In addition to the nutritional, reproductive and management aspects that limit the productivity of cattle (Vite
The importance of endoparasites has been highlighted for a long time (Sardar
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 parasites affect the gastrointestinal tract, causing haemorrhagic inflammation of the intestines after excystation and subsequent migration of the juvenile fluke to the target organ. In acute cases the thickness of mucosa and submucosa of intestines occur (Atcheson
Due to the importance of flukes in cattle health, the objective of this study was to study the risk factors and prevalence of the flukes
The samplings were carried out on 20 cattle farms located in the municipalities of Teapa, Jalapa, Huimanguillo and Tacotalpa corresponding to the southern region of Tabasco state and in the municipalities of Pichucalco, Juarez and Salto de Agua corresponding to the north of the Chiapas state. Samples were also taken in Escarcega, 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
The livestock production systems were mostly for beef production and only two units were dedicated to both milk and beef production. In all farms, cattle were raised on native and introduced pastures, without supplementation, except for dairy cattle that received some type of commercial supplement. The breeds in the region are mostly crossbreeds of
The study was carried out from August to December 2018 and in this year only the presence of flukes 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 fluke eggs were differentiated only by the coloration of the egg. The number of samples obtained by locations are indicated in Table 1.
Number of bovines sampled per year, type of sampling and state of origin of the animals.
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 fluke eggs | Tabasco | 227 |
Chiapas | 34 | ||
Campeche | 50 | ||
Presence of liver and rumen flukes in slaughtered cattle | Tabasco | 83 | |
Chiapas | 325 | ||
Total | 1010 |
The farms were selected for convenience with producers, who participated as volunteers, contacted through the Livestock Producers Association. To obtain the faeces, always during the morning before 8:00 am, the cattle from each farm were moved to a handling 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 addition, other method to determine the prevalence was observing adult flukes, for which three slaughterhouses were visited as routine academic activities of parasitological inspection.
To report prevalence of liver and rumen fluke eggs, the sedimentation technique was used. Briefly, 10 grams of faeces were weighed and diluted in 250 ml of running water. Larger particles were removed 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 water 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 fluke eggs, which differed by colouring; the golden eggs corresponded to liver fluke and the transparent ones to rumen fluke (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 fluke specimens were counted and the average was obtained in the positive animals. Rumen flukes were collected for their subsequent identification based on their morphology (Eduardo, 1982), for which the specimens were fixed 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 differentiate them by their species characteristics (Nikander & Saari, 2007).
Two methods of prevalence were used, one with the differentiation of eggs and the other with the presence of adult flukes. The descriptive statistics using the SAS program (SAS, 2017) allowed calculating the prevalence as the number of positive cases among 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 flukes (0).
For the terrain physiography variable, two options were recorded: flood-prone areas, which were flat or slightly flat sites with clayey soils, generally flood-prone, and hillocks, which were hills or hills with slopes that did not allow water pooling (Zavala Cruz
All applicable international, national and institutional guidelines for the care and use of animals were followed. The procedures were in accordance with the Official 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.
The rumen fluke species identified by morphology corresponded to
The faecal fluke 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 fluke. The average of trematode eggs was 11.1 ± 14.0 epg and only 3.02 ± 4.4 epg for rumen fluke and 8.48 ± 11.04 epg for liver fluke.
Average faecal fluke egg (liver and rumen flukes) counts in cattle in southeastern Mexico according to sex, age and origin.
Variable | N | Mean | SE | Q1 | Median | Q3 |
---|---|---|---|---|---|---|
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 fluke 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.
The highest counts of adult rumen flukes 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.
The prevalence of trematodes (liver and rumen fluke 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 fluke eggs, obtaining a prevalence of liver fluke of 18.6 % (134/719) and of rumen fluke was 33.4 % (240/719).
The prevalence by origin of sample (faeces or adult trematode in slaughterhouse), physiographic zone, locality, sex and age of cattle only for differentiated eggs in 2019 are presented in Table 3.
The prevalence of
Prevalence of flukes in cattle in a humid warm climate of Mexico by study variable.
Risk factor | Rumen fluke | Trematodes | |||
---|---|---|---|---|---|
N | Positives (%) | Positives (%) | N | Positives (%) | |
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.
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 flukes (Table 4). In the case of rumen fluke, no differences were observed in the type of sample, so the diagnosis by eggs in faeces and flukes in rumen showed similar prevalence. No differences were found in sex (Table 5) and there were also no differences in liver flukes in relation to age.
Odds ratio of the study variables that affect the presence of trematodes (
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 significant <0.01,
significant <0.05,
not significant >0.05,
CI confidence interval
Odds ratio of the study variables that affect the presence of liver and rumen fluke in cattle in a hot humid climate.
Rumen fluke | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Risk factor | B | SE | Wald | Odds ratio | 95% CI | B | SE | Wald | Odds ratio | 95% CI |
Constant | −21.31 | 261.6 | 0.006 | −2.05 | 0.71 | 8.23 | ||||
Type of sample | ||||||||||
Fluke | Baseline | 1.0 | 1.0 | |||||||
Eggs in faeces | 2.8 | 0.67 | 17.4 | 16.35** | 4.4–60.8 | 0.43 | 0.45 | 0.88 | 1.53ns | 0.63–3.73 |
Physiographic zone | ||||||||||
Hillocks | Baseline | 1.0 | 1.00 | |||||||
Flood-prone areas | 2.8 | 0.38 | 50.35 | 15.76** | 7.36–33.76 | 1.6 | 0.36 | 19.15 | 4.94** | 2.41–10.1 |
Sex | ||||||||||
Female | Baseline | 1.0 | 1.0 | |||||||
Male | −2.8 | 1.28 | 4.92 | 0.058* | 0.005–0.72 | −0.09 | 0.44 | 0.05 | 0.91ns | 0.38–2.17 |
Age | ||||||||||
Old cows (> 7y) | Baseline | 1.0 | 1.0 | |||||||
Steers | 0.12 | 1.61 | 0.05 | 1.13ns | 0.05–26.67 | −0.59 | 0.52 | 1.28 | 0.55ns | 0.19–1.54 |
Young cows (<7) | 0.96 | 0.98 | 0.96 | 2.6* | 1.38–17.7 | −0.45 | 0.43 | 1.07 | 0.64ns | 0.27–1.49 |
State | ||||||||||
CampecheΩ | - | - | - | - | - | Baseline | 1.00 | |||
Chiapas | Baseline | 1.0 | 1.33 | 0.65 | 4.2 | 3.78* | 1.06–13.5 | |||
Tabasco | −0.31 | 0.6 | 0.29 | 0.73ns | 0.24–2.25 | 0.68 | 0.51 | 1.8 | 1.98ns | 0.72–5.4 |
P-value highly significant <0.01,
significant <0.05,
not significant >0.05,
CI confidence intervals.
Liver fluke was not observed in Campeche.
In the present study, the prevalence of trematodes in Tabasco, Chiapas and Campeche states in Mexico reached 36 – 41 %, while for
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 emerging disease (Huson
Of the two rumen fluke species found in the region,
The average counts of rumen flukes obtained in Mexico were lower (41 adult specimens) than those indicated in Iran (100 – 200 adult flukes) in slaughterhouse studies (Khedri
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 flat areas prone to flooding with soils with a high proportion of clay, the probabilities of occurrence of
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
Females presented higher prevalence than males because this last receive different health and nutritional management that females, 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