Agris category code: L70
SANITARY ASPECTS OF OUTDOOR FARMING SYSTEMS
Kresimir SALAJPAL 1 2, Danijel KAROLYI Zoran LUKOVIC 1
ABSTRACT
Outdoor pig farming include free access to outdoor area and wide use of natural resources of soil and plants in which animals can express their natural behavior. Some management practices that may improve welfare such as outdoor rearing, holding in groups, use of bedding or other housing systems in which it is difficult to implement good sanitation may increase risk to exposure of pigs to the pathogens from the environment. Presence of pathogens or their vectors in outdoor areas in combination with poor environmental conditions may result in high prevalence of various infectious or parasitic diseases, many of which may be zoonotic. Difficulties in implementation of common biosecurity measures and health management principles in outdoor farming impede effective control of diseases. Use of breeds or strains which are adapted to harsh environmental conditions and exhibit favorable disease resistance such as local breeds or their crossbreds, appropriate feeding including plants and fungi that have detrimental effect on pathogens (parasites), and grazing management with integrated use of medicaments (anthelmintic) can be additional methods of controlling diseases in outdoor farming. The common health problems in outdoor pig farming system and their potential impact on human health are reviewed in this paper.
Key words: outdoor farming / pig / diseases / parasites / zoonosis
Invited lecture COBISS: 1.06
1 INTRODUCTION
Outdoor pig farming became more popular in the last 20 years with rise in public interest on animal welfare and products originating from production systems which take care of the environment. It is defined as a system that allows the pigs outside access including contact with soil and growing plants (Honeyman et al., 2001) in which animals can express their natural behavior (Miao et al., 2004). If this production system is coupled with good management practices it can result in acceptable production performance, high quality of pork with superior taste and health benefits for humans due to the high level of unsaturated fatty acids (Simopoulos, 1991) and absence of residues (growth promoters, antibiotics, pesticides) or biological agents (microorganisms, parasites). A successful control of diseases is one of the most impor-
tant roles of management in outdoor farming which can improve pig's health and pork safety. Because, outdoor farming management include free access to outdoor area and wide use of natural resources of soil and plants there is a high possibility of close contact with wildlife. Thus pigs are highly exposed to variable environmental conditions and potential transmission of various infectious or parasitic diseases, many of which may be zoonotic. In addition, cleaning and disinfection are more problematic due to the access to outdoor areas. Therefore, the infection level of pathogenic microorganisms and parasites, the severity of infections, and their effects on production, animal welfare and pork safety depend mostly on the management practices in disease control. The common health problems in outdoor farming system and their potential impact on human health are reviewed in this paper.
1	Faculty of Agriculture University of Zagreb, Department of Animal Science, Svetosimunska c. 25, 10000 Zagreb, Croatia
2	Corresponding author: ksalajpal@agr.hr
2 CHARACTERISTICS OF SYSTEM IN RELATION TO HEALTH
It is generally accepted that outdoor pig farming system is characterized with low production intensity as a result of extensive use of outdoor areas and low investments in housing, equipment and other costs. Lower input which varies between 40 and 70% of the input for conventional indoor systems (Thornton, 1990) makes it economically very attractive and suitable for pork production using breeds of modest production traits such as local breeds. In addition, outdoor farmed pigs generally manifest a favorable welfare with a better immunological status and ability to cope with infections and are less susceptible to stress during preslaughter handling (Warriss et al., 1983; Barton-Gade and Blaabjerg, 1989). On the other hand, some management practices that may affect pig health and welfare such as outdoor rearing, holding in groups, use of bedding or other housing systems in which it is difficult to implement good sanitation may increase risk to exposure of pigs to pathogens from the environment. Presence of pathogens or their vectors in outdoor areas in combination with poor environmental conditions may result in high pig morbidity and mortality or pose a potential risk for human health.
2.1 MANAGEMENT AND BREEDS
Climatic conditions, land availability, soil characteristics and tradition are main factors that must be considered in outdoor pig management. They comprise the management of housing and feeding including the type of buildings and used materials, space allowance, ground cover, group size, type of feeds and feeding regime, management of mating and disease prevention. Low rainfall area without extreme temperatures, with light permeable soil well covered by grass and other plants is favorable for outdoor farming (Miao et al., 2004). In such conditions, possibility for pathogen survival in environment is reduced. Use of breeds or strains which are adapted to harsh environmental conditions and exhibit favorable disease resistance such as local breeds or their crossbreeds are well accepted for outdoor pig production (McGlone and Hicks, 2000). In relation to housing, availability of outdoor area and feed source, the rearing of local breeds is linked to traditional outdoor farming practices. Those include keeping of pigs all year round in simple huts or natural shelters with free access to large outdoor areas except in the cold and wet season (winter) or vulnerable production stage (farrowing and first 10 days of suckling period) in which pigs could be kept indoors. Outdoor feeding is based on utilization of natural resources of pas-
tures (grass) and woods (acorn, chestnuts, fauna in the soil) with addition of some grain or concentrates dependent on the production stage and nutritional requirements of pigs. In Mediterranean countries traditional silvopas-toral system is well developed which involves indigenous breeds that are extensively pastured in natural forests of oak and chestnut, sometimes in extreme conditions in mountain zones. In such conditions health problems are mainly attributed to a direct contact of outdoor pigs with wild boar or other wild animals that act as reservoir of parasite or pathogenic microorganisms (rodents) some of which could be dangerous to public health, or to the ingestion of feed contaminated by pathogens (soil fauna, seeds, scavenged of rodents or other wild animals etc.). In addition, the absence of hygienic measures which are usually carried out indoors may contribute to the emergence of diseases.
