Seasonal patterns

For successful planning and execution of control against hemonchosis, there is a need for improved knowledge of the epidemiology and ecology of all free-living stages of H. contortus under local conditions (Okon and Enyenihi, Reference Okon and Enyenihi1977; Schillhorn Van Veen, Reference Schillhorn Van Veen1978). Previous work in Nigeria revealed that rainfall rather than temperature was the major determinant for development and survival of the free-living stages of H. contortus on pastures (Okon and Akinpelu, Reference Okon and Akinpelu1982; Chiejina and Emehelu, Reference Chiejina and Emehelu1984; Chiejina and Fakae, Reference Chiejina and Fakae1984; Bolajoko, Reference Bolajoko2002). This can be explained because temperatures are generally high enough to permit successful development of eggs to the L3 stage and do not therefore limit L3 availability.

Overall, high burdens of H. contortus generally occur during the rainy season, which corresponds to the period of confinement of animals away from grazing as a way of protecting growing crops on the farm, and lower worm loads are usual when animals are allowed free range grazing during the dry season, which is the period of crop harvesting (Ogunsusi and Eysker, Reference Ogunsusi and Eysker1979; Fakae and Chiejina, Reference Fakae and Chiejina1988; Fakae, Reference Fakae1990a; Bolajoko, Reference Bolajoko2002).

Generally, in Nigeria, the phenomenon of inhibited development and maturation of the larvae of H. contortus has been observed in sheep at the onset of the dry season when field conditions are not favorable for development (Okon and Akinpelu, Reference Okon and Akinpelu1982; Bolajoko, Reference Bolajoko2002). Larvae then presumably mature during the wet season, with the counterintuitive result that worm burdens are often highest during the housing period of confinement.

Hypobiosis in H. contortus in Nigeria

As well as being a nematode with especially high biotic potential, the ability of H. contortus to enter a state of hypobiosis is epidemiologically important in the tropics and subtropics (Schad, Reference Schad and Esch1977), as well as in temperate and European countries (Connan, Reference Connan1975; Dunn, Reference Dunn1978; Ayalew and Gibbs, Reference Ayalew and Gibbs1973; Waller and Thomas, Reference Waller and Thomas1975; Herd et al., Reference Herd, Streitel, McClure and Parker1984). Although there are conflicting reports regarding the precise stimulus triggering this phenomenon, it is thought to be environmental in source and nature (Schad, Reference Schad and Esch1977; Capitini, et al., Reference Capitini, McClure and Herd1990). Hypobiosis occurs at the start of a protracted dry season and permits the parasite to survive in the host as arrested L4 instead of maturing and producing eggs, which will die and fail to develop on the dry pasture. Development resumes just before the onset of the seasonal rainfalls, thereby ensuring carrying over of the infection from one season to another (Fakae, Reference Fakae1990b; Gatongi et al., Reference Gatongi, Scott, Ranjan, Gathuma, Munya, Cheruiyot and Prichard1997; Sissay et al., Reference Sissay, Uggla and Waller2007).

Okon and Enyenihi (Reference Okon and Enyenihi1977) and Chiejina et al. (Reference Chiejina, Fakae and Eze1988) reported that hypobiosis was of no significance in some parts of the south and coastal regions of Nigeria because of the frequent rainfall and short or absent dry season. Later, Tembely et al. (Reference Tembely, Lahlou-kassi, Rege, Sovani, Diedhiou and Baker1997) made similar observations for regions of frequent rainfall in East Africa.

Outbreaks of hemonchosis immediately following the onset of the rainy season are due to the rapid maturation of the pool of arrested larvae in sheep's abomasum. Therefore, factors that increase larval acquisition just before and following the onset of the dry season dictate the subsequent severity of hemonchosis immediately after the start of a new rainy season (Schillhorn Van Veen, Reference Schillhorn Van Veen1973).

Since rainfall is highly seasonal, pasture infestation and infectivity are equally seasonal, with the population of infective larvae the highest during the wet season. At a given location, the population of L3 is largely determined by rainfall distribution (O'Connor et al., Reference O'Connor, Walkden-Brown and Kahn2006; van Dijk and Morgan, Reference van Dijk and Morgan2011). Therefore, sheep that acquire infection at the beginning of a dry season are the only means of maintaining the infection in the population until the next rainy season (Chiejina and Emehelu, Reference Chiejina and Emehelu1984).

