Skip to main content
Download PDF

Effects of season, age and parasite management practices on gastro – intestinal parasites in pigs kept outdoors in Ireland

Irish Veterinary Journal volume 78, Article number: 12 (2025) Cite this article

Abstract

Outdoor farming offers pigs considerable behavioural freedom and better consumer acceptance than intensive, indoor systems. However, gastro – intestinal (GI) parasites pose a significant health and welfare challenge for pigs reared outdoors. The aim of this study was to ascertain effects of management, season and animal factors such as age, on a range of different GI parasites in Irish pigs farmed outdoors. Sixty-five pig faecal samples (a mix from at least 2–4 animals per paddock) were collected from 65 paddocks across 20 outdoor pig farms, over two visits (1st visit – February/May-December 2023, n = 37, 2nd visit– July/October 2023, n = 28). Samples were collected and mixed thoroughly to achieve a paddock level sample. Data were also collected related to pig characteristics (grower/fatteners or sows and boars), anthelmintic usage (Yes/No) and paddock rotation (Yes/No) and categorized at paddock level. Samples were analysed using the McMaster floatation method, faecal egg count (FEC) was calculated, and GI parasites were identified by morphology. Generalized linear mixed models were used to analyse the effect of season, age, anthelmintic usage and paddock rotation on FEC. Four parasite taxa were identified (Eimeria/Isospora spp., strongyles, Ascaris suum and Trichuris suis). Infection rates were > 80% for Eimeria/Isospora spp. and strongyles, 31% for A. suum and 9% for T. suis for both visits. Eimeria/Isospora spp. FEC was higher at the 2nd visit (P < 0.001) and strongyles FEC was higher at the 1st visit (P < 0.05). Fattener pigs had higher FEC for Eimeria/Isospora spp. (P < 0.01) and sows/boars had higher strongyle counts (P < 0.05). Strongyle count was lower with anthelmintic use (P < 0.05) and Eimeria/Isospora spp. count was lower (P = 0.05) with paddock rotation when anthelmintics were used. Lower winter temperatures may have influenced the seasonal variation in strongyle FEC. This study provides a comprehensive picture of GI parasites in outdoor pig farms in Ireland in terms of the taxa, their prevalence and risk factors.

Introduction

Infection with gastro–intestinal (GI) parasites is a cause of ongoing and increasing concern in livestock production because of detrimental economic and animal welfare effects, which negatively impact sustainability of the industry [1,2,3]. Detrimental implications for animal health are associated with morbidity, reduced feed conversion efficiency and growth, as well as treatment costs [4, 5]. Effective control of GI parasites requires a combined use of anti-parasitic drugs and management practices such as rotational grazing [6]. Increasingly there are also concerns for resistance to treatment [7]. GI parasites, particularly helminths, affect domestic pigs in all production systems around the world [8]. In pigs, infections impair intestinal absorption, prolong the fattening period, delay or hamper immunity after vaccination, reduce meat quality, and in the case of young pigs, may cause death, due to diarrhoea and dehydration [9, 10]. In spite of the potential clinical implications, parasitic infections in pigs seldom cause clinical symptoms, especially in the case of helminths, and diagnosis is generally based on laboratory examination [8, 10]. The subclinical nature of helminth parasitic infection means that they receive less attention compared to other parasites in other livestock species. An additional risk of GI infections in pigs is the potential for zoonoses associated with helminth species such as Ascaris and Trichuris [11].

While the majority of pigs in developed countries are farmed intensively indoors, the increasing interest in welfare-friendly meat means that there is growth in the outdoor pig production sector [12]. Outdoor pig farming allows pigs to express a wider range of behaviours in a semi-natural environment [13]. However, outdoor access increases the risk of both endo- and ecto-parasite infection, due to favourable conditions for the development and survival of various stages of parasites in the outdoor environment [14]. Transmission occurs through ingestion of infective eggs, oocytes and larvae. Common parasites in outdoor pigs include protozoa (e.g. Eimeria spp., Isospora suis, Balantidium coli etc.) and helminths (e.g. strongyles, Ascaris suum, Trichuris suis, Metastrongylus spp.) [15]. Several studies report the prevalence of a range of parasite species in outdoor reared pigs in Europe. Deslart et al. [16] assessed 70 alternative farms in France and reported 79% of the farms having coccidia and 47%, 16% and 36% of farms having Oesophagostomum spp., Ascaris suum and Trichuris suis respectively. There are also differences in the prevalence of parasites in different age groups of pigs [17]. Carstensten et al. [18] assessed 9 organic pig herds in Denmark and found Ascaris suum, Oesophagostomum spp. and Trichuris suis among weaners, fatteners and sows with varying levels of prevalence. Băieş et al. [17] examined 960 free-range pigs in Romania and observed that the pigs had Eimeria spp., Balantidium coli, Ascaris suum, Oesophagostomum spp., S. ransomi and Cryptosporidium spp. Furthermore, the abundance of parasites, and hence the potential infective pool in the paddock fluctuated with the seasons, indicating parasite sensitivity to temperature changes [17, 19].

