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Does meatiness of pigs depend on the level of gastro-intestinal parasites infection?
Preventive Veterinary Medicine 99 (2011) 234–239
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Does meatiness of pigs depend on the level of gastro-intestinal parasites infection? Damian Knecht a , Marcin Popiołek b,∗ , Grzegorz Zale´sny c a
Department of Pigs Breeding, Institute of Animal Breeding, Wrocław University of Environmental and Life Sciences, Chełmo´ nskiego 38c, 51-630 Wrocław, Poland b ˙ Institute of Biology, Department of Invertebrate Systematics and Ecology, Wrocław University of Environmental and Life Sciences, Kozuchowska 5b, 51-631 Wrocław, Poland c Department of Parasitology, Institute of Genetics and Microbiology, Wroclaw University, Przybyszewskiego 63, 51-148 Wrocław, Poland
a r t i c l e
i n f o
Article history: Received 12 July 2010 Received in revised form 19 January 2011 Accepted 21 January 2011 Keywords: Intestinal parasites Meatiness Pigs Meat quality
a b s t r a c t The aim of the present paper was to determine an influence of the presence and a level of intestine parasites infection on the quality of pork carcass expressed by the content of meat in carcass (meatiness) in pigs. The experimental part of the study was conducted on pigs farm produced in a closed cycle. The population in the study included 120 fattening pigs maintained in two keeping systems: group I – 60 individuals kept on slatted floor, and group II – 60 individuals kept on deep litter. All the experimental animals were treated in the same manner. The analysed fatteners were slaughtered in Meat Processing Plant when their body mass reached 110 kg, and the post-slaughter assessment was conducted according to the EUROP classification of pigs carcass using the Ultra-Fom 300 device. The study concerning the internal parasites were conducted basing on coproscopic quantitative McMaster method. As a results, the eggs of three nematode taxa were isolated and identified: Oesophagostomum spp., Ascaris suum and Strongyloides ransomi. Overall prevalence of infection of fatteners kept on litter was lower (25% ± 11.2) as compared to those kept on slatted floor (38.3% ± 12.6), however the differences were not statistically significant (2 = 2.465; df = 1; P = 0.116). The mean value of meatiness for pigs free from parasites was 53.68, while in the case of infected pigs the meatiness was statistically lower and was 52.12 (t = 2.35; P = 0.02). The analysed pigs were classified into three categories and conducted analysis of an influence of parasites on meatiness demonstrate the relationship that is statistically significant. The analysis of correlation between meatiness and an average number of helminth eggs also demonstrated the negative, statistically significant, relationship (F = 5.52; P = 0.020), i.e. in fatteners with higher EPG value the meatiness was lower. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Pork accounts for over 60% of meat consumed in Poland in total. Half of that is an unprocessed meat, and culinary
∗ Corresponding author. Tel.: +48 71 3205883; fax: +48 71 3205876. E-mail address: [email protected] (M. Popiołek). 0167-5877/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2011.01.009
meat in processed form is about 50%. People consume more and more preserves, smoke-dried and dry cold meat, and definitely less amounts of canned food and products of higher fat content. Structural changes in an overall meat consumption point also initially increasing, and currently stable trend in poultry meat introduction into a diet. Also an increase in fish and fish products is observed (Małkowski et al., 2010). In a condition of a full market availability, wide
D. Knecht et al. / Preventive Veterinary Medicine 99 (2011) 234–239
range of products and high meat supply, the production of high quality meat that fulfils demands of consumers and producers as well is a very important problem (Przybylski et al., 2008). That issue becomes a significant one in a situation of a continuous trend towards an improvement in fattening pigs meatiness. The results concerning the mass population demonstrate that in a period from 1998 to 2009, the meatiness of pigs in Poland increased from 46.7% to about 54.5%. Selection leads towards an increase in growth rate and lean meat content in carcass is often connected with a decrease in slaughter mass of fattening pigs (the mass that qualifies the fattening pigs to slaughter, currently about 110 kg in Poland) and meat quality deterioration, like fat content, tenderness (Jaworska et al., 2006). For a long time, the slaughter value of carcass and quality of pork meat has been an object of an interest of scientists and also of technologists in meat processing plants. The quality of a product and economic results of a plant are to a very high degree conditioned by the quality of raw material. An intensive animal breeding with industrial fodders, and also the selection of pigs of notably meat genotypes for fattening, influence the quality of meat. The quality of meat include safety aspects (the presence of pathogenic microorganisms and those lowering meat stability, parasites, residues of drugs, heavy metals, and mycotoxins), nutritional value (the content of protein, fat, vitamins, mineral salts, and carbohydrates), its technological properties (water absorbability, pH value, stains content, meatiness, adiposity, and tendinuosity) and sensory features (colour, odour, tenderness, juiciness, and flavour) (Kajak et al., 2007). Also some environmental factors (turnover, slaughter process, and chilling) have a big influence on quality features of meat. Together with meatiness increase of fatteners produced, there is a tendency of a decrease in their stress resistance leading in a certain conditions to the deterioration in meat quality (Po´spiech et al., 1998). Parasites invasions in pigs are a common phenomenon. Their effect in fattening pigs lead to a decrease in body mass daily gains of about 50 g, worse feed utilization for body mass gain of about 3–9%, later date of slaughter body mass attainment of 10–15 days (Smets et al., 1999). An alleviation of parasites infection results is one of the factors of the increase in production level, and thus an increase in a profitability of pigs breeding and husbandry. In a course of parasitic diseases, even without any apparent disease symptoms, parasites infection induce high losses in pigs, since they damage blood vessels, internal organs or intestine epithelium by a migration of developmental forms. The results of such an activity are as follows: (1) worse fodder assimilation, (2) impaired process of intestinal absorption, (3) decrease in daily body mass gains, (4) fertility disorders, (5) delayed or incomplete obtaining of postvaccinal immunity towards infectious diseases, (6) prolongation of fattening period, and (7) deterioration in meat quality. The effect of an unprofitable influence of gastrointestinal parasites infection on the condition, health status and body mass gains of pigs is currently out of the question (Andersen, 1976; Patison et al., 1979; Urban et al., 1989; Gerwert et al., 2004). However, the study so far has not concerned the issues connecting the presence of para-
