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Existence of Angiostrongylus cantonensis in rats (Rattus norvegicus) in Grenada, West Indies
Veterinary Parasitology 162 (2009) 160–162
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Existence of Angiostrongylus cantonensis in rats (Rattus norvegicus) in Grenada, West Indies A. Chikweto a,*, M.I. Bhaiyat a, C.N.L. Macpherson b, C. DeAllie a, R.D. Pinckney a, C. Richards a, R.N. Sharma a a b
Department of Pathobiology, School of Veterinary Medicine, St. George’s University, Box 7, St. George’s, Grenada, West Indies Windward Islands Research and Education Foundation, St. George’s University, Grenada, West Indies
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 October 2008 Received in revised form 5 February 2009 Accepted 16 February 2009
The zoonotic rat lung worm, Angiostrongylus cantonensis is endemic to Asia, North America, Africa and Australia. The parasite is expanding geographically and has recently been recorded in some of the Greater Antilles in the northern part of the Caribbean. In this study A. cantonensis is reported for the first time in the Lesser Antilles in one of the southernmost islands, Grenada. Between September 2005 and September 2006, 192 rats (Rattus norvegicus) were trapped throughout the island. The rats were anesthetized, exsanguinated, necropsied and the lungs were fixed whole in 10% buffered formalin, trimmed, processed, cut at 3 mm, stained with hematoxylin and eosin and examined microscopically. A total of 45 (23.4%) of the 192 rats examined were found to be infected with A. cantonensis and adult worms were found in the cardiopulmonary system of one of the rats. Microscopically, pulmonic lesions, consisting of pulmonary thrombosis, hypertrophy of pulmonary arteries and granulomatous pneumonia were associated with intralesional adults, larvae and embryonated eggs of A. cantonensis. An incidental finding of variably sized (2–7 mm) solitary to multiple cysts containing larvae of Taenia taeniaformis were seen in the livers of 57 rats. This report of A. cantonensis in Grenada provides evidence of the further global expansion of this important zoonotic parasite and the public health implications of this discovery is discussed. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Angiostrongylus cantonensis Rattus norvegicus Prevalence Histopathology Grenada West Indies
1. Introduction Angiostrongylus cantonensis (Metastrongyloidea: Angiostrongylinae) is a lung dwelling parasite of rats (Soulsby, 1982). The parasite lays its eggs in the lungs and first stage larvae hatch in situ. First stage larvae migrate to the pharynx, are swallowed and then passed in the faeces of infected rats. The intermediate hosts, snails and slugs, are infected by first stage larvae, and after 2 molts the larvae reach the infective third stage. Third stage larvae are ingested by rats as they feed on snails and slugs. They migrate to the central nervous system, molt and finally
* Corresponding author. Tel.: +1 473 443 7141; fax: +1 473 439 5068. E-mail address: [email protected] (A. Chikweto). 0304-4017/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2009.02.020
mature in the pulmonary arteries. Humans get infected by eating raw or undercooked intermediate hosts snails and\or slugs or through the ingestion of raw or undercooked paratenic hosts which may include crabs, planarians, prawns, shrimps, frogs and monitor lizards. Some infections may be through the consumption of contaminated raw vegetables (Wang et al., 2008). A. cantonensis is endemic to South East Asia, the Pacific islands and Australia where it is the main cause of eosinophilic meningitis in humans (Wang et al., 2008). This parasite has spread geographically in recent years with the dissemination of one of its intermediate hosts, the giant African land snail (Achatina fulica), which is a popular item of food in some countries (Macpherson, 2005) and by ships infested with rats (Wang et al., 2008). Kliks and Palumbo (1992) reported that the parasite has been found in rats in
