The study of factors affecting the distribution and maintenance of disease agents in the environment is called epidemiology.  Understanding the epidemiology of parasites provides the foundation upon which we design effective prevention and control programs.  Without this information, we cannot use all the tools available to us to control both the adult worms in the host and the larvae on pasture.  As a result, we tend to become dependent strictly on deworming, which becomes a matter of convenience and usually has little impact on the parasite population and little economic value.

We are fortunate when it comes to South American camelids because, with a few exceptions, their gastrointestinal parasites are substantially the same as those that live in other North American livestock.  Consequently, the numerous studies on the epidemiology of cattle and sheep parasites done in the >70s and >80s can give us insights into design of appropriate control  programs for these parasites in llamas/alpacas.

The life cycle patterns of the gastrointestinal nematodes we deal with are generally similar.  They are short and direct (do not require an intermediate host).  Eggs passed in the feces usually hatch in 24 hours under optimal environmental conditions.  The first-stage larva molts to a second-stage larva which molts to the third-stage larva (infective stage).  Once the infective larva is ingested by the animal, the time for development to sexually mature adult nematodes is 2 to 4 weeks for most genera.

In a broad sense, the factors dictating the level and extent of parasitism are climate, management conditions of pasture and animals, and the population dynamics of the parasites within the host and in the external environment.  For the purpose of describing the effect of seasonal climatic differences and management conditions, parasite populations are divided into three components.  The largest component, numerically, is the population of free-living stages on the pasture.  The  next largest component is the number of infective larvae on pasture that are available to the host.  The smallest component is the number of parasites actually present in the host.  Pasture contamination with parasite eggs is a continuous process throughout the year, but hatching of eggs, development of larvae through the free-living to the infective stage, distribution onto herbage and survival on pasture differs during the course of a year.  The prevailing weather conditions are the primary factors influencing these differences.  Changing weather patterns results in fluctuations and discontinuities in the numbers of infective larvae available to the grazing animal in different seasons.  The effect of extreme weather conditions also has an effect on the animals themselves as well as forage growth and quality.  This, in turn, will also influence the general health of the animals and their susceptibility to parasitism..

Temperature is the primary factor regulating the hatching of eggs and development of larvae.  All stages can be killed by extremely low temperatures as well as exposure to direct sunlignt.  Moisture also influences the hatching and development process.  As feces dry, eggs and larvae desiccate and die.

Infective larvae must be available to the grazing animal to be of any consequence in the transmission of the parasite.  The ability of larvae to migrate away from the feces is limited and random.  With rainfall or other sources of moisture, such as sprinkler irrigation, larvae are washed or splattered over surrounding soil, humus, and grass.  Trampling, spreading by farm equipment or any other mechanism by which the feces is disturbed and broken up will help to distribute larvae away from feces.  Once distributed onto surrounding grass, some degree of active vertical migration does occur.  Stocking rates, grazing patterns of the animals and the degree of vertical migration will then influence how many larvae are acquired with a particular mouthful of grass.

Infective larvae live on stored food reserves and, therefore, have a finite life span.  As larval activity increases, food reserves are used up.  Consequently, weather conditions providing moistures and temperatures stimulating low to moderate activity are most conducive to long-term larval survival.  In certain areas, long-term larval survival may mean several months.

In addition to weather, management of animals and pasture also influence larval availability.  Pasture management factors (stocking rates, type of forage, etc.) and animal management procedures (anthelmintic treatment, reproductive schedule, general herd health programs, etc.) are closely related to increases and decreases in all components of the parasite population.  Farm management factors can, in some instances, modulate the negative effects weather can have and enhance parasite survival/transmission.  This is why parasite control programs must be tailored to each individual farm

Regional Patterns of Parasite Transmission

General statements can be made regarding nematode transmission patterns in different geographic regions of the United States and provides a starting point in designing our control programs.

Southeastern States.  Weather patterns over much of the region are largely influenced by the Gulf of Mexico resulting in mild, wet winters and hot, sometimes wet, summers.  Grazing seasons are long and larval availability on pasture is possible the year-round.  Larval availability increases from fall through winter to peak levels in spring.  Acquisition of infections can occur at any time larvae are available, but, spring would be the most dangerous time in terms of the possibility of disease.

Southcentral and Southern Plains States.  Throughout this region where sufficient precipitation allows for prolonged survival of larvae, transmission can occur during 2 different times of the year.  During warm weather, infective larvae develop quickly, which can result in massive infections during spring and early summer.  During winter, larval development is slower, but infections progressively accumulate through winter to early spring.

