Next Article in Journal
The Efficiency of Centrifugation in the Detection of Mollicutes in Bovine Milk
Previous Article in Journal
The Cattle Trading Network and Its Effect on the Spread of Brucellosis in Paraná, Brazil
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Ruminants
Volume 3
Issue 3
10.3390/ruminants3030020
ruminants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

An Overview of Anthelmintic Resistance in Domestic Ruminants in Brazil

by
Lucia Oliveira Macedo
1,
Samuel Souza Silva
1,2,
Leucio Câmara Alves
3,
Gílcia Aparecida Carvalho
1 and
Rafael Antonio Nascimento Ramos
1,*
1
Laboratory of Parasitology, Federal University of the Agreste of Pernambuco, Garanhuns 55292-270, Brazil
2
Postgraduate Program in Animal Bioscience, Federal Rural University of Pernambuco, Recife 52171-900, Brazil
3
Department of Veterinary Medicine, Federal Rural University of Pernambuco, Recife 52171-900, Brazil
*
Author to whom correspondence should be addressed.
Ruminants 2023, 3(3), 214-232; https://doi.org/10.3390/ruminants3030020
Submission received: 27 June 2023 / Revised: 9 August 2023 / Accepted: 23 August 2023 / Published: 29 August 2023
Browse Figures
Versions Notes

Abstract

:
Gastrointestinal nematodes (GIN) significantly, negatively impact livestock worldwide, and their control depends on the use of chemotherapy drugs. However, this approach is unsustainable as anthelmintic resistance (AR) is growing widespread. This article provides a comprehensive overview of the historical and current data published on AR in domestic ruminants in Brazil. Alternative measures of GIN control have been discussed to provide helpful information to prevent the development of AR in the country. This review consisted of a search of technical and scientific publications between January 1960 to January 2023, using online sources such as PubMed, Scielo and Google Scholar. Eighty-three articles published over the last six decades reporting AR in sheep (n = 43), goats (n = 20) and cattle (n = 20) were included. A total of 37.3%, 25.4% and 37.3% evaluated one, two and three or more molecule classes, respectively. Among all studies, 82.1% used fecal egg count reduction test as a method of AR diagnosis. In conclusion, AR is an urgent and emerging issue for ruminant production in Brazil. It is necessary to evaluate on a large scale the distribution and management of anthelmintic drugs and discuss strategies that delay this phenomenon’s development.

Graphical Abstract

1. Introduction

Gastrointestinal nematodes (GIN) are important pathogens of grazing ruminants, responsible for economic losses in animal production worldwide [1,2,3]. The controlling of these parasites has been a challenge for producers and there is an emerging need to seek effective alternatives that do not cause animal toxicity [4]. Among Brazilian ruminant livestock, the most common GIN are those belong to the following genera: Haemonchus and Ostertagia (parasite of abomasum); Trichostrongylus (parasite of small intestine and abomasum); Cooperia (parasite of small intestine); and Oesophagostomum, also known as the nodular worm, which parasitizes the large intestine [5,6,7]. Infections by these parasites are characterized by lesions in the gastrointestinal mucosa, which impair the absorption of nutrients, reducing body weight gain and milk production. In addition, some species (e.g., Haemonchus contortus) are hematophagous [8]. Studies have already been conducted in Brazil to assess the economic impact of GIN infection in ruminants [9,10]. For instance, a reduction of 0.6 kg/cow/day of milk in dairy cattle is estimated, with a potential annual loss of up to USD 1870.48/animal [11]. In sheep, losses may reach approximately USD 400/animal/year [12].
GIN control has been largely achieved by using both broad (benzimidazoles, imidazothiazoles, hydropyrimidines and macrocyclic lactones) and narrow-spectrum (salicylanilides, nitrophenols and organophosphate) anthelmintics [13]. More recently, amino-acetonitrile derivatives have emerged as a new chemical class of synthetic anthelmintics, effective against GIN of sheep [14]. Nevertheless, the excessive dependence on these substances has led to the development of anthelmintic resistance (AR) in all species of domestic ruminants to all classes of anthelmintics [15]. In Europe [16,17,18], Africa [19,20,21], Asia [22,23], Oceania [24,25,26] and the Americas [27,28,29,30], this phenomenon is associated with multiple drugs, threatening the viability of ruminant livestock production, especially small ruminants [18,31,32].
In Brazil, the first AR reports were on thiabendazole and ivermectin in sheep in the country’s southern region [33,34]. Similarly, benzimidazoles resistance was also detected in goats from the northeast region. In the same period, AR was also detected in goats treated with albendazole, parbendazole and levamisole [35], which raises the discussion about different dosages for small ruminants [36]. Soon after, the resistance of Haemonchus spp. to oxfendazole and albendazole was detected in cattle from the southern region [37]. With the recent increase in AR in Brazilian herds, the development of new compounds is pivotal, as well as the integration of rational GIN control [38,39].
No articles have gathered data on AR in domestic ruminants in the country. Few studies have been conducted singly, such as a study on AR in small ruminants [40] and resistance to the class of benzimidazoles [41]. Therefore, this article provides a comprehensive overview of the historical and current data published on AR in domestic ruminants in Brazil. Additionally, alternative measures of GIN control have been discussed to provide helpful information to prevent the development of AR in the country.

2. Methods

Review Procedures and Map Construction

This review consisted of a comprehensive search of technical and scientific reports published from January 1960 to January 2023 using online sources such as PubMed, (US National Library of Medicine National Institutes of Health/National Center for Biotechnology Information Search database), Scielo (Scientific Electronic Library Online) and Google Scholar. Keywords, including “ruminants”, “small ruminants”, “anthelmintic resistance”, “sheep”, “goat”, “cattle” and “Brazil”, were combined for search articles. All articles written in English or Portuguese were included in this review.
Articles were included whether they described AR exclusively through the fecal egg count reduction test (FECRT) or associated with other tests such as the egg hatchability test, larval development test, molecular tests and controlled efficacy tests. Studies that described resistance using necropsy were also included. Finally, they were screened to assess their originality, time of publication, aim, technique employed for diagnosis and reliability in presenting results.
Two maps were constructed to represent graphical data of the distribution of AR and the class of drugs used. Geographic coordinates were used through the Google Maps platform of the municipalities where the studies were carried out; then, these coordinates were incorporated into the QGIS program (version 3.22.10) together with the vector layer (Shapfiles, version 2017) obtained in the database of the Brazilian Institute of Geography and Statistics.

3. Results and Discussion

Eighty-three peer-reviewed articles reporting AR in domestic ruminants (sheep, goats and cattle) were published over the last six decades. Of all these studies, 51.8% (43/83) were reported in sheep, 24.1% (20/83) in goats and 24.1% (20/83) in cattle. Most of the studies were carried out with molecules from different classes. Of all studies, 37.3% (31/83) evaluated only one class, 25.4% (21/83) two drug classes and 37.3% (31/83) three or more drug classes. Figure 1 illustrates the map with a graphical representation of the distribution of the class of drugs used in the considered articles: macrocyclic lactones (24.1%; 20/83), combination of benzimidazole + macrocyclic lactones (14.5%; 12/83) and benzimidazole + macrocyclic lactones + other combinations (37.3%; 31/83). Most of these studies (83.1%) used FECRT as a method of AR diagnosis. Currently, for the interpretation of FECRT, the recommendations of the World Association for the Advancement of Veterinary Parasitology (WAAVP) are based on classification criteria that outline how the observed data (values for the upper and lower 90% CI or results of separate hypothesis tests) are compared to the expected effectiveness and the lower limit of effectiveness (which serve as the values for the upper and lower limits of the gray zone), accepting a Type 1 error rate of 5% [41].
From 1960 to 1999, 18 articles (21.7%) reported AR in domestic ruminants, with one in cattle (5.6%; 1/18), three in goats (16.7%; 3/18) and fourteen (77.8%; 15/18) in sheep. From 2000 to 2023, the number of reports tripled, with 65 articles (78.3%) distributed across 14 states and 127 municipalities. Most of the studies were concentrated in the southern (39.8%; 33/83), northeastern (31.3%; 26/83), southeastern (22.9%; 19/83) and midwestern (6.0%; 5/83) regions. Despite lower reliability, some references [33,38,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73] that do not include animal numbers or locations were considered in this review. Figure 2 illustrates the map with the graphical representation of the distribution of AR in domestic ruminants from Brazil.

3.1. Anthelmintic Resistance in Small Ruminants

Sixty-three (75.9%) peer-reviewed articles have been published on small ruminant AR, including 51.8% (43/83) in sheep and 24.1% (20/83) in goats. Anthelmintic resistance was reported in 92 municipalities from four regions of the country: (i) south—states of Paraná, Rio Grande do Sul and Santa Catarina; (ii) southwest—states of Minas Gerais, Rio de Janeiro and São Paulo; (iii) midwest—state of Mato Grosso do Sul; and (iv) northeast—states of Ceará, Paraíba, Pernambuco and Rio Grande do Norte (Table 1 and Table 2). The lack of information in the north of the country does not mean the absence of AR. However, it is worth mentioning that this region of the country concentrates the smallest number of small ruminants (2.3% of total Brazilian herd—IBGE, 2021), while the northeastern and southern regions possess the vast majority of goats and sheep (91.9%). Additionally, most of the research has been conducted in these regions.
Overall, 24,449 animals were assessed primarily through FECRT (85.7%; 54/63). These studies evaluated different classes of drugs but mainly molecules belonging to the class of benzimidazole (i.e., albendazole, thiabendazole, oxfendazole, mebendazole and febendazole), macrocyclic lactones (i.e., ivermectin, doramectin, abamectin and moxidectin) and imidazothiazole (i.e., levamisole and tetramisole).
The AR is more serious than has been documented so far. The gradual growth from its somewhat sporadic occurrence in the early 1960s to the current situation threatens the sustainability of production systems. The primary tool adopted for controlling GIN parasites is the use of anthelmintics, which generally positively impact the well-being and health of domestic and production animals [3]. It is known that AR is an evolutionary process that is unpredictable if anthelmintics are used intensively in a herd [102]. Nonetheless, it is possible to reduce the rate of resistance development by modifying anthelmintic use strategies [15]. Particularly in sheep, resistance of H. contortus is associated with economic losses and mortality [3,103]. In addition, there is more research and wider availability of drugs for this animal species (51.8%), reflecting more AR reports compared with goats and cattle. For example, the nematodes of sheep treated intensively with monepantel may show resistance to this drug in three months [104]. Similarly, lambs treated with levamisole every 42 days may present resistant nematode populations after the third treatment [7].
With the decreasing effectiveness of anthelmintics, the prophylaxis of GIN infections in small ruminants has become more challenging. Hence, the rational and integrated use of these compounds with sustainable measures of control is necessary to prevent AR [105]. Unfortunately, GIN of sheep developed resistance to a more recent molecule available commercially, the amino-acetonitrile derivatives [14,106,107,108].

3.2. Anthelmintic Resistance in Cattle

Twenty articles were found reporting AR in cattle. These reports originated from 51 municipalities, distributed in the southern (Rio Grande do Sul and Santa Catarina), southeastern (Minas Gerais and São Paulo), midwestern (Mato Grosso do Sul) and northeastern (Paraíba) regions of Brazil (Table 3). In total, 6729 individual animals were assessed for AR. Similarly, to small ruminants, most studies used FECRT (70.0%; 14/20) as a method for resistance detection. These studies evaluated different classes of drugs but mainly evaluated drugs from the class of macrocyclic lactones (avermectins and milbemycins).
In cattle, using chemical compounds to control infections by GIN is commonly conducted with broad-spectrum molecules (macrocyclic lactones, benzimidazoles, imidazothiazoles and salicylanilides). Mainly, macrocyclic lactones are used worldwide in ruminant livestock. They are available in different formulations, concentrations and associations, with ivermectin being the predominant chemical compound [31]. Frequently, these drugs are administered without any technical criteria for drug selection, and this empirical and indiscriminate use has favored AR development. This incorrect use has additional implications for the effectiveness of anthelmintic treatments, as it causes the emergence and spread of parasite resistance [56]. Unlike the development of resistance in small ruminants, in cattle, this phenomenon occurred slower; however, in recent decades, there has been a rapid increase in reports of AR in GIN infection of cattle worldwide [29,56,109,110,111]. It is imperative to address the AR issue in cattle, with the view of a significant threat to cattle productivity [102].
Table 3. Distribution of anthelmintic resistance in cattle from Brazil.
Table 3. Distribution of anthelmintic resistance in cattle from Brazil.
Region/StateMunicipalityAnthelminticsNumber of AnimalsDiagnostic MethodReferences
Southern
RSNIALB, OXF16FECRT[37]
SCNIIVE, LEV, ALB2340FECRT[112]
RSSão Pedro do SulIVE, DOR, ABA, MOX, ALB149FECRT[113]
RSButiáIVE144Necropsy[67]
RSSão Martinho da Serra, Dilermando de Aguiar, Cacequi, São Gabriel, Itaqui, São Borja, Santiago and São Vicente do SulIVE, DOR, EPR, MOX, LEV, ALB, FEB, CLO, NIT, DIS, ALB + CLO, DOR + CLO1704FECRT[114]
RSSão Gabriel, São Martinho da Serra and Dilermando deIVE, DOR, MON, LEV, ALB, CLO384FECRT[56]
RSSão GabrielIVE, DOR, ABA, EPR, MOX70FECRT[115]
Southeastern
SPNIIVE187FECRT[116]
SPCastilhoMOX20FECRT[117]
MGNIIVE24Necropsy[68]
MGTeófilo OtoniIVE, ALB, ABA, DOR84FECRT[118]
MG/SPCandeias, Formiga, Pimenta, Caldas, Prata, Jaboticabal and São José do Rio PardoIVE144Necropsy[67]
MGNIIVE, MOX40FECRT/Necropsy[69]
SPJaú, Botucatu and AvaréIVE99FECRT[119]
Midwest
MSNIIVE, MOXNIFECRT[70]
MSBandeirantes, Campo Grande, Porto Mortinho and Nova Alvorada do SulIVENILMIT[120]
MSNIDOR, IVE24FECRT/Necropsy[71]
MSRibas do Rio PardoMOX, IVE, ABA, ABA + IVE300FECRT[121]
Northeastern
PBNIIVE, ALB, OXF, LEV, TET, CLO, DIS, PYR, MOR200FECRT[72]
PBUiraúna, Aroeira, S. J. Rio do Peixe, Caturité, Barra de Santana, Soledade, Lagoa, Patos, Bom Sucesso, Campina Grande, Santa Cruz, Boa Vista, Gado Bravo, Barra de Santa Rosa, Brejo do Cruz, Joca Claudino, Catolé do Rocha, Belém do Brejo do Cruz, Souza and AparecidaALB, IVE, CLO, LEV800FECRT[29]
ALB: albendazole; OXF: oxfendazole; FEB: febendazole; EPR: eprinomectin; PYR: pyrantel; LEV: levamisole; DOR: doramectin; IVE: ivermectin; MOX: moxidectin; CLO: closantel; TRI: trichloform; NIT: nitroxynil; DIS: disophenol; MON: monepantel; MOR: Morantel; ABA: abamectin; (+): associations of drugs; (NI): not informed; FECRT: fecal egg count reduction test; LMIT: larval migration inhibition test.
The most frequent helminths in Brazilian cattle herds are Cooperia spp. and Haemonchus placei [122], which were identified in several reports of AR [67,71,116]. Resistance of the genus Cooperia is also common in countries such as Argentina [73], United Kingdom [123], Mexico [124], Sweden, Belgium, Germany [125], United States [126,127] and Australia [128,129]. Most of these reports are related to resistance to ivermectin. Infection by Cooperia punctata can significantly impact productivity by reducing weight gain and decreasing feed intake [127]. In addition, it influences phosphorus kinetics, reducing food intake and altering phosphorus absorption and retention [130].

4. Current Methods for Detection of AR

The primary method for detecting resistance is FECRT, which can be used with all anthelmintic groups. Nematode eggs are counted at pre- and post-treatment times defined according to the anthelmintic group used [131]. However, it is unsuitable for detecting resistance levels below 25% [132]. Several factors must be considered when planning an FECRT (i.e., study design, sample size considerations, choice of fecal egg count (FEC) method, statistical data analysis and interpretation) [133]. Other in vitro tests have been used less, such as the EHT, established to detect drug resistance in the benzimidazole class [134]. In addition, it is possible to use tests evaluating larval development and motility (LDT and LMIT) [15]. Particularly in cattle, most animals in a herd, even the young ones, have lower FEC, making diagnosing AR difficult [20]. For example, the McMaster technique is the most used method in studies of AR detection but it has a detection limit of 50 EPG [135]. The use of methods with higher detection, such as FLOTAC (one EPG) and Mini-FLOTAC (five EPG), might be encouraged in this kind of analysis [136,137]. The consensus is that there is a need for improvements in the AR detection methods, such as more reliable parasitological tests and an increase in the number of animals required for simultaneous testing on several drugs [119].
With the limitations of current in vivo and in vitro resistance tests, molecular tools can potentially improve drug resistance diagnosis [138]. The development of molecular diagnostics for anthelmintic resistance has been one of the leading research topics involving the molecular mechanisms of drug resistance [139]. Thus, developing molecular markers for diagnosing resistance can help develop new anthelmintic drugs [140]. The molecular mechanism of resistance is better understood for benzimidazoles; therefore, it offers a potential opportunity to expand molecular diagnostic tests for drugs of this class [141]. For example, in Brazil, some studies were conducted using the β-tubulin isotype gene, a marker to monitor resistance [141,142,143]. In addition, molecular characterization is an essential tool for the validation and phylogenetic analysis of nematodes, such as allele-specific polymerase chain reaction, endpoint polymerase chain reaction (PCR), semi-quantitative PCR, quantitative PCR (qPCR), high-resolution melt curve analysis (HRMC) and “Nemabiome” internal transcribed spacer 2 (ITS-2) amplicon sequencing [144,145].
A recent development in large-scale surveillance is the “Nemabiome” approach, which applies deep amplicon sequencing of barcoded PCR products [146]. Although initially developed for species identification and quantification, it has recently been adapted to assess the presence of resistance by benzimidazoles by deep sequencing of β-tubulin amplicons [147]. In general, molecular tests have greater sensitivity and specificity and can provide powerful tools to overcome many of the disadvantages of classical methods of AR. However, it requires further research to be used as a practical universal tool in the field.

5. How to Prevent AR Development?

It has already been proved that the excessive and incorrect use of anthelmintics to control GIN infections has resulted in AR. However, concerns about the use of these products are more comprehensive than studies of AR itself. Recently, with the improvement in awareness about the consumption of organic products, there has been a rise in concern with the potential residual effect of these products in meat and milk, derived products from ruminants that are widely consumed worldwide [148]. Despite reducing the withdrawal period, the risks associated with residues in milk intended for human consumption and dairy products may be present and should be considered [149]. For example, a study with moxidectin demonstrated that this molecule may be present in goat milk for up to 21 days [150]. Additionally, to the direct consequence of using anthelmintics, the excretion of these by-products may also be considered an essential threat from an environmental perspective [151]. The access of anthelmintic residues into the environment resulting from the direct excretion of the original drugs and metabolites in pastures during grazing, as well as through the dispersion of the manure and slurry containing anthelmintic residues, represents a potential risk for the environment [152].
Hence, studies focusing on controlling GIN but with a rational use of these chemical molecules might be encouraged. Investigating the antiparasitic activity of natural bioproducts can contribute to the development of alternative treatments and a reduction in dependence on conventional chemotherapy [153]. The antiparasitic activity of plants derives mainly from biologically active compounds known as secondary metabolites, which could lead to the detection of new antiparasitic molecules [154]. For example, flavonoids and condensed tannins may have anthelmintic effects, as demonstrated in a study inhibiting in vitro sheathing of larvae (L3) of H. contortus [155]. In addition, using nanoparticles can provide good results in the treatment of parasitic infections because they increase the bioavailability and biodistribution of drugs. However, the safety of using nanoparticles from a broader perspective needs to be better investigated [156,157].
So far, most of the studies have been conducted in lab conditions, as they have low cost, repeatability and allow the use of different stages (i.e., eggs and larvae) [152]. Although these plant alternatives can be cheap and accessible, they have limitations. These molecules’ potential adverse toxicity effects in vivo are generally controversial or completely unknown [157,158]. In vivo studies consist of oral administration of the leaves (fresh, hay and flour), aqueous or ethanolic extracts and oil of plants to ruminants infected naturally or experimentally with GIN [151,159]. Therefore, the association of standardized in vivo and in vitro methods is paramount for evaluating the effectiveness of plant products, especially for the determination of EC50 and EC90 (50% and 90% maximal effective concentration, respectively), which allows comparing the activities of different plants [160].
In order to postpone the development of AR, it is necessary to integrate GIN control measures. Therefore, some factors are essential to be considered: (i) good management has a direct effect on the health of animals with feeders and drinkers that avoid waste and contamination [161]; (ii) strategies such as grazing rotation, co-grazing with other appropriate species and manure management are alternatives to reduce the use of anthelmintics [162]; (iii) the improvement of animal resistance through genetic selection to reduce the use of chemoprophylaxis [163]; and (iv) to optimize the effectiveness of anthelmintics in populations of multiresistant nematodes, drug combinations can be used [114]. It is worth emphasizing the importance of carrying out anthelmintic efficacy tests for choosing the chemical groups to be used. The need to develop new anthelmintics for the management of AR is evident; however, it is a slow and expensive process [164]. Furthermore, it is crucial to use existing anthelmintics in a way that minimizes the impact of AR [165].

6. Conclusion Remarks and Perspective for Future Research

The present review demonstrates that AR is an urgent and emerging issue for ruminant production in Brazil, especially in the southern and northeastern regions, where most of the data discussed herein were produced. It is necessary to evaluate on a large scale the distribution and management of anthelmintic drugs currently available and discuss strategies to prevent the development of this phenomenon. Technological advances in diagnostic tools associated with individual management of animals with continuous monitoring are fundamental issues to better guide the control of GIN infections. Several challenges remain, and we hope to enter a new anthelmintic era, including innovative, integrated control approaches and more sensitive and cost-effective diagnostic tools.

Author Contributions

Conceptualization, L.O.M. and R.A.N.R.; writing—original draft preparation, L.O.M., R.A.N.R., S.S.S., L.C.A. and G.A.C.; writing—review and editing, L.O.M., R.A.N.R., S.S.S., L.C.A. and G.A.C.; figure editing, L.O.M. and S.S.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received external funding from the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) (Grant number: APQ-1481-5.05/22).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

This article is based on the post-doctoral stage of the first author, developed at the Federal University of the Agreste of Pernambuco, and supported by a grant fellowship from the Fundação de Amaparo a Ciência e Tecnologia do Estado de Pernambuco (FACEPE) and Conselho Nacional de Desenvolvimento Centífico e Tecnológico (CNPq).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Income, N.; Tongshoob, J.; Taksinoros, S.; Adisakwattana, P.; Rotejanaprasert, C.; Maneekan, P.; Kosoltanapiwat, N. Helminth infections in cattle and goats in Kanchanaburi, Thailand, with focus on strongyle nematode infections. Vet. Sci. 2021, 8, 324. [Google Scholar] [CrossRef]
  2. Wang, T.; Vineer, H.R.; Redman, E.; Morosetti, A.; Chen, R.; McFarland, C.; Colwell, D.D.; Morgan, E.R.; Gilleard, J.S. An improved model for the population dynamics of cattle gastrointestinal nematodes on pasture: Parameterisation and field validation for Ostertagia ostertagi and Cooperia oncophora in northern temperate zones. Vet. Parasitol. 2022, 310, 109777. [Google Scholar] [CrossRef] [PubMed]
  3. Chagas, A.C.S.; Tupy, O.; Santos, I.B.D.; Esteves, S.N. Economic impact of gastrointestinal nematodes in Morada Nova sheep in Brazil. Rev. Bras. Parasitol. Vet. 2022, 31, e008722. [Google Scholar] [CrossRef] [PubMed]
  4. Ahuir-Baraja, A.E.; Cibot, F.; Llobat, L.; Garijo, M.M. Anthelmintic resistance: Is a solution possible? Exp. Parasitol. 2021, 230, 108169. [Google Scholar] [CrossRef]
  5. Vieira, V.D.; Feitosa, T.F.; Vilela, V.L.; Azevedo, S.S.; Almeida Neto, J.L.; Morais, D.F.; Ribeiro, A.R.; Athayde, A.C. Prevalence and risk factors associated with goat gastrointestinal helminthiasis in the Sertão region of Paraíba State, Brazil. Trop. Anim. Health Prod. 2014, 46, 355–361. [Google Scholar] [CrossRef]
  6. Almeida, F.A.; Bassetto, C.C.; Amarante, M.R.V.; Albuquerque, A.C.A.; Starling, R.Z.C.; Amarante, A.F.T.D. Helminth infections and hybridization between Haemonchus contortus and Haemonchus placei in sheep from Santana do Livramento, Brazil. Rev. Bras. Parasitol. Vet. 2018, 27, 280–288. [Google Scholar] [CrossRef] [PubMed]
  7. Santos, I.B.; Anholeto, L.A.; Sousa, G.A.; Nucci, A.S.; Gainza, Y.A.; Figueiredo, A.; Santos, L.A.L.; Minho, A.P.; Barioni-Junior, W.; Esteves, S.N.; et al. Investigating the benefits of targeted selective treatment according to average daily weight gain against gastrointestinal nematodes in Morada Nova lambs. Parasitol. Res. 2022, 121, 2433–2444. [Google Scholar] [CrossRef]
  8. Flay, K.J.; Hill, F.I.; Muguiro, D.H. A Review: Haemonchus contortus infection in pasture-based sheep production systems, with a focus on the pathogenesis of anaemia and changes in haematological parameters. Animals 2022, 12, 1238. [Google Scholar] [CrossRef]
  9. Heckler, R.P.; Borges, D.G.; Vieira, M.C.; Conde, M.H.; Green, M.; Amorim, M.L.; Echeverria, J.T.; Oliveira, T.L.; Moro, E.; Van Onselen, V.J.; et al. New approach for the strategic control of gastrointestinal nematodes in grazed beef cattle during the growing phase in central Brazil. Vet. Parasitol. 2016, 221, 123–129. [Google Scholar] [CrossRef]
  10. Oliveira, L.D.S.S.C.B.; Dias, F.G.S.; Melo, A.L.T.; Carvalho, L.M.; Silva, E.N.; Araújo, J.V. Bioverm® in the control of nematodes in beef cattle raised in the central-west region of Brazil. Pathogens 2021, 10, 548. [Google Scholar] [CrossRef]
  11. Grisi, L.; Leite, R.C.; Martins, J.R.; Barros, A.T.; Andreotti, R.; Cançado, P.H.; León, A.A.; Pereira, J.B.; Villela, H.S. Reassessment of the potential economic impact of cattle parasites in Brazil. Rev. Bras. Parasitol. Vet. 2014, 23, 150–156. [Google Scholar] [CrossRef] [PubMed]
  12. Oliveira, P.A.; Ruas, J.L.; Riet-Correa, F.; Coelho, A.C.B.; Santos, B.L.; Marcolongo-Pereira, C.; Sallis, E.S.V.; Schild, A.L. Parasitic diseases of cattle and sheep in southern Brazil: Frequency and economic losses estimate. Pesq. Vet. Bras. 2017, 37, 797–801. [Google Scholar]
  13. Coles, G.C.; Jackson, F.; Pomroy, W.E.; Prichard, R.K.; von Samson-Himmelstjerna, G.; Silvestre, A.; Taylor, M.A.; Vercruysse, J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136, 167–185. [Google Scholar] [CrossRef] [PubMed]
  14. Kaminsky, R.; Ducray, P.; Jung, M.; Clover, R.; Rufener, L.; Bouvier, J.; Weber, S.S.; Wenger, A.; Wieland-Berghausen, S.; Goebel, T.; et al. A new class of anthelmintics effective against drug-resistant nematodes. Nature 2008, 452, 176–180. [Google Scholar] [CrossRef]
  15. Fissiha, W.; Kinde, M.Z. Anthelmintic resistance and its mechanism: A Review. Infect. Drug Resist. 2021, 14, 5403–5410. [Google Scholar] [CrossRef]
  16. Borgsteede, F.H.; Dercksen, D.D.; Huijbers, R. Doramectin and albendazole resistance in sheep in The Netherlands. Vet. Parasitol. 2007, 144, 180–183. [Google Scholar] [CrossRef]
  17. Scheuerle, M.C.; Mahling, M.; Pfister, K. Anthelminthic resistance of Haemonchus contortus in small ruminants in Switzerland and Southern Germany. Wien. Klin. Wochenschr. 2009, 121, 46–49. [Google Scholar] [CrossRef] [PubMed]
  18. Geurden, T.; Hoste, H.; Jacquiet, P.; Traversa, D.; Sotiraki, S.; Regalbono, A.F.; Tzanidakis, N.; Kostopoulou, D.; Gaillac, C.; Privat, S.; et al. Anthelmintic resistance and multidrug resistance in sheep gastro-intestinal nematodes in France, Greece and Italy. Vet. Parasitol. 2014, 201, 59–66. [Google Scholar] [CrossRef]
  19. Vattaa, A.F.; Lindberg, A.L. Managing anthelmintic resistance in small ruminant livestock of resource-poor farmers in South Africa. J. S. Afr. Vet. Assoc. 2006, 77, 2–8. [Google Scholar] [CrossRef]
  20. Tsotetsi, A.M.; Njiro, S.; Katsande, T.C.; Moyo, G.; Baloyi, F.; Mpofu, J. Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in Gauteng Province, South Africa. Trop. Anim. Health Prod. 2013, 45, 751–761. [Google Scholar] [CrossRef]
  21. Mphahlele, M.; Tsotetsi-Khambule, A.M.; Moerane, R.; Mashiloane, M.L.; Thekisoe, O.M.M. Risk factors associated with occurrence of anthelmintic resistance in sheep of resource-poor farmers in Limpopo province, South Africa. Trop. Anim. Health Prod. 2019, 51, 555–563. [Google Scholar] [CrossRef]
  22. Rialch, A.; Vatsya, S.; Kumar, R.R. Detection of benzimidazole resistance in gastrointestinal nematodes of sheep and goats of sub-Himalyan region of northern India using different tests. Vet. Parasitol. 2013, 198, 312–328. [Google Scholar] [CrossRef]
  23. Dey, A.R.; Begum, N.; Anisuzzaman; Alim, M.A.; Alam, M.Z. Multiple anthelmintic resistance in gastrointestinal nematodes of small ruminants in Bangladesh. Parasitol. Int. 2020, 77, 102105. [Google Scholar] [CrossRef] [PubMed]
  24. Waghorn, T.S.; Leathwick, D.M.; Rhodes, A.P.; Lawrence, K.E.; Jackson, R.; Pomroy, W.E.; West, D.M.; Moffat, J.R. Prevalence of anthelmintic resistance on sheep farms in New Zealand. N. Z. Vet. J. 2006, 6, 271–277. [Google Scholar] [CrossRef]
  25. Lyndal-Murphy, M.; Ehrlich, W.K.; Mayer, D.G. Anthelmintic resistance in ovine gastrointestinal nematodes in inland southern Queensland. Aust. Vet. J. 2014, 92, 415–420. [Google Scholar] [CrossRef] [PubMed]
  26. Playford, M.C.; Smith, A.N.; Love, S.; Besier, R.B.; Kluver, P.; Bailey, J.N. Prevalence and severity of anthelmintic resistance in ovine gastrointestinal nematodes in Australia (2009–2012). Aust. Vet. J. 2014, 12, 464–471. [Google Scholar] [CrossRef] [PubMed]
  27. Howell, S.B.; Burke, J.M.; Miller, J.E.; Terrill, T.H.; Valencia, E.; Williams, M.J.; Williamson, L.H.; Zajac, A.M.; Kaplan, R.M. Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. J. Am. Vet. Med. Assoc. 2008, 233, 1913–1919. [Google Scholar] [CrossRef] [PubMed]
  28. Falzon, L.C.; Menzies, P.I.; Shakya, K.P.; Jones-Bitton, A.; Vanleeuwen, J.; Avula, J.; Stewart, H.; Jansen, J.T.; Taylor, M.A.; Learmount, J.; et al. Anthelmintic resistance in sheep flocks in Ontario, Canada. Vet. Parasitol. 2013, 193, 150–162. [Google Scholar] [CrossRef]
  29. Melo, L.R.B.; Sousa, L.C.; Menezes, C.S.O.; Alvares, F.B.V.; Ferreira, L.C.; Bezerra, R.A.; Athayde, A.C.R.; Feitosa, T.F.; Vilela, V.L.R. Resistance of bovine gastrointestinal nematodes to four classes of anthelmintics in the semiarid region of Paraíba state, Brazil. Rev. Bras. Parasitol. Vet. 2021, 30, e010921. [Google Scholar] [CrossRef]
  30. Nascimento, L.S.; Evaristo, A.M.C.F.; Oliveira, G.M.B.; Ferreira, M.S.; Silva, D.L.R.; Azevedo, S.S.; Yamamoto, S.M.; Araújo, M.M.; Horta, M.C. Anthelmintic resistance of gastrointestinal nematodes in sheep grazing in irrigated and dry areas in the semiarid region of northeastern Brazil. Trop. Anim. Health Prod. 2021, 53, 267. [Google Scholar] [CrossRef]
  31. Kaplan, R.M. Drug resistance in nematodes of veterinary importance: A status report. Trends Parasitol. 2004, 10, 477–481. [Google Scholar] [CrossRef] [PubMed]
  32. Kaplan, R.M.; Vidyashankar, A.N. An inconvenient truth: Global warming and anthelmintic resistance. Vet. Parasitol. 2012, 186, 70–88. [Google Scholar] [CrossRef]
  33. Santos, V.T.; Gonçalves, P.C. Verificação de estirpe resistente de Haemonchus resistente ao thiabendazole no Rio Grande do Sul (Brasil). Rev. FZVA 1967, 9, 201–209. [Google Scholar]
  34. Echevarria, F.A.M.; Trindade, G.N.P. Anthelmintic resistance by Haemonchus contortus to ivermectin in Brazil: A preliminary report. Vet. Rec. 1989, 124, 147–148. [Google Scholar] [CrossRef]
  35. Vieira, L.S.; Gonçalves, P.C.; Costa, C.A.F.; Berne, M.E.A. Redução e esterilização de ovos de nematódeos gastrintestinais em caprinos medicados com anti-helmínticos benzimidazóis. Pesq. Agrop. Bras. 1989, 24, 1255–1265. [Google Scholar]
  36. Charles, T.P.; Pompeu, J.; Miranda, D.B. Efficacy of three broad-spectrum anthelmintics against gastrointestinal nematode infections of goats. Vet. Parasitol. 1989, 34, 71–75. [Google Scholar] [CrossRef] [PubMed]
  37. Pinheiro, A.C.; Echevarria, F.A.M. Susceptibility of Haemonchus spp. in cattle to anthelmintic treatment with Albendazole and Oxfendazole. Pesq. Vet. Bras. 1990, 10, 19–21. [Google Scholar]
  38. Salgado, J.A.; Santos, C.P. Overview of anthelmintic resistance of gastrointestinal nematodes of small ruminants in Brazil. Rev. Bras. Parasitol. Vet. 2016, 1, 3–17. [Google Scholar] [CrossRef] [PubMed]
  39. Jaeger, L.H.; Carvalho-Costa, F.A. Status of benzimidazole resistance in intestinal nematode populations of livestock in Brazil: A systematic review. BMC Vet. Res. 2017, 13, 358. [Google Scholar] [CrossRef]
  40. Denwood, M.J.; Kaplan, R.M.; McKendrick, I.J.; Thamsborg, S.M.; Nielsen, M.K.; Levecke, B. A statistical framework for calculating prospective sample sizes and classifying efficacy results for faecal egg count reduction tests in ruminants, horses and swine. Vet. Parasitol. 2023, 314, 109867. [Google Scholar] [CrossRef]
  41. Santiago, M.A.M.; Costa, U.C.; Benevenga, S. Trichostrongylus colubriformis resistente ao levamisole. Rev. Cent. Cienc. Rur. Univ. Fed. St. Maria 1977, 7, 421–422. [Google Scholar]
  42. Santiago, M.A.M.; Costa, U.C.; Benevenga, S.F. Haemonchus contortus e Ostertagia circumcincta resistente ao levamisole. Rev. Cent. Ciênc. Rurais Univ. Fed. St. Maria 1979, 9, 101–103. [Google Scholar]
  43. Santiago, M.A.M.; Costa, U.C. Resistência de Haemonchus contortus, Trichostrongylus colubriformis, Trichostrongylus colubriformis e Ostertagia spp., ao levamisole. Rev. Cent. Ciênc. Rurais Univ. Fed. St. Maria 1979, 9, 9315–9318. [Google Scholar]
  44. Santiago, M.A.M.; Costa, U.C.; Benevenga, S.F.; Macedo, N. Resistência de Haemonchus contortus à rafoxanida, em ovinos. Pesq. Agropec. Bras. 1982, 17, 1361–1362. [Google Scholar]
  45. Echevarria, F.; Pinheiro, A.C. Evaluation of anthelmintic resistance in sheep flocks in the municipality of Bagé. Rio Grande do Sul. Pesqui. Vet. Bras. 1989, 9, 69–71. [Google Scholar]
  46. Echevarria, F.; Borba, M.F.S.; Pinheiro, A.C.; Waller, P.J.; Hansen, J.W. The prevalence of anthelmintic resistance in nematode parasites of sheep in Southern Latin America: Brazil. Vet. Parasitol. 1996, 62, 199–206. [Google Scholar] [CrossRef]
  47. Thomaz-Soccol, V.T.; Sotomaior, C.; Souza, F.P.; Castro, E.A.; Silva, M.C.P.; Milczewski, V. Occurrence of resistance to anthelmintics in sheep in Parana State, Brazil. Vet. Rec. 1996, 139, 421–422. [Google Scholar] [CrossRef] [PubMed]
  48. Farias, M.T.; Brodin, E.L.; Forbes, A.B.; Newcomb, K. A survey on resistance to anthelmintics in sheep stud farms of southern Brazil. Vet. Parasitol. 1997, 72, 209–214. [Google Scholar] [CrossRef] [PubMed]
  49. Thomaz-Soccol, V.; Souza, F.P.; Sotomaior, C.; Castro, E.A.; Milczewski, V.; Mocelin, G.; Silva, M.C.P. Resistance of gastrointestinal nematodes to anthelmintics in sheep (Ovis aries). Braz. Arch. Biol. Technol. 2004, 47, 41–47. [Google Scholar] [CrossRef]
  50. Ramos, C.I.; Bellato, V.; Ávila, V.S.; Coutinho, G.C.; Souza, A.P. Gastro-intestinal parasites resistance in sheep to some anthelmintics in Santa Catarina state, Brazil. Cienc. Rural 2002, 32, 473–477. [Google Scholar] [CrossRef]
  51. Cunha, L.F.C.F.; Toledo, G.S.; Grecco, F.C.A.R.; Guerra, J.L. Eficácia da associação closantel albendazol e ivermectina 3,5 no controle da helmintose de ovinos da Região Norte do Estado do Paraná. UNOPAR Cient. Ciênc. Biol. Saud. 2008, 10, 23–28. [Google Scholar]
  52. Klauck, V.; Pazinato, R.; Lopes, L.S.; Cucco, D.C.; Lima, H.L.; Volpato, A.; Radavelli, W.M.; Stefani, L.C.M.; Silva, A.S.D. Trichostrongylus and Haemonchus anthelmintic resistance in naturally infected sheep from southern Brazil. An. Acad. Bras. Cienc. 2014, 86, 777–784. [Google Scholar] [CrossRef]
  53. Cintra, M.C.; Teixeira, V.N.; Nascimento, L.V.; Sotomaior, C.S. Lack of efficacy of monepantel against Trichostrongylus colubriformis in sheep in Brazil. Vet. Parasitol. 2016, 216, 4–6. [Google Scholar] [CrossRef] [PubMed]
  54. Costa, P.T.; Costa, R.T.; Mendonça, G.; Vaz, R.Z. Eficácia anti-helmíntica comparativa do nitroxinil, levamisol, closantel, moxidectina e fenbendazole no controle parasitário em ovinos. Bol. Ind. Anim. 2017, 74, 72–78. [Google Scholar] [CrossRef]
  55. Oliveira, P.A.; Riet-Correa, B.; Estima-Silva, P.; Coelho, A.C.B.; Santos, B.L.D.; Costa, M.A.P.; Ruas, J.L.; Schild, A.L. Multiple anthelmintic resistance in Southern Brazil sheep flocks. Rev. Bras. Parasitol. Vet. 2017, 26, 427–432. [Google Scholar] [CrossRef] [PubMed]
  56. Ramos, F.; Portella, L.P.; Rodrigues, F.D.S.; Reginato, C.Z.; Cezar, A.S.; Sangioni, L.A.; Vogel, F.S. Anthelminthic resistance of gastrointestinal nematodes in sheep to monepantel treatment in central region of Rio Grande do Sul, Brazil. Pesq. Vet. Bras. 2018, 38, 48–52. [Google Scholar] [CrossRef]
  57. Ramos, F.; Marques, C.B.; Reginato, C.Z.; Bräunig, P.; Osmari, V.; Fernandes, F.; Sangioni, L.A.; Vogel, F.S.F. Field and molecular evaluation of anthelmintic resistance of nematode populations from cattle and sheep naturally infected pastured on mixed grazing areas at Rio Grande do Sul, Brazil. Acta Parasitol. 2020, 65, 118–127. [Google Scholar] [CrossRef]
  58. Amarante, A.F.T.; Barbosa, M.A.; Oliveira, M.A.G.; Carmello, M.J.; Padovanni, C.R. Efeito da administração de oxfendazol, ivermectina e levamisol sobre os exames coproparasitológicos de ovinos. Braz. J. Vet. Res. Anim. Sci. 1992, 29, 31–38. [Google Scholar] [CrossRef]
