Overview

Brief Summary

Ancylostoma caninum is related to the main nematode worms known as human hookworms, A. duodenale and Necator americanus. In contrast to these two species, however, although A. caninum nematodes can penetrate the human skin (causing cutaneous larval migrans), they do not develop any further. Occasionally, A. caninum larvae may migrate to the human intestine, causing eosinophilic enteritis, and they have also been implicated as a cause of diffuse unilateral subacute neuroretinitis.

Cutaneous larval migrans (also known as "creeping eruption" or "ground itch") is a zoonotic infection (i.e.,an infection transmitted from non-human animals to humans) caused by hookworm species that do not use humans as a definitive host. The condition results from migrating larvae that cause an intensely itchy track in the upper dermis and is most commonly caused by A. braziliense and A. caninum (the normal definitive hosts for these species are dogs and cats).

The normal life cycle for A. caninum in dogs is very similar to the cycle for human hookworms in humans: Eggs are passed in the stool and under favorable conditions (moisture, warmth, shade) larvae hatch in 1 to 2 days. The released rhabditiform larvae grow in the feces and/or the soil and after 5 to 10 days (and two molts) they become filariform (third-stage) larvae that are infective. These infective larvae can survive 3 to 4 weeks in favorable environmental conditions. On contact with the animal host, the larvae penetrate the skin and are carried through the blood vessels to the heart and then to the lungs. They penetrate into the pulmonary alveoli, ascend the bronchial tree to the pharynx, and are swallowed. The larvae reach the small intestine, where they establish themselves and mature into adults. Adult worms live in the lumen of the small intestine, where they attach to the intestinal wall. Some larvae become arrested in the tissues, and serve as source of infection for puppies via transmammary (and possibly transplacental) routes. Humans may also become infected when filariform larvae penetrate the skin. In a human host, the larvae cannot mature further, but may migrate aimlessly within the epidermis, sometimes as much as several centimeters a day. Some larvae may persist in deeper tissue after finishing their skin migration.

According to Zajac and Conboy (2006), the most important mode of transmission of A. caninum to dogs is transmammary (i.e., via puppies nursing from infected mothers), followed by ingestion of third-stage larvae from the environment or from paratenic hosts (i.e., intermediate hosts in the parasite's life cycle that are not essential to parasite development) and, rarely, by direct skin penetration by larvae.

(Source: Centers for Disease Control Parasites and Health Website)

Mieszczanek and Wedrychowicz (1999) developed a simple genetic test using the polymerase chain reaction (PCR) on DNA from hookworm eggs to distinguish two of the most common hookworms inecting domestic dogs, Ancylostoma caninum and Uncinaria stenocephala, in living hosts.

Ancylostoma caninum is found worldwide, with its distribution in North America extending north to southern Canada (Zajac and Conboy 2006).

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Distribution

Geographic Range

Ancylostoma caninum is cosmopolitan in warm and temperate climates, especially where there is adequate moisture.

Biogeographic Regions: nearctic ; palearctic ; oriental ; ethiopian ; neotropical ; australian

Other Geographic Terms: cosmopolitan

  • Marquardt, W. 2000. Parasitology and Vector Biology. USA: Harcourt Academic Press.
  • Olsen, O. 1974. Animal Parasites: Their Life Cycles and Ecology. Baltimore: University Park Press.
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Physical Description

Morphology

Physical Description

Ancylostoma caninum is usually gray, but appears reddish if there is blood in its alimentary canal. The body is covered by a non-living   cuticle that sheds at molts allowing for growth of the nematode. A male is 10 to 12 mm long and 0.36 mm wide; a female is 14 to 20 mm long by 0.5 mm wide and has a pointed tail. The anterior end is bent dorsally so that the arrangement of the hookworm's ventral and dorsal sides are reversed. In the head of the hookworm is an area called the buccal capsule which contains one the   mouth and teeth. Ventrally, there is one pair of teeth, each with three points. In the depth of the capsule there is a pair of triangular dorsal teeth and a pair of ventro-lateral teeth. At its posterior end, a male A. caninum has a prominent bursa. The rays inside the bursa are used in identifying species of hookworms, so A. caninum has a particular arrangement of rays in its bursa. The female reproductive organ, the vulva, is found near the junction of the second and last thirds of the body.

Range length: 10 to 20 mm.

