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Article

Evaluation of the Level of Parasites Infection in Pigs as an Element of Sustainable Pig Production

by
Anna Jankowska-Mąkosa
*,
Damian Knecht
,
Sandra Wyrembak
and
Anna Zwyrzykowska-Wodzińska
Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, Chelmonskiego 38C, 51-630 Wroclaw, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(4), 3671; https://doi.org/10.3390/su15043671
Submission received: 5 December 2022 / Revised: 4 February 2023 / Accepted: 9 February 2023 / Published: 16 February 2023
(This article belongs to the Special Issue Industrial Biotechnology Applications in Medicine, Agroindustry, Aquaculture, Biofuel, and Environmental Areas)
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Abstract

:
Pig production is based on routine deworming and very rarely includes endoparasitological diagnosis. Monitoring pig production through a consideration of endoparasites in the herd should be part of the pig health program, which will directly translate into the amount of production costs and improve the condition of animals. The aim of this study was the diagnosis of endoparasitic infection in sows and piglets as an element of sustainable pig production. Parasitological examination was performed using coproscopic methods. The experimental material were faeces collected from the same sows from gestation to lactation and their piglets. The total number of coproscopic samples was 840. In the collected material Oesophagostomum spp., Ascaris suum and Eimeria spp. in sows were diagnosed, while in piglets, Eimeria spp. and Oesophagostomum spp were diagnosed. A relationship between the intensity of coccidian infections of lactating sows and the intensity of the infection of piglets was also demonstrated (rs = 0.57; p = 0.035). Sows are the primary source of infections in piglets. The assessment of infection intensity using diagnostic methods in sows should be the basis of an endoparasite control, because deworming without a prior diagnostic gives a short term effect and excludes the principles of the sustainable development of pig production.

1. Introduction

Parasitic diseases contribute to the impaired growth and development of pigs and slower weight gains, which directly translates into prolonged fattening periods [1,2,3]. Laboratory diagnostics on the farm make it possible to assess the situation in terms of infection intensity in the herd and select an antiparasitic agent optimally adapted to the developmental stage of the parasites. This reduces production costs and is more effective than the routine deworming of animals [4,5].
The deworming program used in piggeries is most often based on the administration of active substances (ivermectin, fenbendazole) in the form of injections or addition to water. However, the effectiveness of the administration of the agent does not eliminate the occurrence of endoparasites in the herd. Therefore, in addition to the key parasitological diagnostics, the introduction of natural substances that increase the immunity of animals should be considered as one of the elements of the herd health program [6,7,8].
In the case of pneumonia in pigs, it is manifested by coughing, both the veterinarian, zootechnician and the producer start treatment with the administration of antibiotics, first excluding Ascaris suum infection, because the animal was previously dewormed. The consequence of which is a two-way action, mainly the administration of a deworming agent and an antibiotic. The result of such action is the weakening of the pigs’ body condition an its health in general [9].
Fighting off ecto- and endoparasites consists of treating animals, as well as preventing infection by introducing a biosecurity program or sanitary and veterinary procedures in herds [10].
Some pig producers and veterinarians routinely administer deworming agents and coccidiostats without prior laboratory diagnostics and assessment of the intensity of infection in the herd. It is important to carry out laboratory tests of coproscopic tests in order to identify the parasites as well as the intensity of their occurrence and determine the developmental form. Such a diagnostic picture translates into the possibility of adjusting the active substance to the appropriate group of pigs and, consequently, translates into a better health status of the herd and a reduction in production costs. These elements should be included in the prevention program related to endoparasites [3].
The diagnosis of parasitic infection is typically conducted with coproscopic methods. It is a quick test that does not require too specialized equipment, and it is recommended in particular in sows in which the disease caused by endoparasites is usually subclinical [11]. Roepstorff et al. [12] claim that the effect of antenatal deworming is short-lasting and the regular use of anthelmintic agents in intensive herds shows little effect, which means that deworming brings little benefit. The problem of parasitic diseases is particularly significant with regard to sows, i.e., a technological group that is kept the longest and that usually infects piglets during the rearing period [13,14,15].
There is a legal requirement to test dead pigs for infectious diseases, but this does not take into account the intensity of endoparasite infection [16].
Scientific studies clearly show that the condition of the animals and the quality of raw materials obtained from them have a significant impact on the health of consumers [17,18,19].
Therefore, it should be a priority to act so as to ensure the maximum protection of human health. Thus, a programme for the periodic assessment of the infection of pigs should be implemented, especially given the increasing population of this species in world, which means a greater risk of the spread of internal parasites [20]. The aim of the study was the diagnosis of endoparasitic infection in sows and piglets as an element of sustainable pig production.

