Teladorsagia circumcincta in Sheep: Abomasal Parasitism, Anthelmintic Resistance, and Integrated Control in Temperate Regions

Introduction

Teladorsagia circumcincta (formerly Ostertagia circumcincta) is a highly prevalent abomasal nematode of sheep in temperate regions worldwide [1, 2, 3]. Infection with this parasite is a major cause of production loss, reduced weight gain, and impaired wool growth, particularly in growing lambs and periparturient ewes [1, 2, 65]. The parasite induces a protein-losing gastropathy characterised by abomasal mucosal inflammation, epithelial hyperplasia, and altered gastric function [4, 5, 6, 68]. Widespread and increasing anthelmintic resistance (AR) in T. circumcincta populations has made sole reliance on pharmacological control unsustainable [7, 55, 77, 83, 107]. This article provides a detailed review of T. circumcincta biology, host pathogen interactions, the molecular basis of AR, and the components of integrated parasite management (IPM) programmes applicable to temperate sheep flocks.

Life Cycle and Epidemiology

Teladorsagia circumcincta follows a direct life cycle typical of trichostrongylid nematodes [1, 65]. Adult worms reside in the abomasal mucosa, where females produce eggs that are shed in faeces [1, 68]. Under favourable moisture and temperature conditions (typically 10 to 20 degrees Celsius in temperate climates), eggs develop through first-stage (L1) and second-stage (L2) larvae to the infective third-stage (L3) on pasture [65, 82]. The pre-parasitic development time is temperature-dependent, with L3 appearing on herbage within one to three weeks. Infective L3 are ingested by grazing sheep, exsheath in the rumen, and penetrate the abomasal mucosa, where they moult to fourth-stage larvae (L4) and then to adults, emerging onto the mucosal surface approximately 18 to 21 days after ingestion [1, 4]. A proportion of ingested L3 may undergo hypobiosis (arrested development) as early L4 within the gastric glands, a phenomenon that enables overwintering on pasture in temperate zones and contributes to the spring rise in pasture contamination [65, 82]. The epidemiology of T. circumcincta is influenced by climate, grazing management, and host immunity [8, 65, 76]. In temperate regions, peak pasture larval counts typically occur in late spring and early autumn, with a mid-summer depression due to desiccation. Co-infections with other abomasal nematodes such as Haemonchus contortus and Trichostrongylus axei are common and may influence parasite community dynamics [8, 76].

Abomasal Pathogenesis and Host Parasite Interactions

Adult and larval T. circumcincta induce a proliferative abomasitis characterised by the elevation of abomasal pH, loss of plasma protein into the gut lumen, and disruption of normal gastric secretory functions [4, 5, 68]. The parasites secrete a range of excretory/secretory (E/S) products that include proteases, glycosidases, and immunomodulatory molecules [3, 9, 10, 57, 58, 62, 78]. These E/S products directly damage gastric epithelial cells, increase mucosal permeability, and stimulate a host inflammatory response [9, 62, 79]. Histochemical studies have demonstrated alterations in abomasal mucin composition, including depletion of neutral mucins and increased expression of acidic mucins, which likely facilitates parasite establishment [4, 5]. Infection induces a strong local T helper 2 (Th2) response, with elevated expression of interleukin-4 (IL-4), IL-5, and IL-13 in the abomasal lymph node and mucosa [11, 12, 13, 14, 15, 52, 67]. Mast cell hyperplasia, eosinophil infiltration, and increased local IgA and IgE production are hallmarks of the immune response [16, 13, 17, 66, 75]. Despite this, immunity develops slowly and is often incomplete, particularly in young lambs and during the periparturient period [2, 18, 19, 20, 53, 59, 61, 70, 71, 74]. Regulatory T cell responses and parasite-driven immunosuppression via E/S products, including a calcium-activated apyrase, contribute to the failure of sterile immunity [21, 22, 10]. Transcriptomic studies have identified a suite of long non-coding RNAs, cytokines, and MHC class II genes (e.g., the DRB1*1101 allele) associated with differential resistance between breeds and individuals [23, 24, 11, 12, 25, 26, 27, 14, 28, 29, 30]. For example, Canarian sheep breeds show variability in response, with resistance linked to earlier and stronger humoral responses [2, 16]. Recombinant vaccine candidates targeting larval E/S proteins such as activation-associated secreted proteins (ASPs) and cathepsin F have shown partial protection in experimental challenges, but commercial vaccines are not yet available [1, 16, 31, 32, 33, 58].

