altMost horse owners continue to use worm control programs for horses that were developed decades ago and are based on knowledge that is 30-40 years old.  In this presentation, Dr. Kaplan introduces a new approach to parasite control in horses that is based on the most up-to-date information and the principles of evidence-based medicine.   

Author - Dr. Ray Kaplan

Dr. Kaplan is an Associate Professor at the College of Veterinary Medicine at the University of Georgia, where he teaches and performs research in veterinary and human medical parasitology and is director of the Athens Parasitology Diagnostic Laboratory. Dr. Kaplan received his DVM from Virginia-Maryland Regional College of Veterinary Medicine. He worked as a clinical veterinarian in a mixed-species private practice in Pennsylvania before attending the University of Florida where he earned a PhD in Veterinary Parasitology.

 

Summary
Most veterinarians continue to recommend anthelmintic (dewormer) treatment programs for horses that are based on knowledge and concepts that are more than 40 years old. However, recent studies demonstrate that resistance and multiple-drug resistance in equine parasites is extremely common, but few horse owners or veterinarians take this into account when making treatment decisions.  Parasites are highly over-dispersed in hosts, such that a small percentage of hosts (20%) harbor most (80%) of the parasites. The common practices of recommending the same treatment program for all horses despite great differences in parasite burdens, of recommending frequent preventive treatment of all horses without any indication of parasitic disease or knowing what species of parasites are present, of recommending the use of drugs without knowledge of their efficacy, of failing to perform fecal egg count surveillance and of failing to determine if treatments are effective, are all incompatible with achieving optimal and sustainable parasite control.  Consequently, it is necessary that attitudes and approaches for parasite control in horses undergo a complete overhaul, and that both horse owners and veterinarians become educated in these important issues.

Introduction
The introduction of benzimidazole (BZ) anthelmintics (dewormers) led to a revolution in equine in parasite control (Drudge and Lyons 1966).  With these new tools came new recommendations; horse owners were advised to deworm all horses every 8 weeks.  These recommendations were widely adopted, resulting in a dramatic reduction in morbidity and mortality from parasitic disease.  For the first time ever it was possible to truly control equine parasites, leading to significant improvements in equine health and performance.  By the 1970’s and 80’new dewormers became available and rotation between drugs became a common practice.  Unfortunately, parasites have risen to the chemical challenge.   Anthelmintic resistant small strongyles (small strongyles) now are highly prevalent and even where drugs still are effective, the egg reappearance period (ERP) following treatment has become significantly shorter.  Today most horse owners continue to follow recommendations that are based on knowledge that is more than 40 years old and frequently use dewormers that have become totally ineffective due to the presence of drug-resistant parasites.  Furthermore, the strict adherence to outdated approaches has produced a mentality of fear – horse owners deworm frequently because they think they have to, and because they fear what might happen if they do not.  But the truth is that most adult horses will remain quite healthy with much fewer treatments, and this is the reason why parasite drug resistance usually goes unnoticed for long periods.  Therefore, it is important for horse owners and veterinarians to become educated in the latest knowledge on parasite biology so that parasite control practices can be modernized to meet the new issues and problems we now face.

A shift in emphasis: the downfall of Strongylus vulgaris (large strongyle bloodworm) and the rise of small strongyles (small strongyles)
Prior to the introduction and strategic use of benzimidazole (BZ) anthelmintics, it is estimated that 90% of colics were due to migrating arterial stages of the large strongyle parasite Strongylus vulgaris (Drudge and Lyons 1977).  However, the excellent efficacy of modern dewormers has markedly decreased the prevalence of this parasite, and the once common affliction of colic due to this parasite has become a rare occurrence in managed horses (Lyons, Tolliver et al. 1999).  By the early 1980’s it was recognized that small strongyles frequently accounted for virtually 100% of the strongyle worm egg output of grazing horses.  This major change in species prevalence has caused an important shift in the relative importance of these nematodes; small strongyles are now recognized as the principal parasitic pathogen of horses (Love, Murphy et al. 1999).  Contributing to the pathogenic potential of these parasites is the problem of drug resistance which is now reaching alarming levels.  Disease symptoms in horses infected with small strongyles range from no measureable effect, to a mild subclinical alteration in gastrointestinal function, to a life-threatening disease known as larval cyathostomosis, characterized by severe weight loss, chronic diarrhea, and edema.  It is important to understand that it is the larval worms that come out of the intestinal wall (mucosa) that are the most damaging stage of the infection.  The adult worms, which with few exceptions are the stages killed by dewormer treatments cause very little damage to the horse.  So in order to optimize horse health, it is necessary to prevent new infections.  Consequently, we aim to kill adult worms with our treatments, but it is actually the prevention of egg shedding that does most for horse health and overall worm control because by doing this we reduce numbers of infective larvae on pasture and subsequent infections in the grazing horse.