A. Chikweto et al. / Veterinary Parasitology 162 (2009) 160–162
Madagascar (1963), Cuba (1973), Egypt (1977), Puerto Rico (1986) and Nigeria (1989) and it is spreading down the east coast of Australia (Prociv and Carlisle, 2001). In the USA the parasite was first reported in New Orleans in Rattus norvegicus (Campbell and Little, 1988) and later A. cantonensis was also found in several wildlife species (Kim et al., 2002) including in a non-human primate in Florida (Duffy et al., 2004). In the West Indies eosinophilic meningitis due to A. cantonensis is an emerging zoonosis and cases in humans have been reported from a number of islands starting in the mid 1980s. Such islands include, Puerto Rico in 1986 (Kliks and Palumbo, 1992), among American tourists returning from Jamaica (Slom et al., 2002; Waugh et al., 2005), in several localities in Cuba (Aguiar et al., 1981; Kliks and Palumbo, 1992) and in a German tourist returning from the Dominican Republic (Rau et al., 2006). Recent reports on detection of A. cantonensis adults and larvae in rodents and snails in the West Indies include from the Dominican Republic (Vargas et al., 1992), Jamaica (Lindo et al., 2002) and Haiti (Raccurt et al., 2003). Levett et al. (2004) found no evidence of A. cantonensis in rats in Barbados, a neighbouring island of Grenada. We report A. cantonensis infection in rats from the Lesser Antilles, the island of Grenada, for the first time. 2. Materials and methods From September 2005 to September 2006, 192 rats (R. norvegicus) comprising 101 females and 91 males were trapped from 6 different parishes including St. George, St. Mark, St. John, St. David, St. Andrew and St. Patrick. The rats were anesthetized with diethyl ether, exsanguinated, necropsied and lesions in lungs and other tissues recorded. Lungs were fixed whole in 10% buffered formalin, trimmed, processed, cut at 3 mm, stained with hematoxylin and eosin and examined microscopically. 3. Results Gross lesions of consolidation with multifocal petechiae and congestion of lungs were noted in 2 rats whereas 7 rats showed mild to moderate degrees of petechiation and congestion. In one rat, submitted dead for necropsy, numerous A. cantonensis adults were observed in the right cardiac ventricle and the pulmonary trunk and its branches. The adults were 21 mm 0.5 mm in size. In addition, a barber-pole appearance was seen in female worms. There was marked biventricular dilatation in this particular rat. In histologic sections of lungs, the adults had polymyarian–coelomyarian musculature, smooth cuticle without ornamentations, accessory hypodermal cords, lateral cords, few multinucleated intestinal cells and paired uterus often containing eggs (Gardiner and Poyton, 1999). There was focal mild to severe diffuse granulomatous pneumonia with intralesional larvae and embryonated eggs in alveoli and cross-sections of adult worms with features described above in pulmonary artery branches, often with thrombosis (Fig. 1). There was widespread infection by A. cantonensis in all the 6 parishes of Grenada (St. George, 4/19; St. Mark, 11/
161
Fig. 1. Lung cross-sections of A. cantonensis in the pulmonary artery branch (PA). A. cantonensis can be characterized by its smooth cuticle, polymyarian–coelomyarian musculature, with lateral cords (LC), accessory hypodermal cords (C), paired uterus (U) containing eggs, ovaries (O) and intestine (I). There is infiltration of inflammatory cells in the adjacent lung parenchyma.
