Abstract
One of the major problems in small ruminant farms is emergence of anthelmintic resistance (AR) to commonly used dewormers. This study investigated AR to gastrointestinal nematodes affecting goats in 27 unorganized farms in three different agro-climatic zones (Cauvery delta zone, high altitude zone and high rainfall zone) of Tamil Nadu, India. Two anthelmintics viz., albendazole (AZ) and levamisole (LEV) were used in this study as per the dose recommended by the manufacturer. Status of AR was detected by using the faecal egg count reduction test. Results revealed the presence of high level of resistance to both AZ and LEV. In the high rainfall and high altitude zones, all the farm flocks were found to be resistant to LEV. In the Cauvery delta zone, 13 farm flocks were resistant and four farm flocks showed suspect resistance to AZ. Fifteen farm flocks showed resistance and two showed suspect resistance to LEV. Further, morphological characterization of the infective larvae derived from faecal cultures indicated that by far the most predominant gastrointestinal nematode species found in goats was Haemonchus contortus.
Keywords: Anthelmintic resistance, Albendazole, Levamisole, Goat, Gastrointestinal nematode, Faecal egg count reduction test, Haemonchus contortus
Introduction
Goat farming is one of the most significant and upcoming livestock enterprises in India and it is considered as the backbone of rural economy. The goat farming plays a major role in making the resource poor farmers self-sufficient in Tamil Nadu. The surging goat population during the last two decades in spite of restriction by few government agencies has made to realise its growth. With a highly fragmented goat population reared along with sheep not much of attention had been paid for deworming of goats. Gastro-intestinal parasitism in goats severely affects the economy of goat farming. Benzimidazoles and levamisole (LEV) have been regularly and widely used in India for controlling parasitic gastroenteritis in goats for the last 2–3 decades. There have been complaints on the failure of these anthelmintics to provide the expected degree of control with regard to parasitic gastroenteritis. The reason for inadequate efficacy of these anthelmintics is frequent and indiscriminate usage that has led to the development of resistance which hampers the effective control of GI nematodes (Yadav et al. 1993). The development of anthelmintic resistance (AR) in gastrointestinal nematodes of small ruminants is of major concern in developing countries of the world like India. The rate at which resistance to additional anthelmintics is being reported in India is alarming, as it narrows the choice of alternative anthelmintics (Yadav 1990; Uppal et al. 1992; Yadav and Uppal 1992). Knowledge about the status of AR and its monitoring becomes a vital component of worm management strategy in order to maintain efficacy of available anthelmintics with simultaneous reduction in the selection pressure in worm population (Várady et al. 2007). Studies on multiple AR status have been mostly done in sheep farm flocks and very less is known about the prevalence of multiple AR in goats in India. Hence, the present study was undertaken to detect the status of AR to commonly used anthelmintics such as Albendazole (AZ) and LEV in 27 unorganized goat farms of three different agro-climatic zones of Tamil Nadu.
Materials and methods
Animals and management
The study was carried out in 27 unorganized goat farm flocks from three different agro-climatic zones of Tamil Nadu namely Cauvery delta zone, high altitude zone and high rain fall zone. Each farm flock consisted of a minimum of 45 goats. The samples were collected from farm flocks maintained in semi intensive system of management with 6–8 h of grazing during the day time and housing overnight in raised floor pens. The animals were offered with limited concentrate feed supplements and ad libitum water.
Faecal egg count reduction test (FECRT)
FECRT was carried out as per the guidelines of World Association for Advancement of Veterinary Parasitology (Coles et al. 1992). The study was carried out in two groups of animals (n = 15) in farm flocks that were treated with the two class of commonly used anthelmintics namely benzimidazole and tetra hydropyrimidines as per the manufacturer recommended dose rates. About 5 g of fresh faecal sample was collected per rectum from each animal on day 0 and 10–14 days post-treatment was placed in pre-labelled zip lock polythene covers and were shipped to the laboratory. Egg counting was done as per modified McMaster technique (MAFF 1989; Coles et al. 1992). Resistance to a particular class of anthelmintic was considered to be present if the percentage reduction in egg count was less than 95 % and also the 95 % confidence level was less than 90 %. If only one of the two criteria was met out, the resistance was classed as suspected. Pre- and post-treatment faecal samples were pooled and subjected to jar method of faecal culture and larvae were identified based on the keys provided by MAFF (1986).