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sites with pork meat quality. The exception is the paper by Theodoropoulos et al. (2004) describing the selected indices of meat quality in pigs infected with intestine nematodes maintained on an indoor system. Similar issues, however with respect to other animals (sheep, goats and cattle) have been taken up in the literature (Gilka et al., 1983; Xia et al., 1991; De La Fuente et al., 1993; Daugschies et al., 2000; Arsenos et al., 2007, 2009). The results of above study, not very distinctly however point an unprofitable influence of parasites infection on a quality of meat of infected animals. The aim of the present paper was to determine an influence of the presence and a level of intestine parasites infection on the quality of pork carcass expressed by the content of meat in carcass (meatiness) in pigs kept in an indoor system. 2. Materials and methods 2.1. Field study The experimental part of the study was conducted on pigs farm producing in a closed cycle (based on the maintenance of all production groups on one farm), in a period of June–July 2009. The farm has an area of 28 hectares. The sows are introduced to the parturition department 14 days before farrowing. They stay there together with piglets for about 28–30 days. The sows were selected to the groups keeping the similar ration of primiparous sows to multiparous ones. All the sows were cross-bred of Large Polish White and Polish Landrace covered with cross-bred boars of Pietrain × 990. The experimental population in the study included 120 fattening pigs maintained in two keeping systems: group I – 60 individuals kept on slatted floor, and group II – 60 individuals kept on deep litter. The fattening pigs were kept in collective pens, 60 individuals in each. All the pigs were labelled with ear rings, each group with different colour, and a subsequent number. All the experimental animals were treated in the same manner. Fattening pigs were fed with commercially available complete feed mixtures. Microclimatic conditions were close to the optimal, and identical for the whole experimental population. The zootechnical treatments were unified in all the groups. One day after the birth the piglets were subject to canine cutting off, and at the second day the iron in the form of injection was given, and boar piglets were castrated. At the sixth week of life, the piglets were deworming with IVOMEC preparation in a form of injection just by the weaning. An active component of the preparation is Ivermectin – semi-synthetic avermectins derivative. According to the producers recommendations a dose of 300 g/kg of body mass was applied. Sows were dewormed 2 weeks before farrowing with the preparation of the same company. 2.2. Evaluation of meat quality The system of pigs classification basing on the content of lean meat in carcass is in force in the European Union. Polish slaughterhouses, since the day of the accession of Poland to the European Union, are obliged to classify the pig carcass in an EUROP system. The regulations concern-
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ing the classification of slaughter animals carcass specify the obligation of the classification by slaughterhouses, and an obligation of a supervision of the classification led by The Inspection of Trade Quality of Agricultural-Food Products. The decree of the Ministry of Agriculture and Rural Development determines the classes of the market quality of pigs carcass (EUROP classification), specifies the detailed requirements in the range of market quality of pigs carcass, entities entitled for the opinions concerning the equipment used for the assessment of market quality of pigs carcass and the method of pigs carcass analysis (Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm). The six classes are distinguished: (1) class S contains at least 60% of lean meat in carcass, (2) class E from 55% but less than 60%, (3) class U from 50% but less than 55%, (4) class R from 45% but less than 50%, (5) class O from 40% but less than 45%, and (6) class P contains less than 40% of meat. The analysed fatteners were slaughtered in Meat Processing Plant when their body mass reached 110 kg, and the post-slaughter assessment was conducted according to the EUROP classification of pigs carcass using the Ultra-Fom 300 device (Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm). 2.3. Sample collection and laboratory procedures The study on internal parasites in fattening pigs were conducted basing on coproscopic methods. The samples were collected during the whole fattening (3 months), in 3 periods – at the beginning, in the middle and at the end of the time of fattening, i.e. with fattening pigs body mass of 40, 70 and 110 kg. First samplings were conducted after the pigs reached body mass of about 40 kg, i.e. 2 weeks after fattening beginning, so that the group was adapted for the room. The research material was fresh faeces samples of about 5 g each, collected directly after defecation from the bedding to labelled plastic containers. All pigs were labelled with ear rings, and additionally with colours. Since each time six person took part in samples collection from one pen, there was an attempt to assign the particular faeces samples to particular identified individual. The samples were collected from the same parts of the pen, representing all the places of animals defecation. They were situated in the middle and extreme sectors of the pen. The samples were preserved in 4% formalin solution. The quantitative method of McMaster (Gundłach and Sadzikowski, 2004) with the use of saturated NaCl solution as a flotation agent was applied to the determination and isolation of parasites eggs. Additionally, in order to show the potential invasions of a low intensity, the standard flotation method was used concurrently. The eggs discovered were identified basing on their morphology (shape, sheath structure, number and size of blastomeres or larvae presence) and biometry. The identification was done using the elaborations by Thienpont et al. (1986) and Zajac and Conboy (2006). To estimate the level of analysed animals infection, the basic parasitological indices were applied: extensiveness of infection (%) – understood as the ratio of the number of positive samples to an overall number of analysed samples, and mean number of eggs in 1 g of faeces (EPG). According to the work by Rohlf and Sokal (1995) the prevalence value was given with 95% confidence inter-
val. The mean EPG value in turn, was determined as an arithmetic mean with the range of values obtained. 2.4. Statistical analysis The analysis of the relationship between mean EPG and meatiness class was done using a nonparametric Kruskall–Wallis test. Meatiness class was also analysed by maximum likelihood techniques based on log-linear analysis of contingency tables, beginning with the most complex model involving all possible effects (keeping system and presence/absence of helminths) and interactions. Next the minimum sufficient model was generated where Chi-square result was not significant, indicating that the model was adequate in explaining the data. Additionally the influence of helminth presence on the mean meatiness value was analysed by students t-test. In the next step we analysed the dependence of meatiness in the relation with qualitative (keeping system) and qualitative (EPG values) predictors using GLM (general linear models) method. In the case of that analysis EPG values and meatiness were transformed logarithmically (log(x) + l). In all statistical method applied, the agreed significance level was 0.05. The calculations were conducted using Statistica 9.0 PL packet. 3. Results and discussion One hundred and twenty faeces samples from fatteners maintained in the two different systems, i.e. on a litter (n = 60) and on so-called slatted floor (n = 60) were subject to analysis. An overall extensiveness of infection appeared to be small and was 31.6% ± 8.4. As a results of coproscopic study conducted, the eggs of three nematode taxa were isolated and identified: Oesophagostomum spp., Ascaris suum and Strongyloides ransomi. All determined nematodes are typical and commonly present parasites of pigs. Oesophagostomum spp. determined to the generic level was in Poland represented as far by only one species – Oesophagostomum dentatum. Since Nosal et al. (2007) for the first time described the second species of that type – O. quadrispinulatum, – in pigs in Poland, the detailed identification of morphologically and biometrically eggs appeared to be impossible. The highest prevalence of infection and mean EPG values were noted for nematodes from Oesophagostomum spp.: 20.8% ± 4.1 and 840 EPG, respectively (min. 50, max. 5350 eggs in 1 g of faeces). A bit lower indices were noted for A. suum (15% ± 3.6; 311.1 EPG: 50–1600). The third species – S. ransomi, was observed only in four samples (3.3% ± 1.8; 62.5 EPG: 50–100). Overall prevalence of infection of fatteners kept on litter was lower (25% ± 11.2) as compared to those kept on slatted floor (38.3% ± 12.6), however the differences were not significant statistically (2 = 2.465; df = 1; P = 0.116). The demonstrated lack of the relationship between the maintenance system and helminths infection allowed to conduct the further analysis for the whole sample treated collectively. The mean value of meatiness for pigs free from parasites was 53.68, while in the case of infected pigs the meatiness was statistically lower and was 52.12 (t = 2.35; P = 0.02; Fig. 1).