3 HEALTH PROBLEMS IN OUTDOOR FARMING SYSTEM
Previous papers reported that pigs in outdoor farming showed a superior health status due to less respiratory problems and lower incidence of enteric diseases (Thornton, 1990; Tubbs et al., 1993) which are the most common diseases in intensive indoor farming. In addition, lower incidence of periparturient diseases (mastitis, metritis and agalactia - MMA, 24.5%) and torsion or distension of abdominal organs was reported (Karg and Bilkei, 2002). On the other hand, for outdoor pigs, the same authors report high incidence of deaths caused by urogenital disease (32.4%), heart failure (21.8%), and locomotor problems (33.1%). In other studies, free access to soil area or deep bedding has been connected with low prevalence of foot and limb lesions (Kilbride et al., 2009) as well as with osteochondrosis (Van Grevenhof et al., 2011). Skin lesions linked to the unusual behavior such as tail biting, belly nosing and aggressive biting are also found to be less frequent in outdoor farming (Cagienard et al., 2005; Turner et al., 2006). On the contrary, lesions and scars caused by sun burning, ectoparasites activity or scratching is common in outdoor pigs. Respiratory problems in outdoor farming systems occur sporadically and in relation to occurrence of acute pleuropneumo-niae of multifactorial origin. The most common causes of pneumonia are Mycoplasma hyopneumoniae and/or Actinobacillus pleuropneumoniae with simultaneous lung tissue damage due to the migration of larval stages of internal parasites or other factors that may compromise lung integrity. The poor air quality in pigs' environment is high correlated to incidence of pulmonary problems in pigs. Outdoor pigs are generally less exposed to harmful
air condition, such as high dust content, ammonia and/ or hydrogen sulphide concentration. In addition, lung health problems may arise due to high concentrations of respirable endotoxin (Moller, 2000), as pig lungs are highly sensitive to endotoxin level (Olson et al., 1995). Hence, its presence in bioaerosol where chopped straw is used for floor bedding may lead to pulmonary problems (Ki-jlstra and Eijck, 2006). Gastrointestinal problems in outdoor pigs are associated with the occurrence of diarrhea in piglets and digestive disturbance in older pigs related to endoparasite invasion. Besides crushing or trauma inflicted by sow, diarrhea in pre-weaned period is the main cause of morbidity and mortality in outdoor reared piglets. It is characterized by a sudden appearance, rapid spread and high mortality rate of piglets. Causes include clostridial infection, coccidiosis, E. coli and occasionally viral diseases (Rotavirus, transmissible gastroenteritis; Straw et al., 1999). Post-weaning diarrhea is associated to high susceptibility of piglets to viral and bacterial infections due to stress at weaning. Late weaning (>7 weeks), which is a common practice in outdoor farming, can reduce the weaning stress. Older piglets show trend to a lower severity of diarrhea and a lower mortality rate. The most common pathological agents of diarrhea in post-weaning piglets include E. coli, salmonellosis, Campylobacter, Brachyspira hyodysenteriae and Rotavirus (Straw et al., 1999). It seems that viral infections (Rotavirus) are diseases with a low risk of incidence in outdoor kept piglets. Routine vaccination with Clostridium perfringens and C. enteritis may lead to low neonatal diarrhea in organic pig production (Feenstra, 2000).
3.1 PARASITIC DISEASES
An overview of common parasites found in pigs in relation to type of farming is presented in Table 1. Outdoor pig farming poses a higher risk to both endo- and ectoparasitic invasion due to the favorable conditions for development and survival of different stages of parasites in surrounding environment. Possibility to contact with wild animals as a potential reservoir of parasites or intermediate host of parasite is high. The deleterious effects of parasites on pig's health include organ damage with clinical signs of disease and reduced performances. Because parasitic infections have predominately subclinical character they usually remain undetected except reduced feed conversion ratio and poor growth rate are noted.
