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. 2026 Jun 26;58(6):386. doi: 10.1007/s11250-026-05174-8

Preliminary survey of anthelmintic efficacy in selected smallholder sheep and goat flocks in Sarawak, Malaysia

Ali Saidu 1, Bura Thlama Paul 1,2,3,✉, Maria Eva Barudi 1, Faez Firdaus Abdullah Jesse 4, Juriah Kamaludeen 1, Suhaili Mustafa 1, Masnindah Malahubban 1, Ali Hanafiah Hakim 1, Krishnan Nair Balakrishnan 5, Mohd Azmi Mohd Lila 6, Abubakar Abdullahi Biu 7
PMCID: PMC13309397  PMID: 42360630

Abstract

Smallholder sheep and goat production supports rural livelihoods and food security through the provision of meat, milk, hides and skins, employment, and household income in Malaysia. The control of gastrointestinal nematodes (GINs) in sheep and goats relies on routine deworming using albendazole, levamisole, and ivermectin anthelmintics. While these drugs are effective in reducing worm burden and improving animal productivity, prolonged and often indiscriminate use resulted in the emergence of anthelmintic resistance (AHR) in West Malaysia. Despite extensive evidence of AHR in GINs of sheep and goats in various production systems in Peninsular Malaysia, there is a significant knowledge gap regarding the status of anthelmintic efficacy of albendazole and ivermectin in GINs of sheep and goats in Sarawak. In this study, a preliminary experimental trial was conducted to evaluate the in vivo efficacy of albendazole and ivermectin using faecal egg count reduction test (FECRT) based on pre-treatment and post-treatment faecal egg counts conducted 14 days apart according to the updated World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P) guidelines for diagnosing AHR in ruminants. Coprocultures were also prepared from faecal samples collected post treatment to microscopically identify the third stage larvae (L3) of resistant nematodes using standard morphological criteria. The results of FECRT on albendazole showed a 76.8% (90% CI: 69.9–83.8) reduction in pretreatment epg in White dorper sheep (Group D) while ivermectin treatment showed 85.4% (90% CI: 80.8–89.9) in Barbados blackbelly sheep (Group A), 75.8% (90% CI: 65.3–86.3) in White dorper sheep (Group C), and 75.9% (90% CI: 65.7–86.1) in Saanen goats (Group B). Thus, all the treatment groups did not achieve the W.A.A.V.P recommended post treatment FECR for susceptibility (lower 90% CI ≥ 90% and upper 90% CI ≥ 99%) in sheep and goats, which has led us to reject the null hypothesis and conclude anthelmintic failure in GINs of sheep and goats in Sarawak. This study provides the first evidence of anthelmintic failure involving albendazole and ivermectin in sheep and goat farms in Sarawak. Further study using adjusted dose regime is required to clarify the status of ivermectin resistance in goats because metabolic factors rather than resistance may precipitate a lower efficacy when using standard sheep dose in goats. Nonetheless, this work provides preliminary data that lays a solid foundation for designing sustainable helminth control programs to overcome anthelmintic resistance in Sarawak.

Keywords: Albendazole, Ivermectin, Anthelmintic resistance, Gastrointestinal nematodes, Small ruminants, Sarawak

Introduction

Sheep and goat production supports rural economies through the provision of meat, milk, skin, and income for smallholder households (Devendra 2010; Derbib 2021). However, parasitic gastroenteritis (PGE) complex caused by gastrointestinal nematode (GINs) such as Haemonchus contortus, Teladorsagia circumcincta, and Trichostrongylus species (Halliday et al. 2012; Jesse et al. 2019; Arsenopoulos et al. 2021) significantly affects their productivity and survival (Taylor 2012; Ali et al. 2025). PGE is directly associated with anaemia, weight loss, poor growth, and reduced fertility, threatening food security (Geurden et al. 2014; Paul et al. 2020; Hamid et al. 2023; Nolinda et al. 2024).