2. Materials and Methods

The animal study protocol was approved by the Animal Welfare Advisory Team (decision No. 4/2022, Wrocław, Poland) before the onset of the trial.

2.1. Animal Management

The study was conducted on a closed-cycle pig farm producing about 1000 fattening pigs per year. The size of the basic herd was 55 heads, with the Polish Large White genotype accounting for 15% of the sows, Polish Landrace—25% and hybrids—60%.
The rearing period was 35 days. In the herd, the average number of live-born piglets was approx. 11 piglets, with an average body weight of 1.1 kg. During parturition, the sows were given oxytocin. After birth, the litters were equalized. On the second day of life, the teeth were shortened and the tails were cut off. On the third day of life, the piglets were injected with iron solution (Uniferon). Boars were surgically castrated between 5th and 7th days of life. The animals were fed with a complete feed for sows during pregnancy and lactation, and the piglets with a prestarter. Sows were fed in a dosed manner using a feeding station during pregnancy and lactation, and piglets were fed ad libitum. The experiment included a similar ratio of primiparous to multiparous. During the experiment, all animals had the same environmental conditions and zootechnical treatments.
One hybrid Duromax boar was kept on the farm. Two weeks before parturition, sows in the study received deworming agent by injection (ivermectin 1%), while whole pig farm is using deworming program (using fenbendazole and ivermectin alternately). The veterinarian had not examined the faeces for parasites.

2.2. Sample Collection

Parasitological examination was performed using coproscopic methods. Fourteen sows with their piglets were subjected to diagnostics. The experimental materials were faeces collected from animals covered in the study. Faeces were collected immediately after defecation from selected pigs included in the study and preserved in plastic containers with 4% formalin solution. The experiment was conducted on the same animals that were diagnosed in terms of endoparasitological study from the 108th day of gestation to the 24th day of lactation and their piglets. The total number of coproscopic samples was 840 coming from three production groups, mainly sows in late gestation, sows in lactation and suckling piglets. In each production group faeces samples were collected in order: 42 samples from: sows in late gestation (108, 110 and 112 days of gestation); 112 samples from lactating sows (1, 2, 7, 12, 17, 22, 27, 32 days of lactation) and 686 samples from piglets (5, 6, 7, 10, 15, 20, 25, 35 days of life). Sows were sampled individually while piglets were sampled collectively. Parasitological analysis was performed in the laboratory of the Division of Pig and Horse Breeding at the Institute of Animal Husbandry and Breeding of Wrocław University of Environmental and Life Sciences. The McMaster quantitative technique modified by Gundłach and Sadzikowski [10] was used to perform parasitological diagnosis (detection and isolation of eggs/oocysts from faeces). Eggs/oocysts were diagnosed and identified in accordance with Zajac and Conboy’s recommendations [21].
The parasitological diagnosis established the following:
  • Prevalence—the ratio of the number of positive samples to the number of samples tested;
  • Mean EPG and OPG—the mean number of eggs/oocysts in 1 g of faeces; generic and species diversity of parasites;
  • In order to estimate the intensity of endoparasites infection in piglets, the rearing period was divided into 3 periods, taking into account the development of the gastrointestinal tract in the above-mentioned group as well as infection vectors and the life cycle of endoparasites:
    -
    1st period—from the 5th day of life to the 14th day of life.
    -
    2nd period—from the 15th day of life of life to 26 days of age.
    -
    3rd period—from 27 days of life to 35 days of age.

2.3. Statistical Analysis and Model Procedure

In order to test the significance of the relationship between nominal variables—prevalence and lactation period, as well as between prevalence and gestation period—Pearson’s chi-square (χ2) test of independence of two variables was performed. Taking into account the size of the tables, the calculated chi-square test took into account the continuity correction (χ2 test with Yates correction). For contingency tables in which the number of cases was less than 30 or in any cell the expected number was less than 5, Fisher’s exact test was used. Friedman’s test was used to compare the level of infection intensity on particular measurement day. If there were more than 3 measurements in the analysis, a correction for multiple comparisons was applied. In the conducted analysis in order to determine the nature of the existing differences, a post hoc analysis was performed using Dunn’s test with the correction of the Bonferroni significance level.
Then, in order to determine the relationship between the variables, Spearman’s correlation analysis and ordinal regression analysis were used.
The collected results were statistically processed using IBM SPSS Statistics 25.0 and Office Excel 2016. The adopted level of significance was α = 0.05.

