Gastrointestinal Nematodes in Sheep: Epidemiology, Clinical Signs, and Control

Introduction

Gastrointestinal nematodes (GINs) represent a major constraint to sheep production worldwide, causing substantial economic losses through reduced weight gain, impaired reproductive performance, increased mortality, and costs associated with treatment [1, 2]. The term "worms sheep get" encompasses a diverse array of parasitic nematodes that inhabit the abomasum, small intestine, and large intestine. The most economically relevant genera include Haemonchus contortus, Teladorsagia circumcincta, Trichostrongylus spp., Nematodirus spp., Cooperia spp., Oesophagostomum spp., Chabertia ovina, and Bunostomum spp. [3, 30]. In a comprehensive abattoir survey in central Ethiopia, five genera were identified, with Haemonchus (33.3%) and Trichostrongylus (26.7%) predominating [31]. Similarly, a Ukrainian study of 710 sheep detected 15 nematode species from 12 genera, with H. contortus (61.97% prevalence), O. circumcincta (59.58%), and T. colubriformis (57.35%) being the most prevalent [3]. These parasites typically coexist as mixed-species communities; in infected sheep, 99.12% harboured coinfections, often comprising five to seven species simultaneously [3].

The life cycle of most GINs is direct. Adult females deposit eggs in the gastrointestinal tract, which are passed in faeces. Under favourable environmental conditions (temperature, moisture), eggs hatch into first-stage larvae (L1), moult to L2, and then to infective third-stage larvae (L3) that migrate onto herbage. Sheep ingest L3 during grazing, and larvae exsheath and develop to adults in the target organ [4, 34]. The prepatent period ranges from approximately 14 days for Trichostrongylus spp. to 21 days for Nematodirus spp. [4]. Seasonal variation in larval availability is driven by climate; for example, in West Java, exposure of tracer sheep to T. colubriformis was higher during the dry season, whereas Oesophagostomum columbianum peaked in the wet season [34].

Epidemiology

Global prevalence of GIN infections in sheep remains high. In Ordos, China, a survey of 9622 faecal samples revealed 38.84% positivity in sheep, with significantly lower rates in cattle (4.48%) [5]. In Ukraine, 79.58% of examined sheep were infected [3]. In Dabat district, Northwest Ethiopia, 57.5% of smallholder sheep were positive, with mean faecal egg count (FEC) of 517.5 eggs per gram (EPG) [31]. The infection intensity varied: 55.1% were mild (<500 EPG), 30.4% moderate (500–1500 EPG), and 14.6% heavy (>1500 EPG) [31].

Epidemiological patterns are influenced by grazing management, stocking density, and climatic conditions. The periparturient rise (PPR) in FEC in ewes is a well-documented phenomenon that contaminates pastures for lambs [6, 7]. The relative maturity of the host immune response also affects susceptibility; young lambs are most vulnerable, while adult ewes develop partial immunity after repeated exposure [6, 8]. However, genetic variation in resistance is substantial, with heritability of FEC estimated globally at 0.25 (95% CI 0.22–0.27) [9]. Breeds such as Santa Inês and Morada Nova in Brazil exhibit variable resistance, and genomic prediction using parametric models (GBLUP, BayesA, BayesB, BLASSO) achieves moderate to high accuracy for FEC (0.646–0.793) [10]. Genome-wide association studies in Corriedale sheep have identified significant regions on chromosomes 1, 3, 7, 12, 19, and 24, with candidate genes including TLR5, TLR9, LEPR, and TIMP3 [11].

Clinical Signs and Pathology

The clinical manifestations of GIN infection range from subclinical production loss to acute disease and death. Haemonchus contortus, the barber’s pole worm, is a blood-feeding abomasal nematode that causes anaemia, hypoproteinaemia, submandibular oedema (bottle jaw), and weakness [12, 31]. Teladorsagia circumcincta and Trichostrongylus spp. induce abomasitis and enteritis, leading to inappetence, diarrhoea, weight loss, and reduced wool growth [6, 30]. Nematodirus battus (spring outbreaks in lambs) and Bunostomum trigonocephalum (hookworm) cause similar enteropathic signs [4, 30].

