Animal Diversity Web

Geographic Range

Ancylostoma braziliense is the cat and dog hookworm. Endemic in the southern United States, this species is present in a number of subtropical regions around the world, including Central and South America, and Southern Asia. In Southern Asia, the distribution of Ancylostoma is confined to Indonesia, Borneo, and Malaysia. The reason for this geographical restriction is contrary to an expected widespread distribution of the hookworm due to the intermingling of human populations. Humans and domestic animals have introduced species of Ancylostoma in other places around the world, such as Australia. (Richey, et al., 1996; Traub, et al., 2007)

• Biogeographic Regions
• nearctic
  • native
• oriental
  • introduced
• neotropical
  • native
• australian
  • introduced

Habitat

Ancylostoma braziliense eggs are passed into the environment through feces of cats and dogs. The eggs incubate on warm, moist soil. Adult hookworms live in the small intestines of many vertebrates. (Balfour, et al., 2002; Richey, et al., 1996; Roberts and Janovy Jr, 2009)

• Habitat Regions
• tropical
• terrestrial

• Other Habitat Features
• urban
• suburban
• agricultural

Physical Description

Hookworms in the phylum Nematoda share a common morphology as the anterior end curves like a hook and the buccal capsule is sclerotized and lined with teeth. Within the family Ancylostomidae, the anterior end is curved dorsally. The nematode body is covered with a non-living cuticle shed by molting. The width of the cuticular striation patterns of A. braziliense is 3.45 µm.

Nematode guts consist of a tube with an esophagus composed of the corpus, isthmus, and bulb. Within the Ancylostomidae, the esophogus is stout and muscular. The buccal cavity (between the mouth and esophagus) has a thick cuticular lining which is large and heavily sclerotized, termed a buccal capsule. Males of A. braziliense have a tubercular process that is found at the buccal capsule of the mouth.

Male A. braziliense have two broad lateral lobes and a smaller dorsal lobe with rays on the copulatory bursa. The bursal rays distinguish different species of Ancylostoma. In A. braziliense, the lateral bursal rays are separated at the tips, and the position of attachment of the externodorsal ray is unique in that it is closer to the beginning of the dorsal trunk than in other species.

Females are more difficult to distinguish between different species, and usually the teeth are the only diagnostic tool that can be used. There is a problem with this method, however, because for many species, the size and shape of the teeth do not appear to be significantly unique. (Roberts and Janovy Jr, 2009; Traub, et al., 2007; Yoshida, 1971)

• Other Physical Features
• ectothermic
• heterothermic
• bilateral symmetry

• Sexual Dimorphism
• female larger

• Range length

  7.67 to 8.33 mm

  0.30 to 0.33 in

Development

After the eggs are passed into the environment through the feces of cats or dogs, they hatch into first-stage juveniles. The first-stage juvenile feeds on soil bacteria and feces for about a day. In the early stages of development, A. braziliense is noninfectious, and has a rhabditiform esophagus. The rhabditiform esophagus is characteristic of a feeding stage. Over a period of several days, the nematode molts and reaches the third stage of development where becomes an infectious filariform juvenile. The filariform esophagus is characteristic of non-feeding or liquid feeding stages, and the corpus is reduced. At the third stage, the juvenile stops feeding because it has accumulated all the nutrients needed, and development pauses as the juvenile waits for a host. Once a proper definitive host has been found, the juvenile penetrates the skin. At this stage, A. braziliense is found in the epidermis, follicles, and glands of the skin, sometimes extending to sebaceous glands where they form coils. The juvenile migrates from the skin, and is carried to the heart and lungs by the bloodstream. In the lungs, the juvenile breaks into the alveoli and is propelled by cilia up the respiratory tract, where it is swallowed and ends up in the small intestine. The juvenile attachs to the intestinal mucosa via the buccal capsule, and matures to adult form by molting twice. Once the last molt has finished, the adult hookworm is sexually mature and ready to mate.