3. Results

The coproscopic analysis of 154 faecal samples collected from sows during late gestation (108, 110 and 112 days) and lactation (1, 2, 7, 12, 17, 22, 27 and 32 days) indicated the infection prevalence of the sows at 100%. The number of identified eggs in a single sample ranged from 1 to 630, with an average EPG number of 2174. Oesophagostomum spp., Ascaris suum and Eimeria spp. were diagnosed in the collected material. Figure 1 shows the prevalence of infection in sows with individual parasites during gestation, and Figure 2, during lactation. During gestation, the largest number of sows were infected with coccidia (85.7%), and the lowest, with Ascaris suum (21.4%) (Figure 1).
During the lactation period, coccidia were observed in all sows (100%). In the studied group of sows, Ascaris suum was the least frequent (Figure 2). After the period of late gestation (parturition), an increase in the level of parasitic infection in sows could be observed.
An analysis of samples collected during gestation showed no differences in prevalence by parasite type p = 0.072, which means that there was no relationship between the occurrence of endoparasites in mixed infection.
On the other hand, at the level of the statistical tendency, a lower prevalence in pregnant sows with Ascaris suum parasites is visible in comparison with the other two parasites (21.4%). In addition, the analysis showed that the percentage of sows infected with Ascaris suum parasites was lower (21.4%, p = 0.033) than in uninfected sows, and for coccidia parasites, the percentage of infected sows was higher (85.7%, p = 0.008) than in uninfected sows. For Oesophagostomum spp. parasites, the percentage of infected sows was 35.7% and that of uninfected sows was 64.3%. Similarly, the analysis was carried out for the lactation period of the sows. The conducted analysis showed no differences in prevalence due to the type of parasites p = 0.115. In addition, the analysis showed that the percentage of sows infected with Oesophagostomum spp. parasites was higher (85.7%, p = 0.008) than in uninfected sows. During the summer period all sows were infected with coccidia (Table 1).
The prevalence of parasitic infections in piglets by the sows was 100%. All litters (100%) were infected with Eimeria spp., and one litter (7.14%) was diagnosed with infection with Oesophagostomum spp.
The analysis showed significant differences in the intensity of infections between the periods listed above in terms of the mean EPG of parasites as well as the mean OPG of coccidia. In order to determine the nature of the differences between the periods, an additional analysis was performed with post hoc Dunn’s test with Bonferroni’s significance level correction (Figure 3, Figure 4).
With regard to the mean EPG of parasites (Figure 3), the intensity of infection in piglets in period one was significantly higher than in period three (p < 0.001), while the mean EPG in periods one and two (p = 0.054) and periods two and three (p = 0.392) were similar. An analysis was then performed for the intensity of coccidia OPG (Figure 4). It was significantly higher in period one than in periods two (p = 0.042) and three (p < 0.001), while the intensity of infection in periods two and three was similar (p = 0.558).
In order to determine the relationship between the occurrence of coccidia in lactating sows and the intensity of coccidial infection in piglets, Spearman’s rank correlation analysis was performed. The analysis showed a moderate and positive relationship between the variables (rs = 0.57; p = 0.035), which means that the higher the intensity of coccidial infection in lactating sows, the higher the intensity of coccidial infection in piglets.

