taxonomy, identification, and life cycle of Angiostrongylus cantonensis

Biology: <strong>taxonomy</strong>,<br />

<strong>identification</strong>, <strong>and</strong> <strong>life</strong> <strong>cycle</strong> <strong>of</strong><br />

<strong>Angiostrongylus</strong> <strong>cantonensis</strong><br />

Robert H. Cowie<br />

Pacific Biosciences Research Center, University <strong>of</strong> Hawaii, Honolulu, Hawaii<br />

photo: Juliano Romanzini, courtesy <strong>of</strong> Carlos Graeff Teixeira<br />

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CLASSIFICATION AND DIVERSITY<br />

PHYLUM: Nematoda<br />

CLASS: Rhabditea<br />

ORDER: Strongylida<br />

SUPERFAMILY: Metastrongyloidea<br />

FAMILY: Angiostrongylidae<br />

• Around 19 species are recognized worldwide in the genus<br />

<strong>Angiostrongylus</strong><br />

• Two species infect humans widely:<br />

- <strong>Angiostrongylus</strong> costaricensis Morera & Céspedes, 1971<br />

causes abdominal angiostrongyliasis, especially a<br />

problem in South America<br />

- <strong>Angiostrongylus</strong> <strong>cantonensis</strong> (Chen, 1935)<br />

causes eosinophilic meningitis<br />

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NOMENCLATURE<br />

<strong>Angiostrongylus</strong> <strong>cantonensis</strong> (Chen, 1935)<br />

• First described by Chen (1935) as Pulmonema <strong>cantonensis</strong><br />

• Also described as Haemostrongylus ratti by Yokogawa (1937)<br />

• Pulmonema subsequently synonymized with <strong>Angiostrongylus</strong> <strong>and</strong> ratti with<br />

<strong>cantonensis</strong><br />

• <strong>Angiostrongylus</strong> <strong>cantonensis</strong> then widely accepted as the name <strong>of</strong> this species<br />

• Ubelaker (1986) split <strong>Angiostrongylus</strong> into five genera:<br />

<strong>Angiostrongylus</strong> (in carnivores), Parastrongylus (murids), Angiocaulus (mustelids),<br />

Gallegostrongylus (gerbils <strong>and</strong> one murid), Stefanskostrongylus (insectivores)<br />

• And placed <strong>cantonensis</strong> in the genus Parastrongylus<br />

• But this classification is not widely used <strong>and</strong> most people still refer to the species as<br />

<strong>Angiostrongylus</strong> <strong>cantonensis</strong><br />

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MORPHOLOGY, TAXOMOMY, IDENTIFICATION<br />

Adult males<br />

Caudal bursa<br />

Ubelaker, 1986<br />

1. <strong>Angiostrongylus</strong> vasorum<br />

2. Parastrongylus tateronae<br />

3. Angiocaulus gubernaculatus<br />

4. Rodentocaulus ondatrae<br />

5. Gallegostrongylus ibicensis<br />

Maldonado et al. 2010<br />

<strong>Angiostrongylus</strong> <strong>cantonensis</strong> – 3 locations in Brazil<br />

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MORPHOLOGY, TAXONOMY, IDENTIFICATION<br />

ADULT SIZE<br />

• Female: 17-34 mm long, 0.28-0.56 mm wide<br />

• Male: 15-25 mm long, 0.25-0.42 mm wide<br />

Ash, 1970<br />

1. <strong>Angiostrongylus</strong> <strong>cantonensis</strong><br />

2. Aleurostronglus abstrusus<br />

3. <strong>Angiostrongylus</strong> vasorum<br />

4. Anafilaroides rostratus<br />

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Juliano Romanzini, courtesy <strong>of</strong> Carlos Graeff Teixeira<br />

Adult female with characteristic<br />

red (gut) <strong>and</strong> white (uterine<br />

tubules) spiral appearance<br />

3 rd STAGE SIZE (in snails/slugs)<br />

• 425-524 μm long, 23-34 μm wide<br />

IDENTIFICATION - 3 RD STAGE WORMS<br />

• size<br />

• pointed tail with no transverse striations

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LIGHT MICROSCOPY OF 3 RD STAGE<br />

ANGIOSTRONGYLUS CANTONENSIS<br />

1a. Anterior end showing knob-like tips<br />

(KT), rod-like structure (RS),<br />

esophagus (E) <strong>and</strong> excretory pore (EP)<br />

1b. Posterior end showing tail pointed<br />

tip (TPT) <strong>and</strong> anus (A)<br />

Thiengo et al. 2010. Acta Tropica<br />

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• Definitive host – rats (various species)<br />

• Intermediate host – snails/slugs (various species)<br />

worms mature to 3 rd<br />

stage in snail/slug<br />

feces eaten by<br />

snails/slugs<br />

worms swallowed<br />

expelled as feces<br />

worms penetrate alveoli<br />

move up trachaea<br />

eggs hatch into<br />

1 st stage worms<br />

LIFE-CYCLE<br />

rat eats snail/slug<br />

ingests 3 rd stage worm<br />

worm penetrates intestine<br />

enters bloodstream<br />

worm moves to CNS<br />

matures to 5 th stage – young<br />

adult<br />

young adult worm moves to<br />

bloodstream<br />

matures in right ventricle <strong>and</strong><br />

pulmonary artery<br />

females lay eggs<br />

eggs travel through<br />

bloodstream to alveoli<br />

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<strong>Angiostrongylus</strong> <strong>cantonensis</strong> in a rat brain<br />

Photo: Camila Krug, from Graeff-Teixeira et al 2009<br />

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• Definitive host – rats (various species)<br />