Outdoor pig farming is not an established industry in the island of Ireland; instead, most outdoor farms operate on a small – scale, backyard basis rather than at a commercial level. Menant et al. [20] reported an average of 7 sows/gilts, one boar, 18 grower pigs and 17 piglets in these small scale production units at any one time, which were generally managed by two people. The main breeds were Duroc, Oxford Sandy and Black, Tamworth, and Gloucester old spot pigs. Pigs were reared in agro-forestry systems, on pasture or in a mixture of both. Considering the small-scale nature of the industry, it is poorly characterised, and literature on GI parasites is scarce. In order to address this knowledge gap, the objectives of this study were to:

  1. 1.

    Identify and evaluate the prevalence of GI parasites in outdoor reared pigs on selected farms.

  2. 2.

    Determine the effect, if any, of season, and age on the parasite faecal egg counts of outdoor pigs.

  3. 3.

    Assess the effect of anthelmintic treatment and paddock rotation on the parasite egg burden of outdoor pigs.

Materials and methods

Farms and animals

Twenty farmers were selected from 57 respondents to the survey described by Menant et al. [20], and who expressed an interest in volunteering for the study. Farms were located in 12 out of 32 counties across the island of Ireland (Antrim − 1, Clare − 1, Cork − 3, Down − 1, Galway − 1, Laois − 3, Louth − 1, Sligo − 1, Tipperary − 1, Waterford − 3, Wexford − 1, Wicklow − 3). Each farm was visited twice: once between February and May 2023, plus December 2023 (winter/spring, mean ± sd: temperature: 11 ± 4.3 °C, relative humidity: 75.7 ± 11.2%, wind: 1.7 m/s) and once between July and October 2023 (summer/autumn, mean ± sd: temperature: 14.9 ± 4.3 °C, relative humidity: 78.6 ± 8.6%, wind: 0.9 m/s). The first visit encompassed 19 farms, with 17 farms visited during the second phase (Table 1). All of the assessed farms had an electrified fenced outdoor area where the pigs had access to soil, and 6 operated to an organic standard (Table 1). The average size of the paddocks was 21.6 ha (range 0.02–323 ha) with an average of 32 (range 7–128 pigs) pigs per paddock. Information on animal demographics (breed, age) and management practices such as anthelmintic usage (yes/no) and paddock rotation (yes/no) were also collected (Table 1). Anthelmintic use and paddock rotation practices were recorded through semi-structured interviews with farmers. Farmers reported the life stage at which animals were administered anthelmintics by a veterinarian and the frequency of paddock rotation. Farms were classified as using anthelmintics (“Yes”) if they had administered anthelmintics within the previous year and as not using anthelmintics (“No”) if they had never administered them. The frequency of anthelmintic use varied among farms, ranging from administration after weaning, three times per year, to only when deemed necessary. Among the farms that practiced paddock rotation, one farm rotated weekly, two farms rotated every two weeks, three farms rotated monthly, one farm rotated every six weeks, two farms rotated bimonthly, three farms rotated every four months, and one farm rotated annually. Pigs were raised on natural or sown pastures. In the agroforestry systems, the underfoot surface was a litter layer. Pigs older than 3 months were selected for inclusion, while lactating sows and piglets under 3 months old were excluded due to practical issues with data collection and the aggressive nature of the lactating sow. Animals were stratified into two age categories: fatteners (comprising growing and finishing pigs under 8 months old) and sows and boars (encompassing sows and boars aged 9 months to 4 years, Table 1).

Sample collection

A maximum of 4 faecal samples were collected in each paddock in which pigs were present. The pigs were observed until defecating freely, samples were promptly collected after voiding, then placed into 100 ml plastic cups, and stored in a cool box under chilled conditions (0–4 °C). Each sample within a paddock was combined in equal proportions to create a composite paddock-level sample. Only faecal samples with solid nature were collected. In total, 65 composite paddock level samples were collected over the two visits (Table 1), 37 samples in the first visit, and 28 samples during the second visit. These samples were maintained under chilled conditions during transportation and stored in a cold room at 4 °C until the coprological analysis was conducted. All samples were analysed within 21 days after collection.

