Novel Methods for Sustainable Control of Gastrointestinal Nematodes in Small Ruminants

Final Report for LS01-124

Project Type: Research and Education
Funds awarded in 2001: $12,600.00
Projected End Date: 12/31/2005
Region: Southern
State: Georgia
Principal Investigator:
Thomas Terrill
Fort Valley State University
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Project Information

Abstract:

A team of researchers, extension specialists, and producers from FL, GA, AL, LA, AR, the USVI, Denmark, and New Zealand met for two planning workshops during June and August, 2001, resulting in development of a research and extension program documenting prevalence of anthelmintic resistance in small ruminants, preserving the efficacy of existing chemical anthelmintics, and developing and testing alternative, non-chemical parasite control methodologies while widely disseminating findings to clientele groups through producer workshops. The Southern Consortium for Small Ruminant Parasite Control (SCSRPC.org) was created as a result of the cooperative research and extension started with this planning grant.

Project Objectives:
  1. 1. To assemble a multi-disciplinary, multi-institution team of researchers, extension personnel, producer organization leaders, and farmers to discuss, prioritize, and plan a field-based research program for inclusion of biological control of small ruminant GINs using nematode-trapping fungi as a integrated component of a sustainable GIN control program for the southeastern US.

    2. To develop an education and outreach plan to effectively share research results and prepare informational material for appropriate clientele groups throughout the southeastern US.

    3. To develop a full proposal for submission to the Southern Region SARE Program in 2001.

Introduction:

Problem: Production of small ruminants (sheep and goats) is an attractive enterprise for livestock producers in the southeastern United States (US) due to the relatively low cost of breeding stock and high ethnic demand for small ruminant meat and milk products (Glimp et al., 1986). In addition, there are abundant supplies of forage and browse in the Southeast that would support greatly increased small ruminant production. There are approximately 150 million Ha of non-federal agricultural or rural land classified as pasture, range, forest, or marginal cover that have potential to be utilized as forage for small ruminants in this area (Fernandez, 1994). Despite increased demand for chevon and mutton and ample forage and browse resources, growth of the small ruminant industry in the Southeast has been very slow. A major constraint to economic small ruminant production in this region has been monetary losses due to infection with gastrointestinal nematodes (GINs). Economic losses result from decreased animal productivity, cost of chemical anthelmintics, and death of infected animals. The major GIN affecting small ruminants in the Southeast is the bloodworm (Haemonchus contortus). Haemonchosis, caused by the bloodsucking activity of H. contortus in the abomasum, can result in severe anemia and death losses, particularly in young kids and lambs (Miller, 1996; Williams, 1981). The environment in the southeastern US (warm and moist), is ideal for the survival and growth of H. contortus larvae on pasture. And, with only a few weeks life cycle from egg to infective larvae (on pasture) to mature, egg-laying adult (in host animal), parasite numbers on pasture can rapidly build to dangerous levels. Once pastures are contaminated with infective larvae, it is notoriously difficult to reduce the parasite challenge facing grazing ruminants.
Conventional methods of GIN control in small ruminants include use of anthelmintics and strategic pasture management, but since the use of anthelmintics is easy, this has led to over-dependence on these drugs by producers (Miller, 1996). Overuse of anthelmintics can lead to an increase in the incidence of anthelmintic resistance in GINs of sheep and goats. Recent reports from Virginia (Zajac and Gipson, 2000), Georgia (Samples et al., 2000), and Texas (Miller and Craig, 1996) indicate that anthelmintic resistance is an emerging problem in the US. Samples et al (2000) reported anthelmintic resistance in GINs of goats in Georgia to drugs from all three major classes of anthelmintics. Because of the substantial costs associated with developing new drugs and the relatively small market for these drugs in small ruminants, it is unlikely that any new classes of anthelmintics will be developed for use in small ruminants in the foreseeable future (Geary et al., 1999). In addition, greater public demand for chemical residue-free commodities and concerns over environmental impact of excreted anthelmintics (particularly ivermectin) has increased pressure to find alternatives to anthelmintic control of GINs in livestock.

Rationale: Because of the high fecundity of H. contortus, and ideal environmental conditions for rapid pasture contamination with this parasite and other small ruminant GINs in the Southeast, no single strategy is likely to provide a sustainable GIN control program for this area. Attempts to do this with anthelmintics only has led to the problems described previously. We propose to use an integrated approach to GIN control for small ruminants, combining limited, strategic use of anthelmintics to remove adult worms from the animal, and pasture management and biological control to reduce parasite larval numbers on pasture. Controlling parasite larvae on the pasture is a more sustainable approach to GIN control than repeated treatments to remove adult parasites from the host animal. Thus, our principal focus will be to test the field-applicability of biological control using nematode-trapping fungi.

Research with nematode-trapping fungi in Denmark has demonstrated that these fungi, under both experimental and natural conditions, serve as a good biological control agent against the free-living stages of parasitic nematodes in cattle (Larsen et al., 1997), horses (Larsen et al., 1996), and pigs (Nansen et al., 1996). Tests performed in cattle clearly show that although spores from a variety of species of nematode-trapping fungi are able to trap the developing larval stages of the parasitic nematodes in a fecal environment, they are very poor performers with respect to survival through the gastrointestinal (GI) tract (Larsen et al., 1992). However, one fungus, Duddingtonia flagrans, has repeatedly been shown to rank above the rest with respect to survival and subsequent destruction of parasite larvae in the fecal environment. This fungus traps nematode larvae in a three dimensional, sticky network produced on the mycelium, and it produces many resistant, thick-walled resting spores (chlamydospores) within the growing mycelium.
With respect to small ruminants (sheep and goats), only a limited number of in vivo tests with nematode-trapping fungi have been performed worldwide, almost exclusively with sheep. Various passage experiments have confirmed that only a limited number of fungal species are able to survive passage through the GI tract of sheep in sufficiently high number to subsequently reduce the number of developing parasite larvae (Faedo et al., 1997; Waller et al., 1998). In these studies, D. flagrans isolates were again the most consistent performers, showing high survival and reduction capacity. This work has recently stimulated research interest in biological control of small ruminant GINs in the US, at Louisiana State University and Fort Valley State University in Georgia. In a Louisiana sheep study in which various concentrations of D. flagrans spores were fed to mature ewes, concentrations between 105 and 106 spores/kg body weight were over 90% effective at reducing development of parasite larvae in fecal cultures (Pena et al., 1999). A similar test with goats was recently completed in Georgia, and D. flagrans concentrations of 105 to 5 x 105 spores/kg body weight were also over 90% effective in controlling parasitic larvae (Terrill et al., 2000). With respect to testing biological control agents against small ruminant parasitic nematodes in field situations, there has been only relatively limited, but very encouraging data, exclusively with sheep. A study, performed in Denmark, showed that D. flagrans could significantly reduce worm burdens in lambs on pasture, including Ostertagia spp. in the abomasum and Trichostongylus spp in the small intestine (Githigia et al., 1997). By applying mathematical modeling to biological control of worms in sheep it has been suggested that a 75% reduction in larval yield for at least 60 days will provide equal or better control than three doses of anthelmintics in the chosen scenario (Barnes et al., 1995).

Significance: In many countries, particularly those in warm, humid climates, the prevalence of resistance to anthelmintic drugs amongst the major parasites of sheep and goats has reached alarming proportions and threatens the future viability of small ruminant production (Waller, 1999). It has become obvious that reliance on chemical control for parasites is no longer a viable strategy, and new innovative schemes using sustainable approaches and rational drug use must be implemented. Environmentally-safe biological agents for control of GINs in small ruminants can be incorporated into sustainable, forage-based feeding systems and could greatly impact small ruminant production systems in the Southeast and throughout the world. Reduced dependence upon anthelmintics would greatly lower production costs and increase incentive to expand small ruminant industries to meet consumer demands for meat and milk products from goats and sheep.