Regional differences in seasonal patterns of hemonchosis in Nigeria

Outbreaks of hemonchosis in the north usually occur only in the rainy season, from June to October. The absence of rain and the low humidity in the dry season prevents development; therefore no new infections occur during this period (Ogunsusi and Eysker, Reference Ogunsusi and Eysker1979). However, the parasite has adapted to survive the hostile external conditions by inhibited or arrested development of larvae for the duration of the unfavorable field conditions (Crofton, Reference Crofton1965; Tembely et al., Reference Tembely, Lahlou-kassi, Rege, Sovani, Diedhiou and Baker1997).

In exceptional cases, it has been established that in the north, when the dry season is longer than usual temperature acts as the major determinant of successful completion of development from eggs to L3 (Chiejina and Fakae, Reference Chiejina and Fakae1989). This situation occurs as a result of differences in the environmental temperature, such that during the dry season from December to March, more eggs completed their development following contamination of pastures in December and January than occurred due to contamination in February to March, because February to March was the hottest period of the dry season (Chiejina and Fakae, Reference Chiejina and Fakae1984). Therefore, exceptionally high temperatures can provide an upper constraint to H. contortus larval availability.

In the north, where the dry season is harshest and longest, the pastures and soil appear to be rendered free from L3 (Lee et al., Reference Lee, Armour and Ross1960). L3 found on the pasture at the start of the wet season around May/June therefore originate from fresh pasture contamination by carrier sheep at that time of the year (Lee et al., Reference Lee, Armour and Ross1960; Onyali et al., Reference Onyali, Onwuliri and Ajayi1990).

In the rain forest zone of Nigeria, the nature of outbreaks is similar except that the intensity and length of wet and dry seasons differ from those of the warmer north (Ogunsusi and Eysker, Reference Ogunsusi and Eysker1979) and dictate the period of occurrence, length and severity of hemonchosis (Onyali et al., Reference Onyali, Onwuliri and Ajayi1990; O'Connor et al., Reference O'Connor, Walkden-Brown and Kahn2006). This occurs because farmers across the country practice either extensive, semi-intensive or intensive farm management depending on the season. It is important to note as well that temperature is not a limiting factor in this region, but rainfall is, for the development and survival of all the free-living stages of H. contortus (Okon and Enyenihi, Reference Okon and Enyenihi1977). In this region as well as the coastal zone, pasture contamination by carrier sheep late in the dry season might be of more importance as a contributor to the early wave of pasture infestation and infectivity than fresh contamination by carrier sheep at the start of the rainy season (Chiejina and Emehelu, Reference Chiejina and Emehelu1984; Fakae and Chiejina, Reference Fakae and Chiejina1988).

In contrast, the coastal areas of Nigeria are located along the tropical rain forest belt, where the mean monthly rainfall is over 200 mm, so that rainfall and humidity are high at any time of the year. Unlike other parts of the country, if a dry season occurs in any particular year, it is generally short, about 3 months or less (Okon and Akinpelu, Reference Okon and Akinpelu1982). Hatching of eggs of H. contortus and development of the pre-infective stages to infective larvae is possible throughout the year in the coastal region of Nigeria (Fakae, Reference Fakae1990a). However, the constant and heavy rainfall could result in wash-down or erosion of the free-living stages present on the pasture and soil or create excessive moisture and low oxygen tension in water-logged areas, creating similar conditions in the feces as on flooded paddocks with possible adverse effects on development and survival of the free-living stages (Silverman and Campbell, Reference Silverman and Campbell1959). Also, Chiejina and Emehelu (Reference Chiejina and Emehelu1984) and O'Connor (Reference O'Connor, Walkden-Brown and Kahn2006) suggest possible movement of L3 from herbage into soil and vice versa depending on whether conditions are favorable or not for survival during the wet or dry season.

The coastal area is a region where hypobiosis is less important. The only available strategy for maintenance of H. contortus in the animal population is the ability of the L3 to survive in the dry season particularly when evapotranspiration is minimal (Fakae, Reference Fakae1990a, Reference Fakaeb) and to exist as adults in the host. Owing to the high fecundity of H. contortus, residual populations of adult female worms as seen during the dry season could be advantageous for the transmission of the parasite from one rainy season to the other and for the successful repopulation of the environment during the favorable season (Fabiyi, Reference Fabiyi1973). As emphasized by Crofton (Reference Crofton1965), it is evident that H. contortus displays considerable ecological and biological plasticity to overcome unfavorable intrinsic and extrinsic conditions.