29; St. John, 5/30; St. David, 13/62; St. Andrew, 7/36; St. Patrick, 5/16). Incidental findings of variably sized (2– 7 mm) solitary to multiple cysts containing larvae of Taenia taeniaformis were seen in the livers of 57 rats. There was no association between the presence of hepatic T. taeniaformis cysts with A. cantonensis infestation (p > 0.05, x2). 4. Discussion This is the first report of angiostrongyliasis in rats in Grenada and the first time it has been reported from the Lesser Antilles. It is likely that this parasite was introduced to Grenada by ships infested with rats infected with A. cantonensis. The other possibility could be due to the natural spread of intermediate hosts, the land snails and slugs. Whatever the mode of introduction, the parasite has firmly established itself throughout the island in Norwegian rats (R. norvegicus). In this study all rats caught were R. norvegicus, implying that this species of rat is more predominant in Grenada. Infection rates in other rat species in Grenada is unknown but studies in Puerto Rico (Andersen et al., 1986) and Haiti (Raccurt et al., 2003) demonstrated that R. norvegicus was significantly more infected with A. cantonensis than R. rattus (p < 0.05, x2). In Cuba, infestation rates between R. norvegicus and R. rattus were not significant (p > 0.05, x2) (Aguiar et al., 1981). The other lung parasite of rats to be considered in the differential diagnosis was Angiostrongylus schmidti. This species has been reported to mainly affect rice rats (Oryzomys palustris) in North America (Soulsby, 1982) but was reported in rats in Florida (Kinsella, 1971). We did not find this species in the rats examined in this study. There are several species of aquatic and land snails in Grenada including the giant African land snail, A. fulica, but the local people interviewed during this study said that land snails are not usually consumed. The indigenous diet in Grenada includes the consumption of crabs, aquatic snails and iguanas and these paratenic hosts may provide a risk for the transmission of the parasite to humans. Further
162
A. Chikweto et al. / Veterinary Parasitology 162 (2009) 160–162
studies on infection rates in the intermediate and paratenic hosts in Grenada are indicated. This study which revealed the widespread distribution of the parasite in rats in Grenada also should raise awareness among the local physicians to consider A. cantonensis infection in the differential diagnosis of cases of eosinophilic meningitis. For prevention of human infection in Grenada, rodent control measures and education of the public on the proper preparation of food, particularly snails, crabs and tattoo (iguanas) is recommended. Acknowledgements The authors are indebted to Ray Samuel, Ferron Victor and Sean McCartney for their help with this investigation. This study was supported by a grant from the small research initiative fund, St. George’s University. References Aguiar, P.H., Morera, P., Pascual, J., 1981. First record of Angiostrongylus cantonensis in Cuba. Am. J. Trop. Med. Hyg. 30, 963–965. Andersen, E., Gubler, D.J., Sorensen, K., Beddard, J., Ash, L.R., 1986. First report of Angiostrongylus cantonensis in Puerto Rico. Am. J. Trop. Med. Hyg. 35, 319–322. Campbell, B.G., Little, M.D., 1988. The finding of Angiostrongylus cantonensis in rats in New Orleans. Am. J. Trop. Med. Hyg. 38, 568–573. Duffy, M.S., Miller, C.L., Kinsella, J.M., De Lahunta, A., 2004. Parastrongylus cantonensis in a non-human primate, Florida. Emerg. Infect. Dis. 10 (12), 2207–2210. Gardiner, C.H., Poyton, S.L., 1999. Morphologic characteristics of nematodes in tissue sections. In: An Atlas of Metazoan Parasites in Animal Tissues. Armed forces Institute of Pathology, pp. 2, 3 and 28. Kim, D.Y., Stewart, T.B., Bauer, Mitchelle, M., 2002. Parastrongylus (=Angiostrongylus) cantonensis now endemic in Louisiana Wildlife. J. Parasitol. 88 (5), 1024–1026.
Kliks, M.M., Palumbo, N.E., 1992. Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc. Sci. Med. 34, 199–212. Kinsella, J.M., 1971. Angiostrongylus schmidti sp.n. (Nematoda: Metastrongyloidea) from the rice rat, Oryzomys palustris, in Florida, with a key to the species of Angiostrongylus Kamensky, 1905. J. Parasit. 57, 494–497. Levett, P.N., Douglas, K.A., Waugh, C.A., Robinson, R.D., Lindo, J.F., 2004. Failure to detect Angiostrongylus cantonensis in rats in Barbados. West Indian Med. J. 53, 58. Lindo, J.F., Waugh, C.A., Hall, J., Cunningham-Myrie, C., Ashley, D., Eberhard, M.L., Sullivan, J.J., Bishop, H.S., Robison, D.G., Holtz, T., Robinson, R.D., 2002. Enzootic Angiostrongylus cantonensis in rats and snails after an outbreak of human eosinophilic meningitis, Jamaica. Emerg. Infect. Dis. 8, 324–326. Macpