Abstract
The canine hookworm Ancylostoma caninum is one of the most prevalent parasitic nematodes in dogs worldwide and has the potential for zoonotic transmission to humans, including the development of cutaneous larva migrans. Recent confirmation of anthelmintic resistance (AR) in A. caninum to several anthelmintic classes, mainly in the USA, indicates the potential for this scenario in Canada. We consider various factors that may lead to resistant isolates in Canada, such as the widespread use of antiparasitic drugs without the assessment of efficacy; increased A. caninum prevalence in various Canadian provinces; and the importation of dogs, mostly from the USA, with a history of persistent infection by A. caninum. Our objective was to review factors that influence A. caninum to develop AR and raise awareness regarding the need for a strategic plan to control this parasitic nematode through the appropriate use of anthelmintics.
Résumé
Le ver à crochetAncylostoma caninum : une nouvelle menace de la résistance aux vermifuges au Canada. Le ver à crochet du chien Ancylostoma caninum est un des nématodes le plus répandu chez les chiens dans le monde, avec un potentiel zoonotique, car ils peuvent infecter les humains et provoquer des maladies telles que la larva migrans cutanée. Les récentes découvertes de la résistance d’A. caninum à plusieurs classes d’anthelminthiques aux États-Unis ont attiré notre attention sur ce scénario possible au Canada. Nous considérons que des facteurs tels que l’utilisation répandue de médicaments anthelminthiques sans évaluation de l’efficacité, l’augmentation de la prévalence chez A. caninum dans différentes provinces canadiennes, et la migration de chiens, surtout des É.-U., ayant des antécédents d’infection persistante par A. caninum, peuvent conduire à la présence d’isolats résistants aux anthelminthiques usuels au Canada. L’objectif de cette revue est de réviser tous ces aspects concernant les caractéristiques d’A. caninum à cette résistance et de prendre conscience qu’il pourrait devenir un problème majeur dans la santé des animaux de compagnie au Canada, donc il faudrait mis en place une planification stratégique pour contrôler ce strongle par l’utilisation judicieuse des antihelminthiques.
(Traduit par les auteurs)
Introduction
Control of gastrointestinal nematodes (GIN) in livestock and companion animals is heavily dependent on anthelmintics. The canine hookworm Ancylostoma caninum, an important parasitic nematode affecting dogs, is developing anthelmintic resistance (AR), mainly in the USA (1,2). Various factors may promote the development of AR in A. caninum in Canada, including the arrival of resistant isolates via animal importation (mainly from the USA) and the lack of local data regarding current anthelmintic efficacy against GIN. Numerous anthelmintic formulations are available in Canada for dogs (Table 1), including single, double, and triple combinations of drug classes against helminths, with many that also include a compound to treat arthropod parasites. Although anthelmintic classes used in companion animals (3), such as benzimidazoles (BZs), macrocyclic lactones (MLs), and pyrantel (a nicotinic agonist), historically have had high efficacy against GIN in their hosts, emerging AR among A. caninum in dogs is an impetus to verify the efficacy of current anthelmintic formulations in Canada (4).
Table 1.
List of available anthelmintic formulations to control parasitic nematodes from companion animals in Canada.