Migration of L3

Migration of L3 from feces to the herbage is significant for the transmission of H. contortus, as this enables the presentation of L3 for ingestion by the grazing sheep (Silva et al., Reference Silva, Amarante, Kadri, Carrijio-Mauad and Amarante2008; van Dijk and Morgan, Reference van Dijk and Morgan2011). This behavior is significantly influenced by microclimatic conditions of temperature, relative humidity and light intensity at different heights along pasture stems (Crofton, Reference Crofton1948; Rees, Reference Rees1950; Silangwa and Todd, Reference Silangwa and Todd1964; Misra and Ruprah, Reference Misra and Ruprah1972; Callinan and Westcott, Reference Callinan and Westcott1986; Agyei, Reference Agyei1997; Chaudary et al., Reference Chaudary, Qayyum and Miller2008). Therefore, it is expected that larval migration will be optimal in the wet season (Okon and Enyenihi, Reference Okon and Enyenihi1977). In the dry season, the pattern of larval migration will depend on the timing and distribution of the early rains, which underlines the relationship between the onset of the rainy season and the extent of the early rains and the rise of pasture infectivity on dry season contaminated pastures (Fakae and Chiejina, Reference Fakae and Chiejina1988).

Chiejina and Fakae (Reference Chiejina and Fakae1989) reported that larval migration did not occur until a total of 144 mm of rain fell during the first 7 days, with 65 mm falling 24 h before commencement of the migration. Thus, it is pertinent to establish that if the amount of early rains is not substantial or is interrupted, particularly following the dry season and before the depletion of the fecal larval population, few or no larvae will migrate. This could result in a much later second wave of herbage infestation in response to further rainfall, thereby producing bimodal patterns of early rain-related pasture infestation and infectivity (Young et al., Reference Young, Anderson, Overend, Tweedie, Malafant and Preston1980).

Schillhorn Van Veen (Reference Schillhorn Van Veen1978) reported that outbreaks of hemonchosis occur in the late dry season (March to April), when the previous wet season had extended to the end of October or beyond in some years. This makes it possible for L3 to be available by November or beyond. Generally, it is these extra L3, which when picked up from pasture, raise the number of inhibited larvae to a level necessary for outbreaks to occur (Michel et al., 1976). In turn, outbreaks may occur only if most of the infective larvae ingested at this time become inhibited.

Climate change

Another major factor to be considered in the application of improved understanding of H. contortus to sustainable control of hemonchosis is the effect of climate change on the epidemiology and ecology of H. contortus as well as the host (Thornton et al., Reference Thornton, van de Steeg, Notenbaert and Herrero2009; Nardone et al., Reference Nardone, Ronchi, Lacetera, Ranieri and Bernabucci2010). The impact of climate change on the epidemiology of parasites and the distribution and maintenance of parasitic diseases among the host population will depend largely on the extent to which the ecosystem is affected (Patz et al., Reference Patz, Confalonieri, Amerasinghe, Chua, Daszak, Hyatt, Molyneux, Thomson, Yameogo, Lazaro, Vasconcelos, Rubio-Palis, Campbell-Lendrum, Jaenisch, Mahamat, Mutero, Waltner-Toews and Whiteman2005). This in turn will affect transmission dynamics, pasture growth and availability, health status and susceptibility of the populations at risk, as well as production and reproductive performance. These factors indicate the possible complexities that might be associated with the effect of climate change on the epidemiology of parasites. Morgan and Wall (Reference Morgan and Wall2009) established that the effects of climate change on the epidemiology of parasites of livestock are confounding, controversial and possibly far-ranging, particularly in population dynamics and distribution of livestock parasites, with tendencies for increase in disease incidence and production loss. Thornton et al. (Reference Thornton, van de Steeg, Notenbaert and Herrero2009) reiterated that interactions of climate and increasing climatic variability with other confounding drivers of change in livestock systems such as farm systems and management practice might lead to a very large spatial heterogeneity in the transmission of parasitic disease.