Cooperators

Click linked name(s) to expand
  • Ray Kaplan
  • Larry Krech
  • Michael Larsen
  • James Miller
  • Jorge Mosjedis
  • Elide Valencia
  • Garry Waghorn
  • Mimi Williams
  • Lisa Williamson

Research

Materials and methods:

Objective 1.

A team of scientists, extension personnel, small ruminant organization leaders, and farmer collaborators from Alabama, Arkansas, Florida, Georgia, Louisiana, the US Virgin Islands, Denmark, and New Zealand met at the Fort Valley State University Agricultural Research Station for two discussion and planning sessions during the summer of 2001 with the goal of developing a full proposal concerning field validation of biological control of small ruminant GINs using nematode-trapping fungi as a component of an integrated, sustainable GIN control program for the southeastern US. At the initial meeting in June, 2001, this group discussed the appropriate scope of the project and evaluated the current team and possible additional disciplines, institutions, and personnel needed to complete the project and disseminate information to appropriate clientele groups. In addition to describing strategies for validating the biological control methodology on-farm, the team will discussed methods of incorporating biological control of GINs as a component of an integrated strategy for controlling small ruminant GINs in the Southeast. This included traditional GIN control measures, such as strategic use of anthelmintics and pasture management, as well as novel approaches, including use of vaccines against GINs, breeding to increase host resistance to GIN infection, and use of condensed tannin-containing plants to control GIN infection. Additional discussions were undertaken on validation of the FAMACHA system of anemia detection (developed in South Africa) for use with sheep and goats in the US. Strategies were also discussed for including an integrated GIN control program as a component of existing and potential small ruminant production and marketing systems in the Southeast.
At the follow-up meeting, which was held at FVSU in August, 2001, university and on-farm research protocols were discussed, prioritized, and planned in detail. For both the June and August meetings, minutes were kept at all of the project team meetings, and copies were distributed to all collaborators to assist in developing the final proposal.

Objective 2.

The team discussed and planned the development of an effective education and outreach program to share university and on-farm field research results with appropriate clientele groups. This plan included producer and county agent training sessions in each state on strategic use of anthelmintics and implementation of control strategies validated by on-farm or university research, providing project updates and results to appropriate clientele groups in a quarterly newsletter published by the Georgia Small Ruminant Research and Extension Center (GSRREC) at FVSU, and development of a project web site.

Objective 3:

Based upon the discussions and planning completed in conjunction with Objectives 1 and 2, a full proposal was developed for submission to the Southern Region SARE Program for the 2002 funding cycle.

Research results and discussion:

The two proposal planning sessions associated with this planning grant resulted in submission of a full SARE Research and Education proposal in 1992 (LS02-141). This proposal, entitled Novel Methods for Sustainable Control of Gastrointestinal Nematodes in Small Ruminants, was funded for $242,677.

Participation Summary

Educational & Outreach Activities

Participation Summary:

Education/outreach description:

A large number of scientific publications, proceedings from scientific presentations, abstracts, magazine articles, newsletters, and other producer-oriented materials have been published by the members of the Southern Corsortium for Small Ruminant Parasite Control (SCSRPC), which grew out of the planning meetings funded by this project. The publications from work planned in sessions supported by this project in which I have been directly involved include:

Refereed Journal Articles

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R. M. Kaplan, J.M. Burke, and J. Mosjidis. 2006. Sericea lespedeza hay as a natural deworming agent against gastrointestinal nematode infection in goats. Vet. Parasitol. (In Press).

Burke JM, Miller JE, Larsen M, Terrill TH. 2005. Interaction between copper oxide wire particles and Duddingtonia flagrans in lambs. Veterinary Parasitology 134:141-146.

Terrill, T.H., M. Larsen, O. Samples, S. Husted, J.E. Miller, R.M. Kaplan, and S. Gelaye. 2004. Capability of the nematode-trapping fungus Duddingtonia flagrans to reduce infective larvae of gastrointestinal nematodes in goat feces in the southeastern United States: dose titration and dose time interval studies. Veterinary Parasitology 120:285-296.

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R.K. Kallu, and J.A. Mosjidis. 2004. Effects of feeding sericea lespedeza hay to goats infected with Haemonchus contortus. South African Journal of Animal Science 34 (1):248-250.

Burke, J.M., J.E. Miller, D.D. Olcott, B.M.Olcott, and T.H. Terrill. 2004. Effect of copper oxide wire particles dosage and feed supplement level on Haemonchus contortus infection in lambs. Veterinary Parasitology 123:235-243.

Kaplan, R.M., J.M. Burke, T.H. Terrill, J.E. Miller, W.R. Getz, S. Mobini, E. Valencia, M.J. Williams, L.H.Williamson, M. Larsen, and A.F. Vatta. 2004. Validation of the FAMACHA© eye color chart for detecting clinical anemia in sheep and goats on farms in the southern United States. Veterinary Parasitology 123:105-120.

Mortensen, L.L., L.H. Williamson, T.H. Terrill, R.A. Kircher, M. Larsen, and R.M. Kaplan. 2003. Evaluation of prevalence and clinical implications of anthelmintic resistance in gastrointestinal nematodes in goats. Journal of the American Veterinary Medical Association 223:495-500.

Terrill, T.H., R.M. Kaplan, M. Larsen, O.M. Samples, J.E. Miller, and S. Gelaye. 2001. Anthelmintic resistance on goat farms in Georgia-Efficacy of anthelmintics against gastrointestinal nematodes in two selected goat herds. Veterinary Parasitology 97:261-268

Proceedings papers

Dykes, G.S., T.H. Terrill, S.A. Shaik, J.E. Miller, B. Kouakou, G. Kannan, J.M. Burke, R.M. Kaplan, and J.A. Mosjidis. 2006. Effect of sericea lespedeza hay on gastrointestinal nematode infection in goats. p. 245-249. Proceedings of the 2006 Conference of the American Forage and Grassland Council, March 10-14, 2006, San Antonio, Texas.

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R.M. Kaplan, J.M. Burke, and J.A. Mosjidis. 2005. Anthelmintic effects of sericea lespedeza hay fed to goats infected with Haemonchus contortus. Proceedings of the XX International Grassland Congress, 26 June – 6 July, 2005, Dublin, Ireland.

Miller, J.E., J.A. Stuedemann, and T.H. Terrill. 2005. Nematode parasites and grazing research. Proceedings of the 59th Southern Pasture and Forage Crop Improvement Conference, 11-13 May 2005, Philadelphia, MS.

Terrill, T.H., and J.E. Miller. 2005. Nematode parasites in small ruminant grazing research: Changing perspectives. Proceedings of the 59th Southern Pasture and Forage Crop Improvement Conference, 11-13 May 2005, Philadelphia, MS.

Extension publications

Shaik, A.S., and T.H. Terrill. 2005. Sericea lespedeza hay: Ready to accept the challenge from Haemonchus contortus. Georgia Small Ruminant Research and Extension Center Newsletter, Winter 2005.

Terrill, T.H. 2004. Nematode wars: FVSU assembles parasite control team. P. 1-2. In Winter 2004 Georgia Small Ruminant Research and Extension Center Newsletter.

Abstracts

Burke, J.M., J.E. Miller, M. Larsen, and T.H. Terrill. 2005. Interaction between copper oxide wire particles (COWP) and Duddingtonia flagrans in hair breed lambs. Abstracts of the Southern Section ASAS Meetings, Little Rock, AR, page 15.

Lange, K., D. Olcott, J.E. Miller, J.A. Mosjidis, T.H. Terrill, and J.M. Burke. 2005. Effect of the condensed tannin-containing forage, sericea lespedeza, fed as hay, on natural and experimental challenge infection in lambs. Abstracts of the Southern Section ASAS Meetings, Little Rock, AR, pages 15-16.