Other Physical Features: ectothermic ; heterothermic ; bilateral symmetry

Sexual Dimorphism: sexes shaped differently

  • Cheng, T. 1973. General Parasitology. New York: Academic Press.
  • Jones, A. 1967. Introduction to Parasitology. USA: Addison-Wesley Publishing Co..
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Ecology

Habitat

The first larval stage lives in the soil where it molts twice and then emerges into its infectious third stage. The third stage juvenile is either ingested, in which case it goes through the stomach and ends up in the small intestine, or it enters via the skin. If A. caninum enters through the skin of the host, it finds its way to the circulatory system which takes it to the trachea. In the trachea, the juvenile is swallowed and ultimately ends up in the small intestine.

In abnormal hosts, such as humans, A. caninum larva cannot remain in the subcutaneous layer of the skin, unable to enter the circulatory system to complete its life cycle.

Habitat Regions: temperate ; tropical ; terrestrial

Terrestrial Biomes: desert or dune ; savanna or grassland ; chaparral ; forest ; rainforest ; scrub forest ; mountains

Other Habitat Features: urban ; suburban ; agricultural

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Trophic Strategy

Food Habits

These hookworms live in the small intestines of many animals, predominantly dogs. Other hosts are cats, foxes, wolves, and other carnivores in temperate as well as tropical and subtropical areas. On very few occasions have humans been reported as hosts. Ancyolostoma caninum feeds primarily on the tissue of the small intestine but is also known to suck blood. Adult worms feed at approximately six different sites per day.

Animal Foods: blood; body fluids

Primary Diet: carnivore (Eats body fluids)

  • Chowdhury, N., I. Tada. 1994. Helminthology. Delhi: Rajkamal Electric Press.
  • Lapage, G. 1962. Mönnig’s Veterinary Helminthology and Entomology. Baltimore: The Williams and Wilkin Company.
  • Roberst, L., J. Janovy Jr.. 2000. Foundations of Parasitology. USA: McGraw-Hill Higher Education.
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Associations

Ecosystem Roles

These hookworms live in the small intestines of many animals, predominantly dogs. Other hosts are cats, foxes, wolves, and other carnivores in temperate as well as tropical and subtropical areas. On very few occasions have humans been reported as hosts.

Ecosystem Impact: parasite

Species Used as Host:

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Predation

These parasites are probably not preyed on directly, but are ingested from host to host. Larval mortality is high as most of the parasites do not reach appropriate hosts.

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Life History and Behavior

Behavior

Communication and Perception

Nematodes in general have papillae,   setae and amphids as the main sense organs. Setae detect motion (mechanoreceptors), while amphids detect chemicals (chemoreceptors).

Females may produce a phermomone to attract males.

Communication Channels: tactile ; chemical

Other Communication Modes: pheromones

Perception Channels: tactile ; chemical

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Life Cycle

Development

The eggs of Ancyclostoma caninum pass through several larval instars before becoming an adult. In an environment of 23 degrees Celsius, the egg hatches into the first-stage juvenile in the soil in approximately one day. Within four to five days, the cuticle is molted twice and the infective third-stage juvenile emerges. Infection of the host can occur through ingestion or by penetration of the unbroken skin but either way, the parasite ends up in the small intestine of the host. If ingested, A. caninum travels to the stomach of its host, molts, migrates to the small intestine, molts a fourth and final time, and develops to maturity in about 5 weeks. If entrance is via the skin, A. caninum makes its way through the dermal layers and enters the circulatory system which takes it to the lungs. Once in the lungs, A. caninum leaves the capillaries and travels up the trachea where it is swallowed. It then goes through the same cycle that ingested A. caninum go through until it reaches the small intestine.

Copulation occurs within the small intestine and the female worms pass eggs in the feces. Transplacental and transmammary transmission are known for dogs infected with A. caninum. Occasionally, an A. caninum juveniles will penetrate the skin of a human but cannot complete its life cycle in the inappropriate host. The juvenile wanders about in the upper layers of the skin, causing a conditio called dermal larva migrans.

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Reproduction

Nematode females may produce a phermomone to attract males. The male   coils around a female with his curved area over the female genital pore. The gubernaculum, made of cuticle tissue, guides   spicules which extend through the cloaca and anus. Males use spicules to hold the female during copulation. Nematode sperm are amoeboid-like and lack flagella.

Copulation for Ancylostoma caninum occurs within the small intestine and the female worms pass eggs in the feces.

Key Reproductive Features: gonochoric/gonochoristic/dioecious (sexes separate); sexual ; fertilization (Internal ); oviparous

There is no parental investment beyond egg laying.