Generally, it is projected that climate will get warmer, and with warmer temperature the expectation is an increase in parasite abundance and disease incidence (Morgan and Wall, Reference Morgan and Wall2009; Wall and Ellse, Reference Wall and Ellse2011). There are few documented studies on specific effects of climate change on hemonchosis. A good report on the subject is that of van Dijk et al. (Reference van Dijk, David, Baird and Morgan2008), who observed a highly significant increase in the overall rate of hemonchosis cases over the past 5–10 years in the UK as a result of changes in the climate. Disease incidences were found to be concentrated in late summer with a drift in peak toward autumn. It was also observed that regions with most limiting thermal energy suited H. contortus. So far, there is no documented study on the effects of climate change on H. contortus in Nigeria or Africa. However, the work from Nigeria by Ayinde et al. (Reference Ayinde, Muchie and Olatunji2011) can be used as a reference point from which to draw logical consequences of the effects of climate change on hemonchosis. Ayinde et al. (Reference Ayinde, Muchie and Olatunji2011) noted that temperature displayed a relatively constant increased variation which has had negative effect on vegetation growth. On the other hand, the observed increase in rainfall amount and frequency had a positive effect. It was further explained that there is increasing tendency of prolongation of the dry season. Bearing in mind that Nigeria has only wet and dry seasons with rainfall only during the wet season, it can be argued that the most likely effects of climate change on H. contortus will stem from either lack of pasture or the size and/or density of standing biomass available for grazing.

The negative effects of the thermal changes on pasture growth, if not counteracted by rainfall, will cause scarcity and/or lack of pasture or make the microclimate at the pasture level unsuitable for the survival and development of all the free-living stages. This will cause reduced development and/or increased mortality rate of the free-living stages. The result of these changes will be reduced risk of infection with H. contortus and a prolonged period of hypobiosis of the successfully established L3 in the host. This situation is bound to be experienced in the northern regions where there is a prolonged dry season. If the duration of dry season in the north is further prolonged with a reduced rainy period as a result of climate change effects, then the period and probability of pasture infectivity and transmission to susceptible host will be further reduced, which is detrimental to the survival and maintenance of H. contortus among the host population and its continuity or re-infection of the host.

Regarding the western, eastern and southern regions of the country, the risk of pasture infectivity and host infection with H. contortus will increase during the rainy period as long as there is increased rainfall amount and frequency to counter the adverse effect of thermal changes on pasture growth and microclimate. Unlike the north, these regions do not have prolonged dry seasons. Thus, presumably whenever temperatures are high during the wet season, this might drive an increase in the proportion of ingested larvae that develop to adults and cause disease in the following weeks, rather than hypobiosis (Waller et al., Reference Waller, Rudby-Martin, Ljungstrom and Rydzik2004a) as observed in the north because of the prolonged dry seasons. The incidence of hemonchosis is likely to increase appreciably if the lambing season and concurrent multiple disease conditions of the host coincide with the wet season in these regions. Depending on whether the dry season is prolonged or shortened, the two possible outcomes will be either an increase or decrease in the onset and duration of hypobiosis of the early fourth-stage larvae.

Both Morgan and Wall (Reference Morgan and Wall2009) and Wall and Ellse (Reference Wall and Ellse2011) explained that the interaction between (or combination of) biological mechanisms and modest targeted changes in farm management and husbandry practices, might be able to ameliorate the increased rates of parasite development, thereby preventing any dramatic increase in the overall disease incidence. Requisite to a successful control of any increase in incidence of parasitic disease resulting from climate changes, is a well-established knowledge of the parasite biology and farm practices within the range of expected changes in climate (Morgan and Wall, Reference Morgan and Wall2009; Wall and Ellse, Reference Wall and Ellse2011). Regarding the above context (Ayinde et al., Reference Ayinde, Muchie and Olatunji2011) of possible effects of climate change on the epidemiology of H. contortus in Nigeria, in order to achieve efficient and sustainable control of hemonchosis, it will be crucial to include the optimization of pasture and forage productivity and to improve the capabilities of livestock to cope with environmental stress by management and selection (Nardone et al., Reference Nardone, Ronchi, Lacetera, Ranieri and Bernabucci2010). Research into the effect of climate change on H. contortus is timely and needed for effective design of a sustainable control strategy. Thus, to guide the evolution of efficient livestock production systems it is recommended that environmental and farm-management innovations that can mitigate against climatic fluctuations be encouraged and integrated into a sustainable control strategy (Thornton et al., Reference Thornton, van de Steeg, Notenbaert and Herrero2009; Nardone et al., Reference Nardone, Ronchi, Lacetera, Ranieri and Bernabucci2010; Ayinde et al., Reference Ayinde, Muchie and Olatunji2011).

