Keywords

1 Comparing Parasitic Risks and Their Control in OF in Ruminants, Pigs and Poultry

There is no doubt that organic farming (OF) rules that promote access to pastures or runs for livestock may enhance some parasitic risks in farming systems. On the other hand, other basic OF rules (e.g., reduced stocking rates of animals kept outdoors compared to indoor stocking rates or to conventional systems) are also known to reduce parasitic risks and to favour animal welfare. Therefore, when focusing on gastrointestinal (GI) helminths or protozoan parasites, different hypotheses concerning the consequences of introducing OF rules can be made between:

  1. 1.

    The transmission and level of infections of parasites whose infectious life stages (either as free-living eggs or larvae, or in intermediate hosts/vectors) are found in the outdoor environment (e.g., a whole range of GI helminths from the three main taxonomical groups: nematodes (strongyles), cestodes (taenia) and trematodes (flukes) (Taylor et al. 2007). In this case, OF rules are likely to increase the parasitic risks. The case of transmission of potential zoonoses (e.g., trichinellosis, toxoplasmosis) whose prophylaxis was previously controlled by keeping livestock indoors has to be examined in terms of food safety and human health.

  2. 2.

    The transmission of some parasites (e.g., certain intestinal protozoa such as eimeriosis in poultry and isosporosis in pigs) whose biological traits, rates of infection and associated pathological consequences are strongly linked to the concentration of animals. In this case, the application of OF rules is instead expected to reduce the parasitic risk.

To some extent, these concepts are overstated. For example, it is well known that some helminth transmission occurs indoors (strongyloidosis). On the other hand, severe cases of coccidiosis have been observed outdoors in calves and chickens (Nielsen et al. 2003). Also, the differences in parasitic risks between OF vs. conventional systems depend on the initial status. Major differences in parasitism have been found: (1) when conversion to OF concerns conventional production systems for which, on a large scale, animals were usually kept indoors (pigs and poultry); or (2) when compared to those where grazing was still the common rule (ruminants).

In the first cases and in most places, the required outdoor access for all or a part of the animals’ lives has resulted in deep changes in management when compared to conventional, intensive production. The associated OF changes in nutrition, biosecurity and practices are reflected in changes in disease patterns and food safety risks in OF. In many situations, this has been linked to the “re-emergence” of parasite infections whose life cycles cannot take place indoors. For example, although the availability of data on diseases in organic pig production is still limited, several studies have targeted GI parasites as a significant disease problem in the EU (Thamsborg and Roepstorff 2003; Roepstorff et al. 2011). In contrast, the OF requirements for outdoor access do not fundamentally change the overall husbandry and associated parasitic risks in ruminants for which grazing, at least for part of the animal’s life, is the general situation. This was also reported in a few cases of traditional pig farming systems with outdoor farms in the UK and Spain (Hovi et al. 2003; Trujillo and Mata 2000). However, some other general rules and recommendations in OF (e.g., to replace the usual allopathic antiparasitic treatments by phytotherapy and homeopathy when they have demonstrated their efficacy) can contribute to modulating the intensity or diversity of parasitic infections (Cabaret et al. 2002).

In both ruminant and monogastric hosts, the presence of GI parasites affects animal health and welfare and represents a major economic issue because host-parasite interactions are usually chronic infections that provoke long-term, insidious production losses. Therefore, the control of these parasitic infections is a key issue for the economic viability of farms and for animal welfare. However, in contrast to conventional systems that, until now, almost exclusively relied on chemotherapy to control parasites, the general goal promoted in OF is to achieve a more sustainable, integrated approach by combining solutions related to three main objectives linked to three key targets in the parasites’ life cycles.

  1. 1.

    the environment (hygiene): The aim is to reduce contact between the hosts and the infective parasitic stages through rational pasture management systems (outdoors, for helminths and protozoa) and by rigorous application of hygienic principles (indoors, mainly for protozoa).

  2. 2.

    the farm a nimals (host protective reactions): The aim is to improve the host response against parasitic stages (either resistance or resilience; see Box 8.1) by means of either the use of potential vaccines (immunoprophylaxis), alternated with genetic selection, or well-balanced nutrition.

  3. 3.

    the parasites (treatment): The aim is to eliminate or to modulate the biology of various parasitic stages in the host, either by evaluating the efficacy of novel, recommended approaches (phytotherapy, nutraceuticals and homeopathy) or by proposing more sustainable ways to apply synthetic antiparasitic drugs.

Box 8.1: Host Resistance and Host Resilience

Both concepts correspond to two components of the host response when infected with parasites. These two concepts have been particularly illustrated in the case of gastrointestinal infections with parasitic nematodes.

  • The host resistance is usually described as the ability of a host to affect the nematode biology either by decreasing the establishment of the infective L3, by delaying the worm growth, by reducing the female worm fertility and egg excretion and/ or by expelling existing adult worm populations. It is suspected that the host resistance is mainly dependent on the immune mechanisms acquired after repeated contact with the worms. It is usually estimated through measurements characterising the parasite populations

  • The host resilience is a second component of the host response to parasitism. It is described as the ability of an host to withstand the negative pathological effects due to the presence of worms inhabiting the digestive tract. This ability is usually measured by pathophysiological or production parameters. The underlying mechanisms for the host resilience remain obscure, although the role of some physiological feedback or adaptive mechanisms aiming at maintaining the host tissular and blood homeostasis is suspected.

  • Usually, a better resistance of the host is associated with a better resilience because processes affecting the worm biology and/or number also reduce the lesions and functional disturbances imposed to the host. However, a few examples have been described indicating that a higher host resistance could sometimes be associated with a lower host resilience, confirming the idea that the immune response as “a cost” (Colditz 2002)

It is noteworthy that a trend towards such integrated approaches is increasingly promoted today in conventional husbandry systems, mainly because of the rapid development and widespread diffusion of resistances to chemical drugs in parasite populations (Kaplan 2004; Chapman et al. 2010). In this respect, solutions developed in OF production systems can also largely benefit conventional systems and vice versa. For example, many of the innovative technical options explored in pigs and poultry have benefited from solutions previously explored in ruminants.

Therefore, this review aims at summarising and at illustrating:

  1. 1.

    How these various approaches that refer to the three main principles of disease control can represent the cornerstones of parasite control under OF rules: (i) in different livestock species (ruminants, pigs and poultry, focusing on laying hens); and (ii) within a wide range of epidemiological European conditions,

  2. 2.

    How these solutions need to be adapted depending on the mode of production and/or of some parasitic biological traits.

The framework of this review will be restricted to the main GI helminths and protozoan (coccidian) infections. For pig and poultry production, specific information on “re-emerging” parasites will be provided. For ruminants, because of the continued use of grasslands, the reader can find the list of the main GI helminth and protozoan parasites in the literature (Taylor et al. 2007).

2 The Importance of Parasites in Organic Livestock Farming

2.1 In Ruminants

As previously stated, in ruminants, the changes introduced by the conversion to OF rules do not basically modify the patterns of parasitic infection but are instead associated with changes either in the overall intensity of infection or in higher species diversity (Cabaret et al. 2002). The same dominant helminths and protozoan species are encountered in OF and conventional systems. Most studies have been dedicated to gastrointestinal nematodes (GINs), although trematodes, and to a lesser degree, cestodes, can also severely impair animal health and production by decreasing the quantity or downgrading the quality of products.

2.2 In Pigs

The introduction of outdoor access, whether it be pastures or small, concrete covered runs, is a major risk factor for a range of GI helminths and protozoa with direct life cycles, (e.g., helminth genera Ascaris, Trichuris, Strongyloides, Hyostrongylus and Oesophagostomum spp). Furthermore, outdoor access is a necessity for the completion of a helminth’s indirect life cycle, e.g., Metastrongylus spp. or spiruroids with earthworms and dung beetles, respectively, as intermediate hosts (Taylor et al. 2007).

In contrast, in many intensive indoor herds, Isospora suis is the most pathogenic coccidian, causing severe diarrhea in piglets within the first weeks of life. In contrast to helminth infections, the prevalence of I. suis is lower in OF herds and associated clinical problems are uncommon (Roepstorff et al. 1992).

Studies in Northern Europe on a limited number of farms have identified Ascaris suum, Oesophagostomum spp. and Trichuris suis as the most common and important parasites in OF production (Carstensen et al. 2002). Overall, compared with conventional farms, the prevalence and levels of helminth infection were higher in OF systems. However, some differences have been observed between the studies, depending on the worm species and/or host factors (e.g., piglets vs. adult pigs). These results illustrate how differences between OF and conventional systems with regards to parasite infections depend (i) on the parasitic species, (ii) on the local production practices (e.g., whether growing pigs or farrowing sows are pastured) and management, and (iii) on the epidemiological conditions (Lindgren et al. 2008; Carstensen et al. 2002).

When examined in detail, there is no indication of the reintroduction of parasites on OF farms that were suspected because of the potential occurrence of wild boar reservoirs (Lindgren et al. 2008). In Swedish studies, the stomach worm, Hyostrongylus rubidus and the lungworm Metastrongylus spp were absent due to long history of intensification, and indoor production was not found (Lindgren et al. 2008). spp. A currently on-going survey in eight EU countries is expected to complete these data (Roepstorff et al. 2011).

Besides the recommendation to use outdoors runs, other factors may limit the options for control of parasitism in pigs. They include limitations on preventive use of antiparasitic drugs, use of deep litter bedding and, in general, lower levels of hygiene. Although not proven, the potential shortage of certain amino acids may also affect susceptibility to infections. There are indications that the use of permanent pastures as compared to pastures within the crop rotation may result in more parasites (Carstensen et al. 2002; Lindgren et al. 2008). Other risk factors for helminth infections, based on knowledge acquired from conventional farms, include: solid floors, straw bedding, infrequent dung removal, high indoor humidity, and high intake of insoluble fibre (roughage/forage). On the other hand, the latter may limit problems with certain bacterial infections.

The clinical implications and potential impact of helminths on production remain largely unknown since no intervention studies have been performed on organic farms. Clinical trichuriosis has been reported on an organic farm (Carstensen et al. 2002), but even on conventional farms, a pathological impact as measured in experimental studies has been difficult to demonstrate. However, indirect effects such as a reduced protective response after vaccination against unrelated agents (e.g., Mycoplasma hyopneumoniae) should not be neglected (Steenhard et al. 2009).

2.3 In Poultry

The risk of helminth infestations is higher in hens in free-range systems compared to systems without outdoor runs (Permin et al. 1999) (Fig. 8a, Colour plate 8). The roundworms, Ascaridia galli and Heterakis gallinarum, are the most common species found in the intestines of poultry. Eggs of both species have a long survival rate in the environment, and, thus, a high infection potential. Because of these biological peculiarities and because of the establishment rates of A. galli that strongly decrease with increasing infection doses (Permin et al. 1997), preventive measures, effective in other species, are less efficient in poultry.

Free-range hens are also at an increased risk of being infected by the protozoan, Histomonas meleagridis (blackhead disease), which is transmitted by H. gallinarum. At present, no feed additives against blackhead disease are registered (EC 2002). Helminth control is therefore probably the most effective measure against these protozoan infections.

The chicken is host to seven species of Eimeria spp. These coccidian parasites vary in their pathogenicity, but generally, coccidiosis is a major economically significant intestinal disease of commercially reared poultry. Good management contributes to the prevention of coccidiosis, but additional measures are needed under indoor and outdoor conditions (McDonald and Shirley 2009).

3 Methods of Control

3.1 Hygiene: Reducing the Environmental Sources of Infection

The general objective is to reduce the contact between the host and the infective parasitic stages. Under indoor conditions, this is usually based on the principles of disinfection and hygiene. The main target is protozoan infections, although helminths are also found in poultry. However, methods relying on the overall principles of hygiene to reduce pasture contamination have also been developed.

3.1.1 Management of Indoor Areas

There are four possible sources of coccidian infections in ruminants: (i) oocysts from previous faecal contamination that survive in the environment; (ii) fresh oocysts passed by the ewes; (iii) fresh oocysts passed by the lambs; and (iv) contaminated ewe fleeces and udders (Pout 1973). The management system, hygiene status and nutrition play an important role in the development of subclinical vs. clinical coccidiosis (Gregory and Catchpole 1990). Weaning of lambs/kids in combination with other stress factors such as high stocking densities, multiple lambing with lower colostrum and milk intake, cold and wet weather and depressed immunity predispose animals to disease (Catchpole et al. 1990). However, the use of pastures does not always mean a lack of coccidiosis risk. For example, calves on organic dairy farms have also been found to be heavily exposed to coccidia when they are group-housed in deep-litter pens indoors and later introduced into permanent pastures (Nielsen et al. 2003).

In pigs, continuous housing in permanent deep-litter systems may lead to increasing levels of parasite infections (Holmgren and Nilsson 1998). Similarly, the introduction of enriched environments like sprinkler systems may be associated with the increased risk of helminth transmission (Roepstorff et al. 2011). This can be partly overcome by the ample provision of new straw bedding, but the only rational approach is all-in-all-out systems. In a recent study, some sanitary and management protocols aimed at lowering oocyst uptake and excretion from infected piglets have been described. These include farrowing rooms, no cross-fostering or fostering during the first 24 h after farrowing, plastic flooring in the farrowing pens, farrowing rooms with fewer pens, and measures to prevent caretakers from entering the farrowing pens (Skampardonis et al. 2012).

In poultry, good hygiene of hen houses is also essential to prevent accumulation of the long-lasting infective parasite eggs and/or oocysts over time. Thorough cleaning of the hen house is only possible between flocks. Maurer et al. (2009) found similar helminth egg concentrations at different litter management regimes (replacement or addition of litter during flocks) and no effects of egg density in litter on worm burdens of the layers.

3.1.2 Outdoor Management

Under outdoor conditions, the runs and pastures cannot be “disinfected” to destroy infectious stages. The use of possible chemicals on a large scale has proved to be inefficient under field conditions and is not acceptable according to OF rules. Therefore, different strategies of grazing management have been developed. They were initially designed for ruminants in the late 1960s and mainly aimed at controlling infections with GI nematodes. Their pros and cons were then evaluated under a wide range of epidemiological conditions (Michel 1976; Barger 1999). These different grazing management strategies aim at reducing the parasitic risk over time and/or space

  • by reducing the larval density by applying low stocking rates to dilute the risk;

  • by taking advantage of the natural death rate of infective larvae by pasture rotation systems;

  • by accelerating larval mortality through biological control or co-grazing between different hosts.

Due to the different epidemiological patterns of the parasite species involved, preventive strategies are less effective in monogastrics than in ruminants, although hygiene and proper management of runs and pastures are also the basis for preventing helminth infections in pigs and poultry.

3.1.3 Dilutions

Many studies on GIN infections in ruminants have shown the existence of a relationship between the stocking rate and the level of host infection. However, this phenomenon does not appear to be linear (Thamsborg et al. 1996). The limitation of animal outdoor stocking rates, which is one of the cornerstones of the OF rules, is based on common sense with regard to parasitic control in ruminants. In pigs, the effects of nose rings (to avoid the destruction of the sward) and stocking rate on the uptake of infections are not clearly described (Thomsen et al. 2001). Similarly, stocking rates within the hen house and in the hen run had no effect on A. galli infections (Permin et al. 1998). Moreover, Heckendorn et al. (2009) reported that the stocking rate of hens in the outdoor run did not influence the transmission patterns of A. galli and H. gallinarum, and repeated moving of runs did not reduce helminth infections. Lower stocking rates, however, led to a substantial improvement of the run vegetation.

3.1.4 Rotation of Pastures

Because the survival of infective stages of parasites on pastures is limited in time, systems of pasture rotations aimed at introducing animals in paddocks after the risk related to the infective stages has been substantially reduced because of the natural death rate. This concept has been applied in ruminants and monogastrics but the efficiency of the methods highly depends on (i) the biology of parasitic stages, and (ii) the local/regional climatic and epidemiological conditions.

For example in ruminants, more efficient results have generally been obtained with rotation methods under tropical compared to temperate conditions because of the peculiarities of the biology of Haemonchus contortus, which is a highly prevalent nematode in the tropics (Torres Acosta and Hoste 2008).

In pigs, pasture rotation is also likely to play a central role in the control of some helminth species. Infective larvae of Oesophagostomum spp. and H. rubidus can survive for a maximum of 1 year on pasture and have a poor over-winter survival rate in northern temperate climates (Thomsen et al. 2001; Mejer 2006). Consequently, even pastures heavily contaminated in autumn may be totally clean the following spring, and Oesophagostomum spp. do not constitute a problem in strictly outdoor sow herds (Carstensen et al. 2002).

In contrast, the most common helminths (A. suum and T. suis) are characterised by hard-shelled eggs with a sustained longevity on pasture of up to 10 years (Roepstorff 2003), despite initial high death rates of eggs within the first 6–12 months (Larsen and Roepstorff 1999), indicating that a shorter rest period may still serve to reduce the transmission. Because of this long persistence in the environment of these worm species, it is still unknown as to whether pigs should be moved to clean pasture one or two times per year, and when it is safe to be back to a previously contaminated pasture. Ongoing experiments using naive pigs (never previously exposed to parasites) to trace the levels of contamination on pastures after initial deposition of eggs, have yielded two results: (1) transmission levels increased the first 2 years, indicating an unexpectedly slow development to infectivity in colder climates; and (2) infection levels did not markedly decrease after 4 years (Helena Mejer 2010, unpublished data). Moreover, Carstensen et al. (2002) described a farm that produced organically for 8 years with a stringent 3-year pasture rotation. Ascaris was found with a prevalence > 90 % in the weaners and fatteners. These results may indicate either a failure in the management of the scheme or simply that 3 years are not sufficient to reduce pasture contamination with both parasites.

Last, in some poultry production systems (e.g., free ranging broilers or layer flocks in mobile systems), an all-in-all-out system, where new areas are provided for each batch of animals, is feasible (Thamsborg et al. 1999). Where hens are kept in solid hen houses with surrounding runs, a rotation scheme with sufficient resting time between flocks (> 1 year) is nearly impossible to achieve. In a 2-year on-farm experiment, a rotation scheme where the hen flock returned to the same area during one season helped to maintain the sward, but it was not effective to reduce A. galli and H. gallinarum burdens (Maurer et al. 2013).

For the coccidian parasites, including Isospora suis in pigs, efficient control seems achievable (if pastures ungrazed the previous year are provided at turn-out), in particular in herds where farrowing huts are routinely moved before farrowing (Roepstorff et al. 1992). Isosporosis is thus not a clinical problem in organic pig production.

3.1.5 Co-grazing Between Different Host Species

Coccidia are highly specific to their hosts. For helminths, with the exception of trematodes and a few nematode species (e.g., Trichostrongylus axei) that are ubiquists, most nematodes and cestodes are specific to their hosts, although the phenomenon is not fully exclusive between large and small ruminants. This parasite specificity means that when different animal species graze together in the same pasture, each host contributes to reducing the pasture-related risk for the second animal species by “destroying” the parasitic stages specific to this second host.

Most studies on these co-grazing methods have been performed in ruminants, generally between cattle and sheep. The results obtained under various epidemiological conditions and in situations of either simultaneous or alternate grazing have usually shown a reduced level of infection in sheep, especially with the pathogenic species H. contortus (Hoste et al. 2009). The effects on cattle were more limited. These practices have usually been associated with better resilience (see Box 1) of the animals, including a better use of the grazing rejects (see review by Barger 1999).

When sows have nose rings, it is possible to have them graze together with ruminants. In a 3-year study with heifers and dry sows, mixed grazing has been shown to increase the performance of the sows, although the most important effect was to reduce Ostertagia infections of the heifers and to increase their weight gain (Thamsborg et al. 1999). The effect was attributed to better utilisation of pasture, as well as disruption of cattle faecal pats and the surrounding tussocks. However, the use of nose rings is now an animal welfare issue.

As suggested by Barger (1999), there are also potential risks in mixed systems. One is that previously host-specific helminths adapt to other hosts. For example, cross contaminations with sheep nematodes, leading to clinical diseases, have been reported in calves (Armour et al. 1988). Patent Ascaris infections have also been described in lambs grazing in pastures previously used by pigs. Reciprocally, the ruminant species, Teladorsagia spp and Trichostrongylus vitrinus , were also reported in pigs. Last, the increased risk related to trematodes has to be more closely monitored.

3.1.6 Biocontrol and Use of Nematophagous Fungi

Under laboratory conditions, a range of various biological agents (e.g., Bacillus thuringiensis, or “cannibal” nematodes) have been shown to affect the biology of environmental stages of helminths, particularly nematodes (Torres-Acosta and Hoste 2008). However, under farm conditions, the most outstanding results of biocontrol to decrease pasture infectivity were obtained with some nematophagous fungi that can kill nematode larvae in faeces. Their effects have been studied within a wide range of host species and/or epidemiological conditions, in particular for Duddingtonia flagrans. This fungus species was of particular interest because of the ability of the spores to develop and to trap the nematode larvae in faeces after a digestive passage (Larsen 2000). In ruminants and horses, convincing results have also been repeatedly obtained under both laboratory and farm conditions. However, no commercial product of this promising, innovative option has yet been launched.

D. flagrans was also shown to significantly reduce Oesophagostomum dentatum infections in grazing pigs (Larsen 2000). In contrast, the main parasitic nematodes of monogastric animals have egg-dwelling and not larval infective stages. Therefore, until now, no promising biocontrol agents have been identified for use against these species.

3.2 Improving the Host Response: Immunostimulation

3.2.1 Vaccination

Conceptually, vaccination represents a highly attractive solution to control any infectious disease and is usually well accepted in OF. Therefore, this solution is clearly included in the general “basket of options” explored to address the issues related to parasitism in OF. However, antiparasitic vaccines still face several limits today in terms of their implementation under field/farm conditions because of considerations related to either (i) ethics (GMO vaccines are not acceptable in OF systems; use of live vaccines with potential risks of diffusion of diseases after mutation); (ii) technology (the difficulties to develop vaccines based on recombinant proteins against helminths); or (iii) economy (multivalent vaccines are often demanded).

For gastrointestinal helminths, no commercialised vaccines are currently available despite considerable research efforts to produce a vaccine against H. contortus based on some hidden antigens of the nematode GI tract (Smith and Zarlenga 2006). However, a live vaccine with partly inactivated larvae of the cattle lungworm Dictyocaulus viviparus (Dictol®) has long been commercialised and widely used in some countries where lungworms are endemic (Benitez Usher et al. 1976). For protozoa, the use of live (attenuated or non-attenuated) vaccines (consisting of oocysts of different Eimeria species) to control coccidiosis due to various Eimeria infections in layer and broiler breeder chickens is well established (Chapman et al. 2002; Williams 2002). Vaccination with a reduced number of Eimeria species is also increasingly applied in one-day old organic broiler chickens (Williams 2002), but conventional broiler production still largely relies on anticoccidial drugs (McDonald and Shirley 2009).

3.2.2 Selective Breeding for Resistance and/or Resilience to Parasites

The preference for local livestock breeds, is one of the cornerstones of the OF philosophy to address sanitary problems and to reduce the reliance on chemical drugs. This recommendation relies on the concept of coevolution between parasite and hosts, which, after natural selection, led to hosts that were more adapted to parasite infections depending on the regional/epidemiological conditions. In the case of GI parasite infections, early results that support the hypothesis that some genetic components are involved in differences in resistance to helminths were obtained in sheep because, until recently, helminth challenges remained limited in monogastrics under conventional production systems.

In ruminants, differences in the level of gastrointestinal infections between breeds have been thoroughly documented in sheep. However, most of the studies compared imported vs. local breeds under tropical conditions (Bishop and Morris 2007). In contrast, less data is available comparing local rustic breeds to more intensively selected breeds in temperate conditions.

The existence of possible individual differences in resistance against GI nematodes within a breed has also been widely studied (Bishop and Morris 2007; Vagenas et al. 2002). The level of nematode egg excretion has been the main phenotypical criterion used for selection. Heritabilities (h2) of faecal egg counts (FECs) in sheep range between 0.08 and 0.43 (Gasbarre and Miller 2000). This has promoted programmes (e.g., the commercial DNA-marker WORMSTAR programme for sheep in New Zealand) to select animals with a better response to GINs and responsible for a lower pasture contamination because of significantly decreased FECs after several generations (Hunt et al. 2008; Vagenas et al. 2002). Resilience selection programmes aimed at better animal productivity under parasitic challenges have been another option that was explored to counteract the negative effects of parasites on their hosts. However, this option has received less attention than selection for resistance (Bisset et al. 1996).

Such genetic differences in resistance are progressively assessed in monogastrics. Some Danish results (Schou et al. 2003) indicated that the epidemiology of A. galli infections in chicken may similarly be influenced by a genetic component. Abdelquader et al. (2007) found that there is not only a variation in the genetic background of the hens, but also that A. galli isolates from different geographic areas differ in their ability to infect different chicken genotypes. Gauly et al. (2008) observed significantly higher faecal egg outputs of helminths in white laying hens than in brown hens. They estimated sufficiently high h2 of FECs of A. galli (0.13–0.19 for white hens) as well as for H. gallinarum worm burdens (0.31–0.41) to allow selection for helminth resistance. However, parasite resistance is not a seriously considered criterion in poultry breeding at present because genotypes are mainly selected for best performance under indoor conditions where the parasitic challenges are of minor importance.

In pigs, studies based on examination of 200 offspring of known matings revealed h2 of FECs of 0.3–0.4 for A. suum, and of 0.4–0.7 for T. suis (Nejsum et al. 2009). For T. suis, the h2 depended on time in relation to the onset of infection: during the early expulsion phase, h2 were highest, probably indicating close genetic control of the onset of immunity. For Ascaris, other parameters such as worm burden, total egg output and antibody levels were also heritable, whereas this was not the case for the size and fecundity of the worms (Peter Nejsum, personal communication). It is obvious that breeding for increased host resistance is also an option within the pig industry and may be highly relevant in free-ranging systems, although more studies must to be performed.

3.3 Treatments Affecting Parasite Biology

When treatments are required to cure animals and to improve their welfare, the general OF recommendations are to promote alternative medicines (phytotherapy, homeopathy) rather than synthetic chemical (allopathic) drugs. However, in many circumstances, the efficiency of alternative medicines remains to be fully established.

3.3.1 Herbal Drugs

The use of natural (herbal) remedies (phytotherapy, including the use of essential oils) to cure and/or to prevent diseases is not a novel concept (Githiori et al. 2006; Waller et al. 2001). According to both time and geographical scales, chemical drugs remain the norm. It is worth recalling that more than 70 % of the drugs currently used worldwide are natural and that many of the so called “chemical drugs” are derived from natural products (Wilcox et al. 2001). For example, halofuginone, a quinazolinone alkaloid from Dichroa febrifuga, has been used as a coccidiostat because febrifugine, the original plant extract, possesses antiprotozoan activity (Youn and Noh 2001). Natural (mainly plant) materials used as an alternative to control parasitic diseases can be broken down into two different categories: phytotherapy remedies vs. nutraceuticals. In both cases, the observed antiparasitic activity is usually linked to the presence of plant secondary metabolites (PSMs) in sufficient concentration, including condensed tannins and flavonoids, sesquiterpens, proteinases, etc. (Rochfort et al. 2008).

Herbal drugs are preparations of plants and/or plant extracts that aim at curing infected animals after a short-term administration. Their general therapeutic recommendations are close to those of chemical drugs, except that the active compound(s) are usually not well identified and measurable. Herbal remedies are often a mixture of plants and/or plant extracts obtained by various physical or chemical processes. Accordingly, they are usually composed of a high number of biochemical components. This complexity is a general characteristic of drugs derived from plants. It has consequences on the definition and standardisation of the products and, consequently, on the validation of their therapeutic efficacy as a function of their variations.

A variety of plants worldwide have been shown to affect survival and/or reproduction of helminths of chicken or ruminants in vitro or in vivo. However, in some cases, severe side effects on the host have been observed after use of plant products (e.g., Javed et al. 1994; Akhtar and Riffat 1985). In other studies (e.g., Chota et al. 2009), positive effects of a plant preparation (Carica papaya) were confused with the effects of better nutrition during the experiments. The effect of these herbal drugs was tested by Maurer et al. (unpublished data) under controlled conditions in eight series of hens and chickens artificially infected with A. galli. Although significant effects of some plant preparations were observed in a particular series, none of the plant extracts tested resulted in reductions of egg counts or of worm burdens in a reproducible manner (unpublished data). Similar difficulties have been found in a series of studies comparing the efficacy of plant preparations against helminths in lambs (Bouilhol et al. 2003; Hördegen et al. 2003) and pigs (van Krimpen et al. 2010).

Research on alternative methods for controlling Eimeria spp. with plants showed that the effect on coccidia differs from the one on nematodes. Some plants and plant products such as Azadirachta indica (Tipu et al. 2002) and artemisinin from Artemisia annua (Almeida et al. 2012) reduced the excretion of oocysts of some Eimeria spp. and/or decreased mortality and intestinal lesion rates. Youn and Noh (2001) tested extracts of 15 plants against E. tenella in chickens and found extracts of Sophora flavescens to be the most efficient in terms of survival rates, bloody diarrhoea, lesion scores, body weight gains and oocyst excretion.