Anthelmintic Resistance: a growing threat to parasite control and equine health
Currently used parasite control programs are almost completely dependent upon the intensive use of dewormers.   Presently there are three major chemical classes of dewormers used to control nematode parasites in horses: benzimidazoles (fenbendazole – Safeguard®, Panacur®, oxfendazole -- Benzelmin®, oxibendazole – Anthelcide EQ®), tetrahydropyrimidines (pyrantel salts – Strongid®, others), and avermectin/milbemycins (ivermectin -- Eqvalan®, Equimetrin®, Zimectrin®, others; and moxidectin – Quest®; note that avermectin/milbemycins are also referred to as macrocyclic lactones).  Of these three drug classes, resistance to BZ is the most prevalent and widespread, with reports of resistance from over 21 countries.  Reports of resistance to pyrantel are less common, but the true prevalence of resistance in most of the world is unknown.  In 2001-2002, a large multi-state study was performed to determine the prevalence of resistance on horse farms in the southern United States (Kaplan, Klei et al. 2004).  1274 horses on 44 large stables in Georgia, South Carolina, Florida, Kentucky, and Louisiana were tested in this study.  The fecal egg count reduction test (FECRT) was performed on each farm using 4 different dewormers: fenbendazole, oxibendazole, pyrantel pamoate and ivermectin.  Resistance testing was only done for the small strongyles.  Using fairly conservative criteria that were chosen to minimize the chance that a farm would be designated as having resistant worms if resistance was not present, the percent of farms found to harbor resistant worms were as follows: 97.7% for fenbendazole, 0%, for ivermectin, 53.5% for oxibendazole and 40.5% for pyrantel pamoate.  In terms of actual reductions in fecal egg counts (FEC), the mean percent reductions for all farms were 24.8% for fenbendazole, 99.9% for ivermectin, 73.8% for oxibendazole and 78.6% for pyrantel pamoate.  With the exception of ivermectin, these values are far below the levels needed for effective worm control.  Interestingly, statistical analysis between states for each treatment revealed that in almost all instances there were no statistical differences in results between states.

 

The prevalences of resistance to fenbendazole, oxibendazole, and pyrantel pamoate found in this study were far greater than in any previously published report.  Furthermore, results from all 5 southern states were remarkably similar despite major differences in the types of farms and in physical geography.  This suggests that drug resistance in small strongyles is highly prevalent throughout the entire southern United States and probably nationwide.  It is likely that the situation is not very different in Canada.  These results indicate the following: (1) that drug resistance in small strongyles is much more common than is commonly recognized, (2) that the problem of anthelmintic resistance in small strongyles is worsening, and (3) anthelmintic resistance may be more severe in the United States than elsewhere in the world.  It is interesting to note that the high prevalence of resistance to pyrantel pamoate found in this study has not been detected in studies performed outside the United States.  Many parasitologists have suspected that low-dose daily feeding of pyrantel may lead to resistance.   Because the United States and Canada are the only countries in which daily feeding of low-dose pyrantel tartrate is practiced, one must wonder whether this mode of administration is having a major impact on the selection for resistance to pyrantel.

The results of this study indicate that a serious situation is emerging for small strongyle control in horses.  More than 40% of all farms tested had small strongyle populations that are resistant to fenbendazole (FBZ), oxibendazole (OBZ) and pyrantel pamoate (PP), meaning that on almost half of all farms, only a single drug class (avermectin/milbemycin) that has been in use for 25 years remains effective.  However, in the past 3 years there have been reports out of the United Kingdom, Australia and Brazil indicating the presence of AM-resistant small strongyles.  AM-resistant small strongyles have not yet been reported in the US, but recently a report from the University of Kentucky indicates reduced activity of ivermectin which is suggestive of early resistance (Lyons, Tolliver et al. 2008). These reports are not surprising – what is surprising is how long it took before resistance developed.  AM resistance is extremely common and widespread in closely related parasites of sheep and goats; in the southeastern US the prevalence of ivermectin resistance in Haemonchus contortus (barber pole worm) is approximately 90%.   Reports of AM resistance in parasites of cattle also are becoming increasingly common.  Furthermore, numerous reports suggest that AM resistance is quite common in roundworms (Parascaris equorum) of horses, which is the most important parasite of foals. 

Given the fact that resistance to ivermectin and moxidectin in the small strongyles may already be present in Kentucky, the appropriate solution to the problem of drug resistance is not to simply use more ivermectin and moxidectin because these drugs continue to be effective against small strongyles.  Testing should be done on each farm to determine which drugs work and which do not.  Since OBZ is considerably more effective than FBZ, OBZ should be used in all instances in place of FBZ for single dose usage.  An alternative to AM anthelmintics may be using drug combinations of OBZ and PP.  We recently completed a study to investigate whether combined use of OBZ and PP would produce clinically significant increases in efficacy as compared to the use of these drugs individually.  On 10 of the 12 farms the combination treatment was highly effective in reducing FEC compared to the drugs used singly  (Kaplan, Menigo et al. 2005).  These data suggest that on most farms using OBZ and PP in combination results in clinically significant increases in efficacy, and produces a very high level of FECR.  Overall, based on these results, routine use of OBZ and PP in combination may be considered when the drugs are not highly effective individually.  This may be especially important when treating foals since ivermectin and moxidectin resistance appears to be increasingly common in Parascaris equorum.  However, as always, the effectiveness of these drugs needs to be evaluated before relying upon them, and then monitored by periodic surveillance of FEC pre and post treatment.