D. Knecht et al. / Preventive Veterinary Medicine 99 (2011) 234–239
Fig. 1. The distribution of values of meatiness in infected and uninfected pigs. Table 1 Categories of meatiness of pigs analysed. Categories of meatiness
Range of precentage of meatiness
E U R
55–61 50–54 45–50
Number of pigs 30 70 20
The analysed pigs were classified into the three categories (Table 1), and the conducted analysis of an influence of parasites on meatiness demonstrate the relationship that is statistically significant. In the case of fatteners of R class, the parasites infection (expressed as EPG) was considerably stronger as compared to fatteners from class E, while in class U – the values of EPG were intermediate (H = 5.92; P = 0.051; Fig. 2). As a result of log-linear analysis of contingency tables for the meatiness class we obtained the following model describing the interactions between the analysed factors: meatiness class/keeping system; presence/absence of helminths/meatiness class (2 = 2.790; df = 3; P = 0.425). The results showed that both keeping system and presence of parasites affecting the meatiness class, i.e. in
Fig. 2. The distribution of values of EPG in meatiness classes of pigs.
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Fig. 3. Interactions between helminth infection and keeping system in particular meatiness class of pigs.
pigs kept on litter more individuals have a higher values of meatiness and meatiness class decreased in pigs infected with helminths (Fig. 3). The GLM analysis showed that both keeping system (F = 7.37; P = 0.007) and EPG (F = 5.52; P = 0.020) affecting the meatiness. Lack of interaction between keeping system and EPG in GLM analysis exclude false positive observation and support our prediction that along with increasing value of EPG mean meatiness decreasing (Fig. 4). In view of the lack of any literature data concerning the problems undertaken, the results obtained in the present study seem to be leading and original ones. Thus, it is impossible to compare or discuss with the data obtained by another authors. The quality of pork meat measured by meatiness index and its connection to parasites infection in fatteners were not subject of any scientific research so far. A few other indices used in an assessment of the quality of pork with respect to parasites influence may be only found in the paper by Theodoropoulos et al. (2004). The results of the study by Greek authors point, that natural infections of internal parasites in pigs may unprofitable influence not only their growth, condition but meat quality as well. Meat of infected pigs was different as regards
Fig. 4. Correlation between value of meatiness and the average number of parasite eggs expressed as EPG.
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some quality features from the meat of uninfected individuals. That differences were seen especially in older animals, that the authors explained by the time that must go by so that the negative effect of parasites could be manifested. The results of the present study demonstrate that fatteners with higher EPG value were characterized by statistically significantly lower meatiness. In the literature data the significant effect of sex was ˛ observed on the meat content of carcasses (Krzecio et al., 2004). The gilts were characterized by a higher meat deposition and better indicators of carcass quality than castrates. While gender may impact on lean content of pork, the variation due to sex was not checked in the cause of our studies, it may be of value in future studies to see if the parasite impact is different for males and females. Another problem we were faced with in the results of the experiment was considerably poor effectiveness of deworming conducted. According to the literature data (Várady et al., 1996; Nansen and Roepstorff, 1999; Borgsteede et al., 2007) it is not a surprising result, since an effect of ivermectin on the two, the most abundant in the experiment described, parasites species (A. suum and Oesophagostomum spp.) very rarely reaches 100% effectiveness. The study of another authors concern mainly nematodes of the genus Oesophagostomum. For example, Fernandez-de-Mera et al., 2003 demonstrated 81.5% effectiveness of that medicine in wild boars. Várady et al. (1996) giving to pigs other (150 and 600 g/kg) than the standard (300 g/kg of body mass) doses of the medicine obtained an efficiency on the level from 40.5 to 78.6%, and the effectiveness of the higher dose was also negligible better comparing to the result obtained with a dose recommended by the producer. The reason of that situation is most often seen in widely understood drug-resistance. The log-term application of one medicine or its elevated dose, improper frequency and dates of treatment, animals maintenance system and particular parasites biology are among the factors leading to its occurrence (Gundłach and Sadzikowski, 2004). In the present experiment, mainly the two last factors were taken into consideration. It is possible that considerable density (60 individuals) of fattening pigs in one pen maintained in litter system have favoured quick infection with Oesophagostomum; its commonly accepted incubation period is 5–7 weeks, however it may be shortened even up to about 21 days (Nansen and Roepstorff, 1999). Moreover, the coproscopic analysis does not differentiate the two species of Oesophagostomum that are characterized by various sensitivity on the preparation used in the experiment. According to Várady et al. (1996) invermectin is decidedly less effective on O. quadrispinulatum invasion as compared to O. dendatum. It seems that the influence of parasites invasion on the growth, condition and quality of meat in pigs may be analysed without taking into consideration the keeping conditions. Pigs kept in an indoor system are endangered with an influence of numerous internal factors that can made difficult the interpretation of the results obtained such way. The closed keeping system limits the influence of external factors to considerably higher degree that makes that results much more reliable.