Anthelmintic Resistance Mechanisms

Resistance to all major anthelmintic classes has been reported in T. circumcincta populations [7, 55, 77, 83, 107, 121]. The principal mechanisms parallel those described in H. contortus and other strongly nematodes [83, 93, 110]. For benzimidazoles (BZ), single nucleotide polymorphisms (SNPs) in the beta-tubulin isotype 1 gene at codons 167, 198, and 200 cause reduced drug binding [83, 93, 110]. While much of the literature has focused on H. contortus [83, 110], similar mutations have been identified in T. circumcincta isolates [7]. Resistance to macrocyclic lactones (MLs; ivermectin, moxidectin) is believed to involve multiple genes, including P-glycoprotein efflux transporters and altered glutamate-gated chloride channel subunits [107, 133]. The polygenic nature of ML resistance makes molecular diagnosis more complex than for BZ resistance [107, 133]. A triple combination of derquantel and abamectin, as well as eprinomectin formulations, remain effective against some resistant populations, but treatment failures have been documented [7, 55, 64, 135]. Levamisole resistance is less prevalent but exists, often mediated by altered nicotinic acetylcholine receptors [7, 102]. The widespread nature of multi-drug resistance in temperate flocks necessitates routine faecal egg count reduction tests (FECRT) to guide anthelmintic choice [7, 55, 77]. Decision support tools incorporating on-farm FECRT data and body condition scoring can help target treatments to animals most likely to benefit, thereby reducing selection pressure for AR [109, 130].

Diagnostic Approaches

Diagnosis of T. circumcincta infection relies on a combination of clinical signs, abomasal histopathology, and parasitological methods [1, 4, 5, 130]. Faecal egg counts using the modified McMaster technique or more sensitive flotation methods are the mainstay for quantifying egg excretion and monitoring treatment efficacy [17, 7, 109, 130]. Speciation of strongyle eggs requires larval culture and identification of third-stage larvae based on morphological features, or molecular methods such as species-specific PCR or high-resolution melt analysis [23, 24, 34, 22, 57]. Enzyme-linked immunosorbent assays (ELISAs) that detect anti-T. circumcincta IgA in serum or milk can provide a proxy measure of parasite exposure and are useful for epidemiological surveys [34, 17, 33]. Coproantigen tests and pooled PCR approaches, similar to those developed for Fasciola hepatica, are being explored but are not yet commercially available for this species [34, 17, 86]. Accelerometer-based early detection of declining health in parasitised lambs has been evaluated as a non-invasive screening tool.

Integrated Control in Temperate Regions

Sustainable management of T. circumcincta requires integrated parasite control (IPM) combining targeted selective treatment (TST), grazing management, nutritional optimisation, and, where feasible, biological control [1, 35, 19, 54, 59, 61, 70, 72, 90, 92, 114, 122]. Anthelmintic use should be based on FECRT results and reserved for animals with high FECs or poor body condition [7, 109]. Leaving a proportion of the flock untreated (e.g., 10-20% of the best-performing animals) preserves a refugia of susceptible parasites and delays AR development [7, 109]. Grazing strategies include rotational grazing, mixed or alternate grazing with cattle, and extended rest periods that allow pasture larval burdens to decay. Forage crops with anthelmintic properties, such as chicory (Cichorium intybus) and sainfoin (Onobrychis viciifolia), contain condensed tannins (CTs) that reduce larval establishment and faecal egg output [36, 54, 56, 69, 72]. In vitro studies have shown that CTs inhibit L3 attachment to abomasal explants. Protein supplementation, particularly during the periparturient period, improves the capacity of ewes to mount effective immune responses and reduces the peri-parturient rise in egg excretion [19, 53, 59, 61, 70, 74]. Phytohaemagglutinin lectin supplementation has demonstrated direct anthelmintic effects in vivo [35]. Copper oxide wire particles, though less studied for T. circumcincta than for H. contortus, may provide adjunct control in some systems. Fungal biocontrol agents such as Duddingtonia flagrans are effective at reducing larval survival on pasture but are not yet widely adopted in temperate sheep enterprises [113, 122]. The decision framework for integrated control is illustrated in Figure 1.

graph TD
 A[Annual FECRT for each anthelmintic class] --> B{Resistance detected?}
 B -->|Yes| C[Switch to alternative effective class]
 B -->|No| D[Maintain current product for TST]
 C --> E[Refugia-based TST using body condition and FEC]
 D --> E
 E --> F[Implement grazing management]
 F --> G[Rotational grazing / mixed stocking with cattle]
 G --> H["'Consider bioactive forages (chicory, sainfoin')"]
 H --> I[Optimise protein nutrition, especially periparturient]
 I --> J[Monitor FEC and production quarterly]
 J --> A

Figure 1. Decision tree for integrated control of Teladorsagia circumcincta in temperate sheep flocks, combining diagnostic surveillance, targeted selective treatment, grazing strategies, and nutritional support.

Conclusion

Teladorsagia circumcincta remains a dominant abomasal parasite of sheep in temperate climates, imposing substantial production losses and welfare concerns. The parasite has evolved sophisticated mechanisms to evade host immunity and resist multiple anthelmintic classes. A paradigm shift from routine anthelmintic dosing to evidence-based, integrated management is essential. Routine diagnostic monitoring, adoption of refugia-based treatment protocols, strategic grazing, and use of bioactive forages and nutritional interventions can slow AR development and sustain productivity. Further research into vaccine development and the molecular basis of resistance will be critical for long-term control.

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