These resistance issues need to be appreciated in the context of what can be expected in the future with regard to development and marketing of new dewormers (meaning completely new drug classes, not just new products of existing classes). The great cost associated with the development of new drugs has greatly reduced investment into discovery and development of new dewormers. Of promise is discovery of a new dewormer recently announced by Novartis, but it is unlikely that an equine product will be marketed in the near future, and it is possible that it may never be marketed for horses.  Also of relevance is the fact that any new dewormer products are almost certain to be much more expensive that current products.  Therefore, as we diagnose AM resistance with increasing frequency, options for control with dewormers will be quite limited as there will likely be a delay of many years before any new drugs are available.  The increasingly high prevalence of anthelmintic-resistant small strongyles must therefore be taken into account when designing worm control programs for horses.  It is strongly recommended that prior to using a BZ drug or pyrantel on a horse farm that a FECRT be conducted to rule out the presence of drug-resistant worms on that property.   Furthermore, ivermectin resistance could appear in the US and Canada at any time. 

How can we achieve optimal and sustainable worm control?
Strategies to decelerate further development of drug resistance thereby extending the lifetime of currently effective dewormers should be implemented whenever possible.  This goal can best be achieved by treating the right horse with the right drug at the right time.  Recipe-based treatment programs based solely on the calendar without regard to the medical needs of individual horses, the biology of the parasites, or whether the drug is actually effective against the target parasites can no longer be justified or recommended.  An evidence-based approach where the biology of the target parasites and the effectiveness of drugs are considered, and each horse is viewed as an individual patient with individual medical needs must be adopted.  To develop such a programs we must combine the following: (1) epidemiological principles of nematode control; (2) determine which drugs are effective on each farm; (3) use the correct drug for the correct parasite at the correct time of the year; (4) determine which horses require less or more frequent treatment by performing FEC; and (5) evaluate the overall success of the worm control program by monitoring the FEC of all horses on the property at regular intervals.  Implementation of such programs will only be possible if veterinarians take a central and active role so it is important that horse owners are willing to pay for these services. 

In the course of my studies investigating anthelmintic resistance, I have met many horse owners who refuse to adjust their normal deworming routine even when shown results of FEC that are negative.  This attitude commonly held by horse owners stems partly from the belief that all worms are bad and that no worms should be tolerated in a horse.  This attitude is also influenced by the widely held notion that all horses are highly susceptible to worms and therefore all horses should be treated the same.  However, both of these notions are completely false.  Horses evolved with their intestinal worms and small numbers of most worms do not cause any significant health impairment, but rather help to stimulate immunity that serves to protect the horse from the establishment of a more serious worm burden.  In fact, small strongyles rarely cause severe disease.  Unless parasite control fails miserably, most horses will not show symptoms of disease.  Furthermore, small numbers of eggs shed by untreated horses are critical for slowing the development of anthelmintic resistance (details below).  Finally, all horses are not the same.  Parasite burdens are highly aggregated in hosts, meaning that about 20-30% of horses harbor about 80% of all the worms.   On many farms this distribution is skewed even further.  Thus, some horses carry extremely high worm burdens (even when treated frequently with dewormers) while other horses have strong immunity and are infected with few worms (Figure 1). 

In recent years, parasitologists have come to view the most important factor affecting the rate of development of anthelmintic resistance as the proportion of drug-selected to unselected parasites in a population (Sangster 1999; Van Wyk 2001).  This unselected portion of the population, called refugia, provide a pool of genes susceptible to anthelmintics, thus diluting the frequency of resistant genes.  As the relative size of the refugia increases, the rate of evolution towards resistance decreases.  Therefore, it is likely that, by serendipity, the lack of efficacy of ivermectin against encysted mucosal small strongyle larvae has helped to preserve its efficacy.  These mucosal larvae, which are usually present in far greater numbers than the adult stages, provide a large refugia when ivermectin is administered to a horse. 

Successful nematode parasite control, while maintaining limited refugia, is only possible if routine FECs are performed to identify those horses that require treatment and those that do not.  Although this recommendation is contrary to the treat-all-animals paradigm that often has been taught in the past, it is highly compatible with the host-parasite dynamics of small strongyles.  In our recent study on anthelmintic resistance, most farms deliberately delayed scheduled dewormer treatments (for purposes of the study), and farm data were only included if sufficient horses were passing adequate numbers of small strongyle eggs, a condition met by only 44 of 62 (71%) farms. Nevertheless, we still found that > 33% of all horses on these 44 farms had a FEC < 20 eggs per gram (EPG) and on some farms this value exceeded 50% (see Figure 1). 

In that study we used a very sensitive method for determining FEC, which improved the precision of our measurement.  In contrast, the more commonly used McMaster method, which is the technique I currently recommend for clinical use, has a minimum sensitivity of 25 EPG.  By use of the McMaster method, all of these horses would theoretically have had negative results on fecal examinations.  This skewed distribution of FECs, combined with high degrees of anthelmintic resistance and frequent deworming, suggests that parasite control is being neglected severely in some horses, whereas many other horses are being treated much more frequently than necessary.  Leaving horses with low FECs untreated will have little impact on overall strongyle control, but the small numbers of eggs shed will greatly dilute the contribution to pasture contamination made by treated horses that may be shedding eggs produced by drug-selected (and/or resistant) worms.   Such an approach will succeed in reducing selection pressure for resistance while improving overall parasite control.  Because this will require a fresh view toward parasite control as well as diagnostic capabilities, the only way this treatment scheme can be successful is by having veterinarians once again take an active and leading role in designing and monitoring the effectiveness of parasite control programs. 