| Anthelmintic class | Actual compound | Commercial name | Dosage (mg/kg) | Administration route | Target |
|---|---|---|---|---|---|
| Benzimidazoles | Febantel (pro-benzimidazole) | Drontal Plusa | D: 5.0 to 10.0 | PO | Tapeworms, roundworms, hookworms, and whipworms |
| Fenbendazole | Panacur | D/C: 50 | PO | Nematode infestations (migrating stages of canine roundworm, as well as some cestodes) | |
| Tetrahydropyri-midines | Pyrantel | Drontala | C: 20.0 | PO | Parasitic worm infection (roundworm, hookworm, pinworm, and other worm infections) |
| Drontal Plusa | D: 5.0 to 10.0 | ||||
| Nemex | D: 5.0 | ||||
| Heartgard Plusb | |||||
| Macrocyclic lactones | Ivermectin | Heartgard chewables for cats | C: 0.024 | PO | Commonly used for heartworm Also, mites and internal parasites |
| Heartgard-30 Plusc chewables for dogs | D: 68 to 227 μg | PO | |||
| Moxidectin | Advantage Multid | D: 2.5 to 6.5 C: 1 to 2 |
Spot-on | Heartworms, hookworms, roundworms, and whipworms Fleas, ticks, mosquitoes, chewing lice |
|
| ProHeart | D: 0.17 | Injectable | |||
| Simparica Trioe | D: 3 | PO | |||
| Selamectin | Revolution | D/C: 6.0 | Spot-on | Intestinal parasites and external parasites such as head lice | |
| Selavectinf | Roundworm (Toxocara canis), tick (Dermacentor variabilis) | ||||
| Milbemycin oxime | Interceptor | D: 0.5 to 1.0 | PO | Heartworm larvae and mature hookworms, roundworms, and whipworms | |
| Flavor Tabs Sentinelg | C: 2 | ||||
| Cyclic octadepsipeptides | Emodepsideg | Profenderh | C: 3 | Spot-on | Tapeworms, roundworms, and hookworms |
Combination product, with praziquantel (Cestocide).
Combination product, with ivermectin.
Combination product, with imidacloprid.
Combination product, with pyrantel. Ivermectin dosage is in (μg).
Combination product with pyrantel and sarolaner.
Targets mainly ectoparasites and Ancylostoma tubaeforme in cats.
Combination product, with lufenuron.
Only licensed for use in cats.
C — Cat; D — Dog; PO — Per os, oral administration.
Another aspect to consider when deworming dogs is the biology of this parasite. The life cycle of A. caninum in dogs begins with adult worms attached to the small intestine (Figure 1). After mating, a female hookworm releases eggs (2000 to 17 000 eggs per d) into the environment through the host’s feces (5). Under optimal environmental conditions, embryonated eggs in the feces hatch within 1 to 2 d and transform into 1st-stage larvae (L1) (5). Within 5 to 10 d after this, the larvae (L1, L2) develop into the infective, 3rd-stage larvae (L3). Ingestion or skin penetration of these L3 larva are the 2 common transmission routes for canine hosts. Ingested A. caninum L3s reach the duodenum and develop into adult worms; whereas L3 larvae that penetrate the skin can migrate through the tissues, reach the small intestine, and become adult worms (5). Of note, infective L3s can also penetrate the skin of humans, producing cutaneous larva migrans (Figure 1).
Figure 1.
The life cycle of Ancylostoma caninum. Adult worms mate in the host small intestine [1] and hookworm eggs are released through dog feces [2]. Embryonated eggs form larval stages, hatching and developing into the infective larval stage 3 (L3) in 5 to 10 d in the soil environment [3]. L3s can penetrate human skin [4], leading to zoonotic larva migrans cutanea; or they can be ingested by a canine host [5], reach the small intestine, and become adult worms in 14 to 15 d, completing the life cycle. Alternatively, some L3s could penetrate the digestive mucosa and reach the blood circulation to encyst as somatic larvae [6] or penetrate the dog’s skin at the paw level [7]. These dormant L3s can resume their life cycle either by migrating back to the intestine (“larval leaking”) or through the circulation, passing in colostrum to newborn puppies [8] during the first days of nursing (lactogenic transmission).
Image reproduced with permission from Elanco Animal Health (Greenfield, Indiana, USA). Available from: pet.elanco.com/us/en/interceptorplus/hookworm-lifecycle
Another critical feature of A. caninum that may influence anthelmintic efficacy is the migration of L3s to muscle, fat, and other tissues, where they enter into a hypobiotic state or “encysted somatic larvae,” in which they are encapsulated in the host tissues and exhibit arrested development (6,7). These dormant L3s can resume their life cycle by migrating back to the intestine (“larval leaking”) or, in pregnant dams, L3s can be reactivated from the tissues and migrate to the mammary gland, where they can enter the colostrum and be transmitted to newborn puppies (lactogenic route; Figure 1). Alternatively, paratenic hosts like rodents can carry hookworm larvae and contribute to completing the A. caninum life cycle. In general, the prepatent period for A. caninum in dogs is ~14 d after infection until eggs are released and larval stages begin developing (8).