Morbidity parameters such as packed cell volume (PCV), total plasma protein (TPP), body condition score (BCS), and FAMACHA eye colour score are routinely used to assess disease severity [7, 31]. In a study in Ethiopia, FEC was positively correlated with FAMACHA score and negatively correlated with BCS and PCV [31]. The FAMACHA system, which scores anaemia on a 1–5 scale, has high diagnostic accuracy for Haemonchus infection and is widely recommended as a targeted selective treatment (TST) tool [12, 7]. In Santa Inês sheep, FAMACHA scores in the morning ranged from 2.45 to 2.91 across categories, with lactating ewes showing higher scores [7].

Copper oxide wire particles (COWP) have been used as an adjunct therapy to reduce H. contortus burdens, likely through copper ion release in the abomasum that kills adult worms [32]. However, COWP efficacy is variable and requires further validation.

Diagnostics

Accurate diagnosis of gastrointestinal nematode infections in sheep relies on both traditional and molecular methods.

Faecal egg count (FEC) using the modified McMaster technique or FLOTAC/Mini-FLOTAC is the cornerstone for quantifying infection intensity and monitoring treatment efficacy [5, 13, 14]. FLOTAC techniques provide higher sensitivity, especially for low egg counts [13, 15].

Faecal egg count reduction test (FECRT) is the standard method for detecting anthelmintic resistance (AR). The World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines recommend calculating percentage reduction using pre- and post-treatment FEC, with 95% confidence intervals [16, 15]. Several calculation formulae exist, including RESO and eggCounts, which can yield different resistance frequencies depending on whether an untreated control group is included [15].

Coproculture allows identification of third-stage larvae to genus level. Genera such as Haemonchus, Trichostrongylus, Teladorsagia, Cooperia, Oesophagostomum, and Chabertia can be differentiated morphologically [3, 17].

Molecular diagnostics have revolutionised GIN detection and quantification. Droplet digital PCR (ddPCR) targeting the internal transcribed spacer 2 (ITS-2) region of ribosomal DNA allows absolute quantification and differentiation of Haemonchus, Teladorsagia, and Trichostrongylus in larval cultures [14]. ddPCR has high linearity and reproducibility, comparable to real-time qPCR, and is useful for faecal egg count reduction tests [14]. In Swedish studies, ddPCR on coprocultures detected resistance-associated larval DNA even when conventional FECRT indicated susceptibility, highlighting its sensitivity [16].

ELISA for detecting anti-parasite IgA or IgE in serum or saliva provides measures of host immune response. Salivary IgA has been correlated with FEC and may serve as a non-invasive indicator of resistance [18, 33]. Genetic correlations between immune markers and performance traits are unfavourable, suggesting that selection solely for enhanced IgA may reduce productivity [9].

FAMACHA chart is a practical on-farm tool for diagnosing anaemia and guiding anthelmintic treatment decisions [12, 7].

The diagnostic workflow can be summarised as follows:

flowchart TD
    A[Faecal sample from sheep], > B{FEC by McMaster/FLOTAC}
    B, >|EPG ≥ threshold| C[Consider treatment based on clinical signs and FAMACHA]
    B, >|EPG low| D[Monitor and implement targeted selective treatment]
    C, > E[Perform FECRT 10–14 days post-treatment]
    E, > F{Reduction ≥95%?}
    F, >|Yes| G[Effective drug; continue rotation]
    F, >|No| H[Suspected resistance; confirm with coproculture / ddPCR]
    H, > I[Identify resistant genera]
    I, > J[Switch to alternative anthelmintic class or combination therapy]
    D, > K[Incorporate genetic selection for resistance]
    K, > A

Treatment and Anthelmintic Resistance

The primary strategy for controlling GINs has been administration of broad-spectrum anthelmintics from three main classes: macrocyclic lactones (ivermectin, moxidectin, eprinomectin), benzimidazoles (albendazole, fenbendazole, oxfendazole), and imidazothiazoles (levamisole). Additionally, the amino-acetonitrile derivative monepantel and the salicylanilide closantel (primarily for Haemonchus) are available [19, 20].