Costs of performing FEC must be viewed as a necessary expense for maintaining optimal horse health.  Owners must be warned against embracing the mistaken notion that since the price of a tube of dewormer is the same or less than the price of a FEC that it is cheaper to just go ahead and treat.  Millions of tubes of dewormer are being administered to horses every year that are killing very few parasites either because there are very few worms in the horse to kill, or because the drug is ineffective as a result of resistance.  Furthermore, there are future costs to over-treating in the form of worsening drug resistance.  So not only do current practices of over-treating horses waste money and promote drug resistance, but by not monitoring the success of the program using FEC, there is no way to know how successful the program actually is.  In the early years of the modern age of anthelmintics (1960’s and 1970’s), passage of a nasogastric tube was required for administration of dewormers to horses.  Consequently, deworming of horses was almost an exclusive activity of veterinarians.  However, over the past few decades, the ready availability of safe, effective, inexpensive, and easily administered dewormers to has led to an important decrease in veterinary involvement in parasite control.  This trend must change -- veterinarians need to become more involved in developing and monitoring parasite control programs, because the growing problem of anthelmintic resistance only will worsen in the future.   This can only happen if horse owners appreciate the value of such services and provide a market demand for these services. 

Which parasites are important and which should be targeted in a control program?
Small strongyles (small strongyles) are considered the principal parasitic pathogens of adult horses, but tapeworms (Anoplocephala perfoliata), bots (Gasterophilus spp), and large strongyles (Strongylus vulgaris, S. edentatus, and S. equinus) are also considered to be significant pathogens and worthy of specific targeting in a worm control program.  As mentioned previously, the large strongyles, particularly S. vulgaris are now quite rare in managed horses and require only once or twice (depending on climate) yearly strategic treatments to keep them that way.  Other less common and less important parasites such as stomach spirurid worms (Draschia, Habronema), pinworms (Oxyuris equi), Onchocerca, Trichostrongylus axei, Dictyocaulus arnfeldi, and Strongyloides westeri are expected to be controlled by default in a properly designed program which takes into account the main group of parasites that are targeted.  If any of these “lesser” parasites are diagnosed, they should be treated on a case by case basis.  It is important to note that in areas of the US where suppressive treatment of horses has not been commonly practiced over the past few decades, such as in the desert southwest, some of these parasites of “lesser importance” such as Habronema and Draschia remain quite common and important.  In foals, the same parasites listed above for adult horses are also important, but added to this list is the roundworm, Parascaris equorum, which is considered to be the most important parasite of foals.

When should anthelmintic treatments be given and what criteria should be used to make treatment decisions?
When a treatment is given is just as important as which drug is used.  Reasons for this include the following: (1) virtually all of the parasites listed above are transmitted seasonally (2) each parasite has a different life cycle, and host interaction (3) larval rather than adult stages are most pathogenic for both the large and small strongyles; and (4) the different dewormers have differing spectra of activity against the different worms and in many cases against different stages of the same worms.   With this in mind, it becomes obvious that treatments evenly spaced throughout the year simply do make any biological or medical sense.  Optimal and rational worm control demands that the most appropriate drug be administered at the most appropriate time.  In the large majority of situations, all of the important parasites of adult horses listed above except small strongyles can be satisfactorily controlled with only 2 – 3 treatments each year.  In many horses, 2 - 3 treatments each year will also be sufficient for controlling small strongyles, but other horses will require several more treatments. 

The timing and frequency of treatments must be based on a large number of factors among which are: the time of year, the parasite species being targeted by treatment, the age of the horse, the level of immunity of a particular horse to small strongyles (as revealed by FEC), and which drugs were used previously and when they were used.  Ultimately, treatments should be worked into a logical program that addresses all the parasites of concern, without trying to address each parasite individually.

Tapeworms:  Tapeworms are transmitted to horses predominantly in the summer and fall.  Therefore, one properly timed treatment per year (in the late fall) likely is enough to control tapeworms under most circumstances.  There is little evidence to support the need for more than one annual treatment for tapeworms, but it is possible that in some instances horses could benefit from a second treatment for tapeworms in the spring.  Spring treatment is especially important if a tapeworm treatment is not administered in the late fall.  Of course, in the rare instance where tapeworms are diagnosed as a clinical problem on a farm, then treatment every 4 months would be advisable until the problem is under control. 

Bots:  Bots are transmitted in the summer and fall until the first hard freeze ends bot fly activity for the year.  Therefore, treatment for bots should occur in late autumn after the first hard freeze.  However, in general, years of ivermectin and moxidectin treatments have greatly reduced the magnitude of bot activity, thus bots are not as big a concern as they once were.  Furthermore, bots do not cause any significant health problems to horses.  These are more of an aesthetic problem than a medical problem.