Epidemiological data show an increasing prevalence and widening distribution of canine ancylostomiasis in companion dogs in several Canadian provinces. This pattern, combined with the movement of humans with their pets and the importation of dogs from high-prevalence areas with multidrug resistant (MDR) A. caninum isolates, most notably the USA, highlights the need to control the spread of this helminth. The aim of this review is to address aspects that may promote the emergence of AR in A. caninum in Canada and discuss potential mitigation strategies.
Current anthelmintic formulations in Canada for controlling Ancylostoma caninum in dogs
Anthelmintic drugs are currently the cornerstone of helminthiasis treatment in humans and animals (9). In Canada, there are 3 main groups of chemotherapeutics available for controlling GIN, including A. caninum, in dogs: benzimidazoles (BZs); macrocyclic lactones (MLs); and pyrantel pamoate, which belongs to the tetrahydropyrimidines.
Among the BZs, albendazole, fenbendazole, febantel, mebendazole, oxfendazole, and oxibendazole are most commonly used in companion animals (10). These compounds inhibit microtubule polymerization by attaching to β-tubulin, which is the scaffold protein of the cytoskeleton (3). The BZs have ovacidal, larvicidal, and adulticidal effects. They are formulated as a single molecule or in combination with other anthelmintic drugs (Table 1) and are usually administered PO. Alone or in combination with other compounds, commercial preparations of BZs in Canada have optimal efficacy against hookworms, including A. caninum, in dogs (11,12).
A 2nd group of anthelmintics used in companion animals are the tetrahydropyrimidines, which act as agonists for the nematode nicotinic acetylcholine receptor (13). This group includes oxantel, pyrantel pamoate, and morantel (13). Of these, pyrantel pamoate is used as a single formulation (e.g., Nemex) in tablet or injectable forms; or in combination with other anthelmintic classes (e.g., Drontal Plus), which has been 99.9% effective against A. caninum (13,14). As a single compound, pyrantel pamoate is a first choice for treating clinical ancylostomiasis (anemia, lethargy) in lactating puppies, due to its ability to quickly kill adult worms in debilitated animals (14).
A 3rd class of anthelmintic drugs is the MLs, which have broad-spectrum activity (15). Members of this group used in companion animals include ivermectin, selamectin, moxidectin, and milbemycin oxime (15). The mechanism of action of MLs is via binding on glutamate-gated chloride ion channels (GluCls) at neuro-muscular junctions in nematodes, hyperpolarizing the post-synaptic membrane and causing flaccid paralysis and parasite death (3). This mechanism of action is shared with ectoparasites such as fleas and ticks (that also express GluCls); MLs thus also have an endectocide effect (15). Ivermectin, one of the most widely used MLs in animals, has high efficacy against A. caninum in both natural (16) and experimental infections (17).
In Canada, some anthelmintic formulations that target GIN (including A. caninum) in dogs include a single ML; e.g., Revolution (containing selamectin) as a topical solution and Interceptor (milbemycin oxime) as oral tablets. There are also formulations with 2 anthelmintic groups [e.g., Heartgard Plus (ivermectin with pyrantel) as chewable tablets] or combined with a molecule against ectoparasites [e.g., Nexgard SPECTRA (mibemycin oxime with afoxolaner) as tablets; Advantage Multi (moxidectin plus imidacloprid) as a spot-on treatment; and Simparica TRIO (moxidectin, pyrantel, and sarolaner) as chewable tablets]. This latter formulation had significant efficacy in dogs against various life stages of A. caninum, including immature larvae and adult worms (18).