Coccidiosis could be an important cause of diarrhea in pigs over 7 days of age in both indoor and outdoor farming system. It is caused by Isospora suis and Crypt-osporidium spp. whereas in older pigs it is associated with Eimeria species. Leite et al. (2000) found coccidia
oocysts in 78% of faecal samples in outdoor kept pigs in which anthelmintic administration was not implemented. In addition, Rodriguez-Vivas et al. (2001) reported higher prevalence of Isospora in outdoor than in indoor kept sows (94% vs. 41%). Sows kept outdoors excreted more oocysts from Isospora than sows kept indoors. Cryptosporidium infection can occur together with Isospora infection, as well in older animals (Xiao and Herd, 1994; Quilez et al, 1996). Ryan et al. (2003) found Cryptosporidium spp. more often in outdoor herds (17.2%) than in indoor herds (0.5%) and more common in animals between 5 and 8 weeks of age (69.2%) than in younger animals. The same authors suggest that the opportunities for transmission of Cryptosporidium are much greater in outdoor herds through the contamination of the environment to which the pigs have access. Besides swine specific Cryptosporidium species, pigs can also be infected with the zoonotic Cryptosporidium par-vum or „cattle" species. Therefore, pigs may pose potential reservoirs of infection for humans and other animals (Morgan et al., 1999). Several studies showed high prevalence of helminthes infestation in outdoor pig farming (Carstensen et al., 2002) and emphasized that endopara-sites (Roderick and Hovi, 1999) or both ekto- and en-doparasites (Leeb and Baumgartner, 2000) were the biggest health problem in outdoor pigs. Intestinal nematodes are the most common type of parasites in adult pigs kept outdoors, especially on heavily used pastures or in areas where domestic pigs and wild boars are in frequent contact. Primarily, they compromise host nutritional status, but also malnutrition in turn may predispose the animal to intestinal nematode infection (Koski and Scott, 2001). Outdoor diet is often composed of feeds rich in insoluble dietary fibre and relatively low digestibility which favor establishment and fecundity of worms (Petkevicius et al., 1996; 1999).
Ascaris suum is one of the most common parasites found in both indoor and outdoor pigs. Health problems can occur in heavy invasion with young animals while adult pigs are reservoir and contaminant of pasture due to fecal excretion of high amounts of eggs. Other intestinal parasites (Trichuris suis, Oesophagostomum spp., Hyostrongilus rubidus and Strongyloides ransomi) commonly found in wild boar can also pose a problem in outdoor pigs at extensive use of pasture or woodland. Because, parasites and their eggs or larval stages are highly sensitive to environmental condition such as temperature, radiation, moisture, type of soil and vegetation, seasonal and geographic variation could be observed. In hot and dry areas or during dry summer season eggs survival is reduced due to high temperature and effect of desiccation. Even A. suum and T. suis eggs, which are very resistant to environmental factors, may be dramati-
cally reduced in such conditions (Larsen and Roepstorf, 1999). In addition, low temperatures, more moisture and greater sequestration of eggs in the soil by rain and earthworms could reduce number of eggs deposited in cold mounts (Miao et al., 2004). Roepstorff and Murell (1997a) reported that transmission of both O. dentatum and H. rubidus was reduced during low temperatures in winter. The same authors (Roepstorff and Murell, 1997b) reported that free-living infective larvae such as O. den-tatum and H. rubidus are more sensitive to environmental conditions than eggs of pig parasites.
3.2 ZOONOTIC PARASITES
Outdoor pigs could be an important source of numerous zoonotic diseases in humans (Table 2). The occurrence of some zoonotic parasites in outdoor pigs (e.g. those transmissible to humans' trough meat consumption) is closely related to the exposure of pigs to contact with wild animals (wild boar, rodents, and birds) or their excreta in shared areas. Outdoor pigs are representing an important source of zoonotic parasitosis such as toxoplasmosis, trichinelosis and T. solium-cysticercosis invasion in humans. Toxoplasmosis is a parasitic disease caused by intracellular protozoa Toxoplasma gondii. In humans (especially in pregnant women and immuno-compromised patients) it can cause numerous health problems (Cliver et al., 1990) after consumption of tissue cysts from intermediate host such as pigs. Pigs become infected after intake of sporulated oocysts by feed, water or soil (Cliver et al., 1990). At farms, the prevalence of T. gondii is highly dependent on the production stage and farming system (Wang et al., 2002, Venturini et al., 2004). Lower prevalence was observed in fattening than in breeding pigs (Wang et al., 2002) and under the intensive management (Van der Giessen et al., 2007). Several studies reported that T. gondii seroprevalence was higher in farms with outdoor access which may favor contact of pigs with cats and wildlife that carry the parasite (Davies et al., 1998; Van der Giessen et al., 2007; Garcia-Bocane-gra et al., 2010). In such situations the higher probability of ingestion of feed and water contaminated with sporulated oocysts or tissues cysts of infected animals such as rodents, birds and/or other pigs could be expected (Venturini et al., 2004; Dubey et al., 1995). The presence of cats which scavenge other animals on farms and pastures contribute to the spread of T. gondii due to shedding of oocysts (up to 20 million oocysts units/day during primary infection and 1 million oocysts units/day during secondary infection; Jiang et al., 2012).
Trichinelosis is another parasitic disease in which humans can be infected if they consume meat or meat
products from animals that contain encapsulated larval stage of the parasite. T. suis is the most common species found in domestic pig and the most significantly contributes to foodborne disease in humans (Mead et al., 1999). Trichinela britovi could be responsible for Trichinellosis in humans as well. The natural hosts implicated in life cycle of Trichinella are carnivores and scavenger animals. Pigs and human are implicated in domestic cycle while wild boars (De Bruyne et al., 2006), wild carnivorous (Blaga et al., 2007), as red foxes and rodents are implicated in sylvatic cycle of parasite.
Potential risk factors for pig infestation are feeding raw waste products or animal remains, and exposure to infected rodents or wildlife. Pigs which have free access to outdoor areas could consume small dead mammals or other wild animal carcasses contaminated with Trichine-la species which represents the link between domestic and sylvatic cycles.
The prevalence of Trichinellosis significantly decreased in the past 30 years. Pozio et al. (2007) reported that 21.9% of 198 countries had detectable Trichinella spp. in swine herds and its presence was linked to endemic areas. Some authors (Murrell and Pozio, 2000; Van der Giessen et. al., 2007) emphasize that with increase in organic and free range pig production also increase the risk of Trichinella infestation which could led to a re-emergence of Trichinella in Europe (Dupouy-Camet, 2006).
3.3 ECTOPARASITES
Whereas ectoparasites are of minor importance in intensive pig production, in outdoor farming systems they can have a major impact on the productivity and welfare of pigs (Arends et al., 1990; Rehbein et al., 2003). Through the damage of skin or other subcutaneous tissues, they cause hypersensitivity due to stimulation of immune system by salivary or faecal antigens, including the changes in behavior (Berriatua et al., 2001). In addition, some ectoparasites can contribute to the spreading of other pathogens (protozoa, bacteria, viruses and some helminthes such as tapeworms and round worms). The common ectoparasites in outdoor pigs are mange, lice, fleas and ticks. Their prevalence is associated with farming system and housing condition. In pigs, the most common cause of mange is Sarcoptes scabiei var. suis, while demodectic mange (Demodex phylloides) occurs occasionally. Sarcoptic mange is widespread in both indoor and outdoor pigs and is usually linked to poor housing conditions. In outdoor pigs the occurrence of mange is more common during winter season and early spring due to restricted outdoor access and poor housing condition.
Similar conditions affect the emergence and spread of lice (Haematopinus suis) and fleas. On the other hand, high prevalence of ticks is connected with extensively grazing on pastures and woods. Colebrook and Wall (2004) reported that the high prevalence of tick in Mediterranean region suggests greater importance of these parasites there rather than in northern European countries.
3.4 OTHER ZOONOTIC DISEASES
Additionally to zoonotic parasites, pigs represent an important reservoir of many bacterial pathogens for humans of both infectious or food poisoning characters
(Table 2). For example, Brucella suis caused disease in pigs that could be transmitted to humans. Brucellosis occurs primary in domestic and feral pigs, while wild boar (Sus scrofa) and/or European hare (Lepus europeus) could be assume as a natural reservoir of B. suis. The disease spreads by semen during coitus and by ingestion or inhalation of bacteria in reproductive fluids, placenta, aborted fetuses, urine or milk. Therefore, outdoor farming which includes natural mating and grazing in a large group and together with other species of domestic animals increases the possibility of direct contact among pigs from different owners as well as with wild boar (Cvetnic et al., 2003). In addition, previous study on Turpolje pig in Croatia (Salajpal et al., 2010) suggests
Table 1: Common parasites found in pigs in relation to type of farming (modified according to Nansen and Roepstorff, 1999)
Domestic pig
Wild boar Outdoor Indoor Location Clinical signs
Mode of Infection
Endoparasites
Hyostrongylus rubidus
Ascaris
Strongyloides ransomi
Oesophagostomum dentatum
Trichuris suis
Metastrongylus elongatus
Stephanurus dentatus *
Isospora suis
(+) (+)
(+)
Stomach
Small intestine
Small intestine
Large intestine
Large intestine
Lungs Kidney
Small Intestine
Emaciation Anaemia
Reduced performance Liver damage
Diarrhea
Reduced performance
Diarrhea Dehydration
Coughing Pneumonia
Wasting Blood in urine
10 day old scour
Ingestion of infective larvae
Larvae by percutaneous, oral, transcolostral, prenatal
Larvae by percutaneous, oral, transcolostral, prenatal
Ingestion of infective larvae
Ingestion of infective eggs
Ingestion of infected earthworms
Larvae by percutaneous, oral, possibly prenatal, and ingestion of infected earthworms
Ingestion of infective oocysts
Ectoparasites
Sarcoptic mange	+
(Sarcoptes scabiei)
Demodectic mange +
Ticks Lice
Flies
+
(+)
(+)
(+)
Skin	Irritation
Thickened skin Skin rash
Skin	Rash
Small nodules
Skin	No lesions,
Skin	Evident on the skin
(behind of the ear) No lesions
Skin lesion, Small papules
Direct contact
Direct contact
Direct contact Direct contact
Direct contact
+ regulary occurrence, (+) rarely (conditioned) appearance, * in Southern USA, S. America, Not in Europe
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
that occurrence and high prevalence of brucellosis in domestic pigs can be closely related to enzootic occurrence of B. suis in wild boars present in the same grazing area. Besides wild boar, rodents are another important reservoir of many other pathogens such as Leptospira, Sallmo-nela, Yersinia, Erysipelotrix rhusiopathiae and Brachispira hyodysenteriae (Feenstra et al., 2000). The prevalence of leptospirosis in outdoor pigs is mostly related to regional or local climatic conditions (Boqvist et al., 2012). In area with wet and muddy soil where Leptospira may thrive and where wild vectors or reservoir are present, outdoor pigs can be highly exposed to infection.