Results
The percentage faecal egg count reduction results are shown in Table 1. The study indicated the presence of high level of resistance to both the anthelmintics viz. AZ and LEV. Out of 27 flocks screened, resistance to AZ was observed in 22 farm flocks (81 %), while LEV resistance was observed in 25 farm flocks (92 %). In addition to this, AZ showed suspect resistance in five farm flocks and LEV showed suspect resistance in two farm flocks. High level of resistance to AZ and LEV was observed in high rain fall zone. All the four farm flocks studied in the high altitude zone were resistant to LEV (100 %) whereas three farm flocks (75 %) were resistant to AZ and one farm flock (25 %) showed suspect resistance to AZ. In Cauvery delta zone, 13 farm flocks (76 %) were resistant to AZ and four (24 %) showed suspect resistance to AZ, while fifteen farm flocks showed resistance (88 %) and two showed suspect resistance (11 %) to LEV. Faecal culture results indicated that Haemonchus contortus was the most predominant species of GI nematode identified in the farm flocks followed by Trichostrongylus spp. Hence, the present study indicated that H. contortus is resistant to both AZ and LEV in the screened goat farm flocks of Tamil Nadu.
Table 1.
Prevalence of AR in goat farms of three different agro-climatic zones of Tamil Nadu
| Zone | Farms | Drugs | Faecal egg count reduction (%FECR) | 95 % confidence limits | Status | |
|---|---|---|---|---|---|---|
| Upper | Lower | |||||
| Cauvery delta | 1 | Albendazole | 87.38 | 94.35 | 71.79 | Resistance |
| Levamisole | 89.94 | 95.98 | 74.85 | Resistance | ||
| 2 | Albendazole | 88.50 | 92.69 | 81.88 | Resistance | |
| Levamisole | 88.85 | 93.54 | 80.75 | Resistance | ||
| 3 | Albendazole | 87.54 | 91.75 | 81.17 | Resistance | |
| Levamisole | 86.39 | 92.12 | 76.78 | Resistance | ||
| 4 | Albendazole | 89.72 | 94.54 | 80.64 | Resistance | |
| Levamisole | 84.12 | 91.14 | 71.49 | Resistance | ||
| 5 | Albendazole | 69.23 | 83.04 | 44.18 | Resistance | |
| Levamisole | 77.97 | 88.87 | 56.39 | Resistance | ||
| 6 | Albendazole | 89.38 | 94.31 | 80.16 | Resistance | |
| Levamisole | 88.64 | 93.63 | 79.74 | Resistance | ||
| 7 | Albendazole | 64.71 | 78.63 | 41.71 | Resistance | |
| Levamisole | 83.45 | 91.11 | 69.23 | Resistance | ||
| 8 | Albendazole | 72.50 | 82.72 | 56.24 | Resistance | |
| Levamisole | 88.07 | 94.35 | 74.79 | Resistance | ||
| 9 | Albendazole | 75.00 | 83.98 | 60.98 | Resistance | |
| Levamisole | 87.50 | 93.48 | 76.03 | Resistance | ||
| 10 | Albendazole | 95.00 | 97.50 | 89.99 | Suspect resistance | |
| Levamisole | 50.85 | 50.85 | 66.37 | Resistance | ||
| 11 | Albendazole | 95.77 | 98.60 | 87.25 | Suspect resistance | |
| Levamisole | 95.95 | 98.65 | 87.79 | Suspect resistance | ||
| 12 | Albendazole | 56.25 | 68.59 | 39.05 | Resistance | |
| Levamisole | 57.45 | 65.83 | 47.01 | Resistance | ||
| 13 | Albendazole | 95.60 | 98.51 | 86.96 | Suspect resistance | |
| Levamisole | 95.18 | 98.16 | 87.37 | Suspect resistance | ||
| 14 | Albendazole | 95.55 | 98.24 | 88.79 | Suspect resistance | |
| Levamisole | 79.45 | 87.94 | 64.98 | Resistance | ||
| 15 | Albendazole | 39.58 | 59.32 | 10.25 | Resistance | |
| High altitude | Levamisole | 50.00 | 63.51 | 31.47 | Resistance | |
| 16 | Albendazole | 49.05 | 63.13 | 29.60 | Resistance | |
| Levamisole | 12.12 | 36.04 | −20.74 | Resistance | ||
| 17 | Albendazole | 28.78 | 46.94 | 4.41 | Resistance | |
| Levamisole | 43.39 | 64.57 | 9.56 | Resistance | ||
| 18 | Albendazole | 72.55 | 91.08 | 15.50 | Resistance | |