Although humans can become infected, they are not true definitive hosts of A. braziliense. As a result, the juveniles only migrate along the epidermis, creating lesions. The juvenile eventually dies, never making it to the circulatory system or reaching adulthood in the intestine. (Balfour, et al., 2002; Brand and Hawdon, 2004; Brenner and Patel, 2003; Costa, et al., 2009; Norris, 1971)

• Development - Life Cycle
• diapause

Reproduction

Males and females mate using direct sperm transfer. Males have spicules that keep the female reproductive opening gaping during sperm transfer. (Roberts and Janovy Jr, 2009)

• Mating System
• polygynandrous (promiscuous)

Males and females of A. braziliense have very different roles during infection and reproduction. The primary role of females is to lay eggs, and once a female has successfully infected a definitive host, it takes a minimum of five weeks before eggs are produced. Males likely exist primarily to fertilize eggs, and produce protease inhibitors. The role of protease inhibitors is still largely unknown, but thought that they are important for parasitism and survival within the host.

Few studies have been conducted on the reproductive genes of nematodes, but recent work has identified gender specific genes in A. braziliense. Scientists investigated sex specific genes of unknown function in A. braziliense, and compared them to sex specific genes of known function in other species. By looking for homology, scientists discovered that males of different species also secrete protease inhibitors, and that they somehow function to ensure survival within the host. Similarities among different species of nematodes with known gene function will help to define the function of previously unknown genes in A. braziliense. Such research also promises to better show the different roles of males and females in infection, reproduction, and survival within the host. (Costa, et al., 2009)

• Key Reproductive Features
• sexual
• fertilization
  • internal
• oviparous

After eggs are laid, there is no parental investment. (Costa, et al., 2009)

• Parental Investment
• no parental involvement
• pre-hatching/birth
  • provisioning

Lifespan/Longevity

The longest lifespan is unknown, and the expected lifespan varies depending on the health of the host and the number of adults causing the infection. (Balfour, et al., 2002)

Behavior

The behavior of A. braziliense has not been widely studied. However, behavioral patterns of A. caninum can be used as a way to gain a understanding of how infective larvae locate their hosts.

Temperature, light, and humidity affect the behavioral patterns of A. caninum, whereas carbon dioxide levels, light, and pH have no effect. A temperature of approximately 40 deg C attracts a juvenile, and it creeps towards the warmth in a snake-like way. Temperatures above or below 40 deg C will not as effectively stimulate host penetration.

In addition to warm temperature, host surface extracts and serum also stimulate penetration. Specifically, penetration is stimulated when juveniles of A. caninum come into contact with the surface extract of dogs, a definitive host. Surface extracts and serum of other intermediate hosts such as humans, are not as effective in stimulating penetration.

Lastly, A. caninum and A. braziliense cannot survive ingestion by a definitive host, and as a result, the juveniles do not establish themselves on projections like the juveniles of other nematode species. Instead, A. caninum and A. braziliense penetrate the skin of their hosts. Exceptions have been found among some species of Ancylostoma, however, where the juveniles have survived oral ingestion by their definitive host. (Granzer and Haas, 1991)

• Key Behaviors
• parasite
• motile

Communication and Perception

Sensory organs on nematodes include papillae, which are tactile receptors, and amphids, which are chemoreceptors. Chemical cues are likely used to attract a mate. Sexual pheromones have been identified for at least 40 species of nematodes. Once a male and female encounter each other, tactile cues are used for reproduction.

Males of A. braziliense and A. caninum can monitor the host-parasite relationship, but it is not known exactly how. Ancylostoma caninum acts independently and won't follow juveniles that have already located and penetrated a host. Recent studies have shown that males secrete protease inhibitors, which are thought to play an important role in infection and survival within the host.