Table 1 Characteristics of the farms visited and number of paddocks assessed
Full size table

Coprological analysis

A modified McMaster floatation method described by Taylor et al. [15] was employed for the analysis of faecal egg count (FEC), employing NaCl as the floating solution. Initially, 3 g of faecal matter from the composite sample was placed into a mortar and homogenized with 42 ml of chilled water (0–4 °C). The resulting homogenized sample was sieved through a 150 μm sieve, and the filtrate was transferred to a 15 ml centrifugal tube, which was subsequently centrifuged at 1500 rpm for 2 min. The supernatant was removed after centrifugation and added saturated NaCl solution. A vortex disrupted the pellet to ensure thorough mixing. The tubes were inverted 8–10 times, and the mixture was pipetted from the middle of the tube and transferred to a two-chambered McMaster slide. Subsequently, the grid of the slide was examined using a microscope (Alphaphot – 2 YS2, Nikon Corporation, Tokyo, Japan) at 10x magnification to detect parasite eggs. Parasite eggs and protozoa cysts were identified based on their morphology [15], and the number of different eggs in the grid per chamber were counted. The technique had a lower limit of 50 eggs/g per sample. Three replicates (slides) were analysed for each faecal sample. The analysis was performed by one trained person. The FEC is displayed as eggs per gram of faeces (eggs/g) and calculated using the following equation:

$$\begin{aligned}Faecal\:egg\:count=&(egg\:count\:in\:chamber\:01\\&+egg\:count\:in\:chamber\:02)\times\:50\end{aligned}$$

Statistical Analysis

Statistical analysis of the data were performed using Rstudio (R version 4.2.1, R core team, 2022).

Prevalence of parasites within visits

Prevalence at the farm level was determined considering the presence or absence of parasite eggs or oocysts. A farm was considered infected with a parasite if at least one egg was detected. The prevalence value for a parasite taxon was calculated as a percentage of farms infected from the number of all the farms for both visits separately. Fisher’s exact test was used to analyse the prevalence of a parasite between visits.

Effect of the season and age on the faecal egg count

A Generalized Linear Mixed Effect Model, utilizing the glmmTMB package [21] was employed to investigate the impact of season and age on the FEC. To address the zero-inflation observed in the data, we applied a negative binomial distribution with a log link function, along with zero-inflated adjustments. Fixed effects included season and age while paddock nested within farm was considered as a random effect to account for potential clustering effects. The interaction between season and age was considered. Subsequently, a Type III Analysis of Variance (ANOVA from car package; [22]) was conducted to validate the model’s findings. Estimated marginal means were then derived for further interpretation of the results and pairwise comparisons (emmeans package; [23]) between the visits and the age groups were conducted.

Effect of using anthelmintics and paddock rotation on the faecal egg count

A similar Generalized Linear Mixed Effect Model was used to analyse the effect of using anthelmintics and paddock rotation on FEC. Anthelmintic usage, paddock rotation, and their interaction were included as fixed effects, while paddock nested within farm was used as a random effect.

Results

Parasite taxa

We identified four taxa of parasite eggs based on egg morphology (Fig. 1). They were Eimeria/Isospora spp., strongyles, Ascaris suum and Trichuris suis. Strongyles were grouped because several species (Oesophagostomum spp., Hyostrongylus rubidus, Trichostrongylus spp. etc.) have similar morphology making it impossible to identify to species level.

Fig. 1
figure 1

Photographs of Eimeria/Isospora spp. oocyst (a), strongyle eggs (b), Ascaris suum egg (c) and Trichuris suis egg (d) identified on bright-field microscope (20x magnification)

Full size image

Prevalence of parasites

Prevalence of Eimeria/Isospora spp. and strongyles was high (> 80%) at both visits and Ascaris suum prevalence was moderate, at approx. 30%. T. suis was found on one farm during the 1 st visit and on two farms on the 2nd visit (Table 2). There was no significant effect of the visit on the prevalence of each parasite (Table 2).

Table 2 Number and percentage of farms with the presence and absence of gastro-intestinal parasites during the two visits (Fisher’s exact test to determine the significance between farms in two visits)
Full size table

Effect of season and age on faecal egg count

Eimeria/Isospora spp. count was higher during the 2nd visit compared to the 1 st visit (Estimated marginal means ± sd; 1 st visit – 476 ± 297 vs. 2nd visit – 1527 ± 950 eggs/g; P < 0.001, Fig. 2a). Furthermore, fattener pigs had higher Eimeria/Isospora spp. FEC than sows and boars (fatteners – 1175 ± 745 vs. sows/boars – 619 ± 386 eggs/g; P < 0.05, Fig. 3a). Strongyle FEC was higher in the 1st visit than in the 2nd visit (1 st visit – 370 ± 198 vs. 2nd visit – 141 ± 77 eggs/g; P < 0.01, Fig. 2b) and sows and boars had higher strongyle FEC than fatteners (fatteners – 125 ± 71 vs. sows and boars – 419 ± 223 eggs/g; P < 0.01, Fig. 3b). There was no interactive effect between season and age in the analysis. There was no effect of season or age for Ascaris suum FEC (Figs. 2c and 3c). Since Trichuris suis was found on only two farms it was not statistically analysed.