  59. Nagata, W.B.; Panegossi, M.F.C.; Bresciani, K.D.S.; Gomes, J.F.; Kaneto, C.N.; Perri, S.H.V. Resistance of gastrointestinal nematodes to five different active principles in sheep infected naturally in São Paulo State, Brazil. Small Rumin. Res. 2019, 172, 48–50. [Google Scholar] [CrossRef]
  60. Batista, L.F.; Oliveira, L.L.D.S.; Silva, F.V.E.; Lima, W.D.S.; Pereira, C.A.J.; Rocha, R.H.F.; Santos, I.S.; Dias Júnior, J.A.; Alves, C.A. Anthelmintic resistance in sheep in the semiarid region of Minas Gerais, Brazil. Vet. Parasitol. Reg. Stud. Rep. 2023, 37, 100821. [Google Scholar] [CrossRef]
  61. Vieira, L.S.; Berne, M.E.A.; Cavalcante, A.C.R.; Costa, C.A.F. Haemonchus contortus resistance to ivermectin and netobimin in Brazilian sheep. Vet. Parasitol. 1992, 45, 111–116. [Google Scholar] [CrossRef] [PubMed]
  62. Melo, L.R.; Vilela, V.L.; Feitosa, T.F.; Almeida Neto, J.L.; Morais, D.F. Resistência anti-helmíntica em pequenos ruminantes do semiárido da Paraíba, Brasil. Arq. Vet. 2013, 29, 104–108. [Google Scholar] [CrossRef]
  63. Silva, F.; Bezerra, H.M.F.F.; Feitosa, T.F.; Vilela, V.L.R. Nematode resistance to five anthelmintic classes in naturally infected sheep herds in Northeastern Brazil. Rev. Bras. Parasitol. Vet. 2018, 27, 423–429. [Google Scholar] [CrossRef]
  64. Ahid, S.M.M.; Cavalcante, M.D.A.; Bezerra, A.C.D.; Soares, H.S.; Pereira, R.H.M. Eficácia anti-helmíntica em rebanho caprino no Estado de Alagoas, Brasil. Acta Vet. Bras. 2007, 1, 56–59. [Google Scholar]
  65. Chagas, A.C.S.; Vieira, L.S.; Aragão, W.R.; Navarro, A.M.C.; Villela, L.C.V. Anthelmintic action of eprinomectin in lactating Anglo-Nubian goats in Brazil. Parasitol. Res. 2007, 100, 391–394. [Google Scholar] [CrossRef] [PubMed]
  66. Lima, W.C.; Athayde, A.C.; Medeiros, G.R.; Lima, D.A.; Borburema, J.B.; Santos, E.M.; Vilela, V.L.R.; Azevedo, S.S. Nematóides resistentes a alguns anti-helmínticos em rebanhos caprinos no Cariri Paraibano. Pesq. Vet. Bras. 2010, 30, 1003–1009. [Google Scholar] [CrossRef]
  67. Felippelli, G.; Lopes, W.D.; Cruz, B.C.; Teixeira, W.F.; Maciel, W.G.; Fávero, F.C.; Buzzulini, C.; Sakamoto, C.; Soares, V.E.; Gomes, L.V.; et al. Nematode resistance to ivermectin (630 and 700 μg/kg) in cattle from the Southeast and South of Brazil. Parasitol. Int. 2014, 63, 835–840. [Google Scholar] [CrossRef]
  68. Lopes, W.D.; Santos, T.R.; Borges, F.A.; Sakamoto, C.A.; Soares, V.E.; Costa, G.H.; Camargo, G.; Pulga, M.E.; Bhushan, C.; Costa, A.J. Anthelmintic efficacy of oral trichlorfon solution against ivermectin resistant nematode strains in cattle. Vet. Parasitol. 2009, 166, 98–102. [Google Scholar] [CrossRef]
  69. Lopes, W.D.; Teixeira, W.F.; Felippelli, G.; Cruz, B.C.; Maciel, W.G.; Soares, V.E.; Santos, T.R.; Matos, L.V.; Fávero, F.C.; Costa, A.J. Assessing resistance of ivermectin and moxidectin against nematodes in cattle naturally infected using three different methodologies. Res. Vet. Sci. 2014, 96, 133–138. [Google Scholar] [CrossRef]
  70. Feliz, D.C. Anthelmintic Resistance of Gastrointestinal Nematodes in Beef Cattle in the Mato Grosso do Sul State, Brazil; Federal University of Mato Grosso do Sul: Campo Grande, Brazil, 2011; 51p. [Google Scholar]
  71. Borges, F.A.; Borges, D.G.; Heckler, R.P.; Neves, J.P.; Lopes, F.G.; Onizuka, M.K. Multispecies resistance of cattle gastrointestinal nematodes to long-acting avermectin formulations in Mato Grosso do Sul. Vet. Parasitol. 2015, 212, 299–302. [Google Scholar] [CrossRef] [PubMed]
  72. Silva, W.W.; Delfino, L.J.B.; Medeiros, M.C.; Silva, J.P. Multiple resistances of gastrointestinal nematodes to anthelmintic groups in cattle of semiarid of Paraíba, Brazil. Act. Vet. Bras. 2017, 1, 29–32. [Google Scholar] [CrossRef]
  73. Fiel, C.A.; Saumell, C.A.; Steffan, P.E.; Rodriguez, E.M. Resistance of Cooperia to ivermectin treatments in grazing cattle of the Humid Pampa, Argentina. Vet. Parasitol. 2001, 97, 211–217. [Google Scholar] [CrossRef] [PubMed]
  74. Cunha, L.F.C.F.; Pereira, A.B.L.; Yamamura, M.H. Resistência a anti-helmínticos em ovinos da região de Londrina-Paraná-Brasil. Semin. Cien. Agrárias 1998, 19, 31–37. [Google Scholar] [CrossRef]
  75. Rosalinski-Moraes, F.; Moretto, L.H.; Bresolin, W.S.; Gabrielli, I.; Kafer, L.; Zanchet, I.K.; Sonaglio, F.; Thomaz-Soccol, V. Resistência anti-helmíntica em rebanhos ovinos da região da associação dos municípios do alto Irani (AMAI), Oeste de Santa Catarina. Cienc. Anim. Bras. 2007, 8, 559–565. [Google Scholar]
  76. Cezar, A.S.; Toscan, G.; Camillo, G.; Sangioni, L.A.; Ribas, H.O.; Vogel, F.S. Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Vet. Parasitol. 2010, 173, 157–160. [Google Scholar] [CrossRef] [PubMed]
  77. Buzzulini, C.; Silva, A.G.S.S.; Costa, A.J.; Santos, T.R.; Borges, F.A.; Soares, V.E. Eficácia anti-helmíntica comparativa da associação albendazole, levamisole e ivermectina à moxidectina em ovinos. Pesq. Agrop. Bras. 2007, 42, 891–895. [Google Scholar] [CrossRef]
  78. Almeida, F.A.; Garcia, K.C.; Torgerson, P.R.; Amarante, A.F. Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitol. Int. 2010, 59, 622–625. [Google Scholar] [CrossRef]
  79. Cruz, D.G.; Rocha, L.O.; Arruda, S.S.; Palieraqui, J.G.; Cordeiro, R.C.; Santos, E., Jr.; Molento, M.B.; Santos, C.P. Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil. Vet. Parasitol. 2010, 170, 340–343. [Google Scholar] [CrossRef]
  80. Duarte, E.R.; Silva, R.B.; Vasconcelos, V.O.; Nogueira, F.A.; Oliveira, N.J.F. Diagnóstico do controle e perfil de sensibilidade de nematódeos de ovinos ao albendazol e ao levamisol no norte de Minas Gerais. Pesq. Vet. Bras. 2012, 32, 147–152. [Google Scholar] [CrossRef]
  81. Veríssimo, C.J.; Niciura, S.C.; Alberti, A.L.; Rodrigues, C.F.; Barbosa, C.M.; Chiebao, D.P.; Cardoso, D.; Silva, G.S.; Pereira, J.R.; Margatho, L.F.; et al. Multidrug and multispecies resistance in sheep flocks from São Paulo state, Brazil. Vet. Parasitol. 2012, 187, 209–216. [Google Scholar] [CrossRef]
  82. Bichuette, M.A.; Lopes, W.D.Z.; Gomes, L.V.C.; Felippelli, G.; Cruz, B.C.; Maciel, W.G.; Teixeira, W.F.P.; Buzzulini, C.; Prando, L.; Soares, V.V.E.; et al. Susceptibility of helminth species parasites of sheep and goats to different chemical compounds in Brazil. Small Rum. Res. 2015, 133, 93–101. [Google Scholar] [CrossRef]
  83. Gainza, Y.A.; Santos, I.B.D.; Figueiredo, A.; Santos, L.A.L.D.; Esteves, S.N.; Barioni-Junior, W.; Minho, A.P.; Chagas, A.C.S. Anthelmintic resistance of Haemonchus contortus from sheep flocks in Brazil: Concordance of in vivo and in vitro (RESISTA-Test©) methods. Rev. Bras. Parasitol. Vet. 2021, 30, e025120. [Google Scholar] [CrossRef]
  84. Viana, M.V.G.; Silva, Y.H.; Martins, I.V.F.; Scott, F.B. Resistance of Haemonchus contortus to monepantel in sheep: First report in Espírito Santo, Brazil. Braz. J. Vet. Parasitol. 2021, 30, e013121. [Google Scholar] [CrossRef] [PubMed]
  85. Sczesny-Moraes, E.A.; Bianchin, I.; Silva, K.F.D.; Catto, J.B.; Honer, M.R.; Paiva, F. Resistência anti-helmíntica de nematóides gastrintestinais em ovinos, Mato Grosso do Sul. Pesq. Vet. Bras. 2010, 30, 229–236. [Google Scholar] [CrossRef]
  86. Melo, A.C.F.L.; Bevilaqua, C.M.L.; Selaive, A.V.; Girão, M.D. Anthelmintic resistance of gastrointestinal nematodes from sheep and goats, in Pentecoste county, State of Ceará. Cienc. Anim. Bras. 1998, 8, 7–11. [Google Scholar]
  87. Melo, A.C.F.L.; Reis, I.S.; Bevilaqua, C.M.L.; Vieira, L.S.; Echevarria, F.A.M.; Melo, L.M. Nematódeos resistentes a anti-helmíntico em rebanhos de ovinos e caprinos do estado do Ceará, Brasil. Cienc. Rural 2003, 33, 339–344. [Google Scholar] [CrossRef]
  88. Melo, A.C.F.L.; Rondon, F.C.M.; Reis, I.S.; Bevilaqua, C.M.L. Desenvolvimento da resistência ao oxfendazol em propriedades rurais de ovinos na região do Baixo e Médio Jaguaribe, Ceará, Brasil. Braz. J. Vet. Parasitol. 2004, 13, 137–141. [Google Scholar]
  89. Pereira, R.H.M.A.; Ahid, S.M.M.; Bezerra, A.C.D.S.; Soares, H.S.; Fonseca, Z.A.A.S. Diagnosis of nematodes gastrintestinal resistance to antihelminthic in goats and sheep from Rio Grande do Norte state, Brazil. Acta Vet. Bras. 2008, 2, 16–19. [Google Scholar]
  90. Lima, M.M.D.; Farias, M.P.O.; Romeiro, E.T.; Ferreira, D.R.A.; Alves, L.C.; Faustino, M.A.D.G. Eficácia da moxidectina, ivermectina e albendazole contra helmintos gastrintestinais em propriedades de criação caprina e ovina no estado de Pernambuco. Ciênc. Anim. Bras. 2010, 11, 94–100. [Google Scholar] [CrossRef]
