and eggs per gram of feces in culled dairy cattle in
Peru: A pilot study
Relación entre número de adultos de trematodos del rumen (Calicophoron microbothrioides) y huevos
por gramo de heces en ganado lechero sacrificado en Perú: Estudio piloto
Relação entre o número de vermes adultos no rúmen (Calicophoron microbothrioides) e ovos por grama
de fezes em bovinos leiteiros abatidos no Peru: Estudo piloto
José F Coronado1 ; Teófilo Torrel-Pajares2 ; Luis Vargas-Rocha2,3* .
1Departamento de Ciencias Veterinarias, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av. Atahualpa 1050, 06003 Cajamarca, Peru.
2Laboratorio de Parasitología Veterinaria y Enfermedades Parasitarias, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Peru.
3Círculo de Estudios e Investigación en Ciencias Veterinarias - CEICIVET, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Peru.
To cite this article:
Coronado JF, Torrel-Pajares T, Vargas-Rocha L. Relationship between number of adult rumen fluke (Calicophoron microbothrioides)
and eggs per gram of feces in culled dairy cattle in Peru: A pilot study. Rev Colomb Cienc Pecu 2024; 37(2):113–121. https://doi.
org/10.17533/udea.rccp.v37n3a1
Abstract
Background: Paramphistomosis, a parasitic condition caused by Calicophoron microbothrioides in domestic
ruminants, has garnered limited attention among cattle breeders in the Cajamarca Valley, Peru. Despite its status as
an endemic affliction with considerable risk, scant investigations have been conducted on this parasite within this
region. Objective: This study aimed to assess the correlation between the population of adult parasites (referred to as
“number of adult parasites” or NAP) in rumen and reticulum of naturally infected cows and the number of eggs per gram
of feces (EPG). Methods: A sample of twenty-two cattle harboring adult parasites in their rumen and reticulum was
selected for analysis. Fecal samples were collected from these animals to establish a correlation between NAP and EPG.
Data analysis included linear regression, the Shapiro-Wilk normality test, and the nonparametric Mann-Whitney test.
Received: June 14, 2023. Accepted: September 30, 2023
*Corresponding author. Av. Atahualpa Nº 1050. Facultad de Ciencias Veterinarias - Campus UNC. CEP 060003. Cajamarca, Peru:
E-mail: lvargasr17_1@unc.edu.pe
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License, which permits unrestricted reuse,
distribution, and reproduction in any medium, provided the original work is properly cited.

Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):113–121114
https://doi.org/10.17533/udea.rccp.v37n3a1Number of rumen fluke vs eggs per gram of feces
Results: The study revealed a remarkably strong and directly proportional association between the number of adult parasites
in rumen and reticulum and the coproparazitologic EPG (r = 0.971). Conclusion: According to the linear model (NAP = 60.381
± 3.37; EPG - 22.979) increasing EPG by one lead to an increase by 60 NAP in rumen and reticulum (p<0.01).
Keywords: bovines; Calicophoron microbothrioides; cattle; diagnosis; eggs; epidemiology; feces; paramphistomosis;
parasite load; ruminants; rumen fluke; trematodes.
Resumen
Antecedentes: La paramphistomosis, afección parasitaria causada por Calicophoron microbothrioides en rumiantes
domésticos, ha despertado poco interés entre los ganaderos del valle de Cajamarca, Perú. A pesar de su condición de afección
endémica con riesgo considerable, se han realizado escasas investigaciones sobre este parásito en esta región geográfica.Objetivo:
El presente estudio tuvo como objetivo evaluar la correlación entre la población de parásitos adultos (denominada "número de
parásitos adultos" o NPA) en rumen y retículo de vacas naturalmente infectadas, en relación con la cantidad de huevos por gramo
de heces (HPG). Métodos: Para el análisis se seleccionó una muestra de veintidós bovinos que albergaban parásitos adultos
en rumen y retículo. Se recogieron muestras fecales de estos animales para establecer una correlación entre la población de
parásitos adultos y la HPG. Los datos se analizaron mediante regresión lineal, prueba de normalidad de Shapiro-Wilk, y prueba
no paramétrica de Mann-Whitney. Resultados: El estudio reveló una asociación notablemente fuerte y directamente proporcional
entre la población de parásitos adultos, tanto en el rumen como en el retículo, y la HPG determinada mediante coproparasitología
(r = 0,971). Conclusiones: El modelo lineal (NAP = 60,381 ± 3,37; HPG - 22,979) indica que cada unidad de incremento del HPG
se corresponde con un aumento de 60 en el NPA en rumen y reticulo (p<0,01).