Fig. 2
figure 2

Median and quartiles of (a) Eimeria/Isospora spp., (b) strongyles and (c) A. suum faecal egg counts (FEC) during the 1st (blue, winter/spring) and 2nd visit (green, summer/autumn)

Full size image
Fig. 3
figure 3

Median and quartiles of (a) Eimeria/Isospora spp., (b) strongyles and (c) A. suum faecal egg counts in relation to fatteners (black) and sows/boars (white)

Full size image

Effect of using anthelmintics and paddock rotation on faecal egg count

The farms that used anthelmintics had lower strongyle FEC in both seasons (Yes: 48.2 ± 37.6 eggs/g, No: 668.3 ± 381.7 eggs/g; P < 0.01, Fig. 4a). Neither Ascaris suum nor Eimeria/Isospora spp. FEC levels were affected by anthelmintic use (Fig. 4b, c).

There was no effect of paddock rotation on Eimeria/Isospora spp., strongyles or on Ascaris FEC (Fig. 5). There was no interaction between paddock rotation and use of anthelmintics. However the use of anthelmintics in the farms influenced paddock rotation in the additive model and the farms which practiced paddock rotation had lower levels of Eimeria/Isospora spp. FEC when anthelmintics was administered (Anthelmintics yes, paddock rotation yes – 1629 ± 651 eggs/g vs. Anthelmintics yes, paddock rotation no – 7188 ± 5646 eggs/g; P = 0.05).

Fig. 4
figure 4

Median and quartiles of (a) Eimeria/Isospora spp., (b) strongyles and (c) A. suum in relation to anthelmintic usage (Yes – Brown, No – Yellow)

Full size image
Fig. 5
figure 5

Median and quartiles of (a) Eimeria/Isospora spp., (b) strongyles and (c) A. suum in relation to paddock rotation (Yes – grey, No – light blue)

Full size image

Discussion

This study provides the first data on the prevalence of a range of taxa of GI parasites found in pigs produced outdoors on the island of Ireland. The only other work on pig GI parasites conducted in Ireland reported on liver damage caused by Ascaris suum in intensively produced pigs [24]. In the present study, season, age of the pig, and the anthelmintic usage had significant effects on FEC related to both Eimeria/Isospora spp. and strongyles and influenced paddock rotation with Eimeria/Isospora spp. counts.

Prevalence of the parasites

A high proportion (> 80%) of the farms were infected by Eimeria/Isospora spp. and strongyles at both visits. Similarly, a Romanian study found a high prevalence of Eimeria spp. during both summer (80%) and winter (77.5%) and with a somewhat lower prevalence for strongyles (Oesophagostomum spp.); 27.5% during summer and 37.5% during winter [17]. A survey of 101 pig farms in Western Australia recorded evidence of nematode parasites in 79% of farms with 65% positive for Oesophagostomum spp. and 55% positive for coccidia across all the ages of pigs [25].

The oocysts of Eimeria spp. show great resistance to environmental conditions, making high prevalence and year round presence possible in pigs [26]. The high prevalence of strongyles could also be due to year round shedding of the eggs by the adult worms. Thus, even though the eggs have a low resistance to climatic extremes, compared with other helminth eggs, the possibility of the hatched larvae being ingested is present throughout the year, even while the burden differs.

Prevalence of Ascaris suum (30%) affected farms in this study was more or less similar to some other studies conducted in Europe across all farm systems. Ascaris suum had a 28.6% prevalence in Poland, from 70 pig farms [10]. A study in Estonia found 31.5% prevalence of Ascaris suum in ecological and small pig farms (n = 20 farms; [27]). Free-range farms in Netherlands had a 50% prevalence of Ascaris suum (n = 27 farms; [28]) and Rodrigues Da Costa et al. [24] found, 30% of the commercial pig farms in Ireland had pigs with milk spots, which occurs due to Ascaris suum. The observed similar prevalence (30%) suggesting that outdoor pigs may have no greater a risk of A. suum infection than those raised indoors although the different method of estimation should be considered (i.e. milk spots vs. egg counts).

In the present research, very few farms were affected by Trichuris suis as evidenced by the low presence of faecal eggs (one in the 1 st visit, (5%), and 2 in the 2nd visit, (12%)). Other studies recorded a much higher proportion of farms (ranging from 21.4 to 37.5%) affected by this parasite [10, 28]. However, the relatively quick expulsion of adults, and thus egg-laying individuals, by the host reduces the value of FEC alone in assessing prevalence of this helminth species among hosts [6].