  91. Araújo-Filho, J.V.; Ribeiro, W.L.C.; André, W.P.P.; Cavalcante, G.S.; Santos, J.M.L.; Monteiro, J.P.; Macedo, I.T.F.; Oliveira, L.M.B.; Bevilaqua, C.M.L. Phenotypic and genotypic approaches for detection of anthelmintic resistant sheep gastrointestinal nematodes from Brazilian northeast. Braz. J. Vet. Parasitol. 2021, 30, e005021. [Google Scholar] [CrossRef]
  92. Mattos, M.J.T.D.; Schmidt, V.; Bastos, C.D. Atividade ovicida de dois fármacos em caprinos naturalmente parasitados por nematódeos gastrintestinais, RS, Brasil. Ciênc. Rural 2000, 30, 893–895. [Google Scholar] [CrossRef]
  93. Mattos, M.J.T.; Oliveira, C.M.B.M.; Gouveam, A.S.; Andrade, C.B. Macrocyclic lactone-resistant strains of Haemonchus in naturally infected goats. Cienc. Rural 2004, 34, 883–884. [Google Scholar]
  94. Hammerschmidt, J.; Bier, D.; Fortes, F.S.; Warzensaky, P.; Bainy, A.M.; Macedo, A.A.S.; Molento, M.B. Avaliação do sistema integrado de controle parasitário em uma criação semi-intensiva de caprinos na região de Santa Catarina. Arq. Bras. Med. Vet. Zootec. 2012, 64, 927–934. [Google Scholar] [CrossRef]
  95. Cintra, M.C.R.; Teixeira, V.N.; Nascimento, L.V.; Ollhoff, R.D.; Sotomaior, C.S. Monepantel resistant Trichostrongylus colubriformis in goats in Brazil. Vet. Parasitol. Reg. Stud. Rep. 2018, 11, 12–14. [Google Scholar] [CrossRef]
  96. Vieira, L.S.; Cavalcante, A.C.R. Resistência anti-helmíntica em rebanhos caprinos no Estado do Ceará. Pesq. Vet. Bras. 1999, 19, 99–103. [Google Scholar] [CrossRef]
  97. Rodrigues, A.B.; Athayde, A.C.R.; Rodrigues, O.G. Silva WW, Faria EB. Sensibilidade dos nematóides gastrintestinais de caprinos a anti-helmínticos na mesorregião do Sertão Paraibano. Pesq. Vet. Bras. 2007, 27, 162–166. [Google Scholar] [CrossRef]
  98. Coelho, W.A.C.; Ahid, S.M.M.; Vieira, L.S.; Fonseca, Z.A.A.S.; Silva, I.P. Resistência anti-helmíntica em caprinos no município de Mossoró, RN. Cienc. Anim. Bras. 2010, 11, 589–599. [Google Scholar] [CrossRef]
  99. Sousa, A.L.D.S.O.; Athayde, A.C.R.; Olinto, F.A. Sensibilidade dos nematóides gastrintestinais de caprinos leiteiros à anti-helmínticos no Município de Sumé, Paraíba, Brasil. Agrop. Cient. Semiárido 2010, 9, 33–36. [Google Scholar]
  100. Borges, S.L.; Oliveira, A.A.; Mendonça, L.R.; Lambert, S.M.; Viana, J.M.; Nishi, S.M.; Julião, F.S.; Almeida, M.A.O. Resistência anti-helmíntica em rebanhos caprinos nos biomas Caatinga e Mata Atlântica. Pesq. Vet. Bras. 2015, 35, 643–648. [Google Scholar] [CrossRef]
  101. Castro, E.M.S.; Souza, E.A.R.; Dantas, A.C.S.; Silva, I.W.G.; Araújo, M.M.; Azevedo, S.S.; Sangioni, L.A.; Horta, M.C. Parasitic resistance of gastrointestinal nematodes in goats from the semiarid region of Pernambuco, Northeastern Brazil. Vet. Zootec. 2021, 28, 1–12. [Google Scholar]
  102. Kaplan, R.M. Biology, epidemiology, diagnosis, and management of anthelmintic resistance in gastrointestinal nematodes of livestock. Vet. Clin. N. Am. Food Anim. Pract. 2020, 36, 17–30. [Google Scholar] [CrossRef] [PubMed]
  103. Wang, C.; Li, F.; Zhang, Z.; Yang, X.; Ahmad, A.A.; Li, X.; Du, A.; Hu, M. Recent research progress in china on Haemonchus contortus. Front. Microbiol. 2017, 8, 1509. [Google Scholar] [CrossRef]
  104. Albuquerque, A.C.A.; Basseto, C.C.; Almeida, F.A.; Amarante, A.F.T. Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Vet. Parasitol. 2017, 246, 112–117. [Google Scholar] [CrossRef] [PubMed]
  105. Kenyon, F.; Jackson, F. Targeted flock/herd and individual ruminant treatment approaches. Vet. Parasitol. 2012, 186, 10–17. [Google Scholar] [CrossRef]
  106. Scott, I.; Pomroy, B.; Paul, K.; Greg, S.; Barbara, A.; Moss, A. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet. Parasitol. 2013, 198, 166–171. [Google Scholar] [CrossRef]
  107. Mederos, A.E.; Ramos, Z.; Banchero, G.E. First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasit. Vectors. 2014, 7, 598. [Google Scholar] [CrossRef]
  108. Niciura, S.C.M.; Cruvinel, G.G.; Moraes, C.V.; Chagas, A.C.S.; Esteves, S.N.; Benavides, M.V.; Amarante, A.F.T. In vivo selection for Haemonchus contortus resistance to monepantel. J. Helminthol. 2020, 94, e46. [Google Scholar] [CrossRef]
  109. Gasbarre, L.C. Anthelmintic resistance in cattle nematodes in the US. Vet. Parasitol. 2014, 204, 3–11. [Google Scholar] [CrossRef] [PubMed]
  110. Leathwick, D.M.; Luo, D. Managing anthelmintic resistance—Variability in the dose of drug reaching the target worms influences selection for resistance? Vet. Parasitol. 2017, 243, 29–35. [Google Scholar] [CrossRef]
  111. Baiak, B.H.B.; Lehnen, C.B.; Rocha, R.A. Anthelmintic resistance of injectable macrocyclic lactones in cattle: A systematic review and meta-analysis. Rev. Bras. Parasitol. Vet. 2019, 28, 59–67. [Google Scholar] [CrossRef]
  112. Souza, A.P.D.; Ramos, C.I.; Bellato, V.; Sartor, A.A.; Schelbauer, C.A. Resistência de helmintos gastrintestinais de bovinos a anti-helmínticos no Planalto Catarinense. Ciênc. Rural 2008, 38, 1363–1367. [Google Scholar] [CrossRef]
  113. Cezar, A.S.; Vogel, F.S.; Sangioni, L.A.; Antonello, A.M.; Camillo, G.; Toscan, G.; Araujo, L.O.D. Ação anti-helmíntica de diferentes formulações de lactonas macrocíclicas em cepas resistentes de nematódeos de bovinos. Pesq. Vet. Bras. 2010, 30, 523–528. [Google Scholar] [CrossRef]
  114. Ramos, F.; Portella, L.P.; Rodrigues, F.S.; Reginato, C.Z.; Pötter, L.; Cezar, A.S.; Sangioni, L.A.; Vogel, F.S.F. Anthelmintic resistance in gastrointestinal nematodes of beef cattle in the state of Rio Grande do Sul, Brazil. Int. J. Parasitol. Drugs Drug Resist. 2016, 6, 93–101. [Google Scholar] [CrossRef] [PubMed]
  115. Pivoto, F.L.; Cezar, A.S.; Vogel, F.S.F.; Leal, M.L.D.R. Effects of long-term indiscriminate use of macrocyclic lactones in cattle: Parasite resistance, clinical helminthosis, and production losses. Vet. Parasitol. Reg. Stud. Rep. 2020, 20, 100381. [Google Scholar] [CrossRef] [PubMed]
  116. Soutello, R.G.V.; Seno, M.C.Z.; Amarante, A.F.T. Anthelmintic resistance in cattle nematodes in northwestern São Paulo State, Brazil. Vet. Parasitol. 2007, 148, 360–364. [Google Scholar] [CrossRef]
  117. Condi, G.K.; Soutello, R.G.; Amarante, A.F. Moxidectin-resistant nematodes in cattle in Brazil. Vet. Parasitol. 2009, 61, 213–217. [Google Scholar] [CrossRef]
  118. Costa, M.S.V.L.F.; Araújo, R.N.; Costa, A.J.L.F.D.; Simões, R.F.; Lima, W.D.S. Anthelmintic resistance in a dairy cattle farm in the State of Minas Gerais. Rev. Bras. Parasitol. Vet. 2011, 20, 115–120. [Google Scholar] [CrossRef]
  119. Neves, J.H.; Carvalho, N.; Rinaldi, L.; Cringoli, G.; Amarante, A.F. Diagnosis of anthelmintic resistance in cattle in Brazil: A comparison of different methodologies. Vet. Parasitol. 2014, 206, 216–226. [Google Scholar] [CrossRef] [PubMed]
  120. Almeida, G.D.; Feliz, D.C.; Heckler, R.P.; Borges, D.G.; Onizuka, M.K.; Tavares, L.E.; Paiva, F.; Borges, F.A. Ivermectin and moxidectin resistance characterization by larval migration inhibition test in field isolates of Cooperia spp. in beef cattle, Mato Grosso do Sul, Brazil. Vet Parasitol. 2013, 191, 59–65. [Google Scholar] [CrossRef] [PubMed]
  121. Borges, D.G.L.; Conde, M.H.; Cunha, C.C.T.; Freitas, M.G.; Moro, E.; Borges, F.A. Moxidectin: A viable alternative for the control of ivermectin-resistant gastrointestinal nematodes in beef cattle. Acta Vet. 2022, 72, 16–29. [Google Scholar] [CrossRef]
  122. Santos, T.R.; Lopes, W.D.Z.; Buzulini, C.; Borges, F.A.; Sakamoto, C.A.M.; Lima, R.C.A.; Oliveira, G.P.; Costa, A.J. Helminth fauna of bovines from the Central-Western region, Minas Gerais State, Brazil. Cienc. Rural 2010, 40, 934–938. [Google Scholar] [CrossRef]
  123. Coles, G.C.; Stafford, K.A.; Mackay, P.H.S. Ivermectin-resistant Cooperia species from calves on a farm in Somerset. Vet. Rec. 1998, 7, 255–256. [Google Scholar]
  124. Mena, L.A.E.; Arellano, M.E.L.; Gives, P.M.; Hernandez, E.L.; Prats, V.V.; Ycuspinera, G.V. First report in Mexico on ivermectin resistance on naturally infected calves with gastrointestinal nematodes. Vet. Mex. 2008, 39, 423–428. [Google Scholar]