4. Discussion

According to Balicka-Ramisz et al. [22], Oesophagostomum spp. was most prevalent in the farms—68.6%, followed by Eimeria protozoa—42.9%, and Ascaris suum—28.6%. The same study also identified the occurrence of Trichuris suis—21.4%, and Strogyloides spp.—11.4%. In our study, no nematodes were found. In Karamon and Ziomko’s analysis [23], the presence of coccidia was found in 21.3% of sows. Thamsborg [24] identified Eimeria spp. as the most frequent parasite in sows (17.5%), followed by the nematodes Ascaris summ and Oesophagostomum spp. Research by Bartosik et al. [13] showed that the most common parasite in intensively farmed sows was Oesophagostomum spp.—36%. The studied group of sows also showed the presence of coccidia and Ascaris suum at a prevalence level of 4%. Karamon et al. [25] report that 146 litters of suckling piglets (30.9%) were diagnosed with Isospora suis infection, while 16 litters (3.4%) showed Eimeria spp. infection.
Coccidia in piglets cause diarrhoea. The first studies carried out in the USA showed that coccidia were identified most frequently in suckling piglets [26]. Coccidiosis in piglets is usually acute and manifested by diarrhoea, which directly reduces piglets’ immunity [27]. Older animals, such as sows or fattening pigs, are asymptomatic [28].
Meyer et al. [29] report that many studies showed a correlation between the occurrence of coccidiosis and the farm size. The problem of coccidiosis concerns large closed-cycle farms.
The main source of piglet infection is the environment, followed by the sow. It only takes 100 oocysts to infect a piglet. Oocysts are resistant to external factors and the environment in the piggery is conducive to spreading the disease from one litter to another. The occurrence of coccidiosis in piglets is influenced by zoohygienic conditions, the way the animals are kept (shallow bedding, slat floor), herd size, litter size, time of year and even the organisation of work on the farm [30].
Coccidiosis is a dangerous parasitic disease. It leads to the loss of intestinal villi, thus impairing digestion and food absorption. Symptoms of coccidiosis typically occur between the eighth and fifteenth day of the life of piglets, which is why the disease is commonly known as “diarrhoea of the tenth day.” Isosporosis in litters is characterised by the uneven course of the disease. Some piglets show typical symptoms, while others are asymptomatic. This results in uneven weight gains within the litter, with an average difference of 1.4 kg per piglet [31,32,33,34]. During the course of isosporosis, two or three phases of increased infection—manifested as increased intensity of oocyst excretion—can be observed. Between the phases there are periods of absence of diarrhoea, and lower or no oocyst excretion in the faeces [25].
In the study group, diarrhoea was observed in 10 litters between 9 and 14 days of life. In the first period (days 5–14), a high intensity of infection with coccidia was observed (1410 OPG). Then, in the second period (days 15–26), after the administration of the anticoccidial agent, a decrease in the mean OPG (to 405) was observed. In the third period (days 27–35), there was a renewed increase in the intensity of infection (860 OPG) (Figure 4). Presumably, the anticoccidial drug was ineffective, the piglets were reinfected by the sows because they were carriers, or the course of isosporosis occurred in the phases discussed above.
Chae et al. [35] report that if coccidiosis has occurred in a herd, the elimination of oocysts from the environment is not possible. In order to decrease the number of oocysts in the piggery and to reduce the acuteness of the disease, a prophylactic programme has to be implemented.
The control of coccidiosis is based on treatment, but prevention is key. Currently in the European Union, an effective means of control of isosporosis is the administration of a coccidicide to piglets at an early stage to prevent the development and excretion of oocysts. Additionally, proper zoohygienic conditions should be maintained in the piggery—pens should be properly cleaned and disinfected to remove oocysts from the environment on a regular basis [26]. Research by Knecht and Jankowska-Mąkosa [4] showed that parasitic infection affected the reproductive performance of sows in the first year of exploitation. Infected sows were characterised by a lower number of live piglets—by 0.21 heads, a higher number of stillborn piglets—by 0.21 heads, as well as lower daily weight gains of piglets—by 15 g, which resulted in their lower weaning body weight—by 0.45 kg. No similar relationships were found in this study. Karamon et al. [25] showed that piglets infected with the parasite Isospora suis had shorter intestinal villi and decreased body weight gains, not only during the occurrence of clinical symptoms, but also after the weaning period (6–7 weeks of age). The decrease in body weight gain during coccidiosis is 15%, which results in a lower weaning weight of 500 g per head. Some researchers have found that the decrease in body weight can reach about 1 kg [3,36,37,38].