The control of PGE in ruminants traditionally relies on the use of anthelmintics such as benzimidazoles, imidazothiazoles, tetrahydropyrimidines, and macrocyclic lactones (Traversa and von Samson-Himmelstjerna 2016; Fissiha and Kinde 2021; Hamid et al. 2023; Singh et al. 2023). While these drugs have been used to effectively reduce worm burden in the past (Shalaby 2013; Lamb et al. 2017; Fissiha and Kinde 2021), treatment failure is now becoming increasingly common (Sutherland and Leathwick 2011; Leathwick 2013) due to inaccurate dosing, use of substandard or counterfeit drugs (Hodgkinson et al. 2019; Fissiha and Kinde 2021; Kovaļčuka et al. 2022), indiscriminate deworming (Jackson et al. 2012; Ndwandwe et al. 2025), and repeated use of the same drug without rotation (Chandrawathani et al. 2003; Fissiha and Kinde 2021; Abd Majid et al. 2022). Anthelmintic resistance (AHR) occurs when parasites become less susceptible to previously effective anthelmintics (Saidu et al. 2025) and survive doses of drugs that would normally be effective (Várady et al. 2011; Beleckė et al. 2021; Charlier et al. 2023). AHR is a growing challenge affecting small ruminant health and productivity (Geurden et al. 2014), especially in areas where multiple anthelmintic resistance occurs (Waller 1997). In Malaysia, Dorny et al. (1994) published the first report on benzimidazole-resistant strains of Haemonchus contortus in goat. Following the pioneer works, Chandrawathani et al. (1999), further reported the occurrence of multidrug resistant strains of GINs in sheep and goats in West Malaysia. These initial reports stimulated further studies on AHR culminating in various publications suggesting widespread treatment failure involving benzimidazoles, imidazothiazoles, and macrocyclic lactones in pathogenetic GINs in sheep and goats in West Malaysia (Khadijah et al. 2006, 2018; Basripuzi et al. 2012; Premaalatha et al. 2014; Thongsahuan et al. 2014; Abubakar et al. 2015; Wong and Sargison 2018; Baudinette et al. 2022).

Despite extensive evidence of AHR in GINs of sheep and goats in various production systems in Peninsular Malaysia, there is a significant knowledge gap regarding the status of anthelmintic efficacy of albendazole and ivermectin in GINs of sheep and goat in Sarawak. Therefore, this study evaluates the in vivo efficacy of albendazole and ivermectin in GINs of sheep and goat from selected farms in Sarawak using FECRT. The study also morphologically identifies the third stage larvae (L3) of resistant GINs using faecal culture and microscopic examination.

Materials and methods

Study area and population

This study was conducted in Sarawak, which is the largest state in Malaysia in terms of land mass. The state is located on the northwestern part of Borneo Island between latitude 2.5574° N and longitude 113.0012° E. The state has 9,570 goat and 2,337 sheep population kept by resource-poor individual smallholders having 40–70 heads per farm (DVS, 2024). The farms included in the anthelmintic efficacy trial are located within Miri division with 396 sheep and 350 goats and Bintulu division with 485 sheep and 450 goats. At the time of this study, the animals were reared under an integrated management system where farmers confined sheep and goats in slated roofed pens and fed them with cut-and-carry Nappier grass and occasionally given pellets with mineral supplements. The actual frequency of anthelmintic treatment could not be ascertained at the time of this study because farmers did not keep a formal record, but they reported whole flock dosing with albendazole or ivermectin whenever they think it was necessary.

Experimental design

Following the faecal survey of the 12 approved small ruminant farms in Miri (n = 6) and Bintulu (n = 6), only 4 farms comprising 3 sheep farms and 1 goat farm, which agreed to participate, were included in the experimental anthelmintic efficacy trial. All the apparently healthy adult and young sheep and goat of both sexes having a pre-treatment EPG ≥ 200 was considered eligible for the study. In the null hypothesis, we hypothesized that oral administration of albendazole or subcutaneous administration of ivermectin at label recommended doses in sheep and goat with ≥ 200 epg will produce FECR with a lower 90% CI ≥ 90% and upper 90% CI ≥ 99%. All pregnant, lactating, sick, and young animals < 3 months were excluded from the experimental trial due to safety concerns by farmers. There were 56 naturally infected animals which met our predefined inclusion criteria in the 4 farms: A (n = 13 Barbados blackbelly sheep), B (n = 15 Saanen goats), C (n = 14 White dorper sheep), and D (n = 14 White dorper sheep). The eligible animals were enrolled in the study based on the updated FECRT guidelines for diagnosing resistance in ruminants utilizing a paired study design based on pre-treatment and post-treatment samples from the same animals assuming a grey zone: 90–99% (Kaplan et al. 2023). Since the number of eligible animals on each farm does not significantly exceed the recommended average experimental group size for clinical protocol, each farm was assigned a group status with the animals in the groups treated as the experimental units: Group A – ivermectin (n = 13), Group B – ivermectin (n = 15), Group C – ivermectin (n = 14), and Group D – albendazole (n = 14). The choice of anthelmintic treatments used on each farm was influenced by the farmers. Three farmers preferred injectable ivermectin over oral drenching since they have used drenches with unsatisfactory results in the past.