Small strongyles:  When considering the treatment interval for control of small strongyles (which is typically the primary target of worm control in adult horses), a number of factors must be considered, but foremost among these is the fact that each drug has a different egg reappearance period (ERP).  Small strongyles encyst in the intestinal wall as part of their normal life cycle.  Single-dose dewormers have no activity against these stages (with the exception of moxidectin) and only kill the worms in the lumen of the large intestine (mostly adult worms with some mature larvae).  Following treatment with a dewormer, larvae encysted in the intestinal wall come out and fairly rapidly repopulate the intestinal lumen and begin shedding eggs in the feces.   Frequently used every 8-week rotational treatment strategies will fail to achieve optimal control because the ERP of BZ drugs and pyrantel is only about 4 weeks (assuming the drugs were effective in the first place which is often not the case).  If used at 8-week intervals, significant pasture contamination (from the high egg shedding horses) will occur between treatments ensuring that horses are always ingesting numerous parasite larvae from pasture.  The ERP of ivermectin is approximately 8 weeks and moxidectin is 12-16 weeks.  Thus, treating 8 weeks after moxidectin will be a useless endeavor – there will be virtually no worms to kill. [Note that these ERPs continue to shorten, so one can no longer assume they will see the usual historic intervals.  In fact ERP of 4 weeks are being reported for ivermectin, thus it is worth doing periodic surveillance to check]

Before one can understand why particular recommendations for worm control make sense, he or she must understand what the objective of the control program actually is.  It is an interesting exercise to ask horse owners, “Why should you control parasites?”  Most will offer a response that includes some reference to improved health or enhanced performance.  But the answers differ if one refines the question and asks, “What are you specifically trying to do when you give a dewormer?”  The most frequent answer is, “To kill worms”.  However, killing worms per se is NOT the objective of a parasite control program.  This is especially true for small strongyles, which exert the majority of their pathogenic effects BEFORE they are susceptible to many dewormers.  An important fact that is often overlooked or is simply not appreciated but is extremely important to remember is that the encysted larval small strongyle worms in the intestinal wall are most pathogenic to the horse (and the worst of these effects is when the larvae emerge to repopulate the lumen); and ivermectin, pyrantel pamoate, and BZ (single dose) only kill adult worms.  Only moxidectin and a double-dose 5-day regimen of FBZ (if no high-level resistance to FBZ) will kill the encysted larvae. In contrast, the adult worms in the intestinal lumen that are shedding the eggs are much less damaging than the immature encysted forms.

The true objective of a worm control program is to optimize the health of horses --- NOT to kill all worms.  Small numbers of small strongyle worms cause little harm and treating low level infections can actually cause more harm to the horse than not treating.  With this in mind, the real goal of the worm control program for horses is preventing contamination of the environment with the eggs of the target parasites.  For small strongyles, the direct source of infection is larvae on pasture, and those larvae develop from eggs deposited by grazing horses.  Once strongyle eggs turn into infective larvae, the only factors that can diminish the risk of future infections are hot weather, time, and keeping horses off the pasture.  The only practical way to decrease future infection is by limiting the passage of worm eggs by killing female worms before they reproduce.  So that’s what we aim for with small strongyle control recommendations:  limiting the passage of large numbers of strongyle eggs onto pasture.  To accomplish this goal, treatments must be administered at concentrated intervals for limited “high transmission” times of the year.  At times of the year when survival and/or development of small strongyle eggs and larvae on pasture is minimal (summer in south, winter in north), there is little reason to treat with a non-larvicidal product. 

Back to selective treatment -- how do you decide if a horse should be treated or not?  There is no absolute cutoff in FEC that can be used to determine whether a horse needs treatment or not.  This will change on the basis of season, stocking rates, age of horse, overall health of horse, and tolerance of the owner.  In response to the question “At what FEC value should you deworm a horse?”, 7 equine parasitologists gave answers ranging from 200 to 500 EPG (Uhlinger 1993).  FECs do not directly correlate with luminal worm burdens, but it is very unlikely that horses with FEC less than 200 EPG will be suffering ill effects from those infections.  Another way to examine this issue is to segregate horses into 3 categories based upon their strongyle contaminative potential.  The contaminative potential of a horse can be determined by examining a fecal sample collected approximately four to eight weeks after the expiration of the ERP for the last effective dewormer it received.  Depending upon the last drug used, this may require a break in scheduled deworming treatments if horses are treated at regular intervals year round (something I do not recommend).  The best time to do this would be the late winter/early spring since there is unlikely to be any negative consequence of not treating, and in fact I do not recommend treating over the winter.  Since the relative magnitude of contamination (as measured directly by FEC) is a repeatable characteristic of individual animals, horses can be classified as low, moderate or high egg shedders.  In herds that have not been dewormed recently, certain horses (approximately 20-30% of the herd) have high egg counts, another proportion will have low egg counts (30-50%), and the remainder cluster around the average.  Adult horses with egg counts 500 EPG are classified as High Contaminators/Shedders.  The remainder of horses, with EPGs >200 to <500 EPG, are classified as Moderate Contaminators/Shedders.  

Given this information what is a rational worm control program?  Worm control programs are best viewed as a yearly cycle starting at the time of year when worm transmission to horses changes from negligible to probable.  In Western Canada, this is in the late spring as temperatures begin to increase.  The goals of the program laid out here are to: keep FEC low thereby reducing future worm transmission, kill all important parasites at the correct time of the year, and reduce the development of drug resistance. Please keep in mind that this is just one of many possible programs and there is room for differences of opinion among parasitologists and veterinarians. Ultimately, each farm (with veterinary guidance) should develop its own program tailored to the needs of the farm.  The take home message must be that there is no such thing as a one size fits all program.  But that does not mean that whatever one decides to do is OK -- there are many programs that are clearly poor, because they do not take into account the factors discussed in this paper. 