Central States.  Overwintering larvae are available for ingestion in the spring.  Resulting infections acquired result in additional pasture contamination during spring and early summer.  Summer climatic conditions result in a decrease in transmission during that time which lasts through fall into winter.

Northcentral and Northeastern States.  Climatically, this region is characterized by severe winters and relatively mild summers.  Moisture levels are highest in the central and eastern sections with warmer summer weather and dry conditions in the western section.  Although larvae can overwinter, in general, larvae are not very abundant in the spring.  However, infections acquired during spring and early summer results in a sharp increase in pasture infectivity in summer and fall.  This occurs because conditions become more favorable for the rapid development of infective larvae.

Western States.  Transmission patterns differ between areas with severe winters and those with more moderate conditions.  Latitudinal and elevational extremes within this regions translate into wide variations in temperature and moisture during grazing seasons.  This presents difficulties in predicating transmission patterns for the overall area.  However, in general, those areas with cold winters and hot, dry summers will have the highest pasture contamination during spring.  Those areas where winters are relatively mild but summers are still hot and dry can have 2 peaks of larval availability.  The first peak is in the spring and the second peak occurs  in the fall.  Finally, those areas with severe winters are characterized by poor larval survival.  Some larvae may survive the winter to infect animals in late spring and early summer; however, transmission usually occurs in midsummer and early fall.

Control Strategies

In outbreaks of parasitic gastroenteritis, prompt administration of appropriate anthelmintic therapy (salvage therapy) must be done to minimize weight loss and the likelihood of death.  This treatment occurs only once signs of infection have become apparent and, as a result, does very little to avoid getting into the problem in the first place.  Subclinical (inapparent) effects, such as reduced weight gain and decreased milk production, are also not avoided.  Consequently, to avoid these problems, nematode control strategies in recent years have focused more on preventing infection rather than rescuing the animal from death.  The most desirable programs use a combination of treatment and management to achieve control.  Such programs are designed to:  (1) prevent the accumulation of disease-producing numbers of larvae on pasture by reducing contamination at certain critical points of time and (2) reduce the acquisition of infection by anticipating periods during which large numbers of larvae are likely to occur.  It must be understood, however, that the parasites cannot be eradicated but can be limited.

1.  Supressive anthelmintic treatments.  This is a preventive control method using multiple dosing of anthelmintics alone.  This is differentiated from salvage therapy in that a minimum of 3 consecutive treatments are used.  The anthelmintic is given at regular intervals which, to be completely effective, is done before the worms acquired since the last deworming become reproducing adults.  This interval is about 3 weeks.   Suppresive anthelmintic control programs may be needed when animals have limited pastures and, therefore, pasture rest, tillage or alternate grazing by other species is impossible.   While supressive deworming is probably the most effective method of keeping parasite numbers lowered for a period of time, these programs are expensive and do not utilize the host's own immune defenses.  This method can also lead to the development of anthelmintic resistance more quickly than any other type of control program.

2.  Safe pastures and the integration of anthelmintic treatment with management.  The basis of integrated control is reducing infection rate by combining few anthelmintic treatments with the natural occurrence or deliberate provision of safe pasture.  This does not imply that risk of infection is absent; rather, safe pasture means risk of infection is low enough to be of only minor consequence.  Safe pastures include newly sown pastures, hay aftermath, crop stubbles, and those specially prepared by pasture spelling or by alternate grazing with other livestock.

Production of safe pasture depends on the prevention of significant contamination during critical points in time.  This may not always be simple and may be in conflict with other facets of the farm operation.  However, the need to reduce pasture contamination and reduce dependence on anthelmintics will have to be weighed against the problems raised by management changes.

Safe pastures can be provided directly by pasture spelling (deferred grazing).  In this scheme, we take advantage of our knowledge of the climatic effects on the free-living larvae and rest the pastures during times when weather conditions are not conducive for their development and survival.  In northern regions, this usually occurs in winter when the cold can dramatically decrease the numbers of larvae on pasture.  In southern regions, this usually occurs in summer when the hot, dry weather tends to decrease the development and survival of larvae on pasture.  In deferred grazing systems in more moderate climatic areas, pastures must rest for a minimum of 6 months in the cool season or 3 months in the warm season in order for weather conditions to have an impact on larval survival. Other methods of providing safe pastures include hay harvesting, tilling with reseeding, and burning with reseeding.