Experimental procedure

The pre-treatment body weight (kg), body condition score (3–4), FAMACHA eye colour score (2–3), packed cell volume (PCV), and EPG of individual sheep and goat included in the study were measured and recorded (Table 1). The pre-treatment raw egg counts recorded in the four experimental groups are shown in Table 2. The baseline PCV was determined by microhematocrit centrifugation technique (Grindem 2011), body condition score by palpation in the lumbar and chest region (Thhompson and Meyer, 1984), and FAMACHA score using eye colour chart (Kaplan et al. 2023). Each animal was restrained to collect approximately 5 g of pre-test faecal sample from the rectum into sterile collecting tubes for faecal examination to determine the pretreatment faecal egg count (FEC) using the McMaster technique.

Table 1.

Baseline characteristics of experimental sheep and goats

Group n Mean ± SD
Weight (Kg) Pre-test EPG Pre-test PCV
Group A (IVM) 13 20.9 ± 2.7 557.7 ± 58.5 20.7 ± 3.3
Group B (IVM) 15 20.1 ± 3.1 863.3 ± 254.4 22.7 ± 3.9
Group C (IVM) 14 20.3 ± 2.8 682.1 ± 163.5 22.1 ± 4.3
Group D (ABZ) 14 21.2 ± 2.7 846.4 ± 216.4 23.0 ± 5.8
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IVM: ivermectin, ABZ: albendazole

Table 2.

Raw pre-test egg counts of experimental sheep and goats included in the study

Group A (IVM) Group B (IVM) Group C (IVM) Group D (ABZ)
10 4 40 8
15 6 5 40
13 26 8 7
10 10 20 45
20 8 9 6
10 9 4 28
7 12 8 6
12 4 7 41
5 5 15 4
13 80 8 4
15 22 18 5
10 12 5 7
5 20 4 4
- 36 40 32
- 5 - -
145 259 191 237
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A single dose of Ivomec ®(Ivermectin 1% w/v solution, Boehringer Ingelheim) given at 0.2 mg/kg was injected subcutaneously into the loose skin behind the shoulder as a single dose in Groups A, B, and C. While on the other hand, animals in Group D received a single oral drench of AlbazolⓇ (Albendazole 1% suspension, Life Biopharma) at 5 mg/kg. All treatments were administered on Day 0 according to manufacturer’s instructions.

The treated animals were observed for adverse effects of ivermectin and albendazole such as salivation, weakness, and dilated pupils for 45 min after the last animal was treated before leaving the farm. The characteristics of anthelmintic drugs used in this study is shown below in Table 3. Post-test faecal samples were collected from the same treated animals included in the study on Day 14 and examined using McMaster FEC to determine the post-treatment egg per gram (epg) output.

Table 3.

Characteristics of anthelmintic drugs used in FECRT

Composition Dosage Route Manufacturer
Ivomec 1%® (Ivermectin − 10 mg/ml) 0.2 mg/Kg Subcutaneous injection Boehringer Ingelheim
Albazol 10%® (Albendazole100mg/ml) 5 mg/Kg Oral drench Life Biopharma
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Determination of nematode faecal egg count and epg

The outcome of interest in the anthelmintic efficacy trial is the percent reduction in the mean pre-treatment gastrointestinal nematode FEC in the treatment groups from pre- to post treatment (A, B, C, and D) relative to the post-treatment FEC on day 14. The pre-test and post-test faecal egg counts were determined using the modified McMaster egg count technique with a test sensitivity of 50 eggs per gram (epg) of faeces (Soulsby 1982). In this test, 2 g of the faecal sample was mixed with 28 mL of saturated sodium chloride (NaCl) in a mortar and filtered through a tea strainer to remove the debris. A 3 mL Pasteur pipette was used to gently stir the filtrate and withdraw a portion to fill the two chambers of a McMaster slide 2.3 × 7.6 CM with a sensitivity of 50 epg (FECSource.com® and left undisturbed for 10 min before microscopic examination was done using 100x magnification of a compound microscope to count the total number of eggs inside the grid areas in both chambers of the McMaster slide. Nematode epg was calculated as the total number of eggs present in both chambers (C1 + C2) x 50, where 50 is a factor specific for the 2:28 faeces floatation solution ratio (Lambertz et al. 2018; Paul et al. 2023).

