research updates in small ruminant parasitology

3
252 AABP ANNUAL CONFERENCE PROCEEDINGS — VOL. 53 — NO. 2 — SEPTEMBER 2020 Research updates in small ruminant parasitology Ray M. Kaplan, DVM, PhD, DipACVM, DipEVPC; Leonor Sicalo Gianechini, DVM Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602 Corresponding author: Dr. Ray Kaplan; [email protected] Abstract For years, livestock farmers have relied on the use of an- thelmintics as their sole means for controlling helminth infec- tions; however, this strategy has proven to be unsustainable. The current high levels of anthelmintic resistance to multiple drug classes makes it difficult to control parasites using chemical means alone. Furthermore, the lack of new classes of anthelmintic drugs means that the drugs we have now will be all we have for quite a long time. Thus, parasite control needs to be viewed more holistically within an ecological context and practiced in a multi-pronged integrated manner. Here, we review some of the recent literature on parasite control in small ruminants that addresses these issues. Key words: Haemonchus contortus, drug resistance, parasite control, ruminants Introduction The animal food production industry is facing the challenge to achieve sustainable, efficient ruminant farming systems in order to meet the growing demands for livestock products. 26 Furthermore, this challenge must be addressed in an increasingly complex scenario shaped by climate change, 21 and widespread anthelmintic resistance. 28 These issues are particularly relevant to small ruminant farms, where losses due to parasitic infections have a great impact on the overall flock health and thus, on the profitability of the system. 18 For years, farmers have relied on the use of chemical compounds as their sole way to control helminth infections, but this strategy has proven to be ecologically unsustainable and untenable through time. 14 In recent years, new concepts on precision farming 10,12 have gained strength as a means to bring together the main benefits of genetics, nutrition, reproduction, thorough planning, and applied technology in order to maximize the production outcome, a concept that has long been used by the agriculture sector with success- ful results. Moreover, this approach could improve the flock welfare, reducing susceptibility to infectious diseases in general. In this review we briefly address recent advances in the following parasite control strategies: best practices for parasite control, targeted selective treatment including FAMACHA©, biological control, vaccines, copper oxide wire particles, use of tannin-containing forages, and selective breeding for host resistance. Many of these topics have been reviewed in detail, and the reader is suggested to see these publications for further information. 7,15,25 Parasite Control Strategies: What is New? Parasite control can be achieved through different methods: chemical control, general management, and bio- logical strategies. A recent study 17 conducted in the United Kingdom, evaluated commercial sheep farms for 3 years, comparing SCOPS-managed farms (UK’s Sustainable Control of Parasites in Sheep; https://www.scops.org.uk/), vs tradi- tional ones. In conclusion, SCOPS managed-farms used less anthelmintic treatments and less frequently, without losing productivity or increasing worm burden in animals. Even so, lambs had higher daily weight gains, taking less time to ar- rive to greater finish weights. Best practices from the SCOPS program included use of effective quarantine drenching, selective targeted treatments (TST) of adult ewes around lambing or no treatment at all, selective treatment of lambs, avoidance of “drench and move” practices, correct use of anthelmintics depending on resistance status and nematode genera present, and proper delivery of anthelmintics, i.e., dosing by the heaviest animal and calibrating the dosing gun when treating. It is notable that TSTs were done by leaving the 20% heaviest animals without treatment, or based on diagnostics techniques like FAMACHA© or fecal egg counts. What other strategies have been shown to be effective in recent years? First, regardless of the use of integrated parasite control strategies, effective anthelmintic drugs will still be needed to treat clinical disease, thus there remains a great need for new anthelmintic drugs. 8 However, the newest an- thelmintic drugs (monepantel, derquantel), representing new drug classes that are sold as products for the sheep industry in many countries, are not currently approved or marketed in the US. While these new anthelmintics theoretically could be a valuable tool on farms in the US with multiple-drug resis- tance, it seems unlikely that these products will be approved and marketed in the US in the foreseeable future, if ever. Thus, alternative approaches are necessary. Very recently, a natural biological product containing the nematophagous fungi, Dud- dingtonia flagrans, a became available in the US. A recent study using this product including cattle, goats, and horses under different climatic regions in Australia, showed significant reductions in pasture larval contamination that ranged from 53% to 99%. 11 Other studies in sheep using D. flagrans (but not the marketed product), report larval reductions varying from 76.6% up to 100%, depending on the dose of spores that animals received per kg of live weight. 9,20,31 Though D. flagrans has been proven effective for many years, it was not marketed as a product because of cost-related and ease of delivery-related issues. Though the company has success- © Copyright American Association of Bovine Practitioners; open access distribution.