| Levamisole | 71.86 | 85.98 | 43.49 | Resistance | ||
| 19 | Albendazole | 92.76 | 96.52 | 84.91 | Suspect resistance | |
| Levamisole | 78.10 | 90.15 | 51.34 | Resistance | ||
| 20 | Albendazole | 83.33 | 90.84 | 69.67 | Resistance | |
| Levamisole | 88.56 | 92.69 | 82.08 | Resistance | ||
| 21 | Albendazole | 84.64 | 91.27 | 72.96 | Resistance | |
| Levamisole | 88.47 | 93.01 | 81.03 | Resistance | ||
| High rain fall | 22 | Albendazole | 74.74 | 90.71 | 31.29 | Resistance |
| Levamisole | 86.95 | 92.15 | 78.32 | Resistance | ||
| 23 | Albendazole | 75.68 | 93.55 | 8.20 | Resistance | |
| Levamisole | 65.67 | 79.47 | 42.59 | Resistance | ||
| 24 | Albendazole | 58.06 | 86.57 | −30.95 | Resistance | |
| Levamisole | 74.74 | 86.05 | 54.25 | Resistance | ||
| 25 | Albendazole | 74.67 | 82.94 | 62.41 | Resistance | |
| Levamisole | 73.17 | 83.24 | 57.05 | Resistance | ||
| 26 | Albendazole | 73.75 | 85.83 | 51.35 | Resistance | |
| Levamisole | 74.21 | 85.09 | 55.38 | Resistance | ||
| 27 | Albendazole | 57.35 | 78.47 | 15.52 | Resistance | |
| Levamisole | 66.84 | 80.08 | 44.80 | Resistance | ||
Discussion
Multiple AR in GI nematodes has been well documented from all over the world. The incidence of multiple AR in naturally grazing goats was reported in USA (Anne and Terry 2000). The prevalence of resistance to benzimidazole group and LEV in goat farms in Malaysia has also been well documented (Chandrawathani et al. 1999). In India several studies have indicated the presence of multiple AR in sheep (Varshney and Singh 1976; Yadav et al. 1993; Gill 1996; Swarnkar et al. 1999; Dhanalakshmi et al. 2003). Resistance to the commonly used anthelmintics like AZ and LEV in organised farms is well documented in sheep farms of Southern India also. (Jeyathilakan et al. 2003; Arunachalam et al. 2005; Easwaran et al. 2009). Ram et al. (2007) and Laha et al. (1999) reported the less therapeutic efficacy of AZ against GI nematodes of goats. The results of the present study were found to be in accordance with these findings. The GI nematodes of both sheep and goats were resistant to ivermectin and fenbendazole, whereas LEV was still effective in sheep, but not in goats in Kenya as observed by Mwamachi et al. (1995). Resistance to AZ, Ivermectin and morantel in goats has been investigated by Deepa and Devada (2007). The level and type of AR in the gastrointestinal parasites in different farms appeared to be associated with the type and frequency of anthelmintic used and the management practices followed in the farms. The role of management practices and frequent use of anthelmintics in the development of resistance has been well studied (Martin et al. 1982; Prichard 1994). Hence, there is an urgent need to educate the farmers about the problems of development of AR and the ways to control it. Appropriate use of anthelmintics and good management will lead to delay in onset of AR in gastrointestinal nematodes affecting small ruminants.
In conclusion, this study documented the presence of multiple AR in gastrointestinal nematodes of goats of Tamil Nadu.
Acknowledgments
The authors thank the Biotechnology and Biological Sciences Research Council (BBSRC), United Kingdom for funding the present study under CIDLID grant. The authors also thank the faculty of Veterinary University Training and Research Centre, Tiruchirappalli, Thanjavur; field veterinarians from the Department of Animal husbandry, Government of Tamil Nadu. The authors also thank the farmers for their cooperation throughout the study.