Biological control

Biological control strategy is based on the principle that artificial increase in the density of naturally-occurring predators or antagonists can lower parasite populations and reduce losses to animal production through nematode infection (Gronvold et al., Reference Gronvold, Henriksen, Larsen, Nansen and Wolstrup1996). Of all known antagonistic organisms, only nematophagous fungi, earthworms and dung beetles so far have realistic potential as biological control agents (Gronvold et al., Reference Gronvold, Henriksen, Larsen, Nansen and Wolstrup1996).

The use of the nematode destroying micro-fungus Duddingtonia flagrans in biological control of H. contortus is a relatively new tool that has been researched with appreciable success around the world, covering many different climates and management systems (Waller et al., Reference Waller, Faedo and Ellis2001; Peña et al., Reference Peña, Miller, Fontenot, Gillespie and Larsen2002; Chandrawathani et al., Reference Chandrawathani, Jamnah, Waller, Larsen, Gillespie and Zahari2003). The mechanism of action of the fungus lies in its ability to form sticky traps that catch developing larval stages of parasitic nematodes in the fecal environment and feed on them. The fungus is fed to grazing sheep for a period of time in the resting-spore stages (chlamydospores). The administration of D. flagrans produces reduced pasture infectivity and reduced worm burden, particularly in young lambs (Larsen et al., Reference Larsen, Faedo, Waller and Hennessy1998, Reference Larsen, Wolstrup, Henriksen, Dackman, Grønvold and Nansen1991).

Additional benefits have been observed when the fungus is employed in combination with a fast rotational-grazing system (Chandrawathani et al., Reference Chandrawathani, Jamnah, Waller, Larsen and Gillespie2004) and refined use of existing drugs (Waller et al., Reference Waller, Rudby-Martin, Ljungstrom and Rydzik2004a, Reference Waller, Schwan, Ljungström, Rydzik and Yeatesb). This method holds promise as a control measure toward a sustainable integrated management against H. contortus; however, more refined studies and development are needed in production, dosing and adoption in different, specific geographic regions (Larsen, Reference Larsen2006), including Nigeria.

Grazing and pasture management

The main thrust of any grazing system that uses pasture management to complement nematode control is to provide safe and/or clean pastures for grazing as well as sufficiency in forage availability for grazing animals (Barger, Reference Barger1999). Grazing systems differ in the frequency of stock movement: from no movement at all to frequent changes between pastures. Detailed knowledge of the epidemiology of the free-living stages of H. contortus outside the host is central to an effective and sustainable grazing and pasture management plan. This is the point where the prevailing local climatic conditions become critical to control. In effect, development of the free-living stages varies with different climates and makes it impossible to have a general reliable template for their availability and survival for all climates (Barger, Reference Barger1999). Therefore for effective use of grazing and pasture management as a control strategy against H. contortus on pasture, the following factors have to be considered (Barger, Reference Barger1999): L3 intake will be proportional to the concentration of L3 on herbage; long-term observation of larval availability on pasture will reveal important peaks and troughs and their predictability, information which is valuable for optimal timing of control protocol; detecting the origin of a peak is necessary for further and future evidence-based prevention strategies; and larval survival is different for each climate. It is important to know the survival times for reliable estimation of decline in pasture infectivity.

Grazing system and pasture management have been effective measures in reducing new and re-infection, and can be classified into three categories: preventive strategies – turning out parasite-free animals on clean pastures; evasive strategies – evading worm challenge by moving animals from contaminated pasture; and diluting strategies – relieving worm challenge by diluting pasture infectivity, especially by manipulating effective stocking density of heavily infected or highly susceptible hosts (Barger, Reference Barger1997; Thamsborg et al., Reference Thamsborg, Roepstorff and Larsen1999; Younie et al., Reference Younie, Thamsborg, Ambrosini, Roderick and Vaarst2004).