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252 AABP ANNUAL CONFERENCE PROCEEDINGS — VOL. 53 — NO. 2 — SEPTEMBER 2020

Research updates in small ruminant parasitologyRay M. Kaplan, DVM, PhD, DipACVM, DipEVPC; Leonor Sicalo Gianechini, DVMDepartment of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602Corresponding author: Dr. Ray Kaplan; [email protected]

Abstract

For years, livestock farmers have relied on the use of an-thelmintics as their sole means for controlling helminth infec-tions; however, this strategy has proven to be unsustainable. The current high levels of anthelmintic resistance to multiple drug classes makes it difficult to control parasites using chemical means alone. Furthermore, the lack of new classes of anthelmintic drugs means that the drugs we have now will be all we have for quite a long time. Thus, parasite control needs to be viewed more holistically within an ecological context and practiced in a multi-pronged integrated manner. Here, we review some of the recent literature on parasite control in small ruminants that addresses these issues.

Key words: Haemonchus contortus, drug resistance, parasite control, ruminants

Introduction

The animal food production industry is facing the challenge to achieve sustainable, efficient ruminant farming systems in order to meet the growing demands for livestock products.26 Furthermore, this challenge must be addressed in an increasingly complex scenario shaped by climate change,21 and widespread anthelmintic resistance.28 These issues are particularly relevant to small ruminant farms, where losses due to parasitic infections have a great impact on the overall flock health and thus, on the profitability of the system.18

For years, farmers have relied on the use of chemical compounds as their sole way to control helminth infections, but this strategy has proven to be ecologically unsustainable and untenable through time.14 In recent years, new concepts on precision farming10,12 have gained strength as a means to bring together the main benefits of genetics, nutrition, reproduction, thorough planning, and applied technology in order to maximize the production outcome, a concept that has long been used by the agriculture sector with success-ful results. Moreover, this approach could improve the flock welfare, reducing susceptibility to infectious diseases in general. In this review we briefly address recent advances in the following parasite control strategies: best practices for parasite control, targeted selective treatment including FAMACHA©, biological control, vaccines, copper oxide wire particles, use of tannin-containing forages, and selective breeding for host resistance. Many of these topics have been reviewed in detail, and the reader is suggested to see these publications for further information.7,15,25

Parasite Control Strategies: What is New?

Parasite control can be achieved through different methods: chemical control, general management, and bio-logical strategies. A recent study17 conducted in the United Kingdom, evaluated commercial sheep farms for 3 years, comparing SCOPS-managed farms (UK’s Sustainable Control of Parasites in Sheep; https://www.scops.org.uk/), vs tradi-tional ones. In conclusion, SCOPS managed-farms used less anthelmintic treatments and less frequently, without losing productivity or increasing worm burden in animals. Even so, lambs had higher daily weight gains, taking less time to ar-rive to greater finish weights. Best practices from the SCOPS program included use of effective quarantine drenching, selective targeted treatments (TST) of adult ewes around lambing or no treatment at all, selective treatment of lambs, avoidance of “drench and move” practices, correct use of anthelmintics depending on resistance status and nematode genera present, and proper delivery of anthelmintics, i.e., dosing by the heaviest animal and calibrating the dosing gun when treating. It is notable that TSTs were done by leaving the 20% heaviest animals without treatment, or based on diagnostics techniques like FAMACHA© or fecal egg counts.