Taking into consideration the goals and effects of the implementation of the principles of sustainable pig production, care for the condition and well-being of pigs, deworming without prior diagnosis does not solve the problem of parasitic invasions in the herd. The body is burdened with pharmacological agents, which translates into the functioning of the digestive system, i.e., the effectiveness of nutrition does not eliminate the problem of endoparasites in pigs. As the results shows, one of the underestimated methods in the organization and management of the herd is the lack of a health program including the diagnosis of endoparasites. The welfare and comfort of animals should be a priority and the endoparasite control program should take into account: the improvement of production conditions and an increase in its efficiency, the improvement of the farm’s financial status, a reduction of treatment costs and a reduction of the drug resistance of parasites to antiparasitic agents [4,15].
The health of the herd is the decisive factor for the profitability of pig farming and production. Along with the greater stocking density in pigsties, the risk of pathogens increases. According to Petterson et al. [39], among many studies conducted around the world, one of the main causes of economic losses in pig production is the death of animals due to the occurrence of diseases on farms, despite the use of various prevention and treatment programs. Emerging diseases result in a decrease in the health status of the herd and a deterioration in the quality of the pork produced. The task of each pig farmer is to establish a herd health plan that has a positive effect on animal welfare and production conditions and increases in production efficiency [40]. According to Roepstorff and Nansen [41], the effect of sows deworming before parturition is short-term, and the regular use of the same active substances in high-production herds shows low effectiveness, so the benefit from deworming is insignificant. The prevalence of infection and the average EPG could be related to the length of the use of the sows in the herd (3 years). Assuming that the sows were dewormed twice a year (for a period of about two weeks before farrowing, the frequency of farrowing was twice a year), attention should be paid to their reduced immunity after six farrowings in 3 years, and the possibility of drug resistance to the administered deworming agent (especially in the case of Oesophagostomum spp., the frequent occurrence of which is the result of the emergence of drug resistance to the administered active substance).The effect of using the drug should be long-lasting, because one-time deworming does not bring the expected results. Periodic laboratory tests should be performed to diagnose parasites. The concept of sustainable pig production is fully integrated with such an approach, providing a real perspective against the conventional way of management, which is no longer working. Sustainable pig production practices allow for a more effective use of the means used in pig production and better protection of the environment and surroundings in which the farm operates, limiting the use of antiparasitic drugs used in production [10,42,43].
In pig production, parasites pose a threat to young sucklers, which have low immunity, and cause losses in later exploitation due to stunted growth and reduced body weight [42,44,45,46].
Studies have shown that there is a need to monitor the pig production in order to improve the condition of animals. Diagnostic studies on genus/species endoparasites in pigs are appropriate and should be continued. Animal welfare should be included in the characteristics of modern production chains, and the previous statements leads us towards the broader issue of sustainable pig production. Its concept is based on the effective production of safe, high-quality products in a way that protects and supports the improvement of the natural environment, the socio-economic conditions of farmers, employees and local communities, as well as the protection of animal health and welfare.
Currently, without prior diagnosis, antiparasitic agents are administered to animals, which does not contribute to the improvement of both production and the natural environment. Without mandatory antiparasitic diagnostics, which is not legally sanctioned, there is no way to improve the welfare of pigs in this aspect. The impact of infections, e.g., with endoparasites, on the breeding, fattening and slaughter performance of pigs, confirmed in the studies published so far [43], correlates well with the introduction of environmental diagnostics and prophylaxis of the chain of sustainable pork production. Therefore, the assessment of infection intensity through the introduction of diagnostic methods should be the basis of a parasite control program, especially in sows used in herds.