Salmonella spp., Campylobacter spp. and Lysteria monocytogenes are among the top bacterial pathogens causing foodborne illness which may appear in meat of both indoor and outdoor pigs. Salmonella and Campy-lobacter are common inhabitants of gastrointestinal tract in pigs and does not present a problem for animal. In humans, these bacteria cause typical gastrointestinal symptoms after consumption of meat contaminated during improper slaughtering procedures. Because their prevalence is mostly dependent on biosecurity measures on farm and during and/or after the slaughter, the differences among farming system are not so evident. Listeria monocytogenes is another ubiquitous bacterium with high persistence in environment. Sources of contamination for pigs are feed, soil, water, farm equipment and human (boots, clouts). In relation to farming system, higher inclusion of raw feeds (non-procesed) or silage as an important source of Listeria in livestock (Buncic et al., 1991; Fenlon et al., 1996) can contribute to increase of Listeria prevalence in outdoor farming system. In addition, Fen-
lon et al. (1985) listed wild birds as a carrier of Listeria monocytogenes and a risk factor for pig contamination.
4 DISEASE CONTROL IN OUTDOOR FARMING SYSTEM
Disease control in outdoor pig farming is closely related to the management of housing and feeding and to climatic conditions and the possibility of contact with pathogens or their vectors. In such conditions implementation of common biosecurity measures and the health management principles ("one way" pig flow, "all in/all out" policy, etc.) as recommended methods are difficult.
Use of breeds or strains of favorable disease resistance, appropriate feeding including plants and fungi that have detrimental effect on pathogens (parasites) and grazing management with integrated use of medicaments (anthelmintic) can be additional methods that contribute to the control of disease in outdoor system. Previous studies indicated differences in disease resistance or tolerance among native and modern breeds of several species such as sheep (Goosens et al., 1999; Amarante et al., 2004), cattle (Glass et al., 2005), chicken (Hassan et al., 2004) and pig (Reiner et al., 2002) emphasizing possibility of their use in outdoor farming. Traditional outdoor systems are based on using of local breeds which are well adapted to the wide use of natural feed resources (acorn, chestnuts, soil fauna etc.) from environment, some of which have a protective role. It is well known, however that outdoor farming is more often associated with parasite-related diseases (Hovi et al., 2003) some of which are sensitive to high condensed tannin level in plants
Table 2: Common zoonotic agents associated with wild and farmed pigs
Wild boar
Outdoor
Indoor
Mode of Infection for human
Bacteria
Brucella suis	+
Campylobacter spp.	(+)
Salmonella spp.	(+)
Lysteria monocytogenes	(+)
Erysipelotrix	+ Parasites
Toxoplasma gondii	+
Trichinella spp	+
Cryptosporidium spp.	+
Taenia solium	+
Ascaris suum	+
+
+
+
+
+
(+)
(+)
(+)
(+)
(+)
(+)
+ + + +
Contact with pathogens, Meat consumption Contact with pathogens, Meat consumption Contact with pathogens, Meat consumption Contact with pathogens, Meat consumption Contact with pathogen
Contact with pathogens, Meat consumption
Meat consumption
Meat consumption
Meat consumption
Meat consumption
+ regulary occurrence, (+) rarely (conditioned) appearance 114 Acta agriculturae Slovenica, Supplement 4 - 2013
feed (gastrointestinal nematode) or some other bioactive compound. By grazing in oak woods, especially during acorning or season when alternative forage availability is scarce, pigs may consume huge amounts of tannin rich plant material and reduce total faecal egg count output in pigs infected with large roundworm (Ascaris suum) and other gastrointestinal parasites (Salajpal et al., 2004). Control of parasitic diseases in outdoor farming is based on breaking of life cycle of parasites by grazing management and use of antihelminitics (Nansen and Roepstorff et al., 1999). Pasture rotation, stocking rate and mixed or alternative grazing are important factors in grazing management which influence the prevalence of parasite infections. Extensive use of pasture (low stocking rate, seasonal use of pasture) or frequent pasture rotation reduces the risk of infection. Insufficient effects of these management practices may occur in parasites with long-live eggs such as A. suum (Roepsdorff et al., 2001).