The use of antioxidant compounds in the management of coccidiosis has been shown to be effective because they decrease the degree of intestinal lipid peroxidation, which is associated with coccidian parasite-induced host cell destruction. One of the most potent veterinary anticoccidials, toltrazuril, is believed to achieve some, if not all, of its beneficial effects by limiting the degree of lipid peroxidation (Eraslan et al. 2004).

In support of this hypothesis, in vivo studies in South Africa have included treatment with extracts from Tulbaghia violacea, Vitis vinifera and Artemisia afra (Naidoo et al. 2008), and in China with proanthocyanidin extracts from grape seeds (Wang et al. 2008). Both improved the performance of broiler chickens and relieved the clinical symptoms caused by avian coccidian infection.

3.3.2 Nutritional Approaches and Nutraceuticals

The term “nutraceutical” is defined as “any substance that may be considered as a food or part of a food which provides health benefits, including the prevention and treatment of disease” (Andlauer and Furst 2002). Nutraceuticals are a feed resource, used either fresh or conserved, but the main reason for using them is linked to their potential benefits on animal health. Compared to herbal remedies, they are administered for a longer term (at least a few days), and the first objective is to prevent or limit the level of infections and, consequently, to reduce the reliance on chemotherapy to control parasites. In contrast to allopathic treatments that aim at eliminating worms, nutraceuticals act more by “slowing down” the biology of parasites and the dynamics of infection. Since the end of the 1990s, results on the use of nutraceuticals to control GINs have been obtained either in ruminants or pigs, illustrating how this option might be relevant in various OF systems (Waller and Thamsborg 2004).

In small ruminants (Fig. 8b, Colour plate 8), most current data on the potential represented by nutraceuticals have been obtained on the use of tannin-rich (TR) legume fodders, (e.g. sulla, Sericea lespedeza, big and birdsfoot trefoils, and sainfoin). Overall, the first effect associated with the distribution of tanniniferous legumes is a reduction of GIN egg excretion due to either a reduction in worm number or the reduced fertility of female worms (Hoste et al. 2006; Athanasiadou et al. 2001; Heckendorn et al. 2007; Manolaraki 2011). Reductions in the establishment of infective larvae have also been described (Hoste et al. 2006). Less consistent results have been obtained on possible reduced development from eggs to infective larvae in the environment (Niezen et al. 2002).

In addition to TR legumes, many studies in sheep have focused on chicory (Cichorium intybus) when used as forage. Its consumption has often been associated with some favourable effects on worm biology. For chicory, the suspected bioactive compounds are not tannins but sesquiterpene lactones (Marley et al. 2003; Athanasiadou et al. 2007).

In pigs, the addition of easily fermentable carbohydrates to the diet was shown to significantly diminish O. dentatum numbers and female fecundity (Petkevičius et al. 2003). This promising principle is currently being investigated using inulin-rich diets for sows in OF. Chicory roots and lupin seeds are rich in fermentable carbohydrates, particularly fructans (inulin). In pigs, an almost complete reduction of the Oesophagostomum egg output was obtained by adding purified inulin (Petkevičius et al. 2003) or dried chicory roots to the diet (Mejer 2006). High reductions in worm counts have been observed in some, but not all studies (Petkevičius et al. 2003; Mejer 2006). Incomplete elimination of worms may explain why depression of egg excretion was partially reversible since egg counts were shown to increase when the carbohydrates were withdrawn from the diet. Since the fermentable carbohydrates are only partially degraded in the small intestine, the action mechanism is probably related to the production of short-chain fatty acids by fermentation in the large intestine (Petkevičius et al. 2004). These fatty acids could directly or indirectly cause adverse conditions for the residing nematodes just as there is a shift in microbial composition. Consequently, T. suis, another inhabitant of the large intestine, is moderately affected, but results are inconsistent (Thomsen et al. 2007). Furthermore, penetration of early larval stages of A. suum in the large intestine before the migratory liver phase, and the establishment of incoming infections may be affected (Mejer 2006) but not adult established infections (Mejer, personal communication). Because A. suum and T. suis are the major targets of nematode control in outdoor pig production, these findings require further validation if they are to be considered to be of practical relevance.

3.3.3 Allopathic Treatments

Effective alternative methods for parasite control in poultry are lacking, and the use of conventional anthelmintics is the rule on organic as well as on conventional farms, although the extent of their use may vary. The situation is particularly delicate in the case of laying hens because only one anthelmintic (flubendazole) is registered. This issue is a major problem for organic egg production.

In ruminants, methods aimed at a “tailor-made” (more adapted) use of chemical drugs are also currently being explored in conventional systems because of the increasing challenge represented by the development of resistance to antiparasitic drugs (Kaplan 2004). These approaches might also be of benefit to the OF systems. For an overview of recent results and approaches used for these Targeted Selective Treatments (TST), the reader is referred to a special issue of Veterinary Parasitology (2009) on “Novel Approaches for the Sustainable Control of Nematodes in Ruminants” that summarises the main data from the PARASOL EU project.