Coprocultures and morphological identification of nematode L3 larvae

A bulk sample of pooled individual animal faecal samples in each treatment group (A, B, C, and D) was collected for larval culture and identification post-treatment Day 14. Faecal culture and third stage larvae (L3) identification was done following steps outlined in the Manual of Veterinary Parasitological Laboratory Techniques (MAFF 1986). Post-treatment faecal samples were mixed with vermiculite to adjust the moisture content and incubated in airtight containers kept at 25 °C for 10 days in the laboratory for egg hatching (Emsley et al. 2023). The moisture content of cultures was maintained by spraying aliquot amounts of water and mixing the contents of each culture container every 2 days. After the incubation period, a modified Baermann’s technique was used to recover hatched larvae from cultures. In this technique, the contents of each plastic culture container were poured into loose bandage and partially submerged overnight in a funnel containing tepid water to collect larvae in a closed ballon after 24 h. The contents of each ballon were emptied into a beaker, and a drop of the concentrated larvae suspension was placed on a clean glass slide and mixed with a drop of Lugol’s iodine for identification under the compound microscope using morphological keys described in previous studies. Nematode larvae were morphologically separated into Trichostrongylus group and Haemonchus group based on sheath retention, shape of the tail, and anterior-posterior structures (Soulsby 1982; Van Wyk et al. 2004; van Wyk and Mayhew 2013). Larval measurements and images were obtained with a digital camera using ProgRes CapturePro® 2.10.0.1 software running on Windows OS.

Statistical analysis

Data obtained from field tests on anthelmintic treatment with albendazole and ivermectin using the faecal egg count reduction test (FECRT) using clinical protocol (grey zone: 90–99%) in a paired study design was used to calculate the percent egg count reduction: Inline graphic x 100 (Coles et al. 1992, 2006). As recommended in the updated W.A.A.V. P. guidelines for diagnosing anthelmintic resistance in sheep and goats, we assumed an efficacy of 99%, 90% CI, a one-tailed test, and 5% type 1 error rate in statistical analysis. The FECR and the corresponding 90% CIs were calculated using descriptive statistics in the Statistical Package for Social Sciences (SPSS) Version 25.0. We defined resistance as FECR with an upper 90% CI < 99%, and susceptibility as the lower 90% CI ≥ 90% and upper 90% CI ≥ 99% (Kaplan et al. 2023).

Results

Faecal egg count reduction test (FECRT) on ivermectin and albendazole

The faecal egg count reduction test (FECRT) was conducted on four treatment groups to assess anthelmintic efficacy. Group A (n = 13) had a mean pre-treatment egg per gram (EPG) count of 557.7 ± 58.5, which decreased to 76.9 ± 12.2 post-treatment, resulting in an 85.4% FECR (90% CI: 80.8–89.9). Group B (n = 15) showed a reduction from 863.3 ± 254.4 to 186.7 ± 59.3 EPG, with a 75.9% FECR (90% CI: 65.7–86.1). Group C (n = 14) exhibited a decline from 682.1 ± 163.5 to 507.1 ± 129.1 EPG, yielding a 75.8% FECR (90% CI: 65.3–86.3). Group D (n = 14) had a pre-treatment EPG of 846.4 ± 216.4, decreasing to 714 ± 200.5 post-treatment, with a 76.8% FECR (90% CI: 69.9–83.8). It follows from our results that all the anthelmintic treatments produced an FECR with an upper 90% CI < 99%, suggesting resistance (Table 4).

Table 4.

Results of FECRT on ivermectin and albendazole

Groups (Mean ± SE) FECR (%) 90% CI (%)
Pre-test EPG Post-test EPG
Group A 557.7 ± 58.5 76.9 ± 12.2 85.4R 80.8–89.9
Group B 863.3 ± 254.4 186.7 ± 59.3 75.9R 65.7–86.1
Group C 682.1 ± 163.5 507.1 ± 129.1 75.8R 65.3–86.3
Group D 846.4 ± 216.4 714 ± 200.5 76.8R 69.9–83.8
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R = resistant interpretated based on WAAVP guidelines (Kaplan et al. 2023): Upper 90% CI of FECR < 99%

Morphological identification of nematode L3 larvae from coprocultures

The results of microscopic examination and morphological identification of nematode L3 obtained from post treatment faecal cultures in sheep and goats revealed a mixture of Trichostrongylus, Teladorsagia, and Haemonchus species (Fig. 1). Morphologically, the L3 larvae of all the three species retained the L2 cuticle which appears as a transparent protective sheath under the light microscope. This feature along with the head, tail, mouth parts, and intestinal cells were used to morphologically differentiate the three species: Trichostrongylus L3 larvae was recognised by its distinct slender, elongated, and cylindrical body tapering at both ends with indistinct mouth parts and a filariform oesophagus, and granular intestinal cells. It also retains the L2 sheath which is modified into a unique posterior sheath extension beyond the tail (Fig. 2). Teladorsagia L3 which closely resembles Trichostrongylus also possess a slender and elongated body, filariform oesophagus, indistinct buccal cavity, and conspicuous granular intestinal cells. However, the sheath tail extension in Teladorsagia is shorter, less filamentous, and tapers smoothly into a fine point like Haemonchus. Moreover, the L3 in Teladorsagia does not completely fill the sheath, leaving a visible space at the anterior end (Figs. 3 and 4). Haemonchus L3 was recognised by the typical long slender body, presence of a characteristic rounded or bullet-shaped anterior end and indistinct mouthparts. The entire L3 larvae is completely covered in the L2 sheath like a body suit with a relatively long tail sheath extension that tapers into a fine pointed tip (Figs. 5 and 6).

Fig. 1.

Fig. 1

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Photomicrograph of ensheathed third-stage larva (L3) of resistant nematodes: (A) Trichostrongylus species, (B) Teladorsagia species, and (C) Haemonchus species. Image from light microscope (200x)

Fig. 2.

Fig. 2

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Photomicrograph of ensheathed third-stage larva (L3) of Trichostrongylus species: A: a tapered head with indistinct buccal cavity and partially visible intestinal cells B: a pointed tail showing unique sheath extension and prominent granular intestinal cells visible through the transparent cuticle. Image from light microscope (200x). Scale bar = 20 μm

Fig. 3.

Fig. 3

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Photomicrograph of ensheathed third-stage larva (L3) of Teladorsagia circumcincta identified in small ruminant faecal culture under light microscope (400x). Image shows the full body length enclosed within an intact sheath with partially visible internal anatomy. Image from light microscope (200x). Scale bar = 50 μm

Fig. 4.

Fig. 4

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Photomicrograph of anterior region of ensheathed third-stage larva (L3) of Teladorsagia circumcincta identified in small ruminant faecal culture under light microscope. Image shows the head region partially filling the sheath anteriorly. Image from light microscope (200x). Scale bar = 50 μm

Fig. 5.

Fig. 5

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Photomicrograph of ensheathed third-stage larva (L3) of Haemonchus contortus identified in small ruminant faecal culture under light microscope. Image shows the full body length completely filling up the sheath with partially visible internal structures. Image from light microscope (200x). Scale bar = 50 μm

Fig. 6.

Fig. 6

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Photomicrograph of third-stage larva (L3) of Haemonchus contortus showing A: a tapered head with indistinct buccal cavity and partially visible internal structures B: a tapered tail enclosed within a sheath with internal structures faintly visible through the transparent cuticle. Image from light microscope (200x). Scale bar = 50 μm