What other strategies have been shown to be effective in recent years? First, regardless of the use of integrated parasite control strategies, effective anthelmintic drugs will still be needed to treat clinical disease, thus there remains a great need for new anthelmintic drugs.8 However, the newest an-thelmintic drugs (monepantel, derquantel), representing new drug classes that are sold as products for the sheep industry in many countries, are not currently approved or marketed in the US. While these new anthelmintics theoretically could be a valuable tool on farms in the US with multiple-drug resis-tance, it seems unlikely that these products will be approved and marketed in the US in the foreseeable future, if ever. Thus, alternative approaches are necessary. Very recently, a natural biological product containing the nematophagous fungi, Dud-dingtonia flagrans,a became available in the US. A recent study using this product including cattle, goats, and horses under different climatic regions in Australia, showed significant reductions in pasture larval contamination that ranged from 53% to 99%.11 Other studies in sheep using D. flagrans (but not the marketed product), report larval reductions varying from 76.6% up to 100%, depending on the dose of spores that animals received per kg of live weight.9,20,31 Though D. flagrans has been proven effective for many years, it was not marketed as a product because of cost-related and ease of delivery-related issues. Though the company has success-

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© Copyright American Association of Bovine Practitioners; open access distribution.

SEPTEMBER 2020 — VOL. 53 — NO. 2 — AABP ANNUAL CONFERENCE PROCEEDINGS 253

fully addressed these issues, the product remains expensive since it must be fed daily for relatively long periods of time. Consequently, the cost-benefit of including 1 of these prod-ucts in an integrated parasite control program needs to be carefully assessed for each farm.

Another alternative treatment is copper oxide wire particles (COWP), which has demonstrated high levels of effectiveness against Haemonchus contortus in multiple studies.3,4,27 COWP can be combined with anthelmintics6,24 or even with other biological approaches like bioactive for-ages, for obtaining major benefits.5 A further strategy is the use of bioactive forages. The most studied of these in the US is the use of the condensed tannin containing plant sericea lespedeza, which has exhibited good activity against gastro-intestinal nematodes (GIN) when included in the diet either directly grazed or as hay/pellets.16,19,22

Breeding for resistance and even resilience against GIN shows moderate heritability, representing another long-term sustainable approach. Fecal egg counts and FAMACHA scores are methods used to evaluate and select animals, though more information on decision making tools can be attained through the National Sheep Improvement Programb (NSIP). Data from Australian and New Zealand sheep farms obtained from the MERINOSELECTc database were analyzed, concluding that relatively rapid selection response for worm resistance could be achieved without negative impact on other genetic traits.2 Moreover, selective breeding of the maternal line could represent a powerful tool to reduce selection pressure for anthelmintic resistance, considering future climate change scenarios.29

Some good news in the fight against H. contortus is the development of a vaccined,23 that is now available in Australia, New Zealand, South Africa, and England. This is the first vaccine that works against a GIN in livestock, and its success is due to a novel alternative strategy. This vac-cine uses hidden antigens in the gut of the worm that the sheep immune response typically does not see. However, following vaccination the sheep produce antibodies that are then ingested with the blood meal and attack the gut of the worm. The now marketed vaccine has been shown to reduce fecal egg counts by up to 82% when used in yearling sheep trials.23 In a vaccination trial conducted in a flock from Louisiana, egg-shedding in vaccinated ewes was reduced by 65%.13 A study from Brazil concluded that pregnant or lactating ewes that were provided a supplemented diet along with the vaccination protocol received less treatments and showed more resilience to Haemonchus infections than the vaccinated group without supplementation.1 Though this vaccine is reasonably effective, because of its mode of action there is no anamnestic response, and thus multiple doses must be given each grazing season. Additionally, this vaccine uses native proteins, as multiple attempts at making a recombinant version have repeatedly failed. The need for native antigens (extracted directly from worms) means the cost is high and the supply is limited. Consequently, unless

researchers can figure out how to make the vaccine effective using recombinant proteins, it seems highly unlikely that this vaccine will ever become available in the US.