Survival modes of A. braziliense have only recently been studied. Previous research on other hookworm species, such as Necator americanus, has provided the framework of how hookworms evade the host immune system. Nector americanus parasitizes humans, and it secretes products that bind to human cells, inhibiting a proper immune response. By tampering with the human immune system, N. americanus can ensure its survival. (Granzer and Haas, 1991; Roberts and Janovy Jr, 2009; Teixeira-Carvalho, et al., 2008)

• Communication Channels
• tactile
• chemical

• Perception Channels
• infrared/heat
• tactile
• chemical

Food Habits

Adults feed on blood and intestinal fluids in the gut of their host, leading to iron deficiency and anemia for the host. The way in which hookworms digest their blood meal is still being studied, but it is known that adult hookworms use a cascade of proteins to lyse red blood cells. A. braziliense juveniles do not feed on blood, rather they feed on dung and soil bacteria. (Don, et al., 2007)

• Primary Diet
• carnivore
  • eats body fluids

• Animal Foods
• blood
• body fluids

• Other Foods
• dung
• microbes

Predation

There are no known predators of A. braziliense. (Granzer and Haas, 1991)

Ecosystem Roles

Ancylostoma braziliense is an endoparasite of cats and dogs. Adult hookworms eat blood from the intestine of cats and dogs, causing anemia. (Don, et al., 2007)

• Ecosystem Impact
• parasite

Economic Importance for Humans: Positive

A. braziliense has no positive impact on humans. (Balfour, et al., 2002)

Economic Importance for Humans: Negative

Humans are accidental, dead-end hosts for hookworms. Infectious juveniles can penetrate the epidermis of humans by taking advantage of broken skin or hair follicles. Inside the human host, the juveniles migrate through the epidermis, commonly called the creeping eruption. As the juveniles migrate, they cause serpinginous eruptions on the skin, and they cause a tingling sensation. The lesions on the skin are typically 3 mm wide, but in some cases the lesions can expand to reach 15 to 20 cm. The juveniles advance through the epidermis at a rate of a few mm per day. As the worms migrate, they frequently change direction, and vesicles begin to form in their trail. The vesicles often become inflamed, and as a result the trails of the juvenile are visible on the surface of the skin. The most common site of infection of humans is the feet. Additionally, it is quite common for children to become infected on their buttocks because thin swim wear does not provide a sufficient barrier to the infectious juveniles found in the warm, moist sand of tropical beaches.

Although the juveniles create uncomfortable lesions on the skin, they die before causing any serious harm because humans are dead-end hosts. Typically, infected humans do not need medical attention because the juveniles die after a few weeks or months. The most serious negative impact of A. braziliense on humans comes from infecting their pets. Infected cats and dogs require expensive medical attention to stop the spread of the parasite. (Balfour, et al., 2002; Roberts and Janovy Jr, 2009)

• Negative Impacts
• injures humans
  • bites or stings
• causes or carries domestic animal disease

Conservation Status

As a parasite with only negative affects on its hosts, A. braziliense has no conservation status.

• IUCN Red List

  Not Evaluated

• US Federal List

  No special status

• CITES

  No special status

• State of Michigan List

  No special status

Other Comments

The width of the cuticular striation patterns of A. braziliense is 3.45 micrometers compared to 5.66 micrometers in A. ceylanicum. Males of A. braziliense have a tubercular process that is found at the buccal capsule of the mouth, whereas this feature is completely absent in other species, such as A. ceylanicum. (Traub, et al., 2007; Yoshida, 1971)

Contributors

Stephanie Chapman (author), University of Michigan-Ann Arbor, Heidi Liere (editor), University of Michigan-Ann Arbor, John Marino (editor), University of Michigan-Ann Arbor, Barry OConnor (editor), University of Michigan-Ann Arbor, Renee Mulcrone (editor), Special Projects.

References

Balfour, E., A. Zalka, R. Lazova. 2002. Cutaneous larva migrans with parts of the larva in the epidermis. Cutis, 69: 368-370. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/12041816.

Brand, A., J. Hawdon. 2004. Phosphoinositide-3-OH- kinase inhibitor LY294002 prevents ativation of Ancylostoma caninum and Ancylostoma ceylanicum third-stage infective larvae. International Journal for Parasitology, 34: 909-914. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/15217729.