Discussion

The present study was conducted to investigate the in vivo anthelmintic efficacy of albendazole and ivermectin in GINs of smallholder sheep and goats based on the FECRT in selected farms in Sarawak. The null hypothesis was assumed that there is no reduction in faecal egg counts following treatment. The results of FECRT showed a 76.8% (90% CI: 69.9–83.8) reduction in pre-treatment epg of GINs in White dorper sheep (Group D) for albendazole. On the other hand, 85.4% (90% CI: 80.8–89.9), 75.8% (90% CI: 65.3–86.3), 75.9% (90% CI: 65.7–86.1) reduction in pre-treatment epg outputs of GINs were observed with ivermectin in Barbados blackbelly sheep (Group A), White dorper sheep (Group C), and Saanen goats (Group B), respectively. Thus, all the treatment groups did not achieve the W.A.A.V.P recommended post-treatment FECR for susceptibility (lower 90% CI ≥ 90% and upper 90% CI ≥ 99%) in sheep and goats, suggesting anthelmintic failure, which has led us to reject the null hypothesis. The pioneer works of Dorny et al. (1994) established the presence of 34% Benzimidazole-resistance associated with H. contortus among smallholder goat farms that frequently used anthelmintics in West Malaysia. Later studies reported widespread GIN resistance to ivermectin, albendazole, and levamisole among sheep and goat populations in Peninsular Malaysia (Khadijah et al. 2006; Chandrawathani et al. 2013; Premaalatha et al. 2019; Abd Majid et al. 2022). Additionally, total failure of benzimidazole, imidothiazole, macrocyclic lactone, and salicylanilide anthelmintics against GINs of small ruminants was recorded in state of Sabah in East Malaysia (Chandrawathani et al. 2004). However, to the best of our current knowledge, this is the first study to document anthelmintic failure in GINs of sheep and goats in Sarawak.

The observed anthelmintic failure of both albendazole and ivermectin anthelmintics in smallholder sheep and goat production systems in Sarawak is a significant discovery. Economically, the detection of anthelmintic failure among GINs of sheep and goats undermines chemical control efforts, limits the availability of treatment options for farmers, and threatens the productivity of sheep and goats in Sarawak. The presence of resistant strains of H. contortus is linked to persistent chronic infections associated with stunted growth and mortality in in kids or lambs, and anaemia, slow weight gain, decreased productivity, and poor reproductive performance in adults (Cornelius et al. 2014; Besier et al. 2016b). Anthelmintic failure also causes persistent pasture contamination and sustained transmission of resistant nematode populations (Charlier et al. 2014), significantly affecting the productivity and economic sustainability of sheep and goat production systems (Wong and Sargison 2018). These economic losses are especially important in smallholder systems, because sheep and goats contribute directly to household income, food security, and rural livelihoods (Devendra 2010).

The observed variation in FECR with ivermectin between farms may be associated with differences in the proportions of susceptible worm populations, potentially influenced by management practices such as deworming and pasture management (Jackson et al. 2012; Ndwandwe et al. 2025). Farms with less aggressive deworming practices generally have a lower selection pressure and risk for proliferation of resistant nematode strains (Chandrawathani et al. 2003; Fissiha and Kinde 2021; Abd Majid et al. 2022) due to existence of a refugia untreated worm population (Hodgkinson et al. 2019; Höglund and Gustafsson 2023). Furthermore, the observed differences in FECR between Group A (sheep) and Group B (goats) may be associated with species differences in metabolism of anthelmintics (González Canga et al. 2009). Therefore, the observed discrepancy in reduction of efficacy post-treatment with ivermectin in Saanen goats compared to sheep in the present study is not conclusive because goats are known to rapidly metabolise and eliminate anthelmintics faster than sheep (Kaplan et al. 2023). Consequently, most practitioners administer 1.5-2 times higher extra-label doses for testing AHR in goats (Hoste et al. 2011a). Hence, the administration of label recommended sheep dose of ivermectin to goats in the present study may potentially result in the observation of lower efficacy due to metabolic factors rather than resistance. Further studies using adjusted dose regimen to accommodate their unique physiology will clarify the status of ivermectin resistance in goats.

The occurrence of anthelmintic failure in smallholder production system in Sarawak may be linked to inadequate farmer awareness, absence of targeted treatment strategies, and lack of proper quarantine before introducing new animals in the flock (Sutherland and Leathwick 2011; Leathwick 2013). In previous studies, it was found that most of the farmers in West Malaysia had limited resources, very little or no access to veterinary care, and rely heavily on repeated and unsystematic use of anthelmintics as their primary control strategy (Sani et al. 2004; Chandrawathani and Nurul Aini 2012), which may increase selection pressure and the emergence of AHR in worm populations (Chandrawathani et al. 2003; Fissiha and Kinde 2021; Abd Majid et al. 2022). Moreover, treatment failures are particularly common in smallholder settings, where mass treatments are administered without veterinary supervision, proper dosing, or considerations for drug class rotation (Wong and Sargison 2018). These practices, together with limited grazing land and continuous pasture contamination might have contributed to the emergence of multi-drug-resistant nematodes in Sarawak.