Effect of season and age on the faecal egg count

In intensive systems, Symeonidou et al. [29] found that Crisoisospora suis, a coccidia species similar to Eimeria spp., tended to have a lower burden of oocysts in winter compared to spring. Another investigation by Băieş et al. [17] found a different parasitic load of Eimeria spp. between the seasons winter/spring (higher) and summer/autumn (lower). In this study, the highest mean number of Eimeria/Isospora spp. oocysts was recorded in the 2nd visit, which was during late summer/autumn. Eimeria oocysts can die when the temperature is colder (− 20 °C) or hotter (38 °C), as in the case of Eimeria bovis, a coccidia which infects cows [30]. Mild summer temperatures, such as those that occur in Ireland (mean temperatures between 14 and 15 °C; [31, 32]) result in favourable conditions for the Eimeria oocysts to become infective, causing the higher FEC during the summer and autumn month periods.

Infection from strongyles occurs from the L3 infective larval stage. Eggs are passed through faeces, hatch, and develop infective larvae, which are ingested by the pigs [33]. Harsh, cold, winters and dry, hot, summers have detrimental effects on Oesophagostomum spp. eggs, leading to higher mortality rates [34]. According to Nansen and Roepstorff [31], the lower temperature limit for the Oesophagostomum spp. is ̴10 °C and the eggs deposited during the winter do not survive into the spring. Rose and Small [35] found that transmission of both Oesophagostomum spp. and Hyostrongylus rubidus could not take place during winter in British conditions. Even though a higher temperature average (> 7 °C) was observed during the 1 st visit, Irish winter air temperature averages are at 4–7 °C [32]. The highest mean faecal egg counts (FEC) of strongyle-type nematodes were observed during the 1 st visit, conducted in late winter/spring. The strongyle lifecycle within the pig spans approximately 4–6 weeks [15]. In outdoor environments, most eggs and free-living larvae do not survive the winter months due to harsh conditions. This results in a reduced larval load available for ingestion by pigs, leading to fewer mature adult worms and consequently lower FEC during the summer/autumn months. However, Ireland’s mild summers, compared to other European countries, may not significantly affect the survival of eggs and free-living larvae. This could contribute to the higher FEC observed during the winter/spring period, as larvae surviving through the summer are ingested by pigs and develop into adult worms capable of producing eggs during these colder months.

During this study, the faecal egg counts of Ascaris suum and Trichuris suis did not differ between the two visits, although they were present on only 30% of the farms visited. The eggs of these parasites are more resistant to environmental conditions, which could explain the consistency of their counts relative to those of strongyles [36].

Several studies mention significant differences in the FEC between pigs of different ages in terms of Eimeria spp. and strongyles [16, 17, 37]. In the present analysis, fattener pigs had higher mean FEC for Eimeria/Isospora spp. while the sows and boars had higher mean FEC for strongyles. Older animals (sows and boars) have stronger immunity towards Eimeria spp. due to frequent contact with Eimeria spp. and other coccidia [16]. This could explain the lower FEC in these older animals. In contrast, the patterns for strongyles such as Oesophagostomum spp. and Hyostrongylus rubidus were of higher parasite intensity with increasing host age [18]. Oesophagostomum spp. has low immunogenicity, resulting in almost all larvae surviving into maturity and living inside the pig for 2–4 months [8] thus the higher strongyles FEC observed during our study in these older animals.

In contrast, Ascaris suum and Trichuris suis have high immunogenicity and a large majority of larvae are expelled from the small intestine, leaving a small number of mature worms inside the animal [8]. The results of this study did not indicate an age effect on FEC; however, in several studies from other European countries the prevalence and intensity of A. suum and T. suis differed across age groups (intensity lowered with the age of the animal) [18, 27].

Effect of using anthelmintics and paddock rotation on the FEC

Ireland, being a member of the European Union, has a list of approved anthelmintics for use in pigs. Anthelmintics classes include Benzimidazoles, Levamisole and Macrocyclic lactones [38]. Mooney et al. [39] listed a total of 40 anthelmintic compounds approved for use in Ireland, encompassing a range of drugs applicable to various livestock species, including pigs. In our study only 7 of the 20 farms administered anthelmintics to their pigs. As the results indicated, the farms using anthelmintics had significantly lower strongyle counts. Indeed, the use of anthelmintics on strongyle species such as Oesophagostomum spp. is highly effective, even though anthelmintic resistance is an emerging issue [6]. Although other studies show high efficacy (in some studies > 90%) of anthelmintics on Ascaris suum, regardless of the class used [6, 40], the present study did not find an effect of anthelmintic use on Ascaris suum FEC. However, only 3 of the 7 farms that used anthelmintics had Ascaris suum and this may have influenced the sensitivity of the analysis. A survey of 101 pig herds in Western Australia found that 80% of pig herds treated with anthelmintics still showed evidence of parasitic infection, suggesting that a single-dose treatment may not be the most effective deworming strategy [41].