• Intermediate host – snails/slugs (various species)<br />

worms mature to 3 rd<br />

stage in snail/slug<br />

feces eaten by<br />

snails/slugs<br />

worms swallowed<br />

expelled as feces<br />

worms penetrate alveoli<br />

move up trachaea<br />

eggs hatch into<br />

1 st stage worms<br />

LIFE-CYCLE<br />

rat eats snail/slug<br />

ingests 3 rd stage worm<br />

45 days<br />

worm penetrates intestine<br />

enters bloodstream<br />

worm moves to CNS<br />

matures to 5 th stage – young<br />

adult<br />

young adult worm moves to<br />

bloodstream<br />

matures in right ventricle <strong>and</strong><br />

pulmonary artery<br />

females lay eggs<br />

eggs travel through<br />

bloodstream to alveoli<br />

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• Accidental host – humans (<strong>and</strong> other mammals)<br />

juvenile matures to 3 rd<br />

stage in snail/slug<br />

rat feces eaten by<br />

snails/slugs<br />

larvae penetrate alveoli<br />

move up trachaea<br />

HUMAN INFECTION<br />

person eats snail/slug<br />

ingests 3 rd stage juveniles<br />

juvenile penetrates intestine<br />

enters bloodstream<br />

juvenile moves to CNS<br />

matures to 5 th stage <strong>and</strong> dies<br />

larva moves to bloodstream<br />

matures in right ventricle<br />

eosinophilic meningitis <strong>and</strong> pulmonary artery<br />

angiostrongyliasis<br />

females lay eggs<br />

eggs hatch into<br />

1st RAT LUNG WORM DISEASE SCIENTIFIC WORKSHOP<br />

stage HONOLULU, larvae HAWAII AUGUST 16 - 18, 2011<br />

eggs travel through<br />

bloodstream to alveoli

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SOME KEY PUBLICATIONS<br />

Chen, H.T. 1935. Un nouveau nématode pulmonaire, Pulmonema <strong>cantonensis</strong> n.g., n.sp., des rats de Canton. Annales de<br />

Parasitologie Humaine et Comparé 13: 312-370.<br />

Mackerras, M.J. & S<strong>and</strong>ars, D.F. 1955. The <strong>life</strong>-history <strong>of</strong> the rat lungworm, <strong>Angiostrongylus</strong> <strong>cantonensis</strong> (Chen)<br />

(Nematoda: Metastrongylidae). Australian Journal <strong>of</strong> Zoology 3: 1-21, pls 1-6.<br />

Rosen, L. et al. 1962. Eosinophilic meningoencephalitis caused by a metastrongylid lungworm <strong>of</strong> rats. Journal <strong>of</strong> the<br />

American Medical Association 179: 620-624.<br />

Wallace, G.D. & Rosen, L.R. 1969. Studies on eosinophilic meningitis V. Molluscan hosts <strong>of</strong> <strong>Angiostrongylus</strong> <strong>cantonensis</strong><br />

on Pacific Isl<strong>and</strong>s. American Journal <strong>of</strong> Tropical Medicine <strong>and</strong> Hygiene 18: 206-216.<br />

Ash, L.R. 1970. Diagnostic morphology <strong>of</strong> the third-stage larvae <strong>of</strong> <strong>Angiostrongylus</strong> <strong>cantonensis</strong>, <strong>Angiostrongylus</strong> vasorum,<br />

Aelurostrongylus abstrusus, <strong>and</strong> Anafilaroides rostratus (Nematoda: Metastrongyloidea). Journal <strong>of</strong> Parasitology 56:<br />

249-253.<br />

Ubelaker, J.E. 1986. Systematics <strong>of</strong> species referred to the genus <strong>Angiostrongylus</strong>. Journal <strong>of</strong> Parasitology 72: 237-244.<br />

Kliks, M.M. & Palumbo, N.E. 1992. Eosinophilic meningitis beyond the Pacific basin: the global dispersal <strong>of</strong> a peridomestic<br />

zoonosis caused by A. <strong>cantonensis</strong>, the nematode lungworm <strong>of</strong> rats. Social Science <strong>and</strong> Medicine 34: 199-212.<br />

Prociv, P. et al. 2000. Neuro-angiostrongyliasis: Unresolved issues. International Journal for Parasitology 30: 1295-1303.<br />

Qvarnstrom, Y. et al. 2010. Improved Molecular Detection <strong>of</strong> <strong>Angiostrongylus</strong> <strong>cantonensis</strong> in mollusks <strong>and</strong> other<br />

environmental samples with a species-specific Internal Transcribed Spacer 1-based TaqMan assay. Applied <strong>and</strong><br />

Environmental Microbiology 76: 5287-5289.<br />

Lindo, J.F. et al. 2002. Enzootic <strong>Angiostrongylus</strong> <strong>cantonensis</strong> in rats <strong>and</strong> Snails after an outbreak <strong>of</strong> human eosinophilic<br />

meningitis, Jamaica. Emerging Infectious Diseases 8: 324-326.<br />

Graeff-Teixeira, C. et al. 2009. Update on eosinophilic meningoencephalitis <strong>and</strong> its clinical relevance. Clinical Microbiology<br />

Reviews 22: 322-348.<br />

Lv, S. et al. 2011. The emergence <strong>of</strong> angiostrongyliasis in the People’s Republic <strong>of</strong> China: the interplay between invasive<br />

snails, climate change <strong>and</strong> transmission dynamics. Freshwater Biology 56: 717-734.<br />

RAT LUNG WORM DISEASE SCIENTIFIC WORKSHOP<br />

HONOLULU, HAWAII AUGUST 16 - 18, 2011

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THANKS<br />

Questions?<br />

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