Parental Investment: pre-fertilization (Provisioning)

  • Barnes, R. 1987. Invertebrate Zoology. Orlando, Florida: Dryden Press.
  • Marquardt, W. 2000. Parasitology and Vector Biology. USA: Harcourt Academic Press.
  • Olsen, O. 1974. Animal Parasites: Their Life Cycles and Ecology. Baltimore: University Park Press.
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Molecular Biology and Genetics

Molecular Biology

Barcode data: Ancylostoma caninum

The following is a representative barcode sequence, the centroid of all available sequences for this species.


There are 5 barcode sequences available from BOLD and GenBank.  Below is a sequence of the barcode region Cytochrome oxidase subunit 1 (COI or COX1) from a member of the species.  See the BOLD taxonomy browser for more complete information about this specimen and other sequences.

GCAACTTGATTAGAGAGGTCTAATCATAAAGATATTGGTACGTTATATTTTTTGTTTGGTTTGTGATCAGGTATAGTGGGGACTAGTTTA---TCTTTAATTATTCGTTTGGAATTAGCAAAACCAGGTTTATTGTTAGGTAAT---GGTCAGTTGTATAATTCTATTATTACTGCTCATGCTATTTTAATAATTTTTTTTATGGTAATACCAACAATAATTGGTGGTTTTGGTAATTGAATGGTTCCTTTAATG---TTGGGTGCACCGGATATAAGTTTTCCTCGTTTAAATAATTTAAGTTTTTGATTGTTACCTACTGCTATATTTTTGATTTTAGATTCTTGTTTTGTTGATATAGGTTGTGGTACTAGTTGAACAGTTTATCCTCCTTTAAGA---ACTCTGGGTCACCCGGGTAGAAGAGTGGATTTG---GCGATTTTTAGTTTACATTGTGCTGGTTTGAGTTCAATTTTAGGTGGTATTAATTTTATGTGTACTACAAAAAATTTACGTAGAAGATCTATTTCATTGGAGCATATAAGTTTATTTGTTTGAACTGTATTTGTAACAGTATTTTTATTAGTATTATCTTTACCTGTTTTAGCTGGT---GCAATTACTATGTTATTAACTGATCGTAATTTAAATACTTCTTTTTTTGATCCTAGTACGGGTGGTAATCCTTTAATTTATCAACATTTATTTTGATTTTTTGGTCACCCTGAGGTTTATATTTTAATTTTACCTGCTTTTGGTATTGTTAGACAGTCTACTTTATATTTAACTGGTAAAAAA---GAAGTATTTGGTTCTTTAGGTATGGTATACGCTATTTTAAGAATTGGTTTGATTGGTTGTGTGGTTTGGGCACATCATATGTATACGGTGGGTATGGATTTGGATTCTCGGGCTTATTTTACTGCAGCAACTATAGTAATTGCAGTACCTACTGGTGTAAAGGTTTTTAGGTGATTA---GCAACGTTGTTTGGAATA---AAAATGAATTTTCAACCTTTATTGTTGTGAGTTTTAGGTTTTATTTTTTTGTTTACTATTGGTGGATTAACAGGGGTGGTATTGTCTAATTCAAGATTAGATATTATCTTGCATGATACTTATTATGTTGTTAGTCATTTTCATTATGTT---TTAAGTTTAGGTGCTGTTTTTGGTATTTTTACTGGAATTAGATTGTGGTGAAGTTTTATAACAGGTTATGTTTATGACAAGTTAATAATGTCTTCTGTATTTTTTTTAATGTTTGTTGGTGTAAATTTAACTTTTTTTCCTTTGCATTTTGCTGGATTACATGGTTTTCCGCGTAAG---TATTTAGATTATCCAGATGTTTATTCA---GTTTGAAATGTTATATCGTCATATGGTTCTATAATTAGTGTTTTTGCTTTGTTTTTATTTTTATATGTATTGTTTGAGTCTTTTTTTAGTTACCGTTTGGTT---TTAAGTGATAATTTTATTAATAGAAGT
-- end --

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Statistics of barcoding coverage: Ancylostoma caninum

Barcode of Life Data Systems (BOLDS) Stats
Public Records: 2
Specimens with Barcodes: 2
Species With Barcodes: 1
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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Negative

It is difficult to assess the economic importance of Ancylostoma caninum because they do not infect animals raised for food or labor purposes very often. Domestic dogs, the most common host, can suffer from anemia. If proper precautions are not taken, pet owners with infected dogs can become the host of Ancylostoma caninum. Since infected dogs pass A. caninum larvae out with their feces, anyone who comes in direct contact with feces can obtain the parasite. For example, if a barefoot child is playing in the yard where his infected dog has passed feces, the larvae of A. caninum can enter the child's body via contact of the feet with the feces. Once in the child, an A. caninum will migrate within the subcutaneous layer of the skin for several months causing a condition called dermal larva migrans.