  125. Demeler, J.; Van Zeveren, A.M.J.; Kleinschmidt, N.; Vercruysse, J.; Höglund, J.; Koopmann, R.; Cabaret, J.; Claerebout, E.; Areskog, M.; Von Samson-Himmelstjerna, G. Monitoring the efficacy of ivermectin and albendazole against gastrointestinal nematodes of cattle in Northern Europe. Vet. Parasitol. 2009, 160, 109–115. [Google Scholar] [CrossRef] [PubMed]
  126. Gasbarre, L.C.; Smith, L.L.; Lichtenfels, J.R.; Pilitt, P.A. The identification of cattle nematode parasites resistant to multiple class of anthelmintics in a commercial cattle population in the US. Vet. Parasitol. 2009, 166, 281–285. [Google Scholar] [CrossRef]
  127. Stromberg, B.E.; Gasbarre, L.C.; Waite, A.; Bechtol, D.T.; Brown, M.S.; Robinson, N.A.; Olson, E.J.; Newcomb, H. Cooperia punctata: Effect on cattle productivity? Vet. Parasitol. 2012, 183, 284–291. [Google Scholar] [CrossRef] [PubMed]
  128. Lyndal-Murphy, M.; Rogers, D.; Ehrlich, W.K.; James, P.J.; Pepper, P.M. Reduced efficacy of macrocyclic lactone treatments in controlling gastrointestinal nematode infections of weaner dairy calves in subtropical eastern Australia. Vet. Parasitol. 2010, 168, 146–150. [Google Scholar] [CrossRef]
  129. Rendell, D.K. Anthelmintic resistance in cattle nematodes on 13 south-west Victorian properties. Aust. Vet. J. 2010, 88, 504–509. [Google Scholar] [CrossRef]
  130. Louvandini, H.; Rodrigues, R.R.; Gennari, S.M.; McManus, C.M.; Vitti, D.M.S.S. Phosphorus kinetics in calves experimentally submitted to a trickle infection with Cooperia punctata. Vet. Parasitol. 2009, 163, 47–51. [Google Scholar] [CrossRef]
  131. Coles, G.C.; Bauer, C.; Borgsteede, F.H.; Geerts, S.; Klei, T.R.; Taylor, M.A.; Waller, P.J. 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. [Google Scholar] [CrossRef]
  132. Martin, P.J.; Anderson, N.; Jarrett, R.G. Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Aust. Vet. J. 1989, 66, 236–240. [Google Scholar] [CrossRef] [PubMed]
  133. Kaplan, R.M.; Denwood, M.J.; Nielsen, M.K.; Thamsborg, S.M.; Torgerson, P.R.; Gilleard, J.S.; Dobson, R.J.; Vercruysse, J.; Levecke, B. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guideline for diagnosing anthelmintic resistance using the faecal egg count reduction test in ruminants, horses and swine. Vet. Parasitol. 2023, 318, 109936. [Google Scholar] [CrossRef] [PubMed]
  134. Samson-Himmelstjerna, G.V.; Coles, G.C.; Jackson, F.; Bauer, C.; Borgsteede, F.; Cirak, V.Y.; Demeler, J.; Donnan, A.; Dorny, P.; Epe, C.; et al. Standardization of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes. Parasitol. Res. 2009, 105, 825–834. [Google Scholar] [CrossRef]
  135. Nielsen, M.K. What makes a good fecal egg count technique? Vet. Parasitol. 2021, 296, 109509. [Google Scholar] [CrossRef] [PubMed]
  136. Cringoli, G.; Rinaldi, L.; Maurelli, M.P.; Utzinger, J. FLOTAC: New multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat. Protoc. 2010, 5, 503–515. [Google Scholar] [CrossRef]
  137. Cringoli, G.; Maurelli, M.P.; Levecke, B.; Bosco, A.; Vercruysse, J.; Utzinger, J.; Rinaldi, L. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 2017, 12, 1723–1732. [Google Scholar] [CrossRef] [PubMed]
  138. Kotze, A.C.; Gilleard, J.S.; Doyle, S.R.; Prichard, R.K. Challenges and opportunities for the adoption of molecular diagnostics for anthelmintic resistance. Int. J. Parasitol. Drugs Drug Resist. 2020, 14, 264–273. [Google Scholar] [CrossRef] [PubMed]
  139. Whittaker, J.H.; Carlson, S.A.; Jones, D.E.; Brewer, M.T. Molecular mechanisms for anthelmintic resistance in strongyle nematode parasites of veterinary importance. J. Vet. Pharmacol. Ther. 2017, 40, 105–115. [Google Scholar] [CrossRef]
  140. Silvestre, A.; Humbert, J.F. A molecular tool for species identification and benzimidazole resistance diagnosis in larval communities of small ruminant parasites. Exp. Parasitol. 2000, 95, 271–276. [Google Scholar] [CrossRef]
  141. Niciura, S.C.; Veríssimo, C.J.; Gromboni, J.G.; Rocha, M.I.; Mello, S.S.; Barbosa, C.M.; Chiebao, D.P.; Cardoso, D.; Silva, G.S.; Otsuk, I.P.; et al. F200Y polymorphism in the β-tubulin gene in field isolates of Haemonchus contortus and risk factors of sheep flock management practices related to anthelmintic resistance. Vet. Parasitol. 2012, 190, 608–612. [Google Scholar] [CrossRef]
  142. Chagas, A.M.; Sampaio Junior, F.D.; Pacheco, A.; Cunha, A.B.; Cruz, J.S.; Scofield, A.; Góes-Cavalcante, G. F200Y polymorphism of the β-tubulin isotype 1 gene in Haemonchus contortus and sheep flock management practices related to anthelmintic resistance in eastern Amazon. Vet Parasitol. 2016, 226, 104–108. [Google Scholar] [CrossRef]
  143. Lambert, S.M.; Nishi, S.M.; Mendonça, L.R.; Souza, B.M.P.S.; Julião, F.S.; Gusmão, P.S.; Almeida, M.A.O. Genotypic profile of benzimidazole resistance associated with SNP F167Y and F200Y beta-tubulin gene in Brazilian populations of Haemonchus contortus of goats. Vet. Parasitol. Reg. Stud. Rep. 2017, 8, 28–34. [Google Scholar] [CrossRef] [PubMed]
  144. Qamar, W.; Zaman, M.A.; Faheem, M.; Ahmed, I.; Ali, K.; Qamar, M.F.; Ishaq, H.M.; Atif, F.A. Molecular confirmation and genetic characterization of Haemonchus contortus isolate at the nuclear ribosomal ITS2 region: First update from Jhang region of Pakistan. Pak. Vet. J. 2022, 42, 251–255. [Google Scholar]
  145. Airs, P.M.; Ventura-Cordero, J.; Mvula, W.; Takahashi, T.; Van Wyk, J.; Nalivata, P.; Safalaoh, A.; Morgan, E.R. Low-cost molecular methods to characterize gastrointestinal nematode co-infections of goats in Africa. Parasite Vectors 2023, 16, 216. [Google Scholar] [CrossRef]
  146. Avramenko, R.W.; Redman, E.M.; Lewis, R.; Yazwinski, T.A.; Wasmuth, J.D.; Gilleard, J.S. Exploring the gastrointestinal "Nemabiome": Deep amplicon sequencing to quantify the species composition of parasitic nematode communities. PLoS ONE 2015, 10, e0143559. [Google Scholar] [CrossRef]
  147. Avramenko, R.W.; Redman, E.M.; Melville, L.; Bartley, Y.; Wit, J.; Queiroz, C.; Bartley, D.J.; Gilleard, J.S. Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations. Int. J. Parasitol. 2019, 49, 13–26. [Google Scholar] [CrossRef] [PubMed]
  148. Imperiale, F.; Lanusse, C. The Pattern of blood-milk exchange for antiparasitic drugs in dairy ruminants. Animals 2021, 11, 2758. [Google Scholar] [CrossRef]
  149. Novaes, S.F.D.; Schreiner, L.L.; Silva, I.P.; Franco, R.M. Residues of veterinary drugs in milk in Brazil. Ciênc. Rural 2017, 47, e20170215. [Google Scholar] [CrossRef]
  150. Porto, J.M.; Costa, R.G.; Araújo, A.C.P.; Albuquerque, E.C.; Cunha, A.N.; Cruz, G.R.B.D. Determining anthelmintic residues in goat milk in Brazil. Rev. Bras. Saúde Prod. Anim. 2019, 20, e04102019. [Google Scholar] [CrossRef]
  151. Santos, F.O.; Cerqueira, A.P.M.; Branco, A.; Batatinha, M.J.M.; Botura, M.B. Anthelmintic activity of plants against gastrointestinal nematodes of goats: A review. Parasitology 2019, 146, 1233–1246. [Google Scholar] [CrossRef]
  152. Mooney, D.; Richards, K.G.; Danaher, M.; Grant, J.; Gill, L.; Mellander, P.E.; Coxon, C.E. An analysis of the spatio-temporal occurrence of anthelmintic veterinary drug residues in groundwater. Sci. Total Environ. 2021, 69, 144804. [Google Scholar] [CrossRef] [PubMed]
  153. Oliveira, A.F.; Costa Junior, L.M.; Lima, A.S.; Silva, C.R.; Ribeiro, M.N.; Mesquista, J.W.; Rocha, C.Q.; Tangerina, M.M.; Vilegas, W. Anthelmintic activity of plant extracts from Brazilian savanna. Vet. Parasitol. 2017, 236, 121–127. [Google Scholar] [CrossRef]
  154. Peña-Espinoza, M.; Boas, U.; Williams, A.R.; Thamsborg, S.M.; Simonsen, H.T.; Enemark, H.R. Sesquiterpeno lactona contendo extratos de duas cultivares de chicória forrageira (Cichorium intybus) mostram perfis químicos distintos e atividade in vitro contra Ostertagia ostertagi. Int. J. Parasitol. Drugs Drug Resist. 2015, 5, 191–200. [Google Scholar] [CrossRef] [PubMed]
  155. Klongsiriwet, C.; Quijada, J.; Williams, A.R.; Mueller-Harvey, I.; Williamson, E.M.; Hoste, H. Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. Int. J. Parasitol. Drugs Drug Resist. 2015, 5, 127–134. [Google Scholar] [CrossRef]
  156. Daiba, A.R.; Kagira, J.M.; Ngotho, M.; Kimotho, J.; Maina, N. In vitro anthelmintic efficacy of nano-encapsulated bromelain against gastrointestinal nematodes of goats in Kenya. World’s Vet. J. 2022, 12, 95–104. [Google Scholar] [CrossRef]
