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Factors affecting the prevalence of endoparasites in pre-weaning calves in a warm humid climate of Mexico

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24 mag 2025
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Introduction

Mexico ranks eighth in cattle production, with a territory of 196.4 million hectares, approximately 56 % of which is dedicated to livestock production (Parra-Bracamonte et al., 2020). The country has 1.1 million registered farms (SIAP, 2020) with the largest concentration of cattle fattening farms located in the southeast (Callejas-Juárez, 2024).

Although Mexico has a strong livestock vocation, several challenges hinder the profitable production of beef, including reproductive, nutritional, social, and health-related issues. Among these, parasitism is particularly significant in warm climates, where its main impact is on young animals. These animals are more susceptible to parasitic infections than older animals, which develop immunity after continuous or seasonal exposure (Palkumbura et al., 2024). The primary parasitic infections in ruminants include gastrointestinal nematodes (GIN), lungworms, and trematodes, such as liver and rumen flukes (Claerebout & Geldhof, 2020). Parasitic nematodes, in particular, affect livestock development predominantly in tropical and subtropical regions. The prevalence of GIN is influenced by the interplay between adaptability and environmental factors, including pasture quality and quantity, temperature, humidity, and the grazing behavior of the host (Datta et al., 2024). Parasitic infections result in both direct and indirect negative impacts, such as reduced production and reproduction, high treatment costs, and, in severe cases, animal mortality (Strydom et al., 2023). In female livestock rearing, GIN can impair the development and functionality of the reproductive system, delaying mating to 15 – 18 months of age. This delay affects 60 % – 70 % of females suitable for reproduction (Loyacano et al., 2002). Economically, GIN causes substantial losses in livestock farming world-wide. In Europe, studies estimate annual losses of €941 million in dairy cattle and €423 million in beef cattle, with 81 % of these costs attributed to production losses and 19 % to treatment costs (Ali et al., 2019). Similar studies conducted in Mexico estimate annual losses of approximately US $256 million due to GIN (Rodríguez-Vivas et al., 2017).

The primary method of controlling GIN has been the use of broad-spectrum anthelmintics, which were initially highly effective and had wide safety margins. Producers have relied heavily on these treatments to manage GIN (Rose-Vineer et al., 2020). However, excessive and inappropriate use has led to the development of anthelmintic resistance across major antiparasitic families (Libreros-Osorio et al., 2023). This issue is compounded by the fact that producers often apply anthelmintics without identifying the specific genera or species parasitizing the cattle. Prevalence studies are therefore essential to identify the primary internal parasites in a given region and guide management practices to reduce exposure to these parasites. The objective of this study was to investigate factors influencing the prevalence of internal parasites in pre-weaning calves in a warm, humid climate in Mexico.

Materials and methods
Study area and selection of cattle farms

The study was conducted in northern Chiapas, Teapa, Tabasco, and Escárcega, Campeche, Mexico. Samples were analyzed in the Animal Parasitology Laboratory of the Southeastern Regional University Unit (URUSSE) at the Autonomous University of Chapingo (UACh). The region's climate is warm and humid, with an average annual rainfall of 3,000 to 3,816 mm and an average temperature of 26°C (CONAGUA, 2021).

A total of twelve farms were visited, of which three were monitored monthly during the rainy season to determine gastrointestinal parasites in 2022 and only one farm in 2023. To determine the prevalence of nematodes and trematodes (Fasciola hepatica and paramphistomids), fecal samples were collected from three beef cattle farms in 2022, with monitoring conducted from May to August, but on the farm of Teapa, Tabasco, only nematodes were found. In 2023, one farm was monitored to gastrointestinal parasites from August to December. Additionally, six farms in Pueblo Nuevo, Chiapas were visited, and fecal samples were collected to determine trematodes. Two more farms in Escárcega, Campeche in November 2023 were included.

To know the population dynamics of nematodes. On one farm (DNT), a group of 28 suckling calves aged 1 to 2 months was selected and divided into two treatment groups, each with 14 animals. Treatment 1 involved natural infection with deworming. Anthelmintic treatment was administered three times during the study period using a commercial product containing triclabendazole, albendazole, and ivermectin at a dosage of 7.5 mg/kg of live weight. Treatment 2 consisted of naturally infected calves that did not receive anthelmintic treatment. Nine fecal samples were collected directly from each animal at 21-day intervals.