5. Conclusions

In conclusion, sows are the primary source of infection in piglets. In the collected material Oesophagostomum spp., Ascaris suum and Eimeria spp. in sows were diagnosed, while in piglets Eimeria spp. and Oesophagostomum spp. were diagnosed. The number of sows infected with Ascaris suum was lower (21.4%, p = 0.033) than of uninfected sows, and for coccidia, the percentage of infected sows was higher (85.7%, p = 0.008) than of uninfected sows. Additionally, the analysis showed that the percentage of sows infected with Oesophagostomum spp. was higher (85.7%, p = 0.008) than of uninfected sows. An analysis was then performed for the intensity of coccidia OPG in piglets. The results show that it was significantly higher in period one than in periods two (p = 0.042) and three (p < 0.001), while the intensity of infection in periods two and three was similar (p = 0.558). A relationship between the intensity of coccidian infections in lactating sows and the intensity of infection in piglets was also demonstrated (rs = 0.57; p = 0.035). Sows are the primary source of infection in piglets. The assessment of infection intensity using diagnostic methods in sows should be the basis of an endoparasite control, because deworming without a prior diagnostic gives a short term effect and excludes the principles of sustainable development of pig production.

Author Contributions

Conceptualization, A.J.-M. and D.K.; methodology, A.J.-M. and D.K.; software, A.J.-M.; validation, D.K.; formal analysis, A.J.-M.; investigation, A.J.-M., S.W. and D.K.; resources, A.J.-M.; data curation, A.J.-M.; writing—original draft preparation, A.J.-M. and D.K.; writing—review and editing, A.Z.-W.; visualization, A.J.-M.; supervision, D.K.; project administration, A.J.-M. and D.K.; funding acquisition, D.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Animal Welfare Advisory Team Statement No. 04/2022.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Balicka-Ramisz, A.; Wieczorek-Dąbrowska, M. Pasożytnicze nicienie przewodu pokarmowego świń (Parasitic nematodes gastrointestinal tract in pigs—in Polish). Trzod Chlew 2007, 8/9, 160–162. [Google Scholar]
  2. Chantziaras, I.; Dewulf, J.; Van Limbergen, T.; Klinkenberg, M.; Palzer, A.; Pineiro, C.; Aarestrup Moustsen, V.; Niemi, J.; Kyriazakis, I.; Maes, D. Factors associated with specific health, welfare and reproductive performance indicators in pig herds from five EU countries. Prev. Vet. Med. 2018, 159, 106–114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Jankowska-Mąkosa, A.; Knecht, D. The influence of endoparasites on selected production parameters in pigs in various housing systems. Res. Vet. Sci. 2015, 100, 152–160. [Google Scholar] [CrossRef] [PubMed]
  4. Knecht, D.; Jankowska-Mąkosa, A. Endoparasites in sows and selected reproduction parameters. Acta Vet. Beogr. 2020, 70, 71–80. [Google Scholar] [CrossRef]
  5. Schubnell, F.; von Ah, S.; Graage, R.; Sydler, T.; Sidler, X.; Hadorn, D.; Basso, W. Occurrence, clinical involvement and zoonotic potential of endoparasites infecting Swiss pigs. Parasitol. Int. 2016, 65, 618–624. [Google Scholar] [CrossRef]
  6. Popiołek, M.; Knecht, D.; Boruta, O.; Kot, M. Effect of breeding conditions, phynology and age on the occurrence of helminthes in pig. A preliminary study. Bull. Vet. Inst. Puławy Arch. 2009, 53, 213–220. [Google Scholar]
  7. Waller, P.J. International approaches to the concept of integrated control of nematode parasites of livestock. Int. J. Parasitol. 1999, 29, 155–164. [Google Scholar] [CrossRef]
  8. Sures, B. Environmental parasitology: Relevancy of parasites in monitoring environmental pollution. Parasitol. Today 2004, 20, 170–177. [Google Scholar] [CrossRef]
  9. Boes, J.; Kanora, A.; Havn, K.T.; Christiansen, S.; Vestergaard-Nielsen, K.; Jacobs, J.; Alban, L. Effect of Ascaris suum infection on performance of fattening pigs. Vet. Parasitol. 2010, 172, 269–276. [Google Scholar] [CrossRef]
  10. Gundłach, J.L.; Sadzikowski, A.B. Parasitology and Parasitosis of Animals, 1st ed.; PWRiL: Warszawa, Poland, 2004. [Google Scholar]
  11. Madson, D.M.; Arruda, P.H.E.; Arruda, B.L. Nervous and locomotor systems. In Diseases of Swine, 11th ed.; Zimmerman, J.J., Karriker, L.A., Ramirez, A., Schwartz, K.J., Stevenson, G.W., Zhang, J., Eds.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2019; pp. 339–372. [Google Scholar]
  12. Roepstorff, A.; Nilsson, O.; Oksanen, A.; Gjerde, B.; Richer, S.H.; Ortenberg, E.; Christensson, D.; Martinsson, K.B.; Bartlett, P.C.; Nansen, P.; et al. Intenstinal parasites in swine in the Nordic countries: Prevalence and geographical distribution. Vet. Parasitol. 1998, 76, 305–319. [Google Scholar] [CrossRef]