In relation to parasite species, the failure of both albendazole and ivermectin against Haemonchus, Teladorsagia, and Trichostrongylus species in this study highlights their importance as the major GINs in the region (Fleming et al. 2006), presenting significant challenge for control due to the cost of repeated treatments (Niciura et al. 2019), and fewer alternative treatment options for farmers (Kaplan and Vidyashankar 2012). The current result also agrees with previous studies which suggest that Haemonchus, Trichostrongylus, and Teladorsagia are the most frequently resistant species of GINs in small ruminants worldwide (Taylor et al. 2009; Saidu et al. 2025). Anthelmintic resistant strains of Haemonchus, Teladorsagia, and Trichostrongylus threatens sustainability of small ruminant farming worldwide (Geurden et al. 2014). For instance, resistant strains of these species have been reported in in European countries such as Ireland, Switzerland, and Italy (Ramünke et al. 2016). Similarly, benzimidazole-resistant strains of Haemonchus are prevalent in sheep and goats in Asian countries such as Bangladesh (Dey et al. 2020), India (Nath et al. 2022), and Malaysia where benzimidazole, macrocyclic lactone, and imidazothiazole resistant strains of Haemonchus contortus, Trichostrongylus, Oesophagostomum, and Bunostomum species abound (Khadijah et al. 2006, 2018; Basripuzi et al. 2012; Premaalatha et al. 2014; Thongsahuan et al. 2014; Abubakar et al. 2015; Wong and Sargison 2018; Baudinette et al. 2022). Among the resistant strains of GINs identified in this study, Haemonchus contortus is particularly problematic due to its high pathogenicity, high reproductive index, and widespread multiple drug resistance globally (Soulsby 1982; Roeber et al. 2013).

At the molecular level, anthelmintic resistance is controlled by specific genetic and biochemical adaptations in gastrointestinal nematodes (Wondimu and Bayu 2022; Saidu et al. 2025). Multiple independent sources of resistance have been described in gastrointestinal nematodes of small ruminants (Skuce et al. 2010; Saidu et al. 2025). Point mutations at F200Y, E198A, E198L, and F167Y in the isotype 1-β-tubulin gene are the determinants of resistance to benzimidazole in Haemonchus and other Trichostrongyles of ruminants (Silvestre and Humbert 2002; Palcy et al. 2010; Morrison et al. 2014; Baltrušis et al. 2018, 2020; Kotze et al. 2020). These mutations decrease the binding affinity of benzimidazoles to the β-tubulin transport protein and diminish drug efficacy by decreasing concentration at target sites (Baltrušis et al. 2020). Resistance to ivermectin in H. contortus is mediated by P-glycoprotein (P-gp) gene (Xu et al. 1998) including sex-specific pgp-11 gene in males (Laing et al. 2022), and transcription factor (cky-1) gene (Laing et al. 2022), which influence neuronal function and chloride homeostasis, increasing drug transportation and preventing access to its site of action, making it ineffective (Beech et al. 2012). Collectively, these mechanisms reduce drug efficacy and contribute to treatment failure, as observed in the present FECRT results.

Recent advances in our understanding of host-pathogen and drug interaction systems suggest that treatment failure and the development of resistance are driven by adaptive biological responses and complex host-drug-parasite interactions, emphasizing the need for multifaced integrative parasite control strategies (Yang et al. 2025). Thus, the emergence of anthelmintic failure among smallholder sheep and goats in this study presents an opportunity to explore sustainable alternative control strategies that reduce dependence on traditional anthelmintic dosing to slow down the development of resistance (Hoste and Torres-acosta, 2011b). Integrated management practices incorporates pasture and grazing management (Rahmann and Seip 2006; Colvin et al. 2008; Mbaya et al. 2009), targeted selective treatment (van Wyk et al. 2006; Besier 2008), nutritional supplementation (Hale 2006; Rahmann and Seip 2007), biological control (FAO 1998; Waller 2004; Szewc et al. 2021), selective breeding of resistant stock (Stear and Murray 1994; Rahmann and Seip 2006; Nikbin et al. 2022), and phytotherapy (Chagas 2015). Targeted selective treatment applying body condition scoring (BCS), FAMACHA© scoring, and FEC is widely used to reduce treatment cost and selection pressure by maintaining a refugia of worm populations that are sensitive to anthelmintics (van Wyk et al. 2006; Besier et al. 2016a; Mancilla-montelongo et al., 2023). Biological control using hematophagous fungi, dung beetles, earthworms, and bacterial toxins also show great promise in reducing larval survival and pasture contamination in open grazing systems (Boughton et al. 2024). Selective breeding of nematode-resistant breeds of sheep and goats, characterised by consistently lower FEC and improved packed cell volume values even in the presence of heavy worm burden, is also a promising long-term strategy (Cunha et al. 2024). Phytotherapy using plant-derived bioactive compounds such as condensed tannins, alkaloids, saponins, and flavonoids from Leucaena leucocephala, Calliandra calothyrsus, Sericea lespedeza, and Artemisia spp., reduce larval establishment, worm survival rate, worm burden, and fecundity in small ruminants (Williams et al. 2014; Hoste et al. 2015; Hassan and Ghazy 2022; Manjusa Adak, 2022). Moreover, polysaccharides derived from Christia vespertilionis exerts immunomodulatory effects that support host resistance and influence host-parasite interactions (Xiao et al. 2025), while polysaccharides derived from edible mushrooms, Pleurotus eryngii, exerts anti-inflammatory effects that reduce tissue damage during nematode infection (Wang et al. 2024).