Collection and processing of fecal samples

Trematode eggs were identified using the methylene blue sedimentation technique. For this, 5 g of fecal sample was weighed and dissolved in running water in a 250-mL container. The sample was washed three times, allowing it to settle for 5 minutes between each wash. After the third wash, the volume was adjusted to 100 mL, and two drops of methylene blue were added. Using a Pasteur pipette, the reading chamber was filled and analyzed under an optical microscope at 4× magnification. The results were multiplied by four to calculate the total number of trematode EPG. Nematode and cestode eggs were identified through fecal flotation. For this procedure, 2 g of feces were weighed and macerated with 28 mL of saturated sodium chloride solution (density = 1.20). The mixture was used to fill the McMaster chamber using a Pasteur pipette, and the sample was examined under a compound optical microscope at 10× magnification. The EPG was calculated by multiplying the observed count by 50 (Thienpont et al., 2003). Fecal samples with the highest nematode egg counts were selected for coproculture. The samples were pooled and incubated for 7 days, allowing time for eggs to hatch and develop into infective larvae (L3). Humidity levels were monitored throughout the incubation period. The larvae were recovered using the Baermann apparatus.

Identification of helminth eggs and larvae

For L3 identification, some larvae were placed on a glass microscope slide and stained with Lugol's iodine to aid in visualization. In total, 100 larvae per sample were characterized and identified to estimate the proportion of each genus. Morphological identification was based on features such as the shape of the cranial extremity, the presence of refractile bodies (Cooperia spp.), and the length of the sheath tail extension (van Wyk & Mayhew, 2013). Genera such as Strongyloides were determined by egg morphology and were confirmed in larvae obtained by fecal culture. In the case of Trichuris, it was determined by egg morphology and the same for Toxocara. Dictyocaulus was determined in larvae using the sedimentation technique (Thienpont et al., 2003).

Estimation of prevalence

Using the data obtained from coprocultures and the identification of eggs observed during fecal examinations, the prevalence for each species or genus was determined. Prevalence was calculated using the following formula, and the results were expressed as percentages: Prevalence(%)=numberofparasitizedanimalsnumberofsampleanimals×100 Prevalence\,(\% ) = {{number\,of\,parasitized\,animals} \over {number\,of\,sample\,animals}} \times 100

Statistical analysis

The variables recorded were binomial type to determine the prevalence and discrete type in the fecal egg count (FEC), so for the analysis the variable was transformed to LOG (EPG+1) to reduce variance heterogeneity and approximate a normal distribution (Rodríguez et al., 2015) A repeated-measures model over time was analyzed using the SAS MIXED procedure (SAS, 2017), under the following model: Yijk=μ+ζi+δj(i)+Ψk+ζΨik+εijk {{\rm{Y}}_{{\rm{ijk}}}} = {\rm{\mu }} + {{\rm{\zeta }}_{\rm{i}}} + {{\rm{\delta }}_{{\rm{j}}({\rm{i}})}} + {{\rm{\Psi }}_{\rm{k}}} + {\rm{\zeta }}{{\rm{\Psi }}_{{\rm{ik}}}} + {{\rm{\varepsilon }}_{{\rm{ijk}}}} Yijk = response variable (Log EPG+1), μ = general mean, ζi = effect of the i-th treatment (i = dewormed, no deworming), δj(i) = random effect of individual within treatment, ψk = effect of k-th sampling (k= 1, 2,3,4,….9), ζψjk = interaction of treatment and sampling, and ɛijk ~ N (0, σ2e) = error associated with the individual.

Ethical Approval and/or Informed Consent

The study protocol No 24027-C-67 was approved by the General Directorate of Research and Postgraduate Studies of the Autonomous University of Chapingo. Following the Mexican official standard NOM-051-ZOO-1995 for humane treatment in the mobilization of animals.

Results
Prevalence of gastrointestinal parasites

The prevalence of F. hepatica in the study area, determined by the presence of eggs, was 12.03 % (77/640), while paramphistomids had a prevalence of 20.47 % (131/640). There was significant variation for both species by month and sampling (Table 1), with prevalence ranging from 0 % to 50 % for F. hepatica and from 0 % to 70.6 % for paramphistomids. The prevalence of F. hepatica was higher in adult cattle (17 %) than in pre-weaning calves under 8 months old (3 %). A similar trend was observed for paramphistomids, with a prevalence of 26 % in cows compared with 12 % in calves.

Prevalence of trematodes (Fasciola hepatica and paramphistomids) in cattle in southeastern Mexico in the samplings carried out during 2022 and 2023.