Negative Impacts: injures humans (causes disease in humans ); causes or carries domestic animal disease

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Wikipedia

Ancylostoma caninum

Ancylostoma caninum is a species of nematode which principally infects the small intestine of dogs.[1][2][3] The result of A. caninum infection ranges from asymptomatic cases to death of the dog; better nourishment, increasing age, prior A. caninum exposure or vaccination are all linked to improved survival.[2][4][5][6] Other hosts include carnivores such as wolves, foxes and cats with a small number of cases having been reported in humans.[1][2]

Warm and moist conditions are important to allow survival of A. caninum during the free-living stages of its life cycle and for this reason it is largely restricted to temperate, tropical and sub-tropical regions.[3][7] In parts of the world where these climatic requirements are met such as Sri Lanka, southeast Asia and Malaysia A. caninum is the main cause of hookworm disease in canines.[5][7]

Morphology[edit]

Mouth and teeth of A. caninum.

A. caninum females are typically 14–16 millimetres (0.55–0.63 in) long and 0.5 mm (0.02 in) wide, while the males are smaller at 10–12 mm (0.39–0.47 in) in length and 0.36 mm (0.01 in) in width.[2][3] On males a copulatory bursa exists which, during copulation, attaches the female via ~0.9 mm long spine-like spicules positioned on three muscular rays.[1][2][3] As with other nematodes, the sperm lack flagella.[1] The copulatory bursa is a unique feature of Strongylida members, thus making it a useful means for identifying members of this suborder; it is also used to distinguish members within the suborder due to differences in bursa appearance between species.[2] The vulva of A. caninum females is located at the boundary of the second and final thirds of the body.[1]

The teeth of A. caninum are found in the buccal capsule and divided into three sets.[1][2] Two ventral sets form a lower-jaw equivalent, while a further set projects from the dorsal side and loosely equates to an upper-jaw.[2] Each ventral set has three points with those furthest to the sides being the largest.[1][8] While the ventral sets are prominent, the dorsal set is hidden deeper in the buccal capsule.[1]

A. caninum bends its head end upward (dorsally) which has in the past been noted as a potential source confusion when determining how the hookworm is oriented.[2] If it has recently ingested blood A. caninum is red in colour, if not it appears grey.[1] A. caninum has an alimentary canal made up of an esophagus, intestine and rectum – the esophagus is highly muscular reflecting its role in pulling intestinal mucosa into the body when it feeds.[2][3] Esophageal and anal rings of A. caninum are the source of nerve fibres that extend throughout the body to innervate sensory organs including amphids and phasmids.[1][3]

Eggs are laid by the females typically when at the 8-cell stage.[3] Eggs are 38-43 μM in width with thin walls.[3][5]

Distribution[edit]

Freezing, heating above 37 °C (99 °F), drying or exposing A. caninum to sunlight all give reduced survival of the free-living stage with rates of infection rising with temperature provided 37 °C is not exceeded.[1][2] A. caninum is therefore largely restricted to warm, moist climates though infections are seen in the USA and southern Canada where the temperature is sub-optimal.[2] Specific niches are also able to satisfy the environmental requirements of A. caninum despite not necessarily being in the tropics, such as mines.[2]

Life Cycle[edit]

Transmission via the Environment[edit]

Eggs are excreted from host in the feces and typically hatch within a day on moist, warm soil giving larvae with a non-living cuticle layer.[1][2][5] By four or five days the larvae have moulted twice and are now able to infect a host.[2] Migration occurs from the faeces into the surrounding soil.[2] Two routes of infection from the environment exist. The first route involves penetration of skin at hair follicles or sweat glands, especially between the footpads where contact with soil is frequent and the skin is thinner than otherwise.[2] Secretion of a protease by A. caninum is thought to aid this process.[2] The larvae then migrate through the dermis of the skin, enter the circulatory system and are carried to the lungs.[2] A. caninum larvae exit the blood at the lungs, move from the alveoli up through the trachea and are swallowed to end up in the intestine.[2]