Recommendations for Worm Control in Adult Horses in a Cold Northern Climate
Before a rational “evidence-based” program can be developed, one must know which drugs work and which drugs do not.  Therefore, a prerequisite for establishing a rational program is performing a FECRT.  This is rarely done but is of utmost importance.  Extremely high levels of resistance to dewormers are present in the important small strongyles of horses.  Instructions for how to perform a FECRT will be available on my web page in the near future <www.vet.uga.edu/GO/kaplanlab >

The program outlined below is for adult horses in a cold northern climate.  Foals will require a different program.  The first treatment of the worm control cycle should be given in April and the last treatment given in October or November. 

April 01: Start of Worm Control Cycle

Which Horses? Treat all horses regardless of FEC

Drug(s) of choice: ivermectin or moxidectin

Why these drugs?     These drugs will kill any migrating large strongyles and any strongyles (both large and small) that are in the intestinal lumen.  These drugs are also very broad spectrum so will kill a variety of other worms that might be infecting the horses.  They also have the highest efficacy against strongyles, ensuring that egg shedding will be extremely low during this critical time of the worm transmission cycle. 
 
Is there a reason to use one over the other?     Moxidectin has the advantage of also killing large numbers of the encysted small strongyles and prevents worm eggs from reappearing in the feces for 4-8 weeks longer than ivermectin.  If FEC are performed ahead of treatment, using moxidectin only in horses with FEC >500 or in horses known to have chronically high FEC (High Contaminators), and using ivermectin on the remainder would be a rational decision.  Also worth considering is the fact that late winter/early spring is the time when larval cyathostomosis is most common.  Moxidectin is the only drug that can prevent this serious but rare disease.  Therefore, any horse that has had chronic diarrhea over the winter or early spring should be treated with moxidectin.

Should I perform FEC?     Yes – on all horses.  This is probably the single most important FEC to perform all year (assuming that you follow this program and have not dewormed in the past few months).  The reason for this is that by not deworming for several monthsver the winter and early spring, the FEC seen will be a strong indicator of each horse’s true strongyle contaminative potential.  Based on this FEC you can then categorize your horses to low (500 epg).  This characteristic of individual horses has been shown to be highly repeatable between seasons and years. 

JUNE 01: ONLY IF TREATED WITH IVERMECTIN.  IF MOXIDECTIN WAS USED WAIT UNTIL JULY 01 TO TREAT AGAIN.

Which horses?     All those with FEC > 500 epg on the September fecal check.  Any horses that had a FEC between 150-500 epg in April should have a FEC performed and then only treated if epg >100.  Any horses that had a FEC of <150 epg in April will have very low or negative FEC 8 weeks after ivermectin and will not need to be treated.

Drug(s) of choice:     oxibendazole and/or pyrantel (if effective on your farm!!! You must determine this by doing a FECRT.  You might also consider using both drugs to increase overall effectiveness)

Why these drugs?     To reduce the amount of ivermectin and moxidectin used thereby helping to slow down the development of resistance to ivermectin and moxidectin.  However, resistance has been shown to be fairly common to oxibendazole and pyrantel, therefore, if using these drugs before and after treatment FEC should be performed to determine the levels of egg reduction from treatment.  Also worth considering is recent data which showed that using both oxibendazole and pyrantel together at the same time improves the effectiveness of treatment as compared to using the individual drugs.

Is there a reason to use one over the other?     No – unless resistance to one of these drugs is detected.  If Pyrantel is used at a double dose tapeworms will also be killed, but few tapeworms are likely to be found in horses until autumn.

Should I perform FEC?     Yes – but only on the horses that had a FEC between 150-500 epg in April.  Those with high (>500 epg) and low (<150 epg) FEC do not need to be checked (you can assume they are still high or low).  If you haven’t performed FECRT previously, FEC should be checked again 10-14 days after treatment.

JULY 01:   

Which horses?     Treat high and moderate egg shedders (as based on FEC performed in April)

Drug(s) of choice:     oxibendazole and/or pyrantel

Why these drugs?     As per June explanation

Is there a reason to use one over the other?     As per June explanation

Should I perform FEC?     As per June explanation

AUGUST 01:

Drug(s) of choice:     ivermectin or moxidectin

Why these drugs?     These drugs will kill bots that were acquired since the spring, kill the stomach worms Habronema and Draschia that are transmitted by flies and cause summer sores, sterilize Onchocerca females preventing transmission, and kill pinworms (Oxyuris equi). These drugs will also kill migrating large strongyles and any strongyles (both large and small) that are in the intestinal lumen.

Is there a reason to use one over the other?     Using moxidectin in horses classified as high egg shedders and ivermectin in the other horses would be a good option, but either drug could be used in all horses.  Also, by the end of October it is too cold for eggs to develop to infective larvae -- using moxidectin gets you to November before eggs will be shed.

Should I perform FEC?     Yes – on all horses.  It is important to know how well your program is working – it is important to keep egg shedding down to low levels at this point of the summer.

OCTOBER 01:  ONLY IF TREATED WITH IVERMECTIN IN AUGUST

Which horses?     Treat high egg shedders

Drug(s) of choice:     oxibendazole and/or pyrantel

Why these drugs?     As per June explanation

Is there a reason to use one over the other?     As per June explanation

Should I perform FEC?     Not necessary

NOVEMBER 01: 

Which horses?     Treat all horses (regardless of FEC)

Drug(s) of choice:     Pyrantel at double dose to kill tapeworms (use a product with a label indication for tapeworms)

Why these drugs?     In this climate, tapeworm transmission peaks in autumn so treatment with a drug that kills tapeworms at this time will remove all the tapes acquired over the summer and autumn.  Praziquantel is the most effective drug for tapeworms, but it is only available in combination with ivermectin or moxidectin which are not needed at this time of year since strongyle transmission has ended for the year due to cold.  Therefore, pyrantel which is also highly effective against tapeworms is probably the better choice.  Since strongyle transmission is over for the year, we do not need to worry about these parasites again until the spring.