Palabras clave: bovinos; Calicophoron microbothrioides; carga parasitaria; diagnóstico; epidemiología; ganado; huevos;
heces; paramphistomosis; rumiantes; trematodos; trematodo del rumen.
Resumo
Antecedentes: A paramfistomose, uma condição parasitária causada por Calicophoron microbothrioides em ruminantes
domésticos, tem recebido atenção limitada entre os criadores de gado no Vale de Cajamarca, Peru. Apesar de ser uma aflição
endêmica com considerável risco, investigações escassas foram conduzidas sobre esse parasita nessa região geográfica. Objetivo:
Este estudo teve como objetivo avaliar a correlação entre a população de parasitas adultos (referida como "número de parasitas
adultos" ou NAP) no rúmen e no retículo de vacas naturalmente infectadas, em relação à quantidade de ovos por grama de fezes
(OPG). Métodos: Uma amostra de vinte e dois bovinos portando parasitas adultos em seus rúmens e retículos foi selecionada
para análise. Amostras fecais foram coletadas desses animais para estabelecer uma correlação entre a população de parasitas
adultos e OPG. A análise dos dados envolveu a aplicação de regressão linear, o teste de normalidade de Shapiro-Wilk e o teste
não paramétrico de Mann-Whitney. Resultados: O estudo revelou uma associação notavelmente forte e diretamente proporcional
entre a população de parasitas adultos tanto no rúmen quanto no retículo, e o OPG determinado por meio da coproparasitologia (r
= 0,971). Conclusões: O modelo linear (NAP = 60,381 ± 3,37; OPG - 22,979) indica que, com o aumento de um OPG, o NAP no
rúmen e retículo aumenta em 60 (p<0,01).
Palavras-chave: bovinos; Calicophoron microbothrioides; carga parasitária; diagnóstico; epidemiologia; feze; gado;
ovos; paramfistomose; ruminantes; trematódeos; verme do rúmen.

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Introduction
Paramphistomosis is caused by rumen
trematodes belonging to the family
Paramphistomidae (Trematoda: Digenea;
Eduardo, 1983). These trematodes affect all
types of ruminants around the world, including
domestic animals (Ferreras et al., 2014; Ma et
al., 2015; Cauquil et al., 2016), South American
camelids (Millar et al., 2017), as well as wild
and feral ruminants (Munang'andu et al., 2012;
Pfukenyi et al., 2018). These parasites use a
freshwater snail as an intermediate host, and
animals become infected upon ingestion of
encysted metacercariae present in their feed or
water (Fenemore et al., 2021).
Regarding the lesions caused by these
trematodes, variable outcomes are observed.
For instance, Calicophoron daubneyi does not
induce significant macroscopic pathologies in
the rumen or reticulum, nor does it consistently
trigger acute or chronic inflammatory changes
in the duodenum (Busin et al., 2023). On the
other hand, in cases of acute parasitosis caused
by C. daubneyi, the migration process during
the juvenile phase from the small duodenum to
the abomasum and rumen leads to pathological
disorders, primarily characterized by enteritis,
diarrhea, anemia with elevated morbidity, as
well as emaciation and cachexia. Among the
most susceptible are young ruminants in cases
of extensive infections (O'Shaughnessy et al.,
2018). The attachment of adult C. daubneyi to
the ruminal and reticular epithelium results in
the detachment of ruminal papillae, ultimately
causing local inflammation, fibrotic alterations,
and the emergence of darkened areas (Fuertes et
al., 2015).