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R.M. Kaplan, J.M. Burke, and J.A. Mosjidis, 2005. Effects of feeding sericea lespedeza hay to goats infected with Haemonchus contortus. Abstracts of the Southern Section ASAS Meetings, Little Rock, AR, page 3.

Kallu, R.K., T.H. Terrill, and J.E. Miller. 2005. Efficacy of copper oxide wire particles against gastrointestinal nematodes of goats. Abstracts of the Southern Section ASAS Meetings, Little Rock, AR, page 4.

Miller, J.E., J.M. Burke, and T.H. Terrill. Effect of 0.5, 1.0, and 1.5 gram copper oxide wire particles on natural infection in lambs. Abstracts of the Southern Section ASAS Meetings, Little Rock, AR, page 15.

Burke, J.M., J.E. Miller, M. Larsen, and T.H. Terrill. 2005. Interaction between copper oxide wire particles (COWP) and Duddingtonia flagrans in hair breed lambs. 4th International Conference on Novel Approaches to the Control of Helminth Parasites of Livestock, 10-12 January, 2005, Merida, Yucatan, Mexico, page 24.

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R.M. Kaplan, J.M. Burke, and J.A. Mosjidis. 2005. Effects of feeding sericea lespedeza hay to goats infected with Haemonchus contortus. 4th International Conference on Novel Approaches to the Control of Helminth Parasites of Livestock, 10-12 January, 2005, Merida, Yucatan, Mexico, page 37.

Lange, K.C., D.D. Olcott, J.E. Miller, J.A. Mosjidis, T.H. Terrill, and J.M. Burke. 2005. Effect of the condensed tannin containing forage, sericea lespedeza, fed as hay, on natural and experimental challenge infection in lambs. 4th International Conference on Novel Approaches to the Control of Helminth Parasites of Livestock, 10-12 January, 2005, Merida, Yucatan, Mexico, page 38.

Shaik, S., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R. Kallu, and J.A. Mosjidis. 2004. Effects of feeding sericea lespedeza hay on goats infected with Haemonchus contortus. Abstracts of the AAVP/ASP/AVMA 2004 Joint Meeting, July 24-28, 2004, Philadelphia, PA., page 40.

Kallu, R, T.H. Terrill, J.E. Miller, S.R. Maddineni, S. Shaik, and J.M. Burke. 2004. Efficacy of copper oxide wire particles against Haemonchus contortus in goats. Abstracts of the AAVP/ASP/AVMA 2004 Joint Meeting, July 24-28, 2004, Philadelphia, PA., pages 40-41.

Kaplan, R.M., J. Neiss, L.H. Williamson, and T.H. Terrill. 2004. Moxidectin resistance in gastrointestinal nematodes of goats in Georgia. Abstracts of the AAVP/ASP/AVMA 2004 Joint Meeting, July 24-28, 2004, Philadelphia, PA., pages 55-56.

Miller, J.E., J.M. Burke, D.D. Olcott, B.M. Olcott, and T.H. Terrill. 2004. Effect of copper oxide wire particle dosage on Haemonchus contortus infection in lambs. Abstracts of the AAVP/ASP/AVMA 2004 Joint Meeting, July 24-28, 2004, Philadelphia, PA., page 50.

Terrill, T.H., J.E. Miller, R.M. Kaplan, M. Larsen, R.A. Kircher, O.M. Samples, and S. Gelaye. 2004. Epidemiology of gastrointestinal nematodes of goats in Georgia. Abstracts of the AAVP/ASP/AVMA 2004 Joint Meeting, July 24-28, 2004, Philadelphia, PA, page 89.

Shaik, S.A., T.H. Terrill, J.E. Miller, B. Kouakou, G. Kannan, R.K. Kallu, and J.A. Mosjidis. 2004. Effects of feeding Sericea lespedeza hay to goats infected with Haemonchus contartus. Abstracts of the Eighth International Conference on Goats, Pretoria, South Africa, page 80.