Finally, this study design is constrained by the low level of farmer participation, which influenced our sample size and the number of eligible animals available for inclusion. Although the experimental groups meet our first inclusion criteria of pre-treatment EPG ≥ 200, the raw egg counts obtained from groups A and C were slightly lower than the recommended minimum of 200 raw eggs per group, which may affect the statistical power of this study design. Furthermore, complete randomisation was constrained by the shortage of eligible animals that met our first inclusion criteria, and the study was not designed to address potential breed and species differences in physiological responses to drug dosing which may influence anthelmintic efficacy in goats. However, these limitations do not hinder the translational use of the preliminary data reported here for intervention at the farm level. Therefore, the results of this preliminary trial should be interpreted in the light of these limitations.

In conclusion, this study provides the first evidence of anthelmintic failure involving albendazole and ivermectin against Haemonchus, Trichostrongylus, and Teladorsagia species in sheep and goat farms in Sarawak. In the light of current findings, we developed a structured herd health program in collaboration with the Department of Veterinary Services Sarawak (DVSS) (Paul et al. 2026) as a platform for smallholder farmer and DVS field staff training on proper dosing guided by Targeted Selective Treatment (TST) principle based on FAMACHA© eye colour scoring, BCS, and FEC as prerequisites for selective treatment of sheep and goats, to replace the traditional indiscriminate anthelmintic dosing currently practiced by smallholder farmers to overcome spread of AHR and the burden of GINs in the study area.

Acknowledgements

We would like to thank the staff of the Department of Animal Science and Fisheries, Faculty of Agricultural and Forestry Sciences and staff in the Bintulu and Miri Divisions of the Department of Veterinary Services Sarawak for their participation and contribution in the research work.

Authors’ contributions

SA, BME, MM, AHH, AAB, MLMA, & KNB: Methodology, investigation, data curation, software, formal analysis, writing (original draft), writing (review and editing). BTP: Conceptualisation, funding acquisition, project administration, supervision, validation, writing-review, and editing. KJ, MS, & FFAJ: Supervision, validation, resources. All authors reviewed the manuscript prior to submission.

Funding

Open access funding provided by The Ministry of Higher Education Malaysia and Universiti Putra Malaysia. This study “Ascertaining the current trends in the epidemiology of endoparasites among small ruminants in selected states using high precision diagnostics in Malaysia” was funded by Universiti Putra Malaysia Research and Innovation Unit through Geran Putra Initiatif Mudah (GP-IPM-9737300) and Geran Putra Inisiatif Siswazah (GP-IPS-9830800).

Data availability

The corresponding author may provide the data supporting the results of this study upon reasonable request.

Declarations

Ethics approval and consent to participate

All experimental procedures were approved by the institutional animal care and use committee (IACUC), University Putra Malaysia (UPM/IACUC/AUP-R037/2023) and the Department of Veterinary Services Sarawak. Individual farmers signed written consent for participation in the study prior to enrolment.

Consent for publication

All the authors approved the publication of this manuscript in its entirety, including author details, tables, and figures, in the Tropical Animal Health and Production Journal.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Data Availability Statement

The corresponding author may provide the data supporting the results of this study upon reasonable request.

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