5 REFERENCES
Amarante A.F.T., Bricarello P.A., Rocha R.A., Gennari S.M.
2004. Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology, 120,
1-2:	91-106
Arends J., Stanislaw C., Gerdon D. 1990. Effects of sarcoptic mange on lactating swine and growing pigs. Journal of Animal Science, 68: 1495-1499 Barton-Gade P., Blaagjerg L. O. 1989. In: ProcEedings of the 35th International Congress of Meat Science and Technology. Copenhagen, Denmark: p 1002-1005 Berriatua E., French N.P., Broster C.E., Morgan K.L., Wall R., 2001. Effect of infestation with Psoroptes ovis on the nocturnal rubbing and lying behaviour of housed sheep. Applied Animal Behaviour Science, 71: 43-55 Blaga R., Durand B., Antoniu S., Gherman C., Cretu C.M., Cozma V., Boireau P. 2007. Dramatically increase of human trichinellosis incidence in Romania over the last 25 years: Impact of political changes or regional food habits? The American Journal of Tropical Medicine and Hygiene, 76: 983-986
Boqvist S., Eliasson-Sellin L., Bergstrom K., Magnusson U. 2012. The association between rainfall and seropositivity to Leptospira in outdoor reared pigs. The Veterinary Journal, 1:135-139
Buncic S. 1991. The incidence of Listeria monocytogenes in slaughtered animals, in meat, and in meat products in Yugoslavia. International Journal of Food Microbiology, 12,
2-3:	173-80
Cagienard A., Regula G., Danuser J., 2005. The impact of different housing systems on health and welfare of grower and finisher pigs in Switzerland.
Preventive Veterinary Medicine, 68, 1: 49-61
Carstensen L., Vaarst M., Roepstorff A., 2002. Helminth infec-
tions in Danish organic swine herds. Veterinary Parasitol-ogy, 106: 253-264 Cliver D.O. 1990. Parasites. Foodborne diseases. San Diego, Calif.: Academic Press Inc. p. 296-297 Colebrook E., Wall R. 2004. Ectoparasites of livestock in Europe and the Mediterranean region. Veterinary Parasitol-ogy, 120: 251-274 Cvetnic 2., Mitak M., Ocepek M., Lojkic M., Terzic S., Jemersic L., Humski A., Habrun B. 2003. Wild boars (Sus scrofa) as reservoirs of Brucella suis biovar 2 in Croatia. Acta Veterinaria Hungarica, 51, 4: 465-473 Davies P.R., Morrow W.E.M., Deen J., Gamble H.R., Patton S. 1998. Seroprevalence of Toxoplasma gondii and Trichinella spiralis in finishing swine raised in different production systems in North Carolina, USA. Preventive Veterinary Medicine, 36, 1: 67-76 De Bruyne A., Ancelle T., Vallee I., Boireau P., Dupouy-Camet J. 2006. Human Trichinellosis acquired from wild boar meat: a continuing parasitic risk in France. Eurosurveillance, 11, 37: 3048
Dubey J.P., Weigel R.M., Siegel A.M., Thulliez P., Kitron U.D., Mitchell M.A., Mannelli A., Mateus-Pinilla N.E., Shen S.K., Kwok O.C.H., Todd, K.S. 1995. Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. Journal of Parasitology, 81: 723-729 Dupouy-Camet J. 2006. Trichinellosis: still a concern for Europe. Eurosurveillance 11(1):5 Feenstra A.A. 2000. A Health Monitoring Study in Organic Pig Herds. In: Darcof Report 2/2000. Hermansen J.E., Vonne L., Thuen E. (eds.), Danish Research Centre for Organic Agriculture, DARCOF, Tjele, Denmark: 107- 112 Fenlon D.R. 1985. Wild birds and silage as reservoirs of Listeria in the agricultural environment. The Journal of Applied Bacteriology, 59, 6: 537-43 Fenlon D.R., Wilson J., Donachie W. 1996. The incidence and level of Listeria monocytogenes contamination of food sources at primary production and initial processing. The Journal of Applied Bacteriology, 81, 6: 641-50 García-Bocanegra I., Dubey J.P., Simon-Grifé M., Cabezón O., Casal J., Allepuz A., Napp S., Almería S. 2010. Seroprevalence and risk factors associated with Toxoplasma gondii infection in pig farms from Catalonia, north-eastern Spain. Research in Veterinary Science, 89, 1: 85-7 Glass E.J., Preston P.M., Springbett A., Craigmile S., Kirvar E., Wilkie G., Brown C.G.D. 2005. Bos taurus and Bos indi-cus (Sahiwal) calves respond differently to infection with Theileria annulata and produce markedly different levels of acute phase proteins. International Journal for Parasitology, 35, 3: 337-347