The losses caused by parasites in pigs concern also the parts of all carcass that are not suitable for the consumption. The price obtained by the pigs producer increases with meatiness growth. The price obtained for fattener needs to take into consideration the real cost of its production, mainly costs of fattening. The effects of fattening depend on numerous factors, however they are based on the proper health status. The changing profitability of pigs production exacts the need of a determination of costs of curing, maintenance, especially that currently produced pigs make other genetic material, differently adjusted to keeping conditions as animals kept 5 or 10 years ago. It seems that in a further study the authors would try to find the relationship between the influence of the most common nematodes and a potential distribution of fatteners belonging to the particular meatiness classes. Acknowledgements The authors would like to thank the anonymous Reviewer for his comments that considerably help improve the initial version of the manuscript. References Andersen, S., 1976. The influence of A. suum infection upon growth rates in pigs. Nord. Vet. Med. 28, 322–330. Arsenos, G., Fortomaris, P., Papadopulos, E., Kufidis, D., Stamataris, C., Zygoyiannis, D., 2007. Meat quality of lambs of indigenous dairy Greek breeds as influenced by dietary protein and gastrointestinal nematode challenge. Meat Sci. 76, 779–786. Arsenos, G., Fortomaris, P., Papadopulos, E., Sotiraki, S., Stamataris, C., Zygoyiannis, D., 2009. Growth and meat quality of kids of indigenous Greek goats (Capra prisca) as influenced by dietary protein and gastrointestinal nematode challenge. Meat Sci. 82, 317–323. Borgsteede, F.H.M., Gaasenbeek, C.P.H., Nicoll, S., Domangue, R.J., Abbott, E.M., 2007. A comparison of the efficacy of two ivermectin formulations against larval and adult A. suum and Oesophagostomum dentatum in experimentally infected pigs. Vet. Parasitol. 146, 288–293. Daugschies, A., Hintz, J., Henning, M., Rommel, M., 2000. Growth performance, meat quality and activities of glycolytic enzymes in the blood and muscle tissue of calves infected with Sarcocystis cruzi. Vet. Parasitol. 88, 7–16. De La Fuente, C., Cuquerella, M., Cuquerella, L., Alunda, J.M., 1993. Effect of subclinical coccidiosis in kids on subsequent trichostrongylid infection after weaning. Vet. Parasitol. 45, 177–183. Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm. (Decyzja Komisji UE nr ˛ 2005/240/WE z 11 marca 2005 r. zatwierdzajacej metody klasyfikacji tusz wieprzowych w Polsce). Fernandez-de-Mera, I., Vicente, J., Gortazar, C., Höfle, U., Fierro, Y., 2003. Efficacy of an in-feed preparation of ivermectin against helminths in the European wild boar. Parasit. Res. 10, 436–442. Gerwert, S., Failing, K., Bauer, C., 2004. Husbandry management, worm control practices and gastro-intestinal parasite infections of sows in pig-breeding farms in Munsterland, Germany. Dtsch. Tierarztl. Wochenschr. 111, 398–403. Gilka, J., Habrda, J., Jankova, B., Krejci, P., Matyas, Z., 1983. Characteristics of the meat of cattle with cysticercosis due to experimental infection with the eggs of the tapeworm Taenia saginata and treated with praziquantel. Vet. Med. (Praha) 28, 257–268. Gundłach, J.L., Sadzikowski, A.B., 2004. Parazytologia i parazytozy ˛ PWRiL, Warszawa. zwierzat. ˙ Jaworska, D., Przybylski, W., Kołozyn-Krajewska, D., Czarniecka-Skubina, ˛ E., Wachowicz, I., Trzaskowska, M., Kajak, K., Lech, A., Niemyjski, S., 2006. The assessment of relationships between characteristics determining technological and sensory quality of pork. Anim. Sci. Pap. Rep. 24, 121–135. Kajak, K., Przybylski, W., Jaworska, D., Rosiak, E., 2007. Charakterystyka ˛ wieprzowego jako´sci technologicznej, sensorycznej i trwało´sci miesa ˙ ˙ ´ ´ Nauka. Technol. o zróznicowanej koncowej warto´sci pH. Zywno´ sc. ´ 50, 26–34. Jako´sc.
D. Knecht et al. / Preventive Veterinary Medicine 99 (2011) 234–239 ˛ ´ Krzecio, E., Antosik, K., Zybert, A., Sieczkowska, H., Kocwin Podsiadła, M., ´ Kurył, J., Łyczynski, A., 2004. Meat content and carcass composition as related to sex and RYR1 genotype in pigs from six genetic groups. Anim. Sci. Pap. Rep. 22 (4), 459–467. Małkowski, J., Rycombel, D., Zawadzka, D., 2010. Aktualny i przewidy˛ – stany i wany stan rynku wołowiny. Analizy Rynkowe. Rynek miesa ˙ IX, p. 3. perspektywy, vol. 39. ARR, MRiMW, IERiGZ, Nansen, P., Roepstorff, A., 1999. Parasitic helminthes of: factors influencing transmission and infection levels. Int. J. Parasitol. 29, 877–891. Nosal, P., Nowosad, B., Petryszak, A., 2007. Oesophagostomum quadrispinulatum (Marcone, 1901) Alicata 1935 – a new for Poland parasite of swine. Wiad. Parazytol. 53, 239–243. Patison, H.D., Smith, W.C., Thomas, R.J., 1979. The effects of sub-clinical nematode parasitism on reproductive performance in the sow. Anim. Prod. 29, 321–326. ´ Po´spiech, E., Borzuta, K., Łyczynski, A., Płókarz, W., 1998. Meat defects and their economic importance. Pol. J. Food Nutr. Sci. 7, 7–20. Przybylski, W., Jaworska, D., Czarniecka-Skubina, E., Kajak-Siemaszko, K., ˙ ˛ ˛ kulinarnego o wysokiej 2008. Ocena mozliwo´ sci wyodrebniania miesa ˛ ˛ jako´sci z uwzglednieniem miesno´ sci tuczników, pomiaru barwy i pH ˙ ´ Zywno´ ´ Nauka. Technol. Jako´sc. ´ z zastosowaniem analizy skupien. sc. 59, 43–51. Rohlf, F.J., Sokal, R.R., 1995. Biometry and Statistical Tables. W.H. Freeman & Co, New York.
239
Smets, K., Neirynck, W., Vercruysse, J., 1999. Eradication of sarcoptic mange from a Belgian pig breeding farm with a combination of injectable and in-feed ivermectin. Vet. Rec. 145, 721–724. Theodoropoulos, G., Deligeorgis, S., Fegeros, K., Papavasiliou, D., Rogdakis, E., 2004. Influence of natural parasitism on meat quality criteria and carcass weight of pigs kept under outdoor farming conditions. Agric. Med. 134, 2–9. Thienpont, D., Rochette, F., Vanparijs, O.F.J., 1986. Diagnosing Helminthiasis By Coprological Examination. Janssen Research Foundation, Beerse, Belgium. Urban Jr., J.F., Romanowski, R.D., Steele, N.C., 1989. Influence of helminth parasite exposure and strategic application of anthelmintics on the development of immunity and growth of swine. J. Anim. Sci. 67, 1668–1677. Várady, M., Petersen, M.B., Bjørn, H., Nansen, P., 1996. The efficacy of ivermectin against nodular worms of pigs: the response of treatment using three different dose levels against Oesophagostomum dentatum and Oesophagostomum quadrispinulatum. Int. J. Parasitol. 26, 369–374. Xia, L., Gibbs, H.C., Yang, C., 1991. Pathophysiologic effects of Ostertagia ostertagi in calves and their prevention by strategic anthelmintic treatments. Am. J. Vet. Res. 52, 1706–1711. Zajac, A.M., Conboy, G.A., 2006. Veterinary Clinical Parasitology, vol. 7. Blackwell Publishing, Ames.