Paddock rotation is an important management method to control parasites. Anthelmintics alone are not effective in the long -run, as parasites and eggs can survive in the soil or be re-introduced by other reservoirs [42] so re-infection is inevitable. This could explain why in this study, the FEC of Eimeria/Isospora spp. in the farms that practised paddock rotation was low even when the use of anthelmintics was taken into account.

Conclusions

This analysis observed seasonal variation in the FEC of Eimeria/Isospora spp. and strongyles, with Eimeria/Isospora spp. levels higher in the winter/spring, and strongyle levels higher in the summer/autumn. Grower and fattener pigs had higher Eimeria/Isospora spp. counts while sows and boars had higher strongyle counts, indicating different parasite community dynamics in different age groups. Anthelmintic usage seems to be effective against strongyles, and paddock rotation tended to reduce Eimeria/Isospora spp. counts in the presence of anthelmintics. There is a lack of data on GI parasites in Irish pigs, particularly those kept outdoors, and this study sheds light on the factors that could affect their prevalence.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

GI:

Gastro–intestinal

FEC:

Faecal egg count

References

  1. Charlier J, Rinaldi L, Musella V, Ploeger HW, Chartier C, Vineer HR, et al. Initial assessment of the economic burden of major parasitic helminth infections to the ruminant livestock industry in Europe. Prev Vet Med. 2020;182:105103. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.prevetmed.2020.105103.

    Article  CAS  PubMed  Google Scholar 

  2. Crawley JAH, Chapman SN, Lummaa V, Lynsdale CL. Testing storage methods of faecal samples for subsequent measurement of helminth egg numbers in the domestic horse. Vet Parasitol. 2016;221:130–3. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.vetpar.2016.03.012.

    Article  PubMed  Google Scholar 

  3. Donald AD. Parasites, animal production and sustainable development. Vet Parasitol. 1994;54(1–3):27–47. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/0304-4017(94)90082-5.

    Article  CAS  PubMed  Google Scholar 

  4. Perry BD, Randolph TF. Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Vet Parasitol. 1999;84(3–4):145–68. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0304-4017(99)00040-0.

    Article  CAS  PubMed  Google Scholar 

  5. Maqbool I, Wani ZA, Shahardar RA, Allaie IM, Shah MM. Integrated parasite management with special reference to gastro-intestinal nematodes. J Parasit Dis. 2017;41(1):1–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s12639-016-0765-6.

    Article  CAS  PubMed  Google Scholar 

  6. Pettersson E, Sjölund M, Wallgren T, Lind EO, Höglund J, Wallgren P. Management practices related to the control of Gastrointestinal parasites on Swedish pig farms. Porc Health Manag. 2021;7(1):12. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40813-021-00193-3.

    Article  Google Scholar 

  7. Waller PJ. Anthelmintic resistance. Vet Parasitol. 1997;72:391–412. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0304-4017(97)00107-6.

  8. Roepstorff A, Mejer H, Nejsum P, Thamsborg SM. Helminth parasites in pigs: new challenges in pig production and current research highlights. Vet Parasitol. 2011;180(1–2):72–81. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.vetpar.2011.05.029.

    Article  CAS  PubMed  Google Scholar 

  9. Knecht D, Popiołek M, Zaleśny G. Does meatiness of pigs depend on the level of gastro-intestinal parasites infection? Prev Vet Med. 2011;99(2–4):234–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.prevetmed.2011.01.009.

    Article  PubMed  Google Scholar 

  10. Kochanowski M, Karamon J, Dąbrowska J, Dors A, Czyżewska-Dors E, Cencek T. Occurrence of intestinal parasites in pigs in Poland - the influence of factors related to the production system. J Vet Res. 2017;61(4):459–66. https://doiorg.publicaciones.saludcastillayleon.es/10.1515/jvetres-2017-0053.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Nejsum P, Betson M, Bendall RP, Thamsborg SM, Stothard JR. Assessing the zoonotic potential of Ascaris suum and Trichuris suis: looking to the future from an analysis of the past. J Helminthol. 2012;86(2):148–55. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/S0022149X12000193.

    Article  CAS  PubMed  Google Scholar 

  12. Thorslund CAH, Aaslyng MD, Lassen J. Perceived importance and responsibility for market-driven pig welfare: literature review. Meat Sci. 2017;125:37–45. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.meatsci.2016.11.008.

    Article  PubMed  Google Scholar 

  13. Delsart M, Pol F, Dufour B, Rose N, Fablet C. Pig farming in alternative systems: strengths and challenges in terms of animal welfare, biosecurity, animal health and pork safety. Agriculture. 2020;10(7):261. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/agriculture10070261.