For the anthelmintic control of GIN in dogs, veterinary parasitology reference boards, such as the American Companion Animal Parasite Council (CAPC) and the European Scientific Council Companion Animal Parasites (ESCCAP), recommend an intense deworming strategy in both canine dams and pups, with treatment every 2 wk for the first 8 wk, followed by once-monthly administration (https://capcvet.org/guidelines/hookworms/). Because of its zoonotic potential, this regimen is aimed at preventing the perinatal transmission of A. caninum and targets the canine roundworm, Toxocara canis. Most patent infections are prevented with treatment intervals of 4 to 6 wk, although a frequency of < 3 to 4 × per year has a limited effect on hookworm prevalence (16). This regimen usually includes an ML that targets migrating larvae from parasitic nematodes.
Antecedents of anthelmintic resistance in Ancylostoma caninum
Although anthelmintic resistance (AR) has been mainly described in veterinary nematodes from livestock (19), the failure to control some parasitic nematode species in companion animals has been well-documented, mostly for the canine heartworm, Dirofilaria immitis (20). Furthermore, recent reports have described an emerging problem in the USA of AR in the canine hookworm A. caninum that is linked to greyhound breeding farms, kennels, and racing tracks (1,2,21). The environmental conditions in these facilities (e.g., unlimited access to sand and dirty training tracks) promote the growth and survival of infective A. caninum larvae. Moreover, in order to control nematode infections, dogs from these breeding farms are subjected to a rigorous deworming protocol involving multiple anthelmintic classes. Collectively, these factors have resulted in substantial drug selection pressure on hookworm populations (1,22).
Anthelmintic resistance is described as a genetic trait that confers a lack of drug sensitivity in worm populations previously responsive to the same drug at the proper dosage (19,20). In other words, AR is a phenomenon in which selected parasitic nematodes carrying a resistant phenotype may have a better chance to pass this genetic portrait to their offspring, resulting in “survival of the fittest” among nematode populations. There are reports of A. caninum that have AR to the 3 main anthelmintic classes used in animal health: BZs, MLs, and pyrantel (1,2). Furthermore, AR in A. caninum is not limited to greyhounds in the USA, as BZs also had reduced efficacy against isolates of A. caninum in Brazil (22) and Nigeria (23), implying the global emergence of resistance to this class of anthelmintics. Regarding pyrantel resistance by A. caninum, isolates linked to greyhounds in the USA (1,24,25) and Australia (26) have been documented. Resistance to the MLs by A. caninum has been mainly linked to moxidectin, when it was used in combination with other compounds [e.g., imidacloprid (Advantage Multi)] or as an off-label formulation for dogs (Quest Plus for horses) in the USA (2). Another A. caninum isolate resistant to BZs that also had a significant resistant phenotype to ivermectin was described as the first natural multidrug resistant isolate of A. caninum in the USA (25).
Although it has not been documented, the year-round, prophylactic use of MLs to prevent heartworm infection in dogs could promote AR in GIN such as A. caninum. This practice is controversial in Canada: Although the prevalence of heartworm has been described in southern Ontario in wild canids (27), the epidemiology of canine dirofilariosis in household dogs is largely unknown in the rest of the country, and there are no indications to support a monthly regimen of ML administration as is used in some parts of the USA. In Canada, the frequent use of parasiticide formulations including an anthelmintic from the ML class is more likely justified through most of spring, summer, and early fall, when most internal and external parasites are active, since the endectocide effect of MLs can confer protection against several parasitic pathogens in dogs, including A. caninum.