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Does meatiness of pigs depend on the level of gastro-intestinal parasites infection? Damian Knecht a , Marcin Popiołek b,∗ , Grzegorz Zale´sny c a
Department of Pigs Breeding, Institute of Animal Breeding, Wrocław University of Environmental and Life Sciences, Chełmo´ nskiego 38c, 51-630 Wrocław, Poland b ˙ Institute of Biology, Department of Invertebrate Systematics and Ecology, Wrocław University of Environmental and Life Sciences, Kozuchowska 5b, 51-631 Wrocław, Poland c Department of Parasitology, Institute of Genetics and Microbiology, Wroclaw University, Przybyszewskiego 63, 51-148 Wrocław, Poland
a r t i c l e
i n f o
Article history: Received 12 July 2010 Received in revised form 19 January 2011 Accepted 21 January 2011 Keywords: Intestinal parasites Meatiness Pigs Meat quality
a b s t r a c t The aim of the present paper was to determine an influence of the presence and a level of intestine parasites infection on the quality of pork carcass expressed by the content of meat in carcass (meatiness) in pigs. The experimental part of the study was conducted on pigs farm produced in a closed cycle. The population in the study included 120 fattening pigs maintained in two keeping systems: group I – 60 individuals kept on slatted floor, and group II – 60 individuals kept on deep litter. All the experimental animals were treated in the same manner. The analysed fatteners were slaughtered in Meat Processing Plant when their body mass reached 110 kg, and the post-slaughter assessment was conducted according to the EUROP classification of pigs carcass using the Ultra-Fom 300 device. The study concerning the internal parasites were conducted basing on coproscopic quantitative McMaster method. As a results, the eggs of three nematode taxa were isolated and identified: Oesophagostomum spp., Ascaris suum and Strongyloides ransomi. Overall prevalence of infection of fatteners kept on litter was lower (25% ± 11.2) as compared to those kept on slatted floor (38.3% ± 12.6), however the differences were not statistically significant (2 = 2.465; df = 1; P = 0.116). The mean value of meatiness for pigs free from parasites was 53.68, while in the case of infected pigs the meatiness was statistically lower and was 52.12 (t = 2.35; P = 0.02). The analysed pigs were classified into three categories and conducted analysis of an influence of parasites on meatiness demonstrate the relationship that is statistically significant. The analysis of correlation between meatiness and an average number of helminth eggs also demonstrated the negative, statistically significant, relationship (F = 5.52; P = 0.020), i.e. in fatteners with higher EPG value the meatiness was lower. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Pork accounts for over 60% of meat consumed in Poland in total. Half of that is an unprocessed meat, and culinary
∗ Corresponding author. Tel.: +48 71 3205883; fax: +48 71 3205876. E-mail address: [email protected] (M. Popiołek). 0167-5877/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2011.01.009
meat in processed form is about 50%. People consume more and more preserves, smoke-dried and dry cold meat, and definitely less amounts of canned food and products of higher fat content. Structural changes in an overall meat consumption point also initially increasing, and currently stable trend in poultry meat introduction into a diet. Also an increase in fish and fish products is observed (Małkowski et al., 2010). In a condition of a full market availability, wide
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range of products and high meat supply, the production of high quality meat that fulfils demands of consumers and producers as well is a very important problem (Przybylski et al., 2008). That issue becomes a significant one in a situation of a continuous trend towards an improvement in fattening pigs meatiness. The results concerning the mass population demonstrate that in a period from 1998 to 2009, the meatiness of pigs in Poland increased from 46.7% to about 54.5%. Selection leads towards an increase in growth rate and lean meat content in carcass is often connected with a decrease in slaughter mass of fattening pigs (the mass that qualifies the fattening pigs to slaughter, currently about 110 kg in Poland) and meat quality deterioration, like fat content, tenderness (Jaworska et al., 2006). For a long time, the slaughter value of carcass and quality of pork meat has been an object of an interest of scientists and also of technologists in meat processing plants. The quality of a product and economic results of a plant are to a very high degree conditioned by the quality of raw material. An intensive animal breeding with industrial fodders, and also the selection of pigs of notably meat genotypes for fattening, influence the quality of meat. The quality of meat include safety aspects (the presence of pathogenic microorganisms and those lowering meat stability, parasites, residues of drugs, heavy metals, and mycotoxins), nutritional value (the content of protein, fat, vitamins, mineral salts, and carbohydrates), its technological properties (water absorbability, pH value, stains content, meatiness, adiposity, and tendinuosity) and sensory features (colour, odour, tenderness, juiciness, and flavour) (Kajak et al., 2007). Also some environmental factors (turnover, slaughter process, and chilling) have a big influence on quality features of meat. Together with meatiness increase of fatteners produced, there is a tendency of a decrease in their stress resistance leading in a certain conditions to the deterioration in meat quality (Po´spiech et al., 1998). Parasites invasions in pigs are a common phenomenon. Their effect in fattening pigs lead to a decrease in body mass daily gains of about 50 g, worse feed utilization for body mass gain of about 3–9%, later date of slaughter body mass attainment of 10–15 days (Smets et al., 1999). An alleviation of parasites infection results is one of the factors of the increase in production level, and thus an increase in a profitability of pigs breeding and husbandry. In a course of parasitic diseases, even without any apparent disease symptoms, parasites infection induce high losses in pigs, since they damage blood vessels, internal organs or intestine epithelium by a migration of developmental forms. The results of such an activity are as follows: (1) worse fodder assimilation, (2) impaired process of intestinal absorption, (3) decrease in daily body mass gains, (4) fertility disorders, (5) delayed or incomplete obtaining of postvaccinal immunity towards infectious diseases, (6) prolongation of fattening period, and (7) deterioration in meat quality. The effect of an unprofitable influence of gastrointestinal parasites infection on the condition, health status and body mass gains of pigs is currently out of the question (Andersen, 1976; Patison et al., 1979; Urban et al., 1989; Gerwert et al., 2004). However, the study so far has not concerned the issues connecting the presence of para-