Alternate grazing involving interchange between cattle and sheep is also a potentially useful grazing system that exploits host specificity of H. contortus to sheep, whereby the parasite cannot establish to any great degree in cattle. This should lead to reduced need for treatment. The period of alternation varies with epidemiology and prevailing climate in a given location and time. Decreased survival of L3 at high temperatures means that in warmer regions, pastures left un-grazed or grazed by unsuitable hosts become safe more quickly. This ought to enhance the usefulness of these strategies in parts of Nigeria compared with temperate regions, in which long survival of L3 makes rotational grazing uneconomical in most situations.

Depending on the climatic conditions and length of the grazing season, the moving of weaned lambs to a clean pasture before the expected mid-summer rise in herbage infection can prevent parasitic gastroenteritis and achieve good production whether the move is accompanied by anthelmintic treatment or not (Githigia et al., Reference Githigia, Thamsborg and Larsen2001).

Monitoring the parasitological status of the animals by fecal sampling sentinel sub-flocks for fecal egg counts (FEC), or the use of the FAMACHA^© procedure to assess the impact of H. contortus through anemia (van Wyk and Bath, Reference van Wyk and Bath2002) can provide crucial support to control strategies that rely on grazing management. Also, improvement of the overall nutrition of the flock is an important adjunct to control. As a long-term plan, genetic improvement of flocks toward increased natural resistance or resilience to H. contortus is worthwhile (Waller et al., Reference Waller, Dash, Barger, Le Jambre and Plant1995; Waller, Reference Waller1997).

Selective breeding

Selective breeding is a potential management tactic to counter the rapid spread of anthelmintic resistance of H. contortus (van Wyk and Bath, Reference van Wyk and Bath2002). This involves the selection of animals that show either an inherent resistance or resilience to nematode challenges (Bishop et al., Reference Bishop, Bairden, McKellar and Stear1996). Artificial selection may be used to produce resistance against H. contortus in various breeds of sheep (Gray, Reference Gray1997; Rahman and Seip, Reference Rahmann and Seip2006). Bishop and Stear (Reference Bishop and Stear2003) confirmed that among populations of animals challenged by internal parasites, there are always animals that perform better than others. These are said to be resistant (i.e. have enhanced immunity with reduced parasite establishment and lower egg counts), resilient (i.e. maintained health and production in the face of challenge) or tolerant (i.e. have lowered immunity but with attenuated disease and production loss).

Resistance has earned wider adoption than resilience because resistance is more heritable than resilience and less difficult to measure. Furthermore, resistant animals have the added advantage of producing fewer eggs, leading to epidemiological benefits for the whole flock. However, resilience can be a more desirable trait in some production systems, notwithstanding higher pasture contamination (Aspin, Reference Aspin1999). Further studies are needed to define the best phenotypic and genotypic markers for resistance and resilience, and to establish the leverage for these strategies in common breeds in Nigeria.

Boosting host resilience and resistance via adequate nutrition

Nutritional status enhances the ability of animals to cope with adverse effects of worm challenge (Wells, Reference Wells1999), and enhanced nutrition could therefore be a useful non-chemotherapeutic option for control (Rahmann and Seip, Reference Rahmann and Seip2006). Protein intake is essential to growth as well as to immunity against nematode infection (Valderrábano et al., Reference Valderrábano, Delfa and Uriarte2002; Waller and Thamsborg, Reference Waller and Thamsborg2004). Rahmann and Seip (Reference Rahmann and Seip2006) recommended two measures: first, farmers should ensure sufficient food supply for their stocks at all times to avoid nutritional stress, and secondly, categories of animals that are particularly susceptible can be helped by placing them on protein-rich diets to enhance their immunity. In practice, this is likely to increase feed costs, although within diversified systems creative use of plant by-products can yield cheap and accessible protein sources.

The grazing of forages that contain anti-parasitic compounds or nutraceuticals (plant secondary metabolites) by animals could benefit animal health without necessarily having nutritional value (Waller and Thamsborg, Reference Waller and Thamsborg2004). Studies have shown the benefits of feeding bioactive forages to animals in terms of reduced parasite burdens (Niezen et al., Reference Niezen, Robertson, Waghorn and Charleston1998; Thamsborg, Reference Thamsborg, Hovi and Vaarst2001). However, use of such forages can be limited by their high concentration of condensed tannins, which reduces feed digestibility and consequently lowers productivity.