    Article  CAS  Google Scholar 

  14. Krešimir S, Salajpal K, Karolyi D, Luković Z. Sanitary aspects of outdoor farming systems. Acta Agric Slov. 2013;4:109–17. https://doiorg.publicaciones.saludcastillayleon.es/10.14720/aas-s.2013.4.19032.

    Article  Google Scholar 

  15. Taylor MA, Coop RL, Wall R. Veterinary parasitology. Hoboken: Wiley; 2015.

    Book  Google Scholar 

  16. Delsart M, Fablet C, Rose N, Répérant JM, Blaga R, Dufour B, et al. Descriptive epidemiology of the main internal parasites on alternative pig farms in France. J Parasitol. 2022;108(4). https://doiorg.publicaciones.saludcastillayleon.es/10.1645/21-126.

  17. Băieş MH, Boros Z, Gherman CM, Spînu M, Mathe A, Pataky S, et al. Prevalence of swine Gastrointestinal parasites in two Free-Range farms from Nord-West region of Romania. Pathogens. 2022;11(9):954. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/pathogens11090954.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Carstensen L, Vaarst M, Roepstorff A. Helminth infections in Danish organic swine herds. Vet Parasitol. 2002;106(3):253–64. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0304-4017(02)00080-8.

    Article  PubMed  Google Scholar 

  19. Miao ZH, Glatz PC, Ru YJ. Review of production, husbandry and sustainability of Free-range pig production systems. Asian Australas J Anim Sci. 2004;17(11):1615–34. https://doiorg.publicaciones.saludcastillayleon.es/10.5713/ajas.2004.1615

    Article  Google Scholar 

  20. Menant O, Mullen S, Butler F, Boyle L, O’Driscoll K. Characterizing outdoor pig systems in Ireland. In: Book of Abstracts of the 74th Annual Meeting of the European Federation of Animal Science. Wageningen Academic Publishers; 2023.

  21. Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, et al. GlmmTMB balances speed and flexibility among packages for Zero-inflated generalized linear mixed modeling. R J. 2017;9(2):378. https://doiorg.publicaciones.saludcastillayleon.es/10.32614/RJ-2017-066.

    Article  Google Scholar 

  22. Fox J, Friendly GG, Graves S, Heiberger R, Monette G, Nilsson H, Ripley B, Weisberg S, Fox MJ, Suggests MA. The car package. R Foundation Stat Comput. 2007;1109:1431.

  23. Lenth RV. emmeans: estimated marginal means, aka least-squares means. R package version 1.8.9. 2023. Available from: https://cran.r-project.org/package=emmeans.

  24. Rodrigues Da Costa M, Fitzgerald RM, Manzanilla EG, O’Shea H, Moriarty J, McElroy MC, et al. A cross-sectional survey on respiratory disease in a cohort of Irish pig farms. Ir Vet J. 2020;73(1):24. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13620-020-00176-w.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mercy AR, De Chaneet G, Emms Y. Survey of internal parasites in Western Australian pig herds. 1. Prevalence. Aus Vet J. 1989;66(1):4–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1751-0813.1989.tb09702.x.

    Article  CAS  Google Scholar 

  26. Chartier C, Paraud C. Coccidiosis due to Eimeria in sheep and goats, a review. Small Rumin Res. 2012;103(1):84–92. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.smallrumres.2011.10.022.

    Article  Google Scholar 

  27. Järvis T, Mägi E. Pig endoparasites in Estonia. In: International scientific conference proceedings: Animals. Health. Food Quality. Jelgava: Latvia University of Life Sciences and Technologies; 2008. p. 54–8. https://llufb.llu.lv/conference/animal-health-food/Animal-health-foodhigiene-proceedings-2008-54-58.pdf.

  28. Eijck IAJM, Borgsteede FHM. A survey of Gastrointestinal pig parasites on Free-range, organic and conventional pig farms in the Netherlands. Vet Res Commun. 2005;29(5):407–14. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11259-005-1201-z.

    Article  CAS  PubMed  Google Scholar 

  29. Symeonidou I, Tassis P, Gelasakis AΙ, Tzika ED, Papadopoulos E. Prevalence and risk factors of intestinal parasite infections in Greek swine Farrow-To-Finish farms. Pathogens. 2020;9(7):556. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/pathogens9070556.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lassen B, Lepik T, Bangoura B. Persistence of Eimeria Bovis in soil. Parasitol Res. 2013;112(7):2481–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00436-013-3413-4.

    Article  PubMed  Google Scholar 

  31. Nansen P, Roepstorff A. Parasitic helminths of the pig: factors influencing transmission and infection levels. Int J Parasitol. 1999;29(6):877–91. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0020-7519(99)00048-x.