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sites with pork meat quality. The exception is the paper by Theodoropoulos et al. (2004) describing the selected indices of meat quality in pigs infected with intestine nematodes maintained on an indoor system. Similar issues, however with respect to other animals (sheep, goats and cattle) have been taken up in the literature (Gilka et al., 1983; Xia et al., 1991; De La Fuente et al., 1993; Daugschies et al., 2000; Arsenos et al., 2007, 2009). The results of above study, not very distinctly however point an unprofitable influence of parasites infection on a quality of meat of infected animals. The aim of the present paper was to determine an influence of the presence and a level of intestine parasites infection on the quality of pork carcass expressed by the content of meat in carcass (meatiness) in pigs kept in an indoor system. 2. Materials and methods 2.1. Field study The experimental part of the study was conducted on pigs farm producing in a closed cycle (based on the maintenance of all production groups on one farm), in a period of June–July 2009. The farm has an area of 28 hectares. The sows are introduced to the parturition department 14 days before farrowing. They stay there together with piglets for about 28–30 days. The sows were selected to the groups keeping the similar ration of primiparous sows to multiparous ones. All the sows were cross-bred of Large Polish White and Polish Landrace covered with cross-bred boars of Pietrain × 990. The experimental population in the study included 120 fattening pigs maintained in two keeping systems: group I – 60 individuals kept on slatted floor, and group II – 60 individuals kept on deep litter. The fattening pigs were kept in collective pens, 60 individuals in each. All the pigs were labelled with ear rings, each group with different colour, and a subsequent number. All the experimental animals were treated in the same manner. Fattening pigs were fed with commercially available complete feed mixtures. Microclimatic conditions were close to the optimal, and identical for the whole experimental population. The zootechnical treatments were unified in all the groups. One day after the birth the piglets were subject to canine cutting off, and at the second day the iron in the form of injection was given, and boar piglets were castrated. At the sixth week of life, the piglets were deworming with IVOMEC preparation in a form of injection just by the weaning. An active component of the preparation is Ivermectin – semi-synthetic avermectins derivative. According to the producers recommendations a dose of 300 g/kg of body mass was applied. Sows were dewormed 2 weeks before farrowing with the preparation of the same company. 2.2. Evaluation of meat quality The system of pigs classification basing on the content of lean meat in carcass is in force in the European Union. Polish slaughterhouses, since the day of the accession of Poland to the European Union, are obliged to classify the pig carcass in an EUROP system. The regulations concern-
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ing the classification of slaughter animals carcass specify the obligation of the classification by slaughterhouses, and an obligation of a supervision of the classification led by The Inspection of Trade Quality of Agricultural-Food Products. The decree of the Ministry of Agriculture and Rural Development determines the classes of the market quality of pigs carcass (EUROP classification), specifies the detailed requirements in the range of market quality of pigs carcass, entities entitled for the opinions concerning the equipment used for the assessment of market quality of pigs carcass and the method of pigs carcass analysis (Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm). The six classes are distinguished: (1) class S contains at least 60% of lean meat in carcass, (2) class E from 55% but less than 60%, (3) class U from 50% but less than 55%, (4) class R from 45% but less than 50%, (5) class O from 40% but less than 45%, and (6) class P contains less than 40% of meat. The analysed fatteners were slaughtered in Meat Processing Plant when their body mass reached 110 kg, and the post-slaughter assessment was conducted according to the EUROP classification of pigs carcass using the Ultra-Fom 300 device (Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm). 2.3. Sample collection and laboratory procedures The study on internal parasites in fattening pigs were conducted basing on coproscopic methods. The samples were collected during the whole fattening (3 months), in 3 periods – at the beginning, in the middle and at the end of the time of fattening, i.e. with fattening pigs body mass of 40, 70 and 110 kg. First samplings were conducted after the pigs reached body mass of about 40 kg, i.e. 2 weeks after fattening beginning, so that the group was adapted for the room. The research material was fresh faeces samples of about 5 g each, collected directly after defecation from the bedding to labelled plastic containers. All pigs were labelled with ear rings, and additionally with colours. Since each time six person took part in samples collection from one pen, there was an attempt to assign the particular faeces samples to particular identified individual. The samples were collected from the same parts of the pen, representing all the places of animals defecation. They were situated in the middle and extreme sectors of the pen. The samples were preserved in 4% formalin solution. The quantitative method of McMaster (Gundłach and Sadzikowski, 2004) with the use of saturated NaCl solution as a flotation agent was applied to the determination and isolation of parasites eggs. Additionally, in order to show the potential invasions of a low intensity, the standard flotation method was used concurrently. The eggs discovered were identified basing on their morphology (shape, sheath structure, number and size of blastomeres or larvae presence) and biometry. The identification was done using the elaborations by Thienpont et al. (1986) and Zajac and Conboy (2006). To estimate the level of analysed animals infection, the basic parasitological indices were applied: extensiveness of infection (%) – understood as the ratio of the number of positive samples to an overall number of analysed samples, and mean number of eggs in 1 g of faeces (EPG). According to the work by Rohlf and Sokal (1995) the prevalence value was given with 95% confidence inter-
val. The mean EPG value in turn, was determined as an arithmetic mean with the range of values obtained. 2.4. Statistical analysis The analysis of the relationship between mean EPG and meatiness class was done using a nonparametric Kruskall–Wallis test. Meatiness class was also analysed by maximum likelihood techniques based on log-linear analysis of contingency tables, beginning with the most complex model involving all possible effects (keeping system and presence/absence of helminths) and interactions. Next the minimum sufficient model was generated where Chi-square result was not significant, indicating that the model was adequate in explaining the data. Additionally the influence of helminth presence on the mean meatiness value was analysed by students t-test. In the next step we analysed the dependence of meatiness in the relation with qualitative (keeping system) and qualitative (EPG values) predictors using GLM (general linear models) method. In the case of that analysis EPG values and meatiness were transformed logarithmically (log(x) + l). In all statistical method applied, the agreed significance level was 0.05. The calculations were conducted using Statistica 9.0 PL packet. 3. Results and discussion One hundred and twenty faeces samples from fatteners maintained in the two different systems, i.e. on a litter (n = 60) and on so-called slatted floor (n = 60) were subject to analysis. An overall extensiveness of infection appeared to be small and was 31.6% ± 8.4. As a results of coproscopic study conducted, the eggs of three nematode taxa were isolated and identified: Oesophagostomum spp., Ascaris suum and Strongyloides ransomi. All determined nematodes are typical and commonly present parasites of pigs. Oesophagostomum spp. determined to the generic level was in Poland represented as far by only one species – Oesophagostomum dentatum. Since Nosal et al. (2007) for the first time described the second species of that type – O. quadrispinulatum, – in pigs in Poland, the detailed identification of morphologically and biometrically eggs appeared to be impossible. The highest prevalence of infection and mean EPG values were noted for nematodes from Oesophagostomum spp.: 20.8% ± 4.1 and 840 EPG, respectively (min. 50, max. 5350 eggs in 1 g of faeces). A bit lower indices were noted for A. suum (15% ± 3.6; 311.1 EPG: 50–1600). The third species – S. ransomi, was observed only in four samples (3.3% ± 1.8; 62.5 EPG: 50–100). Overall prevalence of infection of fatteners kept on litter was lower (25% ± 11.2) as compared to those kept on slatted floor (38.3% ± 12.6), however the differences were not significant statistically (2 = 2.465; df = 1; P = 0.116). The demonstrated lack of the relationship between the maintenance system and helminths infection allowed to conduct the further analysis for the whole sample treated collectively. The mean value of meatiness for pigs free from parasites was 53.68, while in the case of infected pigs the meatiness was statistically lower and was 52.12 (t = 2.35; P = 0.02; Fig. 1).