Given the potential that AR in A. caninum may arise in Canada, systematic monitoring of the efficacy of anthelmintic formulations used in companion animals should be undertaken. In collaboration with private and public diagnostic services, all dogs should be routinely subjected to fecal egg counting in order to verify whether deworming protocols are working optimally to control GIN. In the event of suspicious findings, indications of sub-optimal efficacy, or established AR by A. caninum isolates, further analyses should be conducted at research laboratories where anthelmintic efficacy can be assessed with a fecal egg count reduction test (FECRT) (28). Although a FECRT is a first approach to detect AR and the only choice for pyrantel resistance, it should be complemented with in vitro assays, in which A. caninum isolates can be characterized as resistant or sensitive to 1 or more anthelmintic classes. These bioassays will vary depending on the anthelmintic family. For the BZs, the egg hatch assay (EHA) is used to detect resistance (28). The EHA has been widely used in several BZ-resistance isolates from parasitic nematodes and for the identification of A. caninum isolates resistant to this anthelmintic class (1,2,22,24). Nonetheless, as mutations in the β-tubulin isotype 1 gene from various nematode species are well-established as molecular markers for BZ resistance, genetic analysis of this locus can be performed to confirm the presence of A. caninum isolates resistant to BZs (22,23). The larval development assay (LDA) is another research-applied bioassay to detect resistance to MLs (29). Unlike the EHA, the LDA can detect ML resistance for just a few GIN species (30), including A. caninum (1,2,22).
Epidemiology of canine ancylostomiasis in Canada
In Canada, the most recent data available (from 2021) indicated a prevalence rate of 1.28% for hookworms in dogs nationwide, with the highest rates in Saskatchewan and Nova Scotia (https://capcvet.org/maps/#/2021/allyear/hookworm/dog/canada). Specifically, A. caninum is markedly prevalent in the eastern provinces (Quebec: 3%, Ontario: 4.8%) and even more prevalent in the maritime provinces such as New Brunswick (5.7%) and Nova Scotia (4%) (31). However, these antecedents regarding A. caninum prevalence represent only a small portion of the canine population in Canada, such as shelter dogs, and we assume that the actual prevalence of A. caninum is higher, as described in the USA (32). In fact, a recent report from southern Ontario described a 5.8% prevalence rate for hookworm species, including A. caninum, in adult dogs (33). This antecedent is relevant because it was based on microscopic evaluation and antigen fecal analyses from urban dogs living in households, indicating an increase in the prevalence of A. caninum compared to that reported in the study from Villeneuve et al. [in 2015 (31)] that was based on shelter dogs. Taken together, the evidence suggests that the prevalence of A. caninum in dogs across Canada has increased in recent years. Although factors such as climate change (with longer hot seasons) and canine population growth may have contributed to the increase, we cannot exclude the potential emergence of AR in A. caninum in Canada, as has been confirmed in the USA (1).
Considering the epidemiological data from the 2 most recent studies (31,33) of A. caninum prevalence in dogs in Canada, we believe that A. caninum infection is widespread throughout the country, with higher levels in central and eastern Canada and in the Maritimes. In these geographic zones, dogs with access to shared spaces such as urban dog parks, research colonies, and kennels, may be at risk of infection by A. caninum or other canine GIN. Parasitic nematodes, including A. caninum, have several features that can promote the infection of new hosts and perpetuate the life cycle. It is thus important to identify the presence of this canine hookworm, primarily through coprological examination, so we can establish accurate prevalence estimates and optimize control strategies that are based on local assessments of anthelmintic efficacy.
Perspectives regarding the control of anthelmintic-resistant isolates of Ancylostoma caninum in Canada
If A. caninum is resistant to 1 or more anthelmintics, termed multidrug resistant (MDR), the rational use of anthelmintics will be crucial for preventing the spread of this pathogen across canine and, potentially, human populations. Our recommendation is to design a surveillance program across small animal health services that includes regular coprological analyses, starting in spring and conducted monthly during the summer season, when larvae from GIN such as A. caninum are more likely to complete their life cycle and transmission is more likely to occur between canine hosts (32). As stated, the CAPC recommends testing for GIN in puppies at least 4 times in their 1st year and then twice annually in adult dogs.