  13. Bartosik, J.; Rekiel, A.; Klockiewicz, M.; Górski, P.; Batorska, M. The effect of housing system on the incidence of intestinal parasite infestation in pigs. J. Cent. Eur. Agric. 2012, 13, 760–768. [Google Scholar] [CrossRef] [PubMed]
  14. Eijck, J.L.; Borgsteede, F.H.M. A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in the Netherlands. Vet. Res. Commun. 2018, 29, 407–414. [Google Scholar] [CrossRef] [PubMed]
  15. Knecht, D.; Jankowska, A.; Zaleśny, G. The impact of gastrointestinal parasites infection on slaughter efficiency in pigs. Vet. Parasitol. 2012, 184, 291–297. [Google Scholar] [CrossRef]
  16. Tarczyński, S. Parasitic worms of swine and wild boars in Poland. Acta Parasitol. Pol. 1956, 4, 663–780. [Google Scholar]
  17. Beattiea, V.E.; O’Connella, N.E.; Moss, B.W. Influence of environmental enrichment on the behaviour, performance and meat quality of domestic pigs. Livest. Prod. Sci. 2000, 65, 71–79. [Google Scholar] [CrossRef]
  18. Brown, S.N.; Warriss, P.D.; Nute, G.R.; Edwards, J.E.; Knowles, T.G. Meat Quality in Pigs Subjected to Minimal Preslaughter Stress. Meat Sci. 1998, 49, 257–265. [Google Scholar] [CrossRef]
  19. Pérez, M.P.; Palacio, J.; Santolaria, M.P.; Aceña, M.C.; Chacón, G.; Gascón, M.; Calvo, J.H.; Zaragoza, P.; Beltran, J.A.; García-Belenguer, S. Effect of transport time on welfare and meat quality in pigs. Meat Sci. 2002, 61, 425–433. [Google Scholar] [CrossRef]
  20. Dexter, N. Stochastic models of foot and mouth disease in feral pigs in the Australian semi-arid rangelands. J. Appl. Ecol. 2003, 40, 293–306. [Google Scholar] [CrossRef]
  21. Zajac, A.M.; Conboy, G.A.; Little, S.E.; Reichard, M.V. Veterinary Clinical Parasitology, 9th ed.; John Wiley & Sons, Inc: Hoboken, NJ, USA, 2021. [Google Scholar]
  22. Balicka-Ramisz, A.; Wiśniewski, J.; Stadnytska, O. Extensity and intensity of intestinal parasite infections in pigs in different types of farm organization. Acta Sci. Pol. Zootech. 2019, 18, 47–50. [Google Scholar] [CrossRef]
  23. Karamon, J.; Ziomko, I. Występowanie kokcydiów u prosiąt ssących i macior w Polsce (The prevalence of coccidia in suckling piglets and sows in Poland—in Polish). Med. Wet. 2006, 62, 294–296. [Google Scholar]
  24. Thamsborg, S.M.; Roepstorff, A.; Larsen, M. Integrated and biological control of parasites in organic and conventional production systems. Vet. Parasitol. 1999, 84, 169–186. [Google Scholar] [CrossRef] [PubMed]
  25. Karamon, J.; Ziomko, I.; Cencek, T.; Sroka, J.; Kozaczyński, W.; Karpińska, T. Course of experimental Isospora suis infection in piglets. Bull. Vet. Inst. Puławy Arch. 2008, 52, 537–540. [Google Scholar]
  26. Biehl, L.G. Diagnosis, treatment and prevention in diarrhea in 7-14-day-old pigs. J. Am. Vet. Med. Assoc. 1986, 188, 1144–1146. [Google Scholar]
  27. Kipper, M.; Andretta, I.; Gonzales Monteiro, S.; Lavatto, P.A.; Lehnen, C.R. Meta-analysis of the effects of endoparasites on pig performance. Vet. Parasitol. 2011, 181, 316–320. [Google Scholar] [CrossRef] [Green Version]
  28. Martineau, G.P.; del Castillo, J. Epidemiological, clinical and control investigations on field porcine coccidiosis: Clinical, epidemiological and parasitological paradigms? Parasitol. Res. 2000, 86, 834–837. [Google Scholar] [CrossRef]
  29. Meyer, C.; Joachim, A.; Daugschies, A. Occurrence of Isospora suis in larger piglet production units and on specialized piglet rearing farms. Vet. Parasitol. 1999, 82, 277–284. [Google Scholar] [CrossRef]
  30. Stuart, B.P.; Gosser, H.S.; Allen, C.B.; Bedell, D.M. Coccidiosis in swine: Dose and age response to Isospora suis. Can. J. Comp. Med. 1982, 46, 317–320. [Google Scholar]
  31. Mundt, H.C.; Joachim, A.; Becka, M.; Daugschies, A. Isospora suis: An experimental model for mammalian intestinal coccidiosis. Parasitol. Res. 2006, 98, 167–175. [Google Scholar] [CrossRef]
  32. Niestrath, M.; Takla, M.; Joachim, A.; Daugschies, A. The role of Isospora suis as a pathogen in conventional piglet production in Germany. J. Vet. Med. Ser. B Infect. Dis. Vet. Public Health 2002, 49, 176–180. [Google Scholar] [CrossRef]
  33. Torres, A. Prevalence survey of Isospora suis in twelve European countries. In Proceedings of the 18th IPVS Congress, Hamburg, Germany, 1–27 July 2004. [Google Scholar]
  34. Worliczek, H.L.; Buggelsheim, M.; Saalmüller, A.; Joachim, A. Porcine isosporosis: Infection dynamics, pathophysiology and immunology of experimental infections. Wien. Klin. Wochenschr. 2007, 119, 33–39. [Google Scholar] [CrossRef] [PubMed]
  35. Chae, C.; Kwon, D.; Kim, O. Diarrheoa in nursing piglets associated with coccidiosis: Prevalence, microscopic lesions, and coexisting microorganisms. Vet. Rec. 1998, 143, 417–420. [Google Scholar] [CrossRef] [PubMed]