The second and more common route to the small intestine is by direct ingestion of A. caninum by the host, but the subsequent process is identical in either case.[2][3] It is during this third stage of the larva that male or female reproductive organs become established.[3] Larvae of this stage have been shown to secrete a molecule (Ac-asp-2) related to venom allergens in response to host-specific signals; this is thought to have a possible role in helping with the infection process.[9] A third and final moulting occurs to give the mature form of A. caninum which then feeds on mucosa and blood of the small intestine wall.[2] The trigger of feeding is understood to be a receptor-mediated response, however the detail of this process has yet to be established.[10] Sexual reproduction also occurs in the intestine to give a further round of eggs to complete the cycle.[2] Females are thought to produce a pheromone which attracts males and are able to produce approximately 10,000 eggs per day.[1][11]

Direct transmission[edit]

It is also possible for direct transmission between hosts. Larvae having accessed through the skin may avoid exit via the lungs and remain in circulation for transport around the body.[3] At the uterine artery of a pregnant female the larvae are able to cross the placenta to cause pre-natal infection of foetuses.[3] Larvae of an infected foetus will move to the liver until birth at which point migration continues with movement to the intestine via the circulation and lungs as previously described.[3] Alternatively A. caninum larvae evading exit from the circulation at the lungs may instead be carried to the mammary glands and transmitted from the mother in her colostrum or milk to her pups; infection then proceeds in an identical manner to infection by ingestion from the environment.[3][5] Infected bitches have been found to only rarely give prenatal transmission to pups while the likelihood of nursing of pups causing transmission (via the lactational route) is much higher.[12]

Pathogenesis[edit]

Damage during migration to intestine[edit]

Pair of A. caninum hookworms.

Ancylostomum caninum larvae cause damage to the host at the point of entry through the skin leaving a wound vulnerable to secondary infections.[2] As the larvae migrate through the skin an inflammatory response, dermatitis, is often stimulated which can be exacerbated in hosts which give hypersensitive responses.[2][5] Further damage is caused when the larvae leave the circulation and enter the lung with the amount of damage dependent on the extent of the infection; pneumonia and coughing are common consequences.[2]

Damage once in intestine[edit]

Once in the gut A. caninum attaches to and ingests the mucosal lining along with some consumption of blood; up to 0.1mL in 24hrs.[2][5] In a 24hr period A. caninum typically feeds from six sites.[2] This damage to the mucosa compromises the body’s defences and can result in secondary infections by microbes.[7] A group of anticoagulant proteins called AcAPs (A. caninum anticoagulant proteins) which inhibit a range of blood coagulation factors such as Xa are utilised by A. caninum to help in the feeding process by preventing clotting and increasing blood loss.[13][14] These AcAPs are among the most powerful natural anticoagulants that exist and are a key reason for anemia being caused and blood being observed in the faeces of infected hosts.[5][14] Blood losses peak just prior to egg production by the females because this is when their requirements for food are greatest; the amount that they are eating is also peaking and so maximal damage to the intestine is being caused.[3]

Diagnosis[edit]

Analysis of faeces is the definitive method by which a suspected A. caninum infection is confirmed.[2] The faeces are sampled and the characteristic ovular, thin-shelled eggs of A. caninum looked for.[5] Absence of eggs in faeces does not rule out infection; a significant delay of at least 5 weeks exists between initial infection and excretion of eggs in the faeces (larvae must fully mature and reproduce before eggs can be laid).[3][5] In fact, pups frequently die before passing of eggs in the faeces begins.[5] Using the number of eggs in stool samples as an indicator of the extent of infestation requires care to be taken because females have been shown to produce fewer eggs each when the overall number of worms increases.[15]

Signs and symptoms expected to be observed together with A. caninum eggs in the faeces are lethargy, weight loss, weakness, roughness of the hair coat and pale mucous membranes indicative of anemia.[2][5] Well-fed, older dogs with smaller infestations may present few or even none of these symptoms.[2][5] Diarrhoea is rare but stools are typically black due to the blood-derived haemoglobin present in them.[2]

The disease resulting from such A. caninum infection is referred to by the general term hookworm disease or the more specific ancylostomiasis and ancylostomosis diagnoses which recognise the genus of the causative nematode.[2]

Prevention and Control[edit]

Dog kennel: keeping kennels clean reduces risk of A. caninum infection.