References
- Anne MZ, Terry AG (2000) Multiple anthelmintic resistance in a goat herd. Vet Parasitol 87:163–172 [DOI] [PubMed]
- Arunachalam K, Raman M, Jeyathilakan N, Karunanidhi K. Multiple anthelmintic resistance in gastrointestinal nematodes from Mecheri sheep in an organized farm in Tamil Nadu. Indian J Anim Sci. 2005;75:203–205. [Google Scholar]
- Chandrawathani P, Adnan M, Waller PJ. Anthelmintic resistance in sheep and goat farms on Peninsular Malaysia. Vet Parasitol. 1999;82:305–310. doi: 10.1016/S0304-4017(99)00028-X. [DOI] [PubMed] [Google Scholar]
- Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, Waller PJ. World association for the advancement of veterinary parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol. 1992;44:35–44. doi: 10.1016/0304-4017(92)90141-U. [DOI] [PubMed] [Google Scholar]
- Deepa CK, Devada K. Anthelmintic resistance in gastro intestinal nematodes of goats. J Vet Anim Sci. 2007;38:52–54. [Google Scholar]
- Dhanalakshmi H, Jagannath MS, D’souza EP. Multiple anthelmintic resistances in gastrointestinal nematodes of sheep. J Vet Parasitol. 2003;17:89–91. [Google Scholar]
- Easwaran C, Harikrishnan TJ, Raman M. Multiple anthelmintic resistance in gastrointestinal nematodes of sheep in Southern India. Vet Arhiv. 2009;79:611–620. [Google Scholar]
- Gill BS. Anthelmintic resistance in India. Vet Parasitol. 1996;63:173–176. doi: 10.1016/0304-4017(95)00884-5. [DOI] [PubMed] [Google Scholar]
- Jeyathilakan N, Radha G, Gomathinayagam S, John L. Emergence of anthelmintic resistance in nematodes of sheep in Tamil Nadu. J Vet Parasitol. 2003;17:159–160. [Google Scholar]
- Laha R, Hemaprasanth, Harbola PC. Anthelmintic resistance in Pashmina (Cashmere) producing goats in India. Vet Res Commun. 1999;23:187–189. doi: 10.1023/A:1006281702107. [DOI] [PubMed] [Google Scholar]
- MAFF . Ministry of Agriculture, Fisheries and Food Agriculture Development and advisory service manual of veterinary parasitology techniques. London: HMSO; 1986. [Google Scholar]
- Martin PJ, Anderson N, Jarret RG, Brown TH, Ford GE. Effect of a preventive and suppressive control scheme on the development of thiabendazole resistance in Ostertagia spp. Aust Vet J. 1982;58:185–190. doi: 10.1111/j.1751-0813.1982.tb00649.x. [DOI] [PubMed] [Google Scholar]
- Mwamachi DM, Audho JO, Thorpe W, Baker RL. Evidence for multiple anthelmintic resistance in sheep and goats reared under the same management in coastal Kenya. Vet Parasitol. 1995;60:303–313. doi: 10.1016/0304-4017(95)00794-1. [DOI] [PubMed] [Google Scholar]
- Prichard RK. Anthehmintic resistance. Vet Parasitol. 1994;54:259–268. doi: 10.1016/0304-4017(94)90094-9. [DOI] [PubMed] [Google Scholar]
- Ram H, Rasool TJ, Sharma AK, Meena HR, Singh SK. Comparative efficacy of different anthelmintics against fenbendazole-resistant nematodes of Pashmina goats. Vet Res Commun. 2007;31:719–723. doi: 10.1007/s11259-007-0021-8. [DOI] [PubMed] [Google Scholar]
- Swarnkar CP, Singh D, Khan FA, Bhagwan PSK. Multiple anthelmintic resistances in Haemonchus contortus of sheep. Indian J Anim Sci. 1999;63:547–549. [Google Scholar]
- Uppal RP, Yadav CL, Godara P, Rana ZS. Multiple anthelmintic resistance in a field strain of Haemonchus contortus in goats. Vet Res Commun. 1992;16:195–198. doi: 10.1007/BF01839155. [DOI] [PubMed] [Google Scholar]
- Várady M, Cudekova P, Corba J. In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet Parasitol. 2007;149:104–110. doi: 10.1016/j.vetpar.2007.07.011. [DOI] [PubMed] [Google Scholar]
- Varshney TR, Singh YP. A note on development of resistance of Haemonchuscontortus worms against phenothiazine and thiabendazole in sheep. Indian J Anim Sci. 1976;46:666–668. [Google Scholar]
- Yadav CL. Fenbendazole resistance in Haemonchus contortus of sheep. Vet Rec. 1990;126:586. [PubMed] [Google Scholar]
- Yadav CL, Uppal RP. Levamisole-resistant Haemonchus contortus in goats. Vet Rec. 1992;130:228. doi: 10.1136/vr.130.11.228. [DOI] [PubMed] [Google Scholar]
- Yadav CL, Uppal RP, Kalra S (1993) An outbreak of haemonchosis associated with anthelmintic resistance in sheep. Int J Parasitol 23:411–413 [DOI] [PubMed]