We advise veterinarians to contact research laboratories and diagnostic services from veterinary schools whenever possible for assistance in evaluating the performance of various anthelmintic formulations with the FECRT (2,28,30). Although published data from companion animals on anthelmintic efficacy against GIN are limited to controlled trials, there are a few studies on FECRT from canine samples (2,22,34). In the latter reference (34), Jimenez Castro and Kaplan (https://www.cliniciansbrief.com/article/persistent-or-suspected-resistanthookworm-infections) described that fecal egg reduction after anthelmintic treatment in dogs should be interpreted conservatively because numbers of eggs are highly variable from sample to sample. However, the authors suggested a similar interpretation in terms of the percentage of egg reduction, as established for the efficacy of anthelmintics against GIN in ruminants (28). Overall, an optimal anthelmintic treatment should produce a ≥ 95% egg reduction at the FECRT (28,34). Lower egg-reduction percentages from the FECRT should be interpreted as non-optimal efficacy (90 to 95%) and, in the case of A. caninum, the identification of eggs may correspond to larval leakage (34). Egg reduction values from 89 to 75% in the FECRT should be interpreted as potential AR, even though, in the case of A. caninum, larval leakage generating new adult worms that mate may explain persistent egg shedding (34). Egg reduction values < 75% in this method should be interpreted as resistance to the anthelmintic compound used. In this case, further assessments via bioassays and molecular analyses should be conducted at specialized research laboratories. As local data in Canada regarding the efficacy of anthelmintic formulations against GIN from pet animals are not available, we recommend that veterinarians contact research laboratories and perform FECRTs. We should be able to corroborate the efficacy of the anthelmintic drugs used in deworming protocols, and to detect the presence of A. caninum or another GIN species under selection for a particular anthelmintic class at an early stage, and then revise control strategies as required.
Anthelmintic resistance may take several years to emerge; however, once it is established for a drug class, an alternative compound that is still effective in controlling resistant isolates is needed before clinical signs are detected in animals (34). For this reason, we recommend the careful use of anthelmintic formulations. In Canada there are various formulations available with 1 or more anthelmintic classes, sometimes including a compound to control ectoparasites. They are available with various concentrations and routes of administration (Table 1). Our general recommendation is to use any anthelmintic formulation available in Canada, in accordance with the label instructions, and to do routine fecal examinations before and 10 to 14 d after treatment (28,30). We highlight again larval leakage by A. caninum, as it may give rise to the suspicion of anthelmintic failure due to continuous egg shedding, with or without clinical signs such as loose stools or anemia in the case of clinical ancylostomiasis. An alternative deworming strategy should be implemented in these cases (4). In the USA, efficacy against MDR A. caninum isolates was achieved when a combination of anthelmintic classes (febantel/fenbendazole, pyrantel, and moxidectin) was used to completely suppress the shedding of A. caninum ova after 3 to 5 monthly treatments (35). When using this triple combination of anthelmintic drugs against potential A. caninum resistance, we recall that pyrantel only targets the adult stage of this hookworm species because it is poorly absorbed from the digestive tract (10,13). However, the BZs febantel or fenbendazole, and particularly moxidectin (an ML member), have higher concentrations and longer persistence in canine tissues (20). Consequently, they can target larval stages such as those from the larval leakage of A. caninum in their migration back to the intestine (18,20).
Resistance in A. caninum to 1 or more anthelmintic groups may occur in Canada after a long selection process, or an imported isolate, and options to control this parasitic nematode may become restricted. In this scenario, the use of another anthelmintic drug such as off-label emodepside (combined with praziquantel as Profender) could be a last resort to treat MDR A. caninum isolates in dogs after various anthelmintic treatments with single, dual, or triple combinations of drug classes have failed (34). Although emodepside had excellent efficacy against larval and adult forms of A. caninum in dogs (36), we are cautious about the use of this compound. Dogs should be given an accurate dose of 1 mg/kg BW emodepside, whereas the formulation available in Canada for cats has a dose rate of 3 mg/kg BW (Table 1). Moreover, and along with some MLs, emodepside can produce toxicity in some dog breeds, namely those with a non-functional MDR-1 gene encoding for P-glycoprotein, a membrane transporter that extrudes these molecules at the blood-brain barrier (37). Also, in southern regions of Canada where there are antecedents of heartworm (D. immitis) prevalence (33), dogs with this genetic condition should be tested for circulating microfilaria prior to the use of emodepside, which could worsen toxicity if administered along with an ML preventive in dogs that test positive to microfilaria or a D. immitis antigen test.