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Fig. 1. The distribution of values of meatiness in infected and uninfected pigs. Table 1 Categories of meatiness of pigs analysed. Categories of meatiness
Range of precentage of meatiness
E U R
55–61 50–54 45–50
Number of pigs 30 70 20
The analysed pigs were classified into the three categories (Table 1), and the conducted analysis of an influence of parasites on meatiness demonstrate the relationship that is statistically significant. In the case of fatteners of R class, the parasites infection (expressed as EPG) was considerably stronger as compared to fatteners from class E, while in class U – the values of EPG were intermediate (H = 5.92; P = 0.051; Fig. 2). As a result of log-linear analysis of contingency tables for the meatiness class we obtained the following model describing the interactions between the analysed factors: meatiness class/keeping system; presence/absence of helminths/meatiness class (2 = 2.790; df = 3; P = 0.425). The results showed that both keeping system and presence of parasites affecting the meatiness class, i.e. in
Fig. 2. The distribution of values of EPG in meatiness classes of pigs.
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Fig. 3. Interactions between helminth infection and keeping system in particular meatiness class of pigs.
pigs kept on litter more individuals have a higher values of meatiness and meatiness class decreased in pigs infected with helminths (Fig. 3). The GLM analysis showed that both keeping system (F = 7.37; P = 0.007) and EPG (F = 5.52; P = 0.020) affecting the meatiness. Lack of interaction between keeping system and EPG in GLM analysis exclude false positive observation and support our prediction that along with increasing value of EPG mean meatiness decreasing (Fig. 4). In view of the lack of any literature data concerning the problems undertaken, the results obtained in the present study seem to be leading and original ones. Thus, it is impossible to compare or discuss with the data obtained by another authors. The quality of pork meat measured by meatiness index and its connection to parasites infection in fatteners were not subject of any scientific research so far. A few other indices used in an assessment of the quality of pork with respect to parasites influence may be only found in the paper by Theodoropoulos et al. (2004). The results of the study by Greek authors point, that natural infections of internal parasites in pigs may unprofitable influence not only their growth, condition but meat quality as well. Meat of infected pigs was different as regards
Fig. 4. Correlation between value of meatiness and the average number of parasite eggs expressed as EPG.
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some quality features from the meat of uninfected individuals. That differences were seen especially in older animals, that the authors explained by the time that must go by so that the negative effect of parasites could be manifested. The results of the present study demonstrate that fatteners with higher EPG value were characterized by statistically significantly lower meatiness. In the literature data the significant effect of sex was ˛ observed on the meat content of carcasses (Krzecio et al., 2004). The gilts were characterized by a higher meat deposition and better indicators of carcass quality than castrates. While gender may impact on lean content of pork, the variation due to sex was not checked in the cause of our studies, it may be of value in future studies to see if the parasite impact is different for males and females. Another problem we were faced with in the results of the experiment was considerably poor effectiveness of deworming conducted. According to the literature data (Várady et al., 1996; Nansen and Roepstorff, 1999; Borgsteede et al., 2007) it is not a surprising result, since an effect of ivermectin on the two, the most abundant in the experiment described, parasites species (A. suum and Oesophagostomum spp.) very rarely reaches 100% effectiveness. The study of another authors concern mainly nematodes of the genus Oesophagostomum. For example, Fernandez-de-Mera et al., 2003 demonstrated 81.5% effectiveness of that medicine in wild boars. Várady et al. (1996) giving to pigs other (150 and 600 g/kg) than the standard (300 g/kg of body mass) doses of the medicine obtained an efficiency on the level from 40.5 to 78.6%, and the effectiveness of the higher dose was also negligible better comparing to the result obtained with a dose recommended by the producer. The reason of that situation is most often seen in widely understood drug-resistance. The log-term application of one medicine or its elevated dose, improper frequency and dates of treatment, animals maintenance system and particular parasites biology are among the factors leading to its occurrence (Gundłach and Sadzikowski, 2004). In the present experiment, mainly the two last factors were taken into consideration. It is possible that considerable density (60 individuals) of fattening pigs in one pen maintained in litter system have favoured quick infection with Oesophagostomum; its commonly accepted incubation period is 5–7 weeks, however it may be shortened even up to about 21 days (Nansen and Roepstorff, 1999). Moreover, the coproscopic analysis does not differentiate the two species of Oesophagostomum that are characterized by various sensitivity on the preparation used in the experiment. According to Várady et al. (1996) invermectin is decidedly less effective on O. quadrispinulatum invasion as compared to O. dendatum. It seems that the influence of parasites invasion on the growth, condition and quality of meat in pigs may be analysed without taking into consideration the keeping conditions. Pigs kept in an indoor system are endangered with an influence of numerous internal factors that can made difficult the interpretation of the results obtained such way. The closed keeping system limits the influence of external factors to considerably higher degree that makes that results much more reliable.
