Ancylostoma ceylanicum (Looss, 1911) in golden hamsters ( Mesocricetus auratus): pathogenicity and humoral immune response to a primary infection

Menon, Sujaya; Bhopale, M. K.

doi:10.1017/s0022149x00025724

Cited by 15 publications

(21 citation statements)

References 8 publications

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“…Since there is little evidence of anaemia earlier than day 7 pi and no villous atrophy or crypt hyperplasia before day 12 pi (Garside & Behnke, 1989;Menon & Bhopale, 1985), deep grazing on the mucosa with associated blood loss is probably only associated with the pre-adult and adult stages of A. ceylanicum. Therefore, the slow decline of villus height is consistent with the onset of grazing on the mucosal surface by adult worms.…”

Section: Discussionmentioning

confidence: 99%

The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine in hamsters

Alkazmi

Dehlawi

Behnke³

2006

J. Helminthol.

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Hookworms are known to cause marked changes to the intestinal mucosa, especially in relation to erosion of the villi. However, since the development of enteropathy has not been examined thoroughly through quantitative experiments on infected animals, the results of experiments conducted in hamsters infected with Ancylostoma ceylanicum are reported. Changes to intestinal architecture were first apparent between 12 and 14 days after infection, and then increased in intensity for 3-4 weeks, persisting for as long as worms were present (. 63 days). Following infection, the height of villi declined from a mean of 1002 mm in naïve controls to less than 200 mm and as low as 18 mm in one case. The depth of the crypts of Lieberkuhn increased from a baseline value of 166 mm in naïve controls to in excess of 600 mm within 6 weeks of infection. Mitotic figures had a baseline value of 5.5 per villus-crypt unit, and this rose to in excess of 25 in some experiments. Changes were dependent on the intensity of the parasite burden on day 20, but by 30 days after infection changes in all three values were maximal and density-dependent relationships were no longer clearly apparent. Villus height and crypt depth returned to near normal values within a week of the removal of worms, although group means for both remained different from naïve controls for at least 3 weeks after treatment. Cellular division, as reflected in numbers of mitotic figures, stayed elevated for over 5 weeks after removal of worms. The results suggest that enteropathy in hookworm infections stems from a combination of intestinal immune responses and from the grazing activities of the adult worms on the mucosal surface, but is not sufficient per se for expulsion of this parasite.

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Section: Discussionmentioning

confidence: 99%

The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine in hamsters

Alkazmi

Dehlawi

Behnke³

2006

J. Helminthol.

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“…Other inexpensive animal models, such as mice or rats, extensively employed to study other helminth infections, such as Trichinella, Strongyloides, or Nippostrongylus, cannot be employed to study hookworm infections. When the model hamster of A. ceylanicum was developed several decades ago (19,24,32,40,46), few immunological reagents were available, and a meticulous characterization of the immunological components of this model could not be accomplished. In this paper, we developed reagents and methods in order to provide a first description of the humoral and cellular immune response after A. ceylanicum infections in the hamster model, and we discuss its relevance as a model for human hookworm infections.…”

Section: Discussionmentioning

confidence: 99%

“…A. ceylanicum is also a minor cause of human hookworm infection in parts of Asia (11). Unlike mice, which do not permit the development of adult hookworms (12, 41), hamsters are permissive hosts for the hookworm A. ceylanicum (19,24,32,40,46). In most studies to date, hamsters have been infected with A. ceylanicum third-stage infective larvae (L3) via oral gavage.…”

mentioning

confidence: 99%

Host Cytokine Production, Lymphoproliferation, and Antibody Responses during the Course of Ancylostoma ceylanicum Infection in the Golden Syrian Hamster

Méndez

Valenzuela

et al. 2005

Infect Immun

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The Syrian Golden hamster (Mesocricetus auratus) has been used to model infections with the hookworm Ancylostoma ceylanicum. New molecular immunological reagents to measure cellular immune responses in hamsters were developed and used to determine the impact of A. ceylanicum hookworm infection on host cytokine responses and lymphoproliferation. Initial larval infection with 100 third-stage A. ceylanicum larvae resulted in predominant Th1 responses (upregulation of proinflammatory cytokines) that lasted for the duration of larval migration and continued up to 14 days postinfection (prepatency). Subsequently, development of larvae into egg-laying adult hookworms (patency) coincided with a switch to Th2 predominant responses (interleukin-4 [IL-4]) as well as a marked increase in IL-10 production. This switch also concurred with reduced host lymphoproliferative responses to hookworm antigens. The findings demonstrate a similarity in immune responses between hamsters and humans infected with hookworms, suggesting that hamsters will be a useful animal model species for examining host immunity to human hookworm infections.Hookworm infection is one of the most prevalent parasitic diseases infecting over 700 million people in tropical and subtropical regions of the world (16). Clinical symptoms of human hookworm infection include iron-deficiency anemia (18) and protein-losing enteropathy (14) that may lead to physical, mental and cognitive growth retardation effects (25,42,43). Although chemotherapy is effective at eliminating existing adult parasites, reinfection can occur rapidly after treatment (1, 38). This observation, together with the unique epidemiology of hookworm infection, in which the worm burdens increase with age in endemic regions (6), have led to the suggestion that hookworms can either evade or suppress host immune responses (28, 35). Therefore, characterization of the immune response to hookworm in animal models would constitute a valuable tool to understand the underlying immunological mechanisms of human hookworm infections.The Syrian Golden hamster (Mesocricetus auratus) has been developed as a model to study hookworm infection caused by the dog and cat hookworm, Ancylostoma ceylanicum. A. ceylanicum is also a minor cause of human hookworm infection in parts of Asia (11). Unlike mice, which do not permit the development of adult hookworms (12, 41), hamsters are permissive hosts for the hookworm A. ceylanicum (19,24,32,40,46). In most studies to date, hamsters have been infected with A. ceylanicum third-stage infective larvae (L3) via oral gavage. As the human hookworm A. duodenale is both orally infective as well as infective through the percutaneous route, this approximates a natural route of infection. More importantly, this model reproduces weight and blood loss that result from human infection with A. duodenale.In addition to modeling the host-parasite relationship for human hookworm infection, the hamsters have been used with some success for investigating protective immunity from a new generati...

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“…Ancylostoma ceylanicum infection in the Golden Syrian hamster (Mesocricetus auratus) has been used as an experimental hookworm infection model [14][15][16][17][18][19][20][21][22]. Infective larvae administered orally develop in the small intestine to the adult stage without embarking on tissue migration.…”

mentioning

confidence: 99%

The Impact of Concurrent and TreatedAncylostoma ceylanicumHookworm Infections on the Immunogenicity of a Recombinant Hookworm Vaccine in Hamsters

Ghosh

Antoine

et al. 2006

J INFECT DIS

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Ancylostoma ceylanicum (Looss, 1911) in golden hamsters ( Mesocricetus auratus): pathogenicity and humoral immune response to a primary infection

Cited by 15 publications

References 8 publications

The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine in hamsters

The effect of the hookworm Ancylostoma ceylanicum on the mucosal architecture of the small intestine in hamsters

Host Cytokine Production, Lymphoproliferation, and Antibody Responses during the Course of Ancylostoma ceylanicum Infection in the Golden Syrian Hamster

The Impact of Concurrent and TreatedAncylostoma ceylanicumHookworm Infections on the Immunogenicity of a Recombinant Hookworm Vaccine in Hamsters

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