    Article  CAS  PubMed  Google Scholar 

  32. Curley M, Coonan B, Ryan C, Ruth CE. Ireland’s climatological standard normals (CLINO) 1991–2020. In: EMS Annual Meeting 2023. Bratislava: EMS2023-517; 2023. https://doiorg.publicaciones.saludcastillayleon.es/10.5194/ems2023-517.

  33. Zimmerman JJ. Diseases of swine. 10th ed. Hoboken: Wiley; 2012.

    Google Scholar 

  34. Mejer H, Wendt S, Thomsen LE, Roepstorff A, Hindsbo O. Nose-Rings and transmission of helminth parasites in outdoor pigs. Acta Vet Scand. 2000;41(2):153–65. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/BF03549647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Rose JH, Small AJ. Observations on the effect of anthelmintic treatment on the transmission of Hyostrongylus rubidus and Oesophagostomum spp. Among sows at pasture. J Helminthol. 1983;57(1):1–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/s0022149x00007793.

    Article  CAS  PubMed  Google Scholar 

  36. Roepstorff A, Murrell KD. Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and trichuris suis. Int J Parasitol. 1997;27(5):563–72. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s0020-7519(97)00023-4.

    Article  CAS  PubMed  Google Scholar 

  37. Jacobs DE, Dunn AM. Helminths of Scottish pigs: occurrence, age incidences and seasonal variations. J Helminthol. 1969;43(3–4):327–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/S0022149X00004880.

    Article  CAS  PubMed  Google Scholar 

  38. Animal Health Ireland. Good practice regarding the responsible use of anthelmintic medicines in livestock. Animal Health Ireland; 2021. https://animalhealthireland.ie/assets/uploads/2021/04/AHI-Parasite-Control-Good-Practice-in-responsible-use-of-Anthelmintic-Medicines-2021.pdf?dl=1.

  39. Mooney KG, Richards M, Danaher J, Grant L, Gill P-E, Mellander CE. Coxon. An analysis of the spatio-temporal occurrence of anthelmintic veterinary drug residues in groundwater. Sci Total Environ. 2021;769:144804. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.scitotenv.2020.144804.

    Article  CAS  PubMed  Google Scholar 

  40. Boes J, Kanora A, Havn KT, Christiansen S, Vestergaard-Nielsen K, Jacobs J, et al. Effect of Ascaris suum infection on performance of fattening pigs. Vet Parasitol. 2010;172(3–4):269–76. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.vetpar.2010.05.007.

    Article  CAS  PubMed  Google Scholar 

  41. Mercy AR, Chaneet G, Emms Y. Survey of internal parasites in Western Australian pig herds: 2. Relationship to anthelmintic usage and parasite control practices. Aust Vet J. 1989;66(1):6–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/j.1751-0813.1989.tb09703.x.

    Article  CAS  PubMed  Google Scholar 

  42. Olsen A, Permin A, Roepstorff A. Chickens and pigs as transport hosts for Ascaris, Trichuris and Oesophagostomum eggs. Parasitology. 2001;123(3):325–30. https://doiorg.publicaciones.saludcastillayleon.es/10.1017/S0031182001008435.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Élodie Peyrard, Laura Frigerio, Camille Ducher and Lilou Soler for their assistance during the sampling in the field.

Funding

This study was funded by the Department of Agriculture, Food and the Marine in Ireland (Grant number 2021R600).

Author information

Authors and Affiliations

  1. Pig Development Department, Teagasc Animal and Grassland Research and Innovation Centre, Fermoy, Co, Cork, Ireland

    Nipuna Sahan Senanayake, Laura Boyle, Keelin O’Driscoll & Ophélie Menant

  2. School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland

    Nipuna Sahan Senanayake & Fidelma Butler

Authors
  1. Nipuna Sahan Senanayake
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Laura Boyle
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Keelin O’Driscoll
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Ophélie Menant
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Fidelma Butler
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

N.S.S participated in the sampling of fieldwork, conducted the analysis, and wrote the first draft. K.OD. designed and supervised the analysis and revised the article. L.B. designed and supervised the project and revised the article. O.M. designed and participated in the sampling of fieldwork, supervised the analyses and revised the article. F.B. designed, supervised and revised the article. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fidelma Butler.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Teagasc ethics committee (TAEC2022 - 344).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Senanayake, N.S., Boyle, L., O’Driscoll, K. et al. Effects of season, age and parasite management practices on gastro – intestinal parasites in pigs kept outdoors in Ireland. Ir Vet J 78, 12 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13620-025-00297-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13620-025-00297-0

Keywords

Irish Veterinary Journal

ISSN: 2046-0481