Brenner, M., M. Patel. 2003. Cutaneous larva migrans: The creeping eruption. Cutis, 72: 111-115. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/12953933.

Carvalho, R., J. Araujo, F. Braga, S. Ferreira, J. Araujo, A. Silva, L. Frassy, C. Alves. 2009. Biological control of Anclyostomis in dogs using the nematode-trapping fungus Monacrosporium thaumasium in southeastern Brazil. Veterinary Parasitology, 165: 179-183.

Costa, A., A. Gomez- Ruiz, E. Rabelo. 2008. Identification of gender-regulated genes in Ancylostoma braziliense by real-time RT-PCR. Veterinary Parasitology, 153: 277-284. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/18358613.

Costa, A., R. Gasser, S. Dias, E. Rabelo. 2009. Male-enriched transcription of genes encoding ASPs and Kuniz-type protease inhibitors in Ancylostoma species. Molecular and Cellular Probes, 23: 298-303. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/19646525.

Don, T., Y. Oksov, S. Lustigman, A. Loukas. 2007. Saposin-like protein from the intestine of the blood-feeding hookworm, Ancylostoma caninum. Cambridge Journals, 134: 427-436. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/17109779.

Granzer, M., W. Haas. 1991. Host-finding and host recognition of infective Ancylostoma caninum larvae. International Journal for Parasitology, 21 (4): 429-440. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/1917283.

Labarthe, N., M. Lucia Serrao, A. Ferreira, N. Almeida, J. Guerrero. 2004. A survey of gastrointestinal helminths in cats of the metropolitan region of Rio de Janeiro, Brazil. Veterinary Parasitology, 123: 133-139. Accessed February 05, 2010 at http://www.ncbi.nlm.nih.gov/pubmed/1917283.

Norris, D. 1971. The migratory behavior of the infective-stage larvae of Ancylostoma braziliense and Ancylostoma tubaeforme in rodent paratenic hosts. The Journal of Parasitology, 57 (5): 998-1009.

Richey, T., R. Gentry, J. Fitzpatrick, A. Morgan. 1996. Persistant cutaneous larva migrans due to Ancylostoma species. Southern Medical Journal, 89 (6): 609-611. Accessed February 16, 2010 at http://journals.lww.com/smajournalonline/Abstract/1996/06000/Persistent_Cutaneous_Larva_Migrans_Due_to.10.aspx.

Roberts, L., J. Janovy Jr. 2009. Foundations of Parasitology. New York, NY: McGraw- Hill.

Stothard, P., D. Pilgrim. 2003. Sex-determination gene and pathway evolution in nematodes. Bioessays, 25 (3): 221-231.

Teixeira-Carvalho, A., R. Fujiwara, E. Stemmy, D. Oive, J. Damsker, A. Loukas, R. Correa-Oliveira, S. Constant, J. Bethony. 2008. Binding of excreted and/or secreted products of adult hookworms to human NK cells in Necator americanus-infected individuals from Brazil. American Society For Microbiology, 76 (12): 5810-5816.

Traub, R., R. Hobbs, P. Adams, J. Behnke, P. Harris, C.A Thompson. 2007. A case of mistaken identity-reappraisal of the species of canid and felid hookworks (Ancylostoma) present in Australia and India. Parasitology, 134: 113-119.

Williamson, A., S. Lustigman, Y. Oksov, V. Deumic, J. Plieskatt, S. Mendez, B. Zhan, M. Bottazzi, P. Hotez, A. Loukas. 2006. Ancylostoma caninum MTP-1, an astacin-like metalloprotease secreted by infective hookworm larvae, is involved in tissue migration. Infection and Immunology, 74 (2): 961-967. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/16428741.

Yoshida, Y. 1971. Comparative studies on Ancylostoma braziliense and Ancylostoma ceylanicum. I. The adult stage. The Journal of Parasitology, 57 (5): 983-989. Accessed April 16, 2011 at http://www.ncbi.nlm.nih.gov/pubmed/4851100.