Is there a reason to use one over the other?     As per previous discussion.

Should I perform FEC?     Not necessary

Summary of Suggested Control Program for Adult Horses (>2 Years of Age): 
This program is designed to specifically target bots (Gasterophilus), tapeworms (Anoplocephala perfoliata), spirurid nematodes responsible for producing summer sores (Habronema, Draschia), Onchocerca, pin worms (Oxyuris equi), large strongyles (Strongylus spp), and small strongyles (cyathostomes).  A few other uncommon and lesser important nematode, arthropod, and cestode parasites likely will also be controlled by this program, except in rare unusual circumstances when specific measures may be needed.  Treatments in April and August with ivermectin or moxidectin should control all of the worms listed above for the entire year and prevent egg shedding at critical times of the year when eggs will develop to infective stages.  However, there are 2 exceptions to consider: (1) tapeworm transmission peaks in the autumn so a late autumn treatment is needed as a yearly cleanout treatment; and (2) small strongyles will require additional treatments in some horses (i.e., chronically high egg shedders).  Some horses with naturally strong immunity to cyathostomes (demonstrated with very low FEC on each fecal exam) will need no other treatments because the two treatments have covered the needs of the other parasites and these horses are naturally protected from cyathostomes.  In traditional worming programs, repeated treatment of these low egg count horses accomplishes little to nothing.  Some horses in the herd will need an additional treatment for cyathostomes, but only a few horses (should be less than 30% of the herd) should need further treatments.  Now compare this to what you are doing now.  Many farms are treating all horses 6 times each year, and likely are getting results that are significantly less than what will be achieved on the program recommended here.  When examining the program above it is important to remember that the different drugs have differing egg reappearance periods following treatment.  It is important to know these time intervals to understand why the recommendations are made.

If you are concerned that doing all these fecal egg counts will be too expensive, then think again.  A recent cost analysis performed by veterinary students at the University of Georgia College of Veterinary Medicine found that the cost of deworming every horse 6 times per year is about the same or more than treating based upon this schedule and performing the FEC as suggested.  In addition, using this system you know whether your worm control program is working.  By treating blindly there is no way to tell and we know that drug resistance is highly prevalent.  Treating a horse with a drug that does not work because of resistance is very expensive – you waste the money spent on the drug and you risk failure of your worm control program.  Additionally, treating a horse that does not need to be treated promotes drug resistance, which will have future adverse consequences to the health of your horses.

This program is very different from what most horse owners are doing now (and what most vets are recommending) and admittedly is much more complicated.  The reason for this complexity is that parasite biology and the horse-parasite-environment drug-relationship is quite complex.  The commonly used rotational program where all horses are treated on the same schedule with the same drug at frequent intervals may be easy to manage, but it does not properly address the health needs of the horse or the biology and epidemiology of the parasite.  That program was designed more than 40 years ago when the parasites of importance were much different than they are today, and when parasite drug resistance was not an important concern.  A good parasite control program must be based on the most up to date medical and scientific knowledge.  This necessitates a program be used that is medically-based, not convenience-based.   Furthermore, it should be understood by all horse owners that any recommended parasite control program has a finite life-span.  New knowledge, spreading drug resistance, new drugs, changes in parasite prevalence, etc will cause recommendations to change.   The commonly used calendar-based rotational program has been used for more than 40 years – it is time for a change.  Unfortunately, some pharmaceutical companies continue to promote the outdated rotational program.  One can only guess at their motive, but it seems likely that promoting this approach helps them to sell more drugs, while avoiding the issue of drug resistance.

Using the program recommended here, during the first 2 years of implementation it will be important to perform fecal egg counts at fairly regular intervals.  However, this program really is not as complicated as it seems at first.  Once this or a similar program is instituted, the farm/stable will learn which drugs work and which drugs do not work, and will learn which horses are chronically high egg shedders and which horses always have very low or 0 fecal egg counts.  Once this information is known (after about 2 years of regular monitoring), a more simplified program can be designed in which horses are grouped into one of three categories:  (1) high, (2) moderate, and (3) low egg shedders.  Horses within each group then can all receive the same program.  In addition, because egg shedding in a horse is very consistent, fewer egg counts will need to be done.  Once a program is established, 2 fecal egg counts per year per horse are all that should be needed. 