Pasture rotation schemes have been devised as another method of producing safe pastures.  These schemes depend on the alternate grazing of species which do not acquire each others parasites.  Because cattle, sheep, and goats carry the same parasites as llamas and alpacas, alternating between these hosts is not recommended.

Regardless of the mechanism used, animals should probably be treated with an anthelmintic within a few days prior to entering the pasture to prevent introduction of parasites onto the pasture.  If animals remain on the pasture for an extended period of time, they likely will require a second treatment at some later interval to ensure that contamination remains low.

Conclusion

Although much of the epidemiology of the gastrointestinal parasites is already known, a few key questions still remain to be solved in order to design the best control programs possible.  For example, transmission patterns described for each region should be verified with llamas/alpacas.  Part of this verification would include determination of larval inhibition.  Some species of parasites can stop development shortly after infecting the host.  This allows for survival of the parasite during those times of the year when the external environment is not conducive to larval survival.  We know at least one group of nematodes can arrest development in llamas; however, we do not know if it occurs in the more common nematodes that llamas have.  Timing and choice of treatment is affected by the presence of arrested larvae .  Many anthelmintics are ineffective against these larvae or are only effective at higher doses.  Clearing the animal of these larvae before they mature provides a major step in reducing pasture contamination, thus, reducing parasite transmission.

Further clarification of the regional differences in the nematode parasites populations of llamas/alpacas is also necessary.  It appears the parasites of llamas in the Pacific Northwest are dominated by Camelostrongylus mentulatus, a nematode that lives in the third compartment while in areas of the southeast, a different third compartment nematode, Haemonchus contortus, is most troublesome.  These parasites can cause different disease problems.  Then, there are those that seem to more generallly distributed, like whipworms and Nematodirus.  All these nematodes have different susceptibilities to the drugs we use, so knowledge of what parasites are on your farm is essential in picking the right anthelmintic.

Finally, one factor we are getting a better understanding of is whether llamas/alpacas exhibit a periparturient rise (PPR) in the shedding of nematode eggs, a phenomenom common in sheep but not in cattle.  The PPR occurs in lambing ewes, resulting in a massive increase in the numbers of nematode eggs present in the feces.  It is thought this increase in the number of nematode eggs occurs as a result of the hormonal changes associated with parturition and lactation.  These changes result in a relaxation of immunity which allows those nematodes which have arrested development, to proceed to sexual maturity.  In addition, newly acquired nematodes are also more likely to mature.  The corresponding increase in egg production results in massive pasture contamination which, in turn, results in massive numbers of larvae available to lambs as they begin grazing.  Acquisition of large nematode burdens in a short period of time usually results in severe disease.  Effective control programs for sheep must take into account this phenomenon.  We recently finished a study designed to determine whether this event occurs in llamas/alpacas.  The good news is that, in the 3 herds we studied, we found no evidence of a rise in nematode egg shedding near parturition.  The bad news is, the farms studied did not have Haemonchus contortus.  This nematode is a notorious player in the PPR, so we cannot entirely rule-out the possibility that the PPR will occur on those farms where this parasite lives.  Again, this emphasizes the necessity of knowing what parasites are on your farm.

In summary, we can use the general transmission patterns defined for the various regions of the country as a starting point in designing strategic control programs.  However, the programs should be refined based on the specific management practices of the farm and the knowledge of which parasites are present.  Regularly timed fecal examinations should be incorporated into the control program to monitor anthelmintic effectiveness and development of resistance.

The information presented herein is based on the author's experiences as well as the following articles:

Craig, T.M.  1986.   Epidemiology and control of nematodes and cestodes in small ruminants: Southern United States.  Vet Clinics North America Food Animal Practice.  2:367-372.

Herd, R.P.  1986.  Epidemiology and control of nematodes and cestodes in small ruminants: Northern United States.  Vet Clinics North America Food Animal Practice.  2:355-362

Rickard, L.G..  1993.  Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematode: Trichostrongyloidea).  Vet Parasitol.  45:331-335.

Rickard, L.G.  1994.  Parasites.  Vet Clinics North America Food animal Practice.  10:239-247.

Rickard, L.G. and J.K. Bishop.  1991.  Helminths parasites of llamas (Lama glama) in the Pacific Northwest.  J Helminthol Soc Wash.  58:110-115.

Wescott, R.B.   1986.  Epidemiology and control of nematodes and cestodes in small ruminants: Western United States.  Vet ClinicsNorth America Food Animal Practice.  2:363-366.