Mweemba, C., R. Eckhart, G. Kannan, R. A. Kircher, and T.H. Terrill. 2003. Effect of gastrointestinal nematode infection on stress responses in goats. Abstracts of the Thirteenth Biennial Research Symposium of the Association of Research Directors, Inc., Atlanta, GA, page 43.

Galipalli, S., G. Kannan, K.E. Saker, T.H. Terrill, B. Kouakou, S. Gelaye, and K.M. Gadiyaram, 2003. Tasco seaweed extract supplementation increases antioxidant status in stressed goats. Abstracts of the Thirteenth Biennial Research Symposium of the Association of Research Directors, Inc., Atlanta, GA, page 46.

Terrill, T.H., J.E. Miller, M.Larsen, and R.M. Kaplan. 2002. Biological control of gastrointestinal nematodes using nematode-trapping fungi: sheep and goat sutdies from the southeastern US. Proceedings of the 3rd International Conference on Novel Approaches to the Control of Helminth Parasites of Livestock, 1-5 July, 2002, Moredun Research Institute, Edinbrough, Scotland, page 28..

R.M. Kaplan, L.L. Mortensen, L.H. Williamson, T.H. Terrill, M.Larsen, and R. Kircher. 2002. Prevalence of anthelmintic resistance in gastrointestinal nematodes of goats in the southern United States. Proceedings of the 3rd International Conference on Novel Approaches to the Control of Helminth Parasites of Livestock, 1-5 July, 2002, Moredun Research Institute, Edinbrough, Scotland, page 17.

Terrill, T.H., R.M. Kaplan, M. Larsen, and J.E. Miller. 2002. Emerging issues in control of nematode parasites of goats: anthelmintic resistance and biological control using nematophagous fungi. Journal of Animal Science 80 (1):144.

Project Outcomes

Project outcomes:

This planning grant was the spark that initiated formation of the Southern Consortium for Small Ruminant Parasite Control (SCSRPC), which is now recognized as one of the preeminent small ruminant parasitology research and extension groups in the world and includes members from institutions in Georgia, Florida, Alabama, Virginia, Louisiana, Arkansas, Oklahoma, Texas, Puerto Rico, the US Virgin Islands, Denmark, and South Africa. The SARE Research and Education grant that was a direct result of the 2001 planning sessions was funded in 2002, and subsequently, members of the SCSRPC have written six additional successful grants related to this work, including additional SARE R & E and planning grants, as well as a professional development grant. Consortium members have published over 20 refereed journal papers, 15 proceedings papers, and numerous abstracts related to this project since 2001. Since the initial planning grant was funded in 2001, the SCSRPC has held approximately 75 producer or county agent ‘smart drenching’/FAMACHA training sessions (approximately 2000 participants) in 10 states, Puerto Rico, and the US Virgin Islands. Approximately 5000 FAMACHA cards have been sold for direct on-farm use since they were first made available in the US in June 2003. Our Consortium was selected as the sole distributor of these cards in the US by the system’s inventors in South Africa. Our group’s web site (SCSRPC.org) has had over 28,000 hits since its creation in January, 2004.

Farmer Adoption

Approximately 2000 producers have attended Smart Drenching/FAMACHA workshops held by member of the Southern Consortium for Small Ruminant Parasite Control (SCSRPC), the group formed as a result of activities intiated with this planning grant. Approximately 5000 FAMACHA cards have been sold for direct use by producers to reduce their dependency upon chemical anthelmintics for parasite control

Recommendations:

Areas needing additional study

The SARE-supported activities of the Southern Consortium for Small Ruminant Parasite Control has thus far centered primarily on documenting anthelmintic resistance in small ruminants, reducing use of chemical anthelmintics by identification and selected targeting of parasitized animals in the herd or flock using the FAMACHA anemia detection system, and testing of novel, non-chemical control technologies. Additional research is needed in combining these strategies in integrated small ruminant parasite control programs that can be tested on-farm.

Information Products

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.