Farm and sampling date Physiological stage Fasciola hepatica Paramphistomids
Farm 1 DNA May-22 Lactating cows 25.8 % (8/31) 22.6 % (7/31)
Salto de Agua, Chiapas June-22 Lactating cows 50.0 % (13/26) 15.4 % (4/26)
August-22 Lactating cows 0.0 % (0/39) 41.0 % (16/39)
Farm 2 DRG May-22 Calves 0.0 % (0/17) 70.6 % (12/17)
Salto de Agua Chiapas June-22 Calves 0.0 % (0/17) 0.0 % (0/17)
August-22 Lactating cows 20.0 % (7/35) 48.6 % (17/35)
September-22 Lactating cows 0.0 % (0/11) 0.0 % (0/11)
Farm 4 DNT August-23 Calves 4.2 % (1/24) 0.0 % (0/24)
Salto de Agua, Chiapas September-23 Calves 4.0 % (2/50) 0.0 % (0/50)
October-23 Calves 9.8 % (4/41) 7.3 % (3/41)
November-23 Calves 0.0 % (0/25) 4.0 % (1/25)
December-23 Calves 4.2 % (1/24) 0.0 % (0/24)
Farm 5 Rita July-23 Lactating cows 28.6 % (4/14) 28.6 % (4/14)
Farm 6 Frank August-23 Lactating cows 3.4 % (1/29) 0.0 % (0/29)
Farm 7 JSalv September-23 Lactating cows 0.0 % (0/51) 2.0 % (1/51)
Farm 8 PNR2 October-23 Lactating cows 10.3 % (7/68) 13.2 % (9/68)
Farm 9 RNat November-23 Lactating cows 40.6 % (13/32) 56.3 % (18/32)
Farm 10 RNat2 November-23 Lactating cows 26.7 % (12/45) 35.6 % (16/45)
Farm 11 R1CM November-23 Lactating cows 10.0 % (3/30) 33.3 % (10/30)
Farm 12 R2CM November-23 Lactating cows 3.2 % (1/31) 41.9 % (13/31)

Total 12 % (77/640) 20.5 % (131/640)

Farms 5–10. Pueblo Nuevo, Chiapas. Farms 11–12. Escárcega, Campeche.

The prevalence of the family Trichostrongylidae exceeded 30 % in all months of the study except in June 2022, when it dropped to 16 %. The highest recorded prevalence reached 93 %, reflecting the significant presence of species such as Cooperia spp., Oesophagostomum spp., and Haemonchus spp., identified from larvae obtained in fecal cultures. Strongyloides spp. also showed high prevalence, particularly during the initial months of sampling when the calves were younger (Table 2). Other species, including Trichuris spp. and Toxocara spp., were identified sporadically through egg observation, while the prevalence of Dictyocaulus spp. was <17 %, determined from infective larvae. Additionally, the presence of coccidia oocysts varied widely between farms and sampling periods, reaching 54 % of animals during the final sampling. Rarely observed species included Moniezia spp. and Mammomonogamus spp., detected through egg identification.

Prevalence of the main genera of gastrointestinal parasites in cattle from the municipalities of Salto de Agua, Chiapas, and Teapa, Tabasco, Mexico.

Date Trichostrongylids¥ Strongyloides Trichuris Dictyocaulus Toxocara Coccidia
Farm 1 DNA May-22 66.7 73.3 - 6.7 - -
Salto de Agua, Chis. June-22 52.9 88.2 11.8 17.7 - 17.7
August-22 51.4 - - - - -
September-22 81.8 - 10.0 - - -
Farm 2 DRG May-22 76.7 26.7 6.5 3.2 6.5 25.8
Salto de Agua, Chis. June-22 16.0 - 3.9 - 23.1 3.9
August-22 36.8 2.6 2.6 - - -
Farm 3 GCh May-22 92.9 57.4 - - - -
Teapa, Tab. June-22 35.7 71.4 - - - 14.3
Farm 4 DNT June-23ψ 33.3 7.4 4.0 4.0 - 36.0
Salto de Agua, Chis. July-23 44.4 22.2 - 4.0 4.0 12.0
August-23 29.6 14.8 - 4.0 - 4.0
September-23 57.4 20.4 - - - -
October-23θ 63.0 3.7 4.0 - 4.0 -
November-23 63.0 - - - - -
December-23 70.4 3.7 - - - 54.0

Include Haemonchus, Cooperia, and Oesophagostomum.

Mammomonogamus spp.,

Moniezia sp.

Nematode FEC

The intensity of infection by trichostrongylids and Strongyloides spp. exhibited high variability among animals, as indicated by a high standard deviation. Consequently, the coefficients of variation exceeded 100 %. As the calves aged, the FECs decreased, particularly for Strongyloides spp. (Table 3).

Severity of infection by trichostrongylids and Strongyloides spp. in pre-weaning calves in the municipality of Salto de Agua.