The parasitological technique involving
observation of eggs in fecal sedimentation
remains the sole viable approach for diagnosing
rumen trematodes in live animals under field
conditions. However, it is limited to identifying
only patent infections (Sargison et al., 2016). The
detection of immature and adult trematodes can be
accomplished through post mortem examinations
of the reticulum and rumen (Toolan et al., 2015;
Cauquil et al., 2016). While a coproantigen-based
ELISA prototype has been developed (Huson et
al., 2021), its utility is not universally accessible
across all geographical regions.
Presently, the Cajamarca Valley stands
as an endemic region for paramphistomosis,
a condition attributed to Calicophoron
microbothrioides -which has been molecularly
identified in cattle (Manrique et al., 2013). In
addition to the Cajamarca Valley, this parasite
has also been detected in various districts within
Cajamarca. It has been found in cattle -with
prevalence ranging from 5.8 ± 2.4 to 38.5 ±
5.5% in coproparasitological diagnoses (Torrel
et al., 2023)- as well as in sheep -with 4.92%
prevalence from 386 post mortem animals
(Torrel-Pajares et al., 2022). Despite the high
presence of this parasite, several knowledge gaps
persist due to its relatively recent emergence and
limited research attention.
Given these circumstances, the present study
aimed to establish a correlation between adult C.
microbothrioides located in rumen-reticulum and
the number of eggs per gram of feces in naturally
infected slaughtered cattle. The main objective
was to acquire a deeper comprehension of the
parasite load and to establish the capacity to
forecast the estimated count of adult parasites using
coprological analysis within field conditions. This
endeavor is intended to provide a foundational
framework for subsequent investigations aimed
at appraising the effectiveness of antiparasitic
medications by considering parameters such as
egg counts, parasite burden, and potential clinical
manifestations.
Materials and Methods
Ethical considerations
Samples were initially obtained from live
animals and, subsequently, from the same animals
during post-slaughter -carried out at the Camal
Municipal de Cajamarca. This slaughterhouse
operates under the regulatory framework of
Reglamento Sanitario del Faenado de Animales
de Abasto del Perú (D.S. N° 015-2012-AG).

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in labeled polyethylene bags. Subsequently,
these contents were sifted by incorporating
clean water through a metal mesh with 0.5 cm2
opening between threads. This process facilitated
separation of free adult parasites, which remained
on the sieve.
Concurrently, a thorough examination of
rumen and reticular mucosa of the animals was
conducted. Parasites adhering to the mucosa
were precisely detached using surgical forceps
and subsequently placed into a glass container.
These collected parasites were transported to
the laboratory for in-depth enumeration and
assessment.
Statistical analysis
Statistical analyses were conducted using
SPSS Statistics 25.0 (IBM Corp. Armonk, NY,
USA). Initially, a linear regression analysis was
conducted to establish the relationship between
egg count and the count of adult parasites. This
analysis was accompanied by its corresponding
analysis of variance. Furthermore, normality of
all variables under investigation was assessed
with the Shapiro-Wilk statistical test.
Variables demonstrating normal distribution
underwent a completely randomized analysis of
variance using the model Yij = μ + τi + ξij, where
Yij represents the observed data, μ denotes the
overall mean, τi signifies the treatment effect,
and ξij symbolizes the error term associated with
each observation.
Regarding correlation between EPG and
count of adult C. microbothrioides, along with
the presentation of data through Whisker Box
plots, the nonparametric Mann-Whitney test was
used to assess statistical significance.
Results
Figure 1 displays the adult parasites of C.
microbothrioides affixed to the rumen, as well
as a depiction of a characteristic egg from this
trematode.
Location and sample size estimation
The study took place in the city of Cajamarca,
Peru. Guided by a prior investigation by
Torrel (2009), the sample size was established
considering a population of 30 animals already
confirmed as positive for Calicophoron
microbothrioides. Consideing an α = 0.01
significance level, a sample size of 22 positive
cattle from various age groups, breeds, and both
genders was defined.
Sampling and sample processing
To establish a correlation between the
recorded number of adult parasites (NAP) in
the rumen and reticulum and the number of
eggs per gram of feces (EPG), samples were
procured from 22 cattle confirmed as positive for
Paramphistomidae. These cattle were subjected
to slaughter at Camal Municipal de Cajamarca.