However, AR has become a global crisis. Resistance has been reported to all major classes, often with multiple resistance on the same farm. In the Netherlands, 73.3% of flocks showed resistance to oxfendazole, 78.3% to ivermectin, and 46.9% to moxidectin, with 60% resistant to closantel mainly due to H. contortus involvement [19]. In Sweden, 77% of tested groups had reduced ivermectin efficacy and 37% had benzimidazole resistance; multiple resistance was present on 30% of farms [16]. In southern Italy, resistance to albendazole and macrocyclic lactones was documented in two of ten farms, although most farms remained susceptible [13].

In Mexico, a review reported resistance to three anthelmintic families, with Haemonchus and Teladorsagia most commonly resistant [21]. In the Yucatán peninsula, ivermectin resistance was detected in 100% of farms in Campeche and 92.9% in Yucatán, while levamisole resistance was 44.4% and 60%, respectively [15]. In Brazil, monepantel efficacy was only 2.82% on one farm, demonstrating resistance even to newer drugs [20]. In Sudan, ivermectin resistance in H. contortus was confirmed experimentally, with reduced efficacy in sheep and goats [35]. Under mountain farming conditions in Italy, AR to macrocyclic lactones and benzimidazoles was widespread, with Teladorsagia and Trichostrongylus surviving treatment [17].

Alternative and complementary treatments have been investigated to reduce reliance on synthetic anthelmintics. Essential oils from Origanum vulgare, Thymus vulgaris, Satureja montana, and Foeniculum vulgare showed in vitro activity against GIN eggs, with carvacrol and thymol identified as active compounds; however, in vivo efficacy was modest (~25% faecal egg count reduction) [1]. Aqueous extracts from Punica granatum (pomegranate) macerate reduced FEC by about 50% in naturally infected sheep in Italy, offering a sustainable alternative [2]. Piper cubeba fruit extract and its lignans (cubebin, dihydrocubebin, hinokinin) demonstrated high ovicidal and larvicidal activity in vitro [22]. Caryocar brasiliense extract also showed efficacy [23]. These phytotherapeutics may help slow the progression of AR, but require further in vivo validation.

Control Strategies

Integrated control of GINs in sheep requires a multifaceted approach that combines pasture management, grazing practices, genetic selection, and targeted anthelmintic use.

Targeted selective treatment (TST) involves treating only those animals that are most affected, based on FEC, FAMACHA, or weight gain, rather than the entire flock. This maintains a refugia of susceptible parasites in the untreated portion, diluting resistant alleles [4, 12, 7]. In Santa Inês sheep, TST using FAMACHA and FEC reduced anthelmintic usage while maintaining performance [7]. The Morada Nova lamb study showed that routine treatment (every 42 days) improved economic returns but accelerated resistance, making it unsustainable [24]. TST struck a balance.

Pasture management includes alternating grazing between sheep and cattle or with non-ruminant species, resting pastures, and avoiding overstocking [4]. Since most GINs are host-specific, cross-grazing reduces larval contamination for sheep.

Genetic selection for resistance to GINs is feasible. Heritability of FEC is moderate (0.25), and selection can reduce FEC by half in one generation [9, 8]. Genomic prediction using GBLUP or Bayesian methods can accelerate genetic gain [10, 11]. However, selection for enhanced immune markers (IgA, IgE) may negatively affect production traits [9, 33]. Interaction networks and pathway analysis have identified biological processes involved in resistance [25].

Nutritional supplementation can improve resilience. Sheep with higher protein intake better tolerate infection and demonstrate stronger immune responses [6]. Copper oxide wire particles reduce Haemonchus burdens [32].

Phytotherapy using bioactive forages (e.g., sericea lespedeza) or plant extracts with condensed tannins can reduce FEC and larval development [12, 26]. The "art of war" concept in tropical systems advocates using multiple low-cost strategies simultaneously [12].

An integrated control programme should be tailored to farm-specific conditions, as each operation has unique parasite epidemiology and management constraints [4].

Conclusion

Gastrointestinal nematodes remain a persistent threat to sheep health and productivity worldwide. Understanding the epidemiology of worms sheep get, including seasonal transmission, host immunity, and genetic resistance, is essential for effective management. The progressive escalation of anthelmintic resistance demands a shift from routine blanket treatment to evidence-based integrated control: accurate diagnosis using FEC and molecular tools, TST guided by FAMACHA and FEC, genetic selection for resistance, pasture rotation, and judicious use of synthetic and natural anthelmintics. Only through such multifaceted approaches can producers sustain profitable and ethical sheep production.

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