Farms Month N Trichostrongylids¥ Strongyloides


Mean SD Mean SD
Farm 1 DNA May 31 216 240 71 210
June 26 29 87 2 10
August 39 46 94 0 0
Farm 2 DRG May 15 353 616 16,877 54,504
June 17 100 129 959 1566
August 46 92 122 0 0

Include Haemonchus, Cooperia, and Oesophagostomum

The FEC of nematodes in calves aged 2 to 8 months showed a decreasing trend (p < 0.05), although the FECs were similar between dewormed and non-dewormed animals (Fig. 1). At the beginning of the study, high EPG was found in some calves, so they were dewormed and formed the group that was dewormed three times during the study. At the age of 153 days, a high EPG was observed in the dewormed group compared to the group without anthelmintic treatment, but the differences were only numerical and not statistical (P>0.05), which implies that the animals generate resistance to nematodes gradually.

Fig. 1.

Fecal nematode egg counts during the study for two groups of calves (dewormed and non-dewormed) on farm 4 (DNT). One calf had a notably high count of 35,000 eggs per gram of feces (EPG), resulting in an average value of 3,690 EPG for the dewormed group.

The presence of Strongyloides spp. was identified based on egg morphology and confirmed through larvae obtained from fecal cultures. The prevalence of this species was notably high during the initial samplings in non-dewormed animals. However, starting at 6 months of age, the FEC of Strongyloides spp. decreased to <50 EPG in both groups (Fig. 2).

Fig. 2.

Fecal egg count trends of Strongyloides spp. throughout the study, categorized by treatment.

Effect of animal sex on nematode FEC

In farm 4, the mean nematode FEC (± SE) for females was 256 ± 49 EPG, while that for males was 591 ± 311 EPG. For Strongyloides spp., the mean FEC for females was 369 ± 256 EPG, what that for males was 590 ± 353 EPG. Although the effect of animal sex on parasite egg counts was not statistically significant (p > 0.05), females consistently showed lower FECs than males (Table 4).

Average fecal nematode egg count by treatment and sex of calves.

Treatment Sex EPG* Strongyloides
Deworming Female 193 376
Male 814 722
No deworming Female 316 246
Male 278 84

Eggs per gram of feces of trichostrongylids

Trematode FEC

The FECs of F. hepatica varied significantly between farms (Table 5) and samplings (p < 0.05) but showed no significant difference between the sexes of pre-weaning calves (p > 0.05). For paramphistomids, FEC differences were observed only between farms (p < 0.05), with no significant variation between samplings or between the sexes of the calves (p > 0.05).

Severity of Fasciola hepatica and paramphistomid infection in cattle in the municipality of Salto de Agua, Chiapas.

Fasciola hepatica
Paramphistomid
N Mean SE Rank Mean SE Rank
Farm DNA 96 3.9a 1.2 0 – 88 3.3a 1.0 0 – 60
Farm DRG 78 0.3b 0.1 0 – 4 1.0b 0.2 0 – 8
Sampling-May 46 3.5a 2.0 0 – 88 2.2a 1.2 0 – 52
Sampling-June 43 5.0ab 1.6 0 – 44 1.1a 0.8 0 – 32
Sampling-August 85 0.3b 0.1 0 – 4 2.8a 0.8 0 – 60
Females 66 2.2a 0.9 0 – 44 2.1a 0.6 0 – 32
Males 51 4.4a 2.0 0 – 88 1.4a 1.0 0 – 52

Different letters for each variable represent significant differences (p<0.05). SE: Standard error

Morphological identification of infective larvae

The predominant genus was Cooperia spp., accounting for approximately 80 % of the larvae identified, followed by Strongyloides spp. and Oesophagostomum spp. A high quantity of Trichostrongylus spp. was observed in only one month (Fig. 3).

Fig. 3.

Genera of gastrointestinal nematodes identified morphologically in the larval stage.

Discussion

Gastrointestinal parasites are a major cause of reduced weight gain in cattle and negatively impact overall health (Rose-Vineer, 2020). This condition is one of the most significant diseases globally because of the economic losses it causes. A key challenge in parasite control is the accurate identification of the etiological agent to implement specific control measures (Vande et al., 2018), as some anthelmintics target specific parasites. For example, oxy closanide is effective against paramphistomids (Sanabria et al., 2014). This study focuses on the prevalence of the main nematodes and trematodes in a warm, humid climate, where environmental conditions promote the proliferation of these parasites in cattle, buffaloes (Nurhidayah et al., 2020) and equids (Nielsen et al., 2007).