We emphasize that Profender should be the main alternative in dogs when all other anthelmintic formulations have been unsuccessful in controlling MDR A. caninum. Veterinarians should prescribe this off-label drug with accurate dosages for dogs and should provide instructions to pet owners, as emodepside shows its highest absorption and efficacy when given to fasted dogs (36,38). In contrast to other anthelmintic classes, the cyclooctadepsipeptide emodepside works by binding to presynaptic latrophilin receptors in nematodes, thereby inducing flaccid paralysis due to the inhibition of Ca2+ influx into pharyngeal muscle cells and resulting in worm destruction by starvation or expulsion (38). Resistance to emodepside has not yet been described.
Complementary to monitoring the emergence of A. caninum resistance to the anthelmintic drugs currently available, a research program should be established to focus on AR surveillance for A. caninum and other zoonotic parasitic nematodes among companion animals in Canada. Under the current framework of One Health, animal health experts should monitor parasitic zoonoses, such as cutaneous larva migrans by A. caninum (39), and work with qualified parasitology researchers to assess the efficacy of anthelmintics and detect the presence of A. caninum isolates with a resistant phenotype to 1 or more drug classes. In that sense, closer collaborations among companion animal clinics, researchers in academia and industry, and public health entities are fundamental to successfully monitor anthelmintic use and anticipate any emergence of AR in A. caninum in dogs that is accompanied by transmission to human populations (40) following the failure of anthelmintic formulations to control this zoonotic parasitic nematode.
Another subject to consider in the wider control of potential A. caninum isolates with AR phenotypes is the importation of dogs that may carry this parasite. As with many infectious diseases in companion animal health, it is essential to know the background information related to anthelmintic treatment history and geographic origin of dogs imported to Canada (40). Current guidelines for importing dogs into Canada from abroad, including the USA, require a broad-spectrum antiparasitic treatment against endo- and ectoparasites at least 7 d before the travel date (https://inspection.canada.ca/importing-food-plants-or-animals/pets/eng/1326600389775/1326600500578). As illustrated in the present review, features regarding the biology of A. caninum, such as lactogenic transmission and larval leakage, may aid in the transmission of resistant isolates that are not detected by a standard fecal examination (which is only useful for patent infections). Therefore, we advise veterinarians caring for imported dogs with previous antecedents of hookworm infection to conduct follow-up coprological analyses in these animals, and in other dogs in contact with them, for up to 2 mo after arrival.
People who take their dogs to areas where A. caninum larvae are prevalent should contact animal health practitioners to discuss the clinical signs of hookworm infection after they return. An antecedent report regarding clinical ancylostomiasis in a dog imported from the USA in Canada (41) highlights the importance of detecting A. caninum and anthelmintic efficacy.
Although uncommon, infection with larvae from A. caninum is a consideration for pet owners who do not regularly remove dog feces from the environment, including in sand pits and dog parks (42,43). For the owners of dogs positive for A. caninum, recommendations are to frequently retrieve dog feces and wear closed shoes to avoid contact with infective larvae.
Anticipating these scenarios is part of our commitment to raise awareness within the pan-Canadian small animal health community regarding the potential risks of A. caninum AR emergence in Canada. We should establish a strategic plan that includes education on key aspects of the parasite biology, the appropriate use of anthelmintics, and methods to monitor the efficacy of these chemotherapeutics; and is complemented with a traceable record of all dogs entering Canada with exposure to hookworms. Our goals are to minimize the emergence of AR in A. caninum in Canada and to keep our dogs in good health. CVJ
Footnotes
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