The losses caused by parasites in pigs concern also the parts of all carcass that are not suitable for the consumption. The price obtained by the pigs producer increases with meatiness growth. The price obtained for fattener needs to take into consideration the real cost of its production, mainly costs of fattening. The effects of fattening depend on numerous factors, however they are based on the proper health status. The changing profitability of pigs production exacts the need of a determination of costs of curing, maintenance, especially that currently produced pigs make other genetic material, differently adjusted to keeping conditions as animals kept 5 or 10 years ago. It seems that in a further study the authors would try to find the relationship between the influence of the most common nematodes and a potential distribution of fatteners belonging to the particular meatiness classes. Acknowledgements The authors would like to thank the anonymous Reviewer for his comments that considerably help improve the initial version of the manuscript. References Andersen, S., 1976. The influence of A. suum infection upon growth rates in pigs. Nord. Vet. Med. 28, 322–330. Arsenos, G., Fortomaris, P., Papadopulos, E., Kufidis, D., Stamataris, C., Zygoyiannis, D., 2007. Meat quality of lambs of indigenous dairy Greek breeds as influenced by dietary protein and gastrointestinal nematode challenge. Meat Sci. 76, 779–786. Arsenos, G., Fortomaris, P., Papadopulos, E., Sotiraki, S., Stamataris, C., Zygoyiannis, D., 2009. Growth and meat quality of kids of indigenous Greek goats (Capra prisca) as influenced by dietary protein and gastrointestinal nematode challenge. Meat Sci. 82, 317–323. Borgsteede, F.H.M., Gaasenbeek, C.P.H., Nicoll, S., Domangue, R.J., Abbott, E.M., 2007. A comparison of the efficacy of two ivermectin formulations against larval and adult A. suum and Oesophagostomum dentatum in experimentally infected pigs. Vet. Parasitol. 146, 288–293. Daugschies, A., Hintz, J., Henning, M., Rommel, M., 2000. Growth performance, meat quality and activities of glycolytic enzymes in the blood and muscle tissue of calves infected with Sarcocystis cruzi. Vet. Parasitol. 88, 7–16. De La Fuente, C., Cuquerella, M., Cuquerella, L., Alunda, J.M., 1993. Effect of subclinical coccidiosis in kids on subsequent trichostrongylid infection after weaning. Vet. Parasitol. 45, 177–183. Dz. U. UE, L 74 z dnia 19.3.2005, poz. 62, ze zm. (Decyzja Komisji UE nr ˛ 2005/240/WE z 11 marca 2005 r. zatwierdzajacej metody klasyfikacji tusz wieprzowych w Polsce). Fernandez-de-Mera, I., Vicente, J., Gortazar, C., Höfle, U., Fierro, Y., 2003. Efficacy of an in-feed preparation of ivermectin against helminths in the European wild boar. Parasit. Res. 10, 436–442. Gerwert, S., Failing, K., Bauer, C., 2004. Husbandry management, worm control practices and gastro-intestinal parasite infections of sows in pig-breeding farms in Munsterland, Germany. Dtsch. Tierarztl. Wochenschr. 111, 398–403. Gilka, J., Habrda, J., Jankova, B., Krejci, P., Matyas, Z., 1983. Characteristics of the meat of cattle with cysticercosis due to experimental infection with the eggs of the tapeworm Taenia saginata and treated with praziquantel. Vet. Med. (Praha) 28, 257–268. Gundłach, J.L., Sadzikowski, A.B., 2004. Parazytologia i parazytozy ˛ PWRiL, Warszawa. zwierzat. ˙ Jaworska, D., Przybylski, W., Kołozyn-Krajewska, D., Czarniecka-Skubina, ˛ E., Wachowicz, I., Trzaskowska, M., Kajak, K., Lech, A., Niemyjski, S., 2006. The assessment of relationships between characteristics determining technological and sensory quality of pork. Anim. Sci. Pap. Rep. 24, 121–135. Kajak, K., Przybylski, W., Jaworska, D., Rosiak, E., 2007. Charakterystyka ˛ wieprzowego jako´sci technologicznej, sensorycznej i trwało´sci miesa ˙ ˙ ´ ´ Nauka. Technol. o zróznicowanej koncowej warto´sci pH. Zywno´ sc. ´ 50, 26–34. Jako´sc.
D. Knecht et al. / Preventive Veterinary Medicine 99 (2011) 234–239 ˛ ´ Krzecio, E., Antosik, K., Zybert, A., Sieczkowska, H., Kocwin Podsiadła, M., ´ Kurył, J., Łyczynski, A., 2004. Meat content and carcass composition as related to sex and RYR1 genotype in pigs from six genetic groups. Anim. Sci. Pap. Rep. 22 (4), 459–467. Małkowski, J., Rycombel, D., Zawadzka, D., 2010. Aktualny i przewidy˛ – stany i wany stan rynku wołowiny. Analizy Rynkowe. Rynek miesa ˙ IX, p. 3. perspektywy, vol. 39. ARR, MRiMW, IERiGZ, Nansen, P., Roepstorff, A., 1999. Parasitic helminthes of: factors influencing transmission and infection levels. Int. J. Parasitol. 29, 877–891. Nosal, P., Nowosad, B., Petryszak, A., 2007. Oesophagostomum quadrispinulatum (Marcone, 1901) Alicata 1935 – a new for Poland parasite of swine. Wiad. Parazytol. 53, 239–243. Patison, H.D., Smith, W.C., Thomas, R.J., 1979. The effects of sub-clinical nematode parasitism on reproductive performance in the sow. Anim. Prod. 29, 321–326. ´ Po´spiech, E., Borzuta, K., Łyczynski, A., Płókarz, W., 1998. Meat defects and their economic importance. Pol. J. Food Nutr. Sci. 7, 7–20. Przybylski, W., Jaworska, D., Czarniecka-Skubina, E., Kajak-Siemaszko, K., ˙ ˛ ˛ kulinarnego o wysokiej 2008. Ocena mozliwo´ sci wyodrebniania miesa ˛ ˛ jako´sci z uwzglednieniem miesno´ sci tuczników, pomiaru barwy i pH ˙ ´ Zywno´ ´ Nauka. Technol. Jako´sc. ´ z zastosowaniem analizy skupien. sc. 59, 43–51. Rohlf, F.J., Sokal, R.R., 1995. Biometry and Statistical Tables. W.H. Freeman & Co, New York.
239
Smets, K., Neirynck, W., Vercruysse, J., 1999. Eradication of sarcoptic mange from a Belgian pig breeding farm with a combination of injectable and in-feed ivermectin. Vet. Rec. 145, 721–724. Theodoropoulos, G., Deligeorgis, S., Fegeros, K., Papavasiliou, D., Rogdakis, E., 2004. Influence of natural parasitism on meat quality criteria and carcass weight of pigs kept under outdoor farming conditions. Agric. Med. 134, 2–9. Thienpont, D., Rochette, F., Vanparijs, O.F.J., 1986. Diagnosing Helminthiasis By Coprological Examination. Janssen Research Foundation, Beerse, Belgium. Urban Jr., J.F., Romanowski, R.D., Steele, N.C., 1989. Influence of helminth parasite exposure and strategic application of anthelmintics on the development of immunity and growth of swine. J. Anim. Sci. 67, 1668–1677. Várady, M., Petersen, M.B., Bjørn, H., Nansen, P., 1996. The efficacy of ivermectin against nodular worms of pigs: the response of treatment using three different dose levels against Oesophagostomum dentatum and Oesophagostomum quadrispinulatum. Int. J. Parasitol. 26, 369–374. Xia, L., Gibbs, H.C., Yang, C., 1991. Pathophysiologic effects of Ostertagia ostertagi in calves and their prevention by strategic anthelmintic treatments. Am. J. Vet. Res. 52, 1706–1711. Zajac, A.M., Conboy, G.A., 2006. Veterinary Clinical Parasitology, vol. 7. Blackwell Publishing, Ames.