GIN species are predominantly found in mixed infections, as observed in this study. While the highest prevalence of nematodes was associated with the family Trichostrongylidae (Haemonchus spp., Cooperia spp., and Oesophagostomum spp.) and Strongyloides spp., eggs of Trichuris spp., Toxocara spp., and Mammomonogamus spp. were detected in smaller proportions. Additionally, Monezia spp. eggs, Dictyocaulus spp. larvae, and coccidia oocysts were also identified.

This study compared FEC dynamics over time, considering the age and sex of calves, as genetic factors in host resistance to gastrointestinal parasites significantly influence parasite prevalence (Berton et al., 2019). In line with previous findings, males were observed to be more susceptible than females (Barger, 1993), a trend that was evident only in the FEC of dewormed calves. However, no statistical differences were observed between sexes for the FEC of Trichostrongylidae or trematodes, consistent with another study reporting no sex-based differences (Ngetich et al., 2019). The effect of age was confirmed, as observed in several studies indicating that calves' immunity increases with age (Thamsborg et al., 2017) As the animals grew, a marked reduction in the FEC of Strongyloides spp. was evident, and Trichostrongylidae counts decreased in both dewormed and non-dewormed calves. This is concerning because it suggests that the anthelmintics were ineffective. The resistance of calves to parasites increased with age, with both dewormed and non-dewormed groups showing similar patterns, indicating the development of anthelmintic resistance, which is widely reported globally (Baiak et al., 2018). Nearly all sampled animals tested positive for internal parasites, especially nematodes, reinforcing the idea that young animals grazing on pastures previously used by adult cattle are more likely to contract GIN (Romero-Hurtado et al., 2022). The high variability in EPG among calves of different ages suggests immunological development because higher FEC was observed early in the study, with a significant reduction in EPG by 8 months of age in both the de-wormed and control groups, aligning with findings reported in the literature (Greer & Hamie, 2016).

Climate is one of the main factors influencing the presence of parasites, as pre-parasitic periods depend on humidity and temperature. Some studies suggest that the highest number of infected animals occurs during summer and autumn due to rainfall, while infections gradually decrease in winter due to low temperatures, and parasitosis cases rise again in spring (Heckler & Borges, 2016). However, in the study region, a consistently high prevalence of trematodes and nematodes is observed year-round (Muñiz-Lagunes et al., 2015; Hernández-Hernández et al., 2023) attributed to ideal temperature and humidity conditions. As a result, the prevalence percentages for both nematodes and trematodes were notably high on the studied farms.

Various studies have identified Cooperia spp. as one of the most persistent parasites in fecal matter (Robi et al., 2023), posing a significant challenge in grazing livestock due to its high prevalence (80 %) and widespread anthelmintic resistance in tropical and temperate regions (Felippelli et al., 2014; Suarez et al., 2018; García-Ruíz et al., 2019). Research highlights the pathological effects of Cooperia spp. infection on the small intestine mucosa, which negatively impacts animal health and production, leading to economic losses (Stromberg et al., 2012; Höglund et al., 2018; Neves, Das et al., 2020). Despite the damage caused by Cooperia spp., infection in calves induces an immune response to regulate the infection, although acquiring immunity takes time (Matamoros-Mercado et al., 2021). By contrast, Haemonchus spp. and Trichostrongylus spp. were present at relatively lower levels, reflecting the complex interactions between parasite species and their environmental conditions.

The low prevalence of other parasite species observed in this study aligns with similar findings (Romero-Hurtado et al., 2022), where a prevalence of 1.7 % for Dictyocaulus viviparus was reported in cattle of various ages, including animals under 1 year old. The low prevalence of trematodes observed was consistent with previous reports from the region (Hernández-Hernández et al., 2023). For example, a study conducted in southeastern Mexico found a mean trematode egg count of 11.1 ± 14.0 EPG. However, another study reported high prevalences of F. hepatica (62.4 %) in cattle, particularly in animals raised on pasture (Jara-Campos et al., 2018).

Conclusions

The results of this study demonstrated a significant reduction in nematode FECs with increasing age; however, no differences in egg counts were observed between dewormed and non-de-wormed animals after the second treatment application. The prevalence of internal parasites fluctuated throughout the study, with coccidia being the most prevalent, detected in 54 % of animals during the final sampling in December. The primary genera of parasites were identified in the suckling calves, with Cooperia spp. being the predominant species among the larvae, accounting for approximately 80 % of the total.

With the results of this study, it is possible to reduce the use of anthelmintics by applying them only during the first three months of age of the calves to reduce the high initial counts of nematode eggs, since later the calves develop natural resistance, and the high prevalence of trematodes requires the use of specific products for their control which impacts livestock production in the tropical region.