Lastly, modelling and forecasting methods are making their way into parasite control. Decision support systems that integrate environmental data along with host-parasite dynamics, while modelling and predicting different scenarios, are now offered mainly in Australia and the UK (e.g. Flyboss, Liceboss, SCOPS’ Nematodirus alerts, among others).30 This allows farmers and veterinarians to be made aware of high risk of infection in particular geographical regions and sea-sons for different parasites, in order to plan accordingly. It is noteworthy that these initiatives in Australia and the UK were supported with significant funding from government sources, a mechanism sorely lacking in the US. Without sub-stantial long-term financial support, these types of initiatives are not possible, thus it is unlikely that similar tools will be available in the US any time soon. Two modelling tools de-signed specifically for analyzing fecal egg count reduction test data are available on the internet and can be used by veterinarians in the US.

Endnotes

a BioWorma®, and Livamol® with BioWorma (International Animal Health Products, Huntingwood, NSW, Australia; https://www.bioworma.com/)

b National Sheep Improvement Program (NSIP; http://nsip.org/)

c http://www.sheepgenetics.org.au/Breeding-services/MERINOSELECT-Home

d Barbervax® (http://barbervax.com.au/)e (http://shiny.math.uzh.ch/user/furrer/shinyas/shiny-

eggCounts/; https://mdenwood.shinyapps.io/fecrt_bnb/)

References

1. Bassetto CC, et al. Trials with the Haemonchus vaccine, Barbervax((R)), in ewes and lambs in a tropical environment: Nutrient supplementation improves protection in periparturient ewes. Vet Parasitol 2018; 264:52-57.2. Brown DJ, Fogarty NM. Genetic relationships between internal parasite resistance and production traits in Merino sheep. Anim Production Sci 2017; 57:209-215.3. Burke JM, et al. Effect of copper oxide wire particles dosage and feed supplement level on Haemonchus contortus infection in lambs. Vet Parasitol 2004; 123:235-243.4. Burke JM, Morrical D, Miller JE. Control of gastrointestinal nematodes with copper oxide wire particles in a flock of lactating Polypay ewes and offspring in Iowa, USA. Vet Parasitol 2007; 146: 372-375.5. Burke JM, et al. Using copper oxide wire particles or Sericea lespedeza to prevent peri-parturient gastrointestinal nematode infection in sheep and goats. Livestock Sci 2010; 132:13-18.6. Burke JM, et al. Examination of commercially available copper oxide wire particles in combination with albendazole for control of gastrointestinal nematodes in lambs. Vet Parasitol 2016; 215:1-4.7. Burke JM, Miller JE. Sustainable approaches to parasite control in ruminant livestock. Vet Clin North Am Food Anim Pract 2020; 36:89-107.8. FDA. New antiparasitic drugs needed for sheep and goats. 2019 [cited 2020; Available at: https://www.fda.gov/animal-veterinary/safety-health/new-antiparasitic-drugs-needed-sheep-and-goats.

196

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Dr. D

on W

illia

ms,

Ada

, O

K,

pres

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ABP

; Dr

. Joe

Kna

ppen

berg

er,

Ola

the,

KS,

pre

side

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A;

Dr. R

. A. /

vie,

Fol

lett,

Tex

as, p

resi

dent

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ct o

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BP;

and

Dr.

John

B.

Her

rick,

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es,

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A Dr

. /vi

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, Pur

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Boa

rd o

f Dir

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rs

mee

ting.

15

© Copyright American Association of Bovine Practitioners; open access distribution.

254 AABP ANNUAL CONFERENCE PROCEEDINGS — VOL. 53 — NO. 2 — SEPTEMBER 2020

9. Fontenot ME, et al. Efficiency of feeding Duddingtonia flagrans chlamydo-spores to grazing ewes on reducing availability of parasitic nematode larvae on pasture. Vet Parasitol 2003; 118:203-213.10. Halachmi I, et al. Smart animal agriculture: Application of real-time sensors to improve animal well-being and production. Annu Rev Anim Biosci 2019; 7:403-425.11. Healey K, et al. Field evaluation of Duddingtonia flagrans IAH 1297 for the reduction of worm burden in grazing animals: Pasture larval studies in horses, cattle and goats. Vet Parasitol 2018; 258:124-132.12. Hostiou N, et al. Impact of precision livestock farming on work and human-animal interactions on dairy farms. A review. Biotechnologie, Agrono-mie, Société et Environnement 2017. 21.13. Kabagambe EK, et al. Attempts to control haemonchosis in grazing ewes by vaccination with gut membrane proteins of the parasite. Vet Parasitol 2000; 92:15-23.14. Kaplan RM, Vidyashankar AN. An inconvenient truth: Global worming and anthelmintic resistance. Vet Parasitol 2012; 186:70-78.15. Kearney PE, et al. The ‘Toolbox’ of strategies for managing Haemonchus contortus in goats: What’s in and what’s out. Vet Parasitol 2016; 220:93-107.16. Lange KC, et al. Effect of sericea lespedeza (Lespedeza cuneata) fed as hay, on natural and experimental Haemonchus contortus infections in lambs. Vet Parasitol 2006; 141:273-278.17. Learmount J, et al. Three-year evaluation of best practice guidelines for nematode control on commercial sheep farms in the UK. Vet Parasitol 2016; 226:116-123.18. McLeod RS. Costs of major parasites to the Australian livestock industries. Int J Parasitol 1995; 25: 1363-1367.19. Moore DA, et al. The effects of feeding sericea lespedeza hay on growth rate of goats naturally infected with gastrointestinal nematodes. J Anim Sci 2008; 86:2328-2337.20. Pena M, et al. Evaluation of Duddingtonia flagrans in reducing infec-tive larvae of Haemonchus contortus in feces of sheep. Vet Parasitol 2002; 103:259-265.

21. Rojas-Downing MM, et al. Climate change and livestock: Impacts, adapta-tion, and mitigation. Climate Risk Management 2017; 16:145-163.22. Shaik SA, et al. Sericea lespedeza hay as a natural deworming agent against gastrointestinal nematode infection in goats. Vet Parasitol 2006; 139:150-157.23. Smith WD. Development of a commercial vaccine for Haemonchus con-tortus, the barber’s pole worm. Final report. Meat & Livestock Australia 2014.24. Spickett A, et al. Tactical treatment with copper oxide wire particles and symptomatic levamisole treatment using the FAMACHA((c)) system in indigenous goats in South Africa. Vet Parasitol 2012; 184:48-58.25. Terrill TH, et al. Experiences with integrated concepts for the control of Haemonchus contortus in sheep and goats in the United States. Vet Parasitol 2012; 186:28-37.26. Thornton PK. Livestock production: Recent trends, future prospects. Philos Trans R Soc Lond B Biol Sci 2010; 365:2853-2867.27. Vatta AF, et al. The potential to control Haemonchus contortus in indig-enous South African goats with copper oxide wire particles. Vet Parasitol 2009; 162:306-313.28. Vercruysse J, et al. Control of helminth ruminant infections by 2030. Parasitol 2018; 145:1655-1664.29. Vineer H, et al. Reduced egg shedding in nematode-resistant ewes and projected epidemiological benefits under climate change. Intl J Parasitol 2019; 49.30. Vineer H. What modeling parasites, transmission, and resistance can teach us. Vet Clin North Am Food Anim Pract 2020; 36:145-158.31. Waghorn TS, et al. Efficacy of the nematode-trapping fungus Duddingtonia flagrans against three species of gastro-intestinal nematodes in laboratory faecal cultures from sheep and goats. Vet Parasitol 2003; 118:227-234.

196

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d AV

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Chi

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. 24

-26,

196

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ght:

Dr. D

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Irw

in

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KS;

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f Dir

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rs

mee

ting.

15

© Copyright American Association of Bovine Practitioners; open access distribution.