The animals were identified one day prior to
slaughter, and fecal samples (approximately 100
g) were directly collected from the rectum using
veterinary obstetric gloves.
Collected samples were then placed
in polyethylene bags, each labeled with
the corresponding animal identification
and sequential numbers. These bags were
subsequently deposited into an expanded
polystyrene container for safe transportation
to Laboratorio de Parasitología Veterinaria of
Facultad de Ciencias Veterinarias at Universidad
Nacional de Cajamarca (Peru). Once there, the
samples underwent thorough analysis using the
Natural Sedimentation technique (Foreyt et al.,
2001) for egg detection and EPG count.
Fecal samples from animals in which adult
paramphistomids were not detected in rumen
and reticulum during post mortem examination
were excluded from the study. In addition,
fecal samples from animals displaying Fasciola
hepatica in their bile ducts during post mortem
liver inspection were also eliminated from
consideration.
Through macroscopic observation, the contents
of positive rumen and reticulum were gathered

117Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):113–121
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The most frequently occurring (mode) EPG
value was 150, while for NAP, it was 9500. Half
of the cattle (n = 11) displayed EPG levels below
the median of 106 and NAP levels of 5810 in their
rumen and reticulum. Conversely, the highest
quantity of EPG and NAP were observed in the
first quartile, spanning from 4 to 8.75 (with a range
of 4.75 for EPG) and 235 to 646.25 (with a range
of 411.25 for NAP), respectively. Additionally,
the third quartile showcased EPG values ranging
from 106 to 156.25 (a range 50.25 for EPG), and
NAP ranging from 5810 to 9500 (with a range of
3690 for NAP). These findings indicate reduced
variability within the first quartile (Table 1 and
Figure 2).
Figure 1. Adult Calicophoron microbothrioides within the rumen 1.6X (1) and egg with 40X view (2).
Table 1. Eggs per gram (EPG) of feces and number
of adult Calicophoron microbothrioides (NAP) in
rumen and reticulum.
Parameter EPG NAP
Mean 95.77 5,759.86
Median 106.00 5,810.00
Mode 150.00 9,500.00
Standard deviation 77.947 4,848.09
Range 213.00 15,285.00
Minimum 4.00 235.00
Maximum 217.00 15,520.00
Percentiles
25 8.75 646.25
50 106.00 5,810.00
75 156.25 9,500.00
Figure 2. Box-and-whisker plot illustrating estimated eggs per gram (EPG; 1) and number of adult Calicophoron
microbothrioides (NAP; 2) in rumen and reticulum showing lower dispersion in the first quartile.

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Linear model validation for establishing
relationship between EPG and NAP
To ascertain the reliability of the model,
regression analysis was used. The linear model
generated the following equation: NAP = 60.381
EPG - 22.979. Statistical significance was
confirmed with p<0.01. The correlation coefficient
(r) was computed to be 0.971, demonstrating a
strong and positive relationship. Furthermore, the
coefficient of determination (R²) was determined
to be 0.939 (corrected).
Within the linear model, the significance
of the coefficient (-22.979) was evaluated
and found to be non-significant (p>0.05). The
estimated coefficient for EPG was 60.381 with
a 95% confidence interval of ±3.337. This result
is particularly noteworthy; for each additional
gram of eggs per gram of feces, the parasite count
increases by approximately 60.381 (equivalent
to 60 parasites). This coefficient was highly
significant (p<0.0001), meaning that it is distinct
from zero and thereby confirming the validation of
the model. The correlation coefficient (r = 0.971)
underscores a robust and positive correlation
(p<0.01).
Normality of residuals. The evaluation of the
normal distribution of residuals was conducted
through graphical examination, as depicted in
Figure 3. Upon observation, it becomes evident
that the scatter plot of points closely aligns with
the reference straight line, indicating a strong fit
to the linear regression model. Consequently, it
is reasonable to affirm that the residuals exhibit a
normal distribution.
The equation’s analysis indicates absence of
autocorrelation among residuals, as evidenced
by the Durbin-Watson test result of DW =
1.806. In addition, coefficient of determination
(R2) within the linear equation signifies that
94.2% of the variability in adult parasites can
be elucidated by the number of eggs per gram
in fecal samples. Given the findings and the
establishment of optimal fitting linear equation,
the rationale for using linear equation in the
current study becomes evident.