  36. Koudela, B.; Kucerová, S. Role of acquired immunity and natural age resistance on course of Isospora suis coccidiosis in nursing piglets. Vet. Parasitol. 1999, 82, 93–99. [Google Scholar] [CrossRef] [PubMed]
  37. Larsen, K. Isospora suis—neonatal coccidiosis in pigs. Dan. Vet. Tidsskr. 1996, 79, 387–392. [Google Scholar]
  38. Robinson, Y.; Morin, M.; Girard, C.; Higgins, R. Experimental transmission of intestinal coccidiosis to piglets: Clinical, parasitological and pathological findings. Can. J. Comp. Med. 1983, 47, 401–407. [Google Scholar] [PubMed]
  39. Pettersson, E.; Sjölund, M.; Wallgren, T.; Osterman Lind, E.; Höglund, J.; Wallgren, P. Management practices related to the control of gastrointestinal parasites on Swedish pig farms. Porc. Health Manag. 2021, 7, 12. [Google Scholar] [CrossRef] [PubMed]
  40. Delsart, M.; Fablet, C.; Rose, N.; Reperant, J.-M.; Blaga, R.; Dufour, B.; Pol, F. Descriptive Epidemiology of the Main Internal Parasites on Alternative Pig Farms in France. J. Parasitol. 2022, 108, 306–321. [Google Scholar] [CrossRef] [PubMed]
  41. Roepstorff, A.; Nansen, P. Epidemiology and control of helminth infections in pigs dunder intensiva and non-intensive production systems. Vet. Parasitol. 1994, 54, 69–85. [Google Scholar] [CrossRef]
  42. Daugschies, A.; Imaron, M.; Ganter, M.; Bollwahn, W. Prevalence of Eimeria spp. in sows at piglet-producting farms in Germany. J. Vet. Med. B 2004, 51, 135–139. [Google Scholar] [CrossRef]
  43. Nosal, P.; Eckert, R. Gastrointestinal parasites of swine in relation to the age group and management system. Med. Wet. 2005, 61, 435–437. [Google Scholar]
  44. Villee, C.A.; Martin, D.W.; Solomon, E.P.; Berg, L.R. Biology, 10th ed.; Cengage Learning: Stamford, CT, USA, 2015. [Google Scholar]
  45. Wieler, L.H.; Ilieff, A.; Herbat, W.; Bajer, C.; Vieler, E.; Bauerfeind, R.; Failing, K.; Klos, H.; Wengert, A.; Baljer, G.; et al. Prevalence of enteropathogens in suckling and weaned piglets with diarrhea in South Germany. J. Vet. Med. B 2001, 48, 151–159. [Google Scholar] [CrossRef]
  46. Knecht, D.; Popiołek, M.; Zaleśny, G. Does meatiness of pigs depend on the level of gastro-intestinal parasites infection? Prev. Vet. Med. 2011, 99, 234–239. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Parasitic infection of sows during late gestation.
Figure 1. Parasitic infection of sows during late gestation.
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Figure 2. Parasitic infection of sows during lactation.
Figure 2. Parasitic infection of sows during lactation.
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Figure 3. Mean EPG in piglets in particular periods.
Figure 3. Mean EPG in piglets in particular periods.
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Figure 4. Mean OPG in piglets in particular periods.
Figure 4. Mean OPG in piglets in particular periods.
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Table
Table 1. Prevalence of parasites during gestation and lactation.
Table 1. Prevalence of parasites during gestation and lactation.
Physiological PhaseUninfected SowsInfected Sows
n%n%χ2(1)p
Gestation period
Oesophagostomum spp.535.7964.31.140.285
Ascaris suum1178.6 a321.4 b4.570.033
Eimeria spp.214.3 A1285.7 B7.140.008
Lactation period
Oesophagostomum spp.214.3 A1285.7 B7.140.008
Ascaris suum964.3535.71.140.285
Eimeria spp.0014100.0--
Explanation: n—abundance, χ2—degrees of freedom, p—significance level; a, b—different letters denoting statistically significant differences within the columns p ≤ 0.05; A, B—different letters denoting highly statistically significant differences within the columns p ≤ 0.01.
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Jankowska-Mąkosa, A.; Knecht, D.; Wyrembak, S.; Zwyrzykowska-Wodzińska, A. Evaluation of the Level of Parasites Infection in Pigs as an Element of Sustainable Pig Production. Sustainability 2023, 15, 3671. https://doi.org/10.3390/su15043671

AMA Style

Jankowska-Mąkosa A, Knecht D, Wyrembak S, Zwyrzykowska-Wodzińska A. Evaluation of the Level of Parasites Infection in Pigs as an Element of Sustainable Pig Production. Sustainability. 2023; 15(4):3671. https://doi.org/10.3390/su15043671

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Jankowska-Mąkosa, Anna, Damian Knecht, Sandra Wyrembak, and Anna Zwyrzykowska-Wodzińska. 2023. "Evaluation of the Level of Parasites Infection in Pigs as an Element of Sustainable Pig Production" Sustainability 15, no. 4: 3671. https://doi.org/10.3390/su15043671

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