Mathematical modeling

Lately, mathematical modeling has received increasingly wide application in ecological and epidemiological studies of infectious diseases. This is the result of increased understanding of what models can offer in terms of prediction and understanding of a disease process (Smith and Grenfell, Reference Smith and Grenfell1994; Cornell, Reference Cornell2005; Keeling and Rohani, Reference Keeling and Rohani2008; Vynnycky and White, Reference Vynnycky and White2010).

A typical model is a conceptual tool that elucidates and gives simplified representation of how a system and/or multiple systems will behave (Keeling and Rohani, Reference Keeling and Rohani2008; Vynnycky and White, Reference Vynnycky and White2010). In epidemiology and ecology, models permit the prediction of disease dynamics at the level of the entire population and contribute to understanding of epidemiological factors at the individual level (Gettinby and Paton, Reference Gettinby and Paton1981; Paton et al., Reference Paton, Thomas and Waller1984; Keeling and Rohani, Reference Keeling and Rohani2008; Vynnycky and White, Reference Vynnycky and White2010). Modeling also enables the design and experimental evaluation of the impact of specific management practices or control measures based on the predicted parasite dynamics (May, Reference May1977; Smith, Reference Smith1988; Dobson et al., Reference Dobson, Donald, Barnes and Waller1990; Roberts and Heesterbeek, Reference Roberts and Heesterbeek1993; Smith and Grenfell, Reference Smith and Grenfell1994).

Mathematical models have been used to consider and describe the epidemiology of parasitic nematodes (Paton et al., Reference Paton, Thomas and Waller1984; Anderson and May, Reference Anderson and May1991) and cestodes of farm animals as well as diseases of humans (Anderson and May, Reference Anderson and May1991) and wildlife (Morgan et al., Reference Morgan, Milner-Gulland, Torgerson and Medley2004, Reference Morgan, Medley, Torgerson, Shaikenov and Milner-Gulland2006). Mathematical modeling of parasite transmission processes can provide useful information about the biology and dynamics of parasite populations as well the host–parasite relationship (Roberts and Heesterbeek, Reference Roberts and Heesterbeek1995). Further work needs to be done on how modeling can be adapted as a tool for predicting risk in practice (van Wyk and Reynecke, Reference Van Wyk and Reynecke2011), and to guide targeted selective treatment (TST) and targeted treatment (TT) as part of holistic and sustainable control against H. contortus.

Herd management

The type of herd management practiced on a farm depends on the strategies adopted, including organic, integrated, or conventional methods of managing a farm (Rahmann and Seip, Reference Rahmann and Seip2006). These in turn affect variables important to parasite epidemiology, including stocking rate and opportunities for monitoring and intervention.

Stocking rate

An important factor to consider for successful herd health is the stocking rate in relation to grazing systems and the prevailing climate. Research results have demonstrated the possible correlations between migration heights of L3 and stocking rate, even though the results are dissonant and controversial (Rahmann and Seip, Reference Rahmann and Seip2006).

It has been documented that the majority of L3 move only an inch or two from the ground onto herbage under most normal climatic conditions (Wells, Reference Wells1999; Schoenian, Reference Schoenian2005), meaning that grazing below these levels will result in increased infection (Rahmann and Seip, Reference Rahmann and Seip2006). Additionally, it can be argued that reduced vegetation creates conditions unfavorable for larval development (O'Connor et al., Reference O'Connor, Walkden-Brown and Kahn2006; van Dijk et al., Reference van Dijk, Sargison, Kenyon and Skuce2010) and that feces deposited on short grass result in significantly reduced L3 on the surrounding pasture (Secher et al., Reference Secher, Gronvold and Thamsborg1992). Thamsborg et al. (Reference Thamsborg, Jörgensen, Waller and Nansen1996) revealed that increased stocking rate has a long-term effect rather than short-term consequences because insignificant levels of infection were recorded in the first year of the experiment as opposed to the high degree of infection in the second year after the stocking rate was increased. Thus, it is logical to conclude that decreased stocking rate may contribute to an integrated control plan.