4 Discussion/Conclusions

Parasite infections are also described as “long term interactions”. Therefore, they probably represent a paradigm to illustrate how the control of any livestock disease can be challenged in OF systems whose general aim is sustainable production. Moreover, the issues related to the control of parasitic infections in livestock illustrate some key features of both the societal and scientific questions raised by the development of OF systems. Obviously, one main keyword underlying the concept of OF disease control is “variability”.

Consequently, a whole range of questions are emerging, for example: (i) How can we challenge the differences between the consequences of this variability in parasitic risks with the consumer’s image of OF production? (ii) How can we analyse the variability of situations and host-parasite interactions? (iii) How can this variability in OF production systems be integrated into the general framework, which includes the three main principles of disease control? (iv) Do we have the appropriate methodological tools to measure the effects of the different methods of control?

Promoting OF rules in livestock is usually linked to improved animal welfare and better product quality by the consumer public. However, when considering the parasitic challenge, several pros and cons must be taken into account. Indoor breeding is usually associated with higher animal concentrations, less possibility of expressing social behaviour and, consequently, a lower status of animal welfare. However, outdoor breeding, which is promoted by OF, also means a higher risk of parasitic infections, degradation of animal health and welfare and, in some cases, can raise questions about the safety of livestock products (e.g., increased risk of zoonoses related to possible wildlife reservoirs).

Throughout this chapter, we aimed at illustrating the robustness of the three well-defined principles for controlling all pathogenic processes (Torres-Acosta and Hoste 2008): (1) by reducing the contact between the host and the infective agents [including the disinfection/elimination of pathogens in the environment (hygiene)]; (2) by improving the host response to the parasites (immunostimulation); and (3) by eliminating the parasites in the hosts (treatment). These principles still remain the cornerstones of actions against any pathogen, including parasites. They have generic implications, as illustrated for the different parasitic agents in the different livestock species under both conventional (CF) and OF systems.

The main difference between the two modes of production is probably linked to the order of priorities given to the different actions. In CF, the reliance on curative and supposedly fully suppressive synthetic antiparasitic drugs has been the first and nearly exclusive part of the tripod because of the difficulty to develop vaccines against parasitic agents. According to OF rules, disease prevention based on hygienic principles relies first on the stimulation of the host response as a result of genetic, nutritional factors and/or use of homeopathy, whereas curative synthetic drugs are only used as a last-ditch option when phytotherapy or natural substances have been proven inefficient (EC 2002).

The variability of interactions with the environment makes it necessary to adapt the solutions derived from these three main principles of control. This can be illustrated by two examples.

In pigs and poultry, the difficulty in applying genetic selection for resistance to parasites from genotypes selected primarily for performance under indoor conditions has been reported. A second option is to better evaluate and possibly to use local breeds that have been traditionally maintained outdoors. This corresponds to one of the general recommendations in OF rules. However, the reduced size of the remaining populations is usually a limiting factor.

Compared to the well-standardised synthetic antiparasitic drugs, the variability in resources is also a key factor to consider when assessing the efficacy of nutraceuticals. The amount and/or quality of PSMs, which are usually thought to be responsible for the activity, vary with genetic, environmental and even technological factors (Manolaraki 2011). This leads to the need for research to identify the main active compounds and to develop simple, affordable methods to measure biological and/or biochemical markers of activity. The situation is even more complex with phytotherapy and herbal remedies that often correspond to mixtures of plants. Last, for homeopathy, which is often assumed to have some long-term effects, the methodology to demonstrate the activity in experimental studies needs to be adapted to livestock species.

Specific studies performed under OF conditions to evaluate adapted solutions for the control of digestive parasitism have existed for nearly 10 years, although differences in progress still exist in the different livestock species (Lund and Algers 2003; Hovi et al. 2003). Because conventional production systems in ruminants have involved extensive use of grazing for many years, some agronomical and technical solutions have been widely explored in cattle, sheep and goats, compared to pig and poultry production. One of the objectives of this review was to illustrate how results acquired on ruminants can be of benefit to monogastrics since the principles for controlling parasitic diseases remain the same, regardless of the host species. It is also worth emphasizing that many of the solutions explored in OF can be of benefit to conventional systems of production. For example, because of the widespread diffusion of resistances to antiparasitic drugs, the sole reliance on chemotherapy in conventional systems is increasingly recognised as being unsustainable, and the need for alternative options is evident. Another reason is the implementation of more restrictive regulations on the use of chemical treatments in livestock, sparking a major interest in alternative approaches. A more restrictive use will delay the diffusion of resistance to antiparasitic drugs in both protozoa and helminths in any system. In both OF and conventional systems, the general goal today is to promote integrated control that relies on a “basket of options” adapted to on-farm situations. In this respect, the current development of software models to integrate abiotic and/or biotic factors at the farm level in the analysis of the parasitic risk of GIN infection in cattle and to propose adapted control measures seems promising (Chauvin 2009).