  157. Kandeel, M.; Akhtar, T.; Zaheer, T.; Ahmad, S.; Ashraf, U.; Omar, M. Anti-parasitic Applications of Nanoparticles: A Review. Pak. Vet. J. 2022, 42, 2074–7764. [Google Scholar]
  158. Wasso, S.; Maina, N.; Kagira, J. Toxicity and anthelmintic efficacy of chitosan encapsulated bromelain against gastrointestinal strongyles in Small East African goats in Kenya. Vet. World 2020, 13, 177–183. [Google Scholar] [CrossRef]
  159. Tariq, K.A.; Chishti, M.Z.; Ahmad, F.; Shawl, A.S. Anthelmintic efficacy of Achillea millifolium against gastrointestinal nematodes of sheep: In vitro and in vivo studies. J. Helminthol. 2008, 82, 227–233. [Google Scholar] [CrossRef]
  160. Borges, D.G.L.; Borges, F.A. Plants and their medicinal potential for controlling gastrointestinal nematodes in ruminants. Nematoda 2016, 3, e92016. [Google Scholar] [CrossRef]
  161. Maqbool, I.; Wani, Z.A.; Shahardar, R.A.; Allaie, I.M.; Shah, M.M. Integrated parasite management with special reference to gastro-intestinal nematodes. J. Parasit. Dis. 2017, 41, 1–8. [Google Scholar] [CrossRef]
  162. Leathwick, D.M.; Besier, R.B. The management of anthelmintic resistance in grazing ruminants in Australasia—Strategies and experiences. Vet. Parasitol. 2014, 204, 44–54. [Google Scholar] [CrossRef] [PubMed]
  163. Zvinorova, P.I.; Halimani, T.E.; Muchadeyi, F.C.; Matika, O.; Riggio, V.; Dzama, K. Breeding for resistance to gastrointestinal nematodes—The potential in low-input/output small ruminant production systems. Vet. Parasitol. 2016, 225, 19–28. [Google Scholar] [CrossRef] [PubMed]
  164. Geary, T.G.; Sakanari, J.A.; Caffrey, C.R. Anthelmintic drug discovery: Into the future. J. Parasitol. 2015, 101, 125–133. [Google Scholar] [CrossRef] [PubMed]
  165. Shalaby, H.A. Anthelmintics Resistance; How to Overcome it? Iran J. Parasitol. 2013, 8, 18–32. [Google Scholar]
Ruminants 03 00020 g001
Figure 1. Geographic distribution of anthelmintic resistance according of the class of drugs used in ruminants from Brazil.
Figure 1. Geographic distribution of anthelmintic resistance according of the class of drugs used in ruminants from Brazil.
Ruminants 03 00020 g001
Ruminants 03 00020 g002
Figure 2. Geographic distribution of anthelmintic resistance according to published records in cattle, goats and sheep from Brazil.
Figure 2. Geographic distribution of anthelmintic resistance according to published records in cattle, goats and sheep from Brazil.
Ruminants 03 00020 g002
Table 1. Distribution of anthelmintic resistance in sheep from Brazil.
Table 1. Distribution of anthelmintic resistance in sheep from Brazil.
Region/StateMunicipalityAnthelminticsNumber of AnimalsDiagnostic MethodReferences
Southern
RSNITHI308FECRT[34]
NINILEVNINI[41]
NINILEVNINI[42]
NINILEV6Necropsy[43]
RSUruguainaRAF9FECRT[44]
RSBagéALB, LEVNIFECRT[45]
RSBagéIVE89FECRT[34]
RSNIALB, LEV, IVE, CLO, ALB + LEVNIFECRT[46]
PRNIALB, CLO, LEV, FEB, IVE, TET, DIS + TET480FECRT[47]
RSNILEV, ALB, FEB, OXF, MEB870FECRT[48]
PRCambé, Tamarana and LondrinaIVE, ALB, MOX850FECRT[74]
PRNIOXF, IVE, CLO, CLO + OXF, LEV, MOXNIFECRT[49]
SCNIIVE, LEV, CLO, ALB7529FECRT[50]
SCPassos Maia, Vargeão, Ponte Serrada, Faxinal dos Guedes, Xanxere and XaximIVE, ALB, MOX, CLO, LEV450FECRT[75]
PRNICLO + ALB, IVE120FECRT[51]
RSNILEV, MON, ALB, IVE, NIT, DIS, TRI, CLO, IVE + LEV + ALB500FECRT[76]
SCNICLO, LEV, ALB, ALB + LEV135FECRT[52]
PRNIMON50FECRT/CT[53]
RSNIMOX, FEB78FECRT[54]
RSNIABA, ALB, CLO, LEV, MON, TRI1540FECRT[55]
RSSão Pedro do Sul, São Gabriel and São Martinho da SerraMONNIFECRT[56]
RSSão Gabriel, São Martinho da Serra, Dilermando deIVE, DOR, MON, LEV, ALB, CLO366FECRT [57]
Aguiar, Bagé, Capão do Cipó, São Francisco de Assis and Santa Maria
Southeastern
SPSão ManuelOXF, IVE, LEV540FECRT[58]
SPJaboticabalMOX24FECRT[77]
SPPratâniaALB, LEV, MOX, IVE, TRI, CLO42FECRT[78]
RJCampos dos Goytacazes, Cardoso Moreira, Quissamã, São Francisco de Itabapoana, Santo Antonio de Pádua and São João da BarraALB, CLO, DIS, FEB, IVE, MON, NIT770FECRT[79]
MGMontes Claros, Bocaiúva, Janaúba, Pirapora, Francisco Sá, Coração de Jesus and JanuáriaALB252FECRT[80]
SPNIALB, CLO, IVE, LEV, MON1617FECRT[81]
SPJaboticabal, Viradouro, Pontal, Morro Agudo, Sertãozinho, Ribeirão Preto, Taquaritinga and São João da Boa VistaIVE, MOX160Necropsy[82]
SPAraçatubaALB, LEV, IVE, MON, CLO, IVE + LEV + ALB350FECRT[59]
SPNIALB, LEV, IVE, MON, THI245FECRT/LDT[83]
ESAlegreMON20FECRT/Necropsy[84]
MGNIALB, IVE, LEV381FECRT[60]
Midwest
MSAngélica, Camapuã, Campo Grande, Corumbá, Coxim, Ivinhema, Miranda, Porto Murtinho, Ribas do Rio Pardo, São Gabriel do Oeste, Sidrolândia, Terenos, Camapuã, Campo Grande, Miranda and Porto Murtinho ALB, CLO, IVE, LEV, MOX, TRI, ALB + IVE + LEV120FECRT[85]
Northeastern
CESobralNET, IVE20FECRT[61]
CEPentecosteCLO, OXF38FECRT[86]
CELimoeiro do Norte, Palhano, Jaguaruana, Itaiçaba, Aracati, Alto Santo, Morada Nova and JaguaribeOXF, LEV, IVE768FECRT[87]
CELimoeiro do Norte, Aracati e JaguaribeOXF144FECRT[88]
RNNIALB, IVE54FECRT[89]
PERecife, Vitória de Santo Antão and GaranhunsALBNIFECRT[90]
PBGado BravoIVE, LEV234FECRT[62]
PBAparecida, Marizópolis, Patos, Souza, São José da Lagoa Tapada, São josé de Piranhas and São José do Rio do PeixeALB, IVE, CLO, LEV, MON600FECRT[63]
CECaucaiaALB, IVE, LEV74EHT, FECRT/LDT/qPCR[91]
ALB: albendazole; OXF: oxfendazole; FEB: febendazole; PYR: pyrantel; RAF: rafoxanide; THI: thiabendazole; TET: tetramisole; LEV: levamisole; DOR: doramectin; IVE: ivermectin; MOX: moxidectin; CLO: closantel; TRI: trichloform; NIT: nitroxynil; DIS: disophenol; NET: netobimin; MEB: mebendazole; MON: monepantel; ABA: abamectin; (+): associations of drugs; (NI): not informed; FECRT: fecal egg count reduction test; CT: controlled efficacy test; LDT: larval development test; EHT: egg hatch test; qPCR: quantitative real-time PCR.
Table 2. Distribution of anthelmintic resistance in goats from Brazil.
Table 2. Distribution of anthelmintic resistance in goats from Brazil.
Region/StateMunicipalityAnthelminticsNumber of AnimalsDiagnostic MethodReferences
Southern
RSGravataíCLO, LEV40FECRT[92]
RSPorto AlegreIVE12FECRT[93]
SCSão Francisco do SulALB, ABA, CLO, NIT, LEV, MOX, IVE, IVER + LEV + ALB63FECRT[94]
PRNIMOX45FECRT[95]
Southeastern
SPJaboticabal, Viradouro, Pontal, Morro Agudo, Sertãozinho, Ribeirão Preto, Taquaritinga and São João da Boa VistaIVE, MOX160Necropsy[82]
Northeastern
CESobralOXF, FEB, ALB, THI25FECRT[35]
CEPentecosteIVE, CLO29FECRT[87]
CENIOXF, LEV1020FECRT[96]
CELimoeiro do Norte, Palhano, Jaguaruana, Itaiçaba, Aracati, Alto Santo, Morada Nova and JaguaribeOXF, LEV, IVE336FECRT[88]
ALMar VermelhoIVE, ALB40FECRT[64]
CESobralEPR24FECRT[65]
PBNIALB, IVE120FECRT[97]
RNNIALB, IVE54FECRT[89]
RNMossoróALB, IVE1350FECRT[98]
PBMonteiroALB, IVE, LEV264FECRT[66]
PESertânia, Paudalho, Camocim de São Félix and Taquaritinga do NorteALB, IVENIFECRT[90]
PBGado BravoIVE270FECRT[62]
PBSuméALB40FECRT[99]
BASanta Inês, Cravolândia and UbaíraALB, IVE, LEV, MOX, CLO360FECRT[100]
PEPetrolinaALB, IVE, LEV, MOX, CLO420FECRT[101]
ALB: albendazole; OXF: oxfendazole; FEB: febendazole; PYR: pyrantel; THI: thiabendazole; LEV: levamisole; NIT: nitroxynil; IVE: ivermectin; MOX: moxidectin; CLO: closantel; TRI: trichloform; EPR: eprinomectin; (+): associations of drugs; (NI): not informed; FECRT: fecal egg count reduction test.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Macedo, L.O.; Silva, S.S.; Alves, L.C.; Carvalho, G.A.; Ramos, R.A.N. An Overview of Anthelmintic Resistance in Domestic Ruminants in Brazil. Ruminants 2023, 3, 214-232. https://doi.org/10.3390/ruminants3030020

AMA Style

Macedo LO, Silva SS, Alves LC, Carvalho GA, Ramos RAN. An Overview of Anthelmintic Resistance in Domestic Ruminants in Brazil. Ruminants. 2023; 3(3):214-232. https://doi.org/10.3390/ruminants3030020

Chicago/Turabian Style

Macedo, Lucia Oliveira, Samuel Souza Silva, Leucio Câmara Alves, Gílcia Aparecida Carvalho, and Rafael Antonio Nascimento Ramos. 2023. "An Overview of Anthelmintic Resistance in Domestic Ruminants in Brazil" Ruminants 3, no. 3: 214-232. https://doi.org/10.3390/ruminants3030020

APA Style

Macedo, L. O., Silva, S. S., Alves, L. C., Carvalho, G. A., & Ramos, R. A. N. (2023). An Overview of Anthelmintic Resistance in Domestic Ruminants in Brazil. Ruminants, 3(3), 214-232. https://doi.org/10.3390/ruminants3030020

Article Metrics

Back to TopTop