Figure 3. Relationship between eggs per gram (EPG)
and number of adult Calicophoron microbothrioides
(NAP) of cattle infected with C. microbothrioides.
Where, R2: Coefficient of determination; r: Correlation;
p<0.01 (significance at 99%).
Discussion
The relationship found between NAP
in rumen-reticulum and EPG determined
through coproparasitology exhibited a strong
positive relationship (r = 0.971) that is directly
proportional. Specifically, the derived model
obtained (NAP = 60.381 ± 3.37; EPG -22.979)
demonstrates that for each increase in one
EPG, NAP in rumen-reticulum increases by 60.
This trend is similar to another study involving
Limousin bulls infected with Paramphistomum
daubneyi, where a direct proportional correlation
was identified: for every 1 to 12 paramphistomes,
the average EPG ranged from 7 to 15.
Furthermore, animals harboring an average of
215 (29 to 620) adult parasites displayed an
average EPG of 41.5 (Mage and Dorchies, 1998).
The findings from the present study surpass
those reported by Fuertes et al. (2015), who
recorded a total animal parasite burden of 19,487
adult C. daubneyi, with variations ranging from
8 to 8005 parasites per animal (median 144). In
a separate investigation, a significant correlation
was established between EPG count and adult
parasite burden, where an EPG count exceeding
100 indicated the presence of 100 adult C.
daubneyi in the rumen or reticulum; however,
their correlation between both variables was not
direct (Rieu et al., 2007). In other words, a higher
NAP

119Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):113–121
https://doi.org/10.17533/udea.rccp.v37n3a1Number of rumen fluke vs eggs per gram of feces
EPG count wouldn’t necessarily be obtained
even if the number of parasites in the rumen
increased. This phenomenon stems from the fact
that parasite overpopulation tends to decrease the
rate of egg laying (Horak, 1971). Contrastingly,
none of the various coproparasitological methods
currently available exhibit 100% sensitivity and
specificity (Rieu et al., 2007; Malrait et al., 2015).
To the authors' best knowledge, no studies
have been conducted on cattle, sheep, or other
ruminants in Peru concerning rumen fluke and their
correlation to EPG. The greater quantity of eggs
detected in heavily infected cattle could be linked
to intrinsic host variability, where progression
of parasitic infection can manifest as slow or
rapid due to varying immunological resistance
of the animal. Such resistance is influenced by
factors such as age, reinfection, and nutritional
status (Atcheson et al., 2020; Hajipour et al.,
2021; Torrel-Pajares et al., 2022). Discrepancies
between these findings and those of other
researchers might be attributed to specific parasitic
load stemming from site-specific conditions, such
as pasture attributes (including the abundance
of infected intermediate hosts), seasonal and
climatic variations, and characteristics of surface
water and soil. Additionally, the age of the
definitive host in relation to acquired immunity
might play a role. Further research is warranted
to ascertain the risk factors associated with
C. microbothrioides in the Cajamarca region.
Considering the objective and outcomes,
the correlation between NAP and eggs per
gram of feces was highly significant (r =
0.971; p<0.01). For each one EPG increase in
feces, the number of adult parasites in both the
rumen and reticulum increases by 60 (p<0.01).
Declarations
Acknowledgements
We want to acknowledge the administrator
of Camal Municipal de Cajamarca for providing
the facilities and collaboration to conduct this
study.
Funding
This study did not receive any specific grant
from funding agencies in the public, commercial,
or not-for-profit sectors.
Conflict of interest
The authors declare they have no financial
interests or personal relationships that could have
influenced the results presented in this article.
Author contributions
TTP and JFC conceptualized, designed the
methodology, supervised, and managed the
study. JFC executed and carried out field and
laboratory work. LV-R and JFC contributed to
software, validation, data curation and writing-
preparation of the original draft. All authors
collaborated in the visualization, writing-
revising and editing of the manuscript. All
authors approved the final manuscript and
accept responsibility for its content.
Use of artificial intelligence (AI)
No AI or AI-assisted technologies were used
during the preparation of this work.
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