A clean environment minimises the risk of A. caninum infection; this can include regularly washed concrete or gravel in kennels instead of soil.[2][5] Bitches are typically checked prior to using them for breeding purposes for nematodes such as A. caninum and birth and suckling can be restricted to sanitised areas to lower the risk of health complications to the pups.[5] When infection of a pregnant bitch is known or suspected fenbendazole or ivermectin can be administered to the bitch to help avoid transmission to the pups.[5]

Canines have been seen to develop significant resistance to A. caninum naturally with age; this protection develops faster in bitches than in dogs and fully mature bitches show substantially greater resistance than fully mature dogs.[4] Specifically the age-related resistance means A. caninum takes longer to reach sexual maturity in older animals and fewer larvae fully develop.[11]

Vaccination[edit]

Numerous vaccines have been developed with varying success against A. caninum. Use of an enzyme important in the worm’s feeding process is popular with one example being AcCP2, a protease, which when used to vaccinate dogs gives a strong antibody response, lowering of numbers of eggs found in stools and a decrease in intestinal worm size.[16] These effects are attributed to reduced AcCP2 activity upon antibody binding.[16] A similar approach has been taken using another A. caninum digestive enzyme, AcGST1, but it failed to give statistically significant results in dogs.[17]

An alternative approach has been to disrupt the migratory ability of A. caninum, this was done so successfully using the AcASP1 protein of A. caninum which gives increases in antibody levels of all subclasses and a reduced worm burden.[6] Other studies using the same vaccine have shown statistically significant 79% reductions in worm burden resulting from this approach.[18]

Animals with prior exposure to A. caninum show enhanced resistance but careful removal of all worms from the previous infection results in loss of this improvement.[11] Studies in mice show resistance due to past exposure can protect against otherwise lethal worm doses and that this is a general form of resistance - defence is offered against subsequent infections via either mouth or skin.[19]

Medication[edit]

Drugs used in treatment of A. caninum infections of dogs include: dichlorvos, fenbendazole, flubendazole, mebendazole, nitroscanate, piperazine, pyrantel, milbemycin, moxidectin, diethylcarbamazine, oxibendazole, and ivermectin.[5]

In Humans[edit]

In inappropriate hosts such as humans A. caninum is able to enter the skin but cannot proceed into the circulation and on to the intestine; instead the disease dermal larva migrans results, caused by movement of the nematode within the skin and which can persist for several months without intervention.[1]

While access to the intestine is not possible via this route, it can occur via ingestion; in a report of 93 enteritis cases in northern Queensland, Australia which were possibly caused by A. canium infection, all those interviewed described behaviour consistent with A. caninum exposure and a colonoscopy of one patient gave positive identification of an adult A. caninum worm.[20][21] Since then work has shown A. caninum can easily go unnoticed or fail to be preserved in specimens making the true incidence of infection in humans likely to be higher than is officially recorded.[22]

Economic Burden[edit]

The animals affected by A. caninum infection are not used for food or labour purposes thus the economic burden from animal illness is low.[1] Work showing that human A. caninum infections are likely underestimated and misdiagnosed indicates the economic impact of A. caninum through human work days lost may be underestimated and significant.[22]

References[edit]

  1. ^ a b c d e f g h i j k l m n o Saeed, Sophia (2003). "Ancylostoma caninum". Animal Diversity Web. Retrieved March 20, 2013. 
  2. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z aa ab ac ad ae af ag ah Marquardt W; Demaree; Grieve (2000). Parasitology and Vector Bology (2nd ed.). Harcourt Academic. pp. 370–376. ISBN 0124732755. 
  3. ^ a b c d e f g h i j k l m n o p Olsen W (1986). Animal Parasites: their life cycles and ecology (3rd ed.). Dover. pp. 399–416. ISBN 0486651266. 
  4. ^ a b Miller (1965). "Influence of Age and Sex on Susceptibility of Dogs to Primary Infection with Ancylostoma caninum". The Journal of Parasitology 51 (5): 701–704. doi:10.2307/3276142. PMID 5857264. 
  5. ^ a b c d e f g h i j k l m n o p q Peregrine, Andrew (March 2012). "Hookworms in Small Animals". The Merck Veterinary Manual. Retrieved March 20, 2013. 
  6. ^ a b Ghosh K, Hotez, P (January 1999). "Antibody-Dependent Reductions in Mouse Hookworm Burden after Vaccination with Ancylostoma caninum Secreted Protein 1". J Infect Dis. 180 (5): 1674–1681. doi:10.1086/315059. 
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