Goosens B., Osaer S., Ndao M., Van Winghem J., Geerts S. 1999. The susceptibility of Djallonké and Djallonké-Sahelian crossbred sheep to Trypanosoma congolense and helminth infection under different diet levels. Veterinary Parasitol-ogy, 85, 1: 25-41 Hassan M.K., Afify M.A., Aly M.M. 2004. Genetic resistance of Egyptian chickens to infectious bursal disease and Newcastle disease. Tropical Animal Health and Production, 36, 1: 1-9
Honeyman M.S., McGlone J.J., Kliebenstein J.B., Larson B.E.,
2001. Outdoor Pig Production. PIH-145. Pork Industry Handbook. Purdue University, W. Lafayette, IN: 9 p. Hovi M., Sundrum A., Thamsborg S.M. 2003. Animal health and welfare in organic livestock production in Europe. current state and future challenges. Livestock Production Science, 80: 41-53
Jiang W, Sullivan A.M., Su C., Zhao X. 2012. An agent-based model for the transmission dynamics of Toxoplasma gondii. Journal of Theoretical Biology, 293: 15-26 Karg H., Bilkei G. 2002. Causes of sow mortality in Hungarian indoor and outdoor pig production units. Berliner und Munchener Tierarztliche Wochenschrift, 115: 366-368 Kijlstra A., Eijck I.A.J.M. 2006. Animal health in organic livestock production: a review. Wageningen Journal of Life Sciences, 54: 77-94 Kilbride A.L., Gillman C.E., Green L.E. 2009. A cross-sectional study of the prevalence of lameness in finishing pigs, gilts and pregnant sows and associations with limb lesions and floor types on commercial farms in England. Animal Welfare, 18, 3: 215-224 Koski K.G., Scott M.E. 2001. Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition, 21: 297-321 Larsen M.N., Roepstorff A. 1999. Seasonal variation in development and survival of Ascaris suum and Trichuris suis eggs on pasture. Parasitology, 119: 209-220 Leeb T., Baumgartner J. 2000. Husbandry and health of sows and piglets on organic farms in Austria. Animal health and welfare aspects of organic pig production. In: Proceedings of the 13th International IFOAM Scientific Conference, 28-31 August 2000, Basel. Alföldi T., Lockeretz W., Nig-gli U. (eds.), VDF Hochschulverlag an der Eidgenössische Technische Hochschule Zürich, Zürich (2000): 361 Leite D.M.G., Pereira N.W., Costa A.O.D., Vargas G.A., Silva A. 2000. Parasitoses in outdoor pig production. A Hora Veterinaria, 19: 8-10 McGlone J.J., Hicks T.A. 2000. Farrowing hut design and sow genotype (Camborough-15 vs. 25% Meishan) effects on outdoor sow and litter productivity. Journal of Animal Science, 78: 2832-2835 Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., Tauxe R.V. 1999. Food-related illness and death in the United States. Emerging of Infectious Disease, 5, 5: 607-25
Miao Z.H., Glatz P.C., Ru Y.J. 2004. Review of production, husbandry and sustainability of free- range pig production. Asian Australasian Journal of Animal Sciences, 17, 11: 1615-1634
Moller F. (2000). Housing of finishing pigs within organic farming. In: Ecological Animal Husbandry in the Nordic Countries, Proceedings from NJF-seminar No 303, 16-17 September 1999. DARCOF report, 2: 93-98 Morgan U.M., Buddle R., Armson A., Thompson R.C.A. 1999. Molecular and biological characterisation of Cryptosporidium in pigs. Australian Veterinary Journal, 77: 44-47 Murrell K.D., Pozio E. 2000. Trichinellosis: the zoonosis that won't go quietly. International Journal for Parasitology, 30, 12-13: 1339-49
Nansen P., Roepstorff A. 1999. Parasitic helminths of the pig:
factors influencing transmission and infection levels. International Journal of Parasitology, 29: 877-891 Olson N.C., Hellyer P.W., Dodam J.R. 1995. Mediators and vascular effects in response to endotoxin. British Veterinary Journal, 151: 489-522 Petkevicius S., Bach Knudsen K. E., Nansen P., Roepstorff A. 1996. The influence of diet on infections with Ascaris su-umand Oesophagostomum dentatum in pigs on pasture. Helminthologia, 33: 173-180 Petkevicius S., Nansen P., Knudsen K.E.B., Skjoth F. 1999. The effect of increasing levels of insoluble dietary fibre on the establishment and persistence of Oesophagostomum den-tatum in pigs. Parasite, 6: 17-26 Pozio E., Kapel C.M., Gajadhar A.A., Boireau P., Dupouy-Camet J., Gamble H.R. 2006. Trichinella in pork: current knowledge on the suitability of freezing as a public health measure. EuroSurveillance, 11(11): E061116 Quilez J., Sanchez-Acedo C., Clavel A., del Cacho E., Lopez-Bernad F. 1996. Prevalence of Cryptosporidium infections in pigs in Aragon (North-Eastern Spain). Veterinary Para-sitology, 67: 3-88 Rehbein S., Visser M., Winter R., Trommer B., Matthes H.