Recommendations for Foals and Yearlings (<18 Months Old):
Parascaris equorum (roundworms/ascarids) are usually the most important parasite of young horses with small strongyles next most important.  Strongylus vulgaris has its greatest effect on young horses so this parasite cannot be ignored, but luckily is very uncommon in managed horses.  When addressing the treatment needs of these different parasite species, the issue of drug resistance becomes central.  Therefore, it is critical to perform FECRT on all drugs used in foals, and to monitor the ERP following effective treatment.  Since there is a high prevalence of ivermectin/moxidectin resistance in P equorum, and there is a high prevalence of BZ and pyrantel resistance in small strongyles, in many cases it will not be possible to control both of these important parasites with a single drug.  Therefore it may be necessary to use a full dose of two of these drugs together at the same time.  Treatments should begin when the foal is 2 months of age.  Most treatments for P equorum, if effective should keep eggs out of the feces for 8 weeks.  But ERP for small strongyles for BZ drugs and pyrantel are only 4 weeks (if they are effective in the first place), and ERP for ivermectin and moxidectin are less in young horses than in older horses.  Additionally, as mentioned earlier there is a recent report from Dr. Gene Lyons of the University of Kentucky demonstrating very short ERP with ivermectin -- as short as 4 weeks.   Therefore, it is difficult to know what the optimal interval for treatments should be in foals, as it will depend on a number of factors.  Treating too often will waste money and promote drug resistance, but treating too infrequently, or with the wrong drugs can result in failure of control and clinical disease problems.  Thus it cannot be overemphasized that FEC surveillance in young horses is critical, including yearly tests of drug effectiveness using FECRT, and monitoring of ERPs.  No matter what the program used for P. equorum and small strongyles turns out to be, it is very important in foals to be sure to include an ivermectin or moxidectin treatment at a minimum of 6-month intervals to control any S. vulgaris that may be around.  Also, in young horses, one must be concerned about encysted larval burdens of small strongyles.  Therefore, all horses between 6 months and about 2 years of age likely will benefit from receiving a larvicidal treatment once per year.  In most situations, moxidectin would be my recommendation for this treatment, but 5-day 2X fenbendazole (Power Pack) can also be used.  Lastly, one keep in mind that very frequent treatment of foals (every 3-4 weeks), as is often done on some farms, does not ensure adequate parasite control because the drugs likely are not working at expected levels due to resistance.  Furthermore, even if the drugs are working, one must not be too over-confident because resistance could appear at any time.  Once multiple-drug resistance is present, there may be no good options for control.  Thus, doing things that will help to slow the development of resistance (as discussed above) will help to ensure that farms will be able to properly control parasites in the future.

References
Drudge, J. and E. Lyons (1977). Pathology of infections with internal parasites in horses. The Blue Book, Hoechst: 267-275.
Drudge, J. H. and E. T. Lyons (1966). “Control of internal parasites of the horse.” J Am Vet Med Assoc 148(4): 378-383.
Kaplan, R. M., T. R. Klei, et al. (2004). “Prevalence of anthelmintic resistant cyathostomes on horse farms.” Journal    of the American Veterinary Medical Association 225(6): 903-910.
Kaplan, R. M., E. Menigo, et al. (2005). Use of pyrantel pamoate and oxibendazole in combination for the treatment
  of equine strongyles American Association of Veterinary Parasitologists, 50th Annual Meeting.     Minneapolis, MN, July 16-19, 2005.
Love, S., D. Murphy, et al. (1999). “Pathogenicity of cyathostome infection.” Veterinary Parasitology 85(2-3): 113-121.
Lyons, E., S. Tolliver, et al. (1999). “Historical perspective of cyathostomes: prevalence, treatment and control  
 programs.” Veterinary Parasitology 85: 97-112.
Lyons, E. T., S. C. Tolliver, et al. (2008). “Field studies indicating reduced activity of ivermectin on small strongyles
 in horses on a farm in Central Kentucky.” Parasitology Research 103(1): 209-215.
Sangster, N. C. (1999). “Pharmacology of anthelmintic resistance in cyathostomes: will it occur with the avermectin/
 milbemycins?” Veterinary Parasitology 85: 189-204.
Uhlinger, C. A. (1993). “Uses of fecal egg count data in equine practice.” Compendium on Continuing Education for
 the Practicing Veterinarian 15(5): 742-748.
Van Wyk, J. A. (2001). “Refugia - overlooked as perhaps the most potent factor concerning the development of
 anthelmintic resistance.” Onderstepoort Journal of Veterinary Research 68(1): 55-67.
Further Suggested Reading
The Horse Magazine 12-part “Parasite Primer” Series Vol. XXI, No.1-12, JAN 04 – DEC 04
 
Figure 1:  Graphs of the distribution in fecal egg counts (FEC) on horse farms
Graphs of farms 1, 2 and 3 show FEC of horses on 3 individual farms in Georgia and the 4th graph shows FEC of all horses on 44 farms in Florida, Georgia, Kentucky, and Louisiana.  Farms 1 and 2 only had adult horses, farm 3 had only yearling horses, and the combined graph represents horses of all ages.  Each square represents the FEC of a single horse which is read on the Y axis.  On the combined graph the large numbers of data points converge to produce what looks like a solid line.  Note that in each case the distribution of FEC is virtually the same.  The shape of these graphs shows the aggregated nature of parasite infections, where a small percent of the animals harbor most of the parasites.  Data displayed on the combined farm graph reveals that horses with FEC of 500 EPG or greater accounted for 88% of total egg output, yet made up only 31% of the population.  In yearlings (Farm 3), because many have not yet reached their immune potential, the shape of the graph is a little less steep, i.e. fewer horses have very low FEC.  This aggregated pattern of parasite distribution among animals is always seen.  The only thing that changes is the relative magnitude of the parasite level depending on management and parasite control practices.  From these graphs it is obvious that some horses need much more attention to worm control than do others. 

 


 

 

 

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