Monitoring and intervention

Organic farming relies on the principle of effective and timely monitoring and intervention since the prophylactic use of traditional conventional chemotherapy is prohibited (Rahmann and Seip, Reference Rahmann and Seip2006). Regular intensive monitoring should be fundamental in the design of integrated and sustainable farm management against H. contortus for protection of animals from preventable suffering, thereby maintaining herd health (Thamsborg et al., Reference Thamsborg, Larsen and Busch2004). These principles are applicable even on non-organic farms as a means of supporting reduced use of chemical control while safeguarding animal health and productivity.

Rahmann and Seip (Reference Rahmann and Seip2006) explained that scoring general body condition, FEC and scoring deviations in physical condition are the three commonly applied methods to determine worm infestation in animals. An important tool in this context is the FAMACHA^© chart to determine the extent of hemonchosis in sheep (van Wyk and Bath, Reference van Wyk and Bath2002). The chart gives farmers the ability to evaluate the clinical status of the animals by examining the color of the eye mucosa using scores that range from 1 to 5 and the decision is to treat animals with scores above 3 (TST strategy, although the threshold for treatment can be adapted to local conditions and production aims) (Bath et al., Reference Bath, Hansen, Krecek, van Wyk and Vatta2001; van Wyk and Bath, Reference van Wyk and Bath2002). FAMACHA^© is the most relevant indicator for treatment in regions where H. contortus is the nematode with greatest impact on animal health, while other indicators can provide supportive information for this and other species (Kenyon et al., Reference Kenyon, Greer, Coles, Cringoli, Papadopoulos and Cabaret2009). These indicators can be used to appropriately target whole-flock or whole-herd treatments or to select individuals that are in greatest need of treatment, thus enabling adequate parasite control without excessive treatment (Kenyon et al., Reference Kenyon, Greer, Coles, Cringoli, Papadopoulos and Cabaret2009).

Southern, eastern, western Nigeria: long rainy season and short dry season

In the south, east and west, the rainy season is long with a very short dry season. The practical implication of this scenario in the formulation of a comprehensive control program is that pastures grazed by infected animals during the dry season may not be safe for susceptible animals to graze at the start of the succeeding rainy season (Chiejina and Fakae, Reference Chiejina and Fakae1984). Also, as reported by Fakae (Reference Fakae1990a), hypobiosis is insignificant in eastern Nigeria and, apart from survival of L3 on the pasture, the only real means of surviving the dry season is the persistence of adults in the host. In this situation, effective grazing system and pasture management will be vital to control.

One should bear in mind the different host categories in terms of age and immunity status that constitute the flock as well as the three important goals: preventive strategies, evasive strategies and diluting strategies (Barger, Reference Barger1997; Thamsborg et al., Reference Thamsborg, Roepstorff and Larsen1999; Younie et al., Reference Younie, Thamsborg, Ambrosini, Roderick and Vaarst2004).

Importantly, flocks should be intensively monitored using FAMACHA^© during high-risk periods to ensure that whenever chemotherapy (TST or TT) is used, it will be based on sound clinical judgment to reduce selection of drug resistance in H. contortus to the minimum. Effective and adequate usage of FAMACHA^© also prevents unforeseen outbreaks of hemonchosis on the farm because it serves as a warning and stimulus for pre-emptive farm management measures against challenge from H. contortus. In addition, high-quality nutrition should be provided particularly during the known or predicted season of high levels of herbage infectivity.

Northern Nigeria: short wet season and long dry season

To effectively control small ruminant hemonchosis on a flock or herd basis in the north where the dry season is very long and the rainy season is short, it is equally important to design and adhere strictly to the principle of monitoring and intervention (e.g. using FAMACHA^©). Individual or group cases of hemonchosis can then be dealt with as they occur during or outside the hemonchosis season. To enhance this regimen, good management practices such as rotational grazing where possible, improved hygiene and supplementary feeding of animals during periods of little or no availability of safe pasture will complement the control of hemonchosis (Nwosu et al., Reference Nwosu, Ogunrinade and Fagbemi1996).

The long dry season provides additional opportunities for control, such that rotation using periods of pasture rest or alternative grazing can be of shorter duration when L3 mortality is high in dry and hot conditions. These conditions also make integrated control and the application of TST more important than ever since whole-group treatment when animals are on pasture hostile to L3 survival will result in little or no refugia for drug-susceptible genotypes.