-F., Maciel A.E., Marley S.E. 2003. Productivity effects of bovine mange and control with ivermectin. Veterinary Parasitology, 114: 267-284 Reiner G., Eckert J., Peischl T., Bochert S., Jäkel T., Mackenstedt U., Joachim A., Daugschie A., Geldermann H. 2002. Variation in clinical and parasitological traits in Pietran and Meishan pigs infected with Sarcocystis miescheriana. Veterinary Parasitology, 106, 2: 99-113 Rodriguez-Vivas L., Ortega-Pacheco A., Machain-Williams C. Y., Santos-Ricalde R. 2001. Gastrointestinal parasites in sows kept in two production systems (indoor and outdoor) in the Mexican tropics. Livestock Research for Rural Development, 13: 1-9 Roderick S., Hovi M. 1999. Animal Health and Welfare in Organic Livestock Systems: Identification of Constraints and Priorities. Report to the Ministry of Agriculture, Fisheries and Food (MAFF), London: 65 p. Roepstorff A., Murrell K.D. 1997a. Transmission dynamics of helminth parasites of pigs on continous pasture: Oesophagostomum dentatum and Hyostrongylus rubidus. International Journal for Parasitology, 27: 553-562 Roepstorff A., Murrell K.D. 1997b. Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis. International Journal for Parasitol-ogy, 27: 563-572 Roepstorff A., Murrell K.D., Boes J., Petkevicius S. 2001. Ecological influences on transmission rates of Ascaris suum to pigs on pastures. Veterinary Parasitology, 101: 143-153 Ryan U., Xiao L., Read C., Zhou L., Lal A.A., Pavlasek I. 2003. Identification of novel Cryptosporidium genotypes from the Czech Republic. Applied and Environmental Microbiology, 69: 4302-4307 Salajpal K., Karolyi D., Beck R., Kis G., Vickovic I., Dikic M., Kovacic D. 2004. Effect of acorn (Quercus robur) intake on faecal egg count in outdoor reared Black Slavonian pig. Acta Agriculturae Slovenica, 1: 173-178 Salajpal K., Dikic M., Spicic S., CvetnicZ., Karolyi D., Klisanic
V., Mahnet Z. 2010. Limits in extensive swine husbandry -a case study of Turopolje pig production system in Croatia. Acta Agraria Kaposvariensis, 14, 2: 215-220. Simopoulos A.P. 1991. Omega-3 fatty acids in health and disease and in growth and development. American Journal of Clinical Nutrition, 54: 438-463 Straw B.E., Dewey C.E., Wilson M.R. 1999. Differential diagnosis of swine diseases. In: Straw, B.E., D_Allaire, S., Menge-ling, W.L., Taylor, D.J. (eds.), Diseases of Swine, eighth ed. Iowa State University Press, Ames, Iowa: 41-89 Thornton K. 1990. Outdoor Pig Production. Farming Press Ltd, Ipswich, UK
Tubbs R.C., Hurd S., Dargatz D., Hill G. 1993. Preweaning morbidity and mortality in the United States swine herd. Swine Health and Production, 1: 21-28 Turner S.P., White I.M.S., Brotherstone S., Farnworth M.J., Knap P.W., Penny P., Mendl M., Lawrence A.B. 2006. Herit-ability of post-mixing aggressiveness in grower-stage pigs and its relationship with production traits. Animal Science, 82: 615-620
Van der Giessen J., Fonville M., Bouwknegt M., Langelaar M., Vollema A. 2007. Seroprevalence of Trichinella spiralis and
Toxoplasma gondii in pigs from different housing systems in The Netherlands. Veterinary Parasitology, 148, 3-4: 371-4 Van Grevenhof E.M., Ott S., Hazeleger W., van Weeren P.R., Bijma P., Kemp B. 2011. The effects of housing system and feeding level on the joint-specific prevalence of osteochondrosis in fattening pigs. Livestock Science, 135: 53-61 Venturini M.C., Bacigalupe D., Venturini L., Rambeaud M., Basso W., Unzaga J.M., Perfumo C.J. 2004. Seroprevalence of Toxoplasma gondii in sows from slaughterhouses and in pigs from an indoor and an outdoor farm in Argentina. Veterinary Parasitology, 124, 3-4: 161-165 Wang C., Diderric V., Kliebenstein J., Patton S., Zimmerman J., Hallam A., Bush E., Faulkner C., McCord R. 2002. Toxo-plasma gondii levels in swine operations: differences due to technology choice and impact on costs of production. Food Control, 13: 103-106 Warriss P.D., Kestin S.C., Robinson J.M. 1983. A note on the influence of rearing environment on meat quality in pigs. Meat Science, 9: 271-279 Xiao L., Herd R. P. 1994. Infection pattern of Cryptosporidium and Giardia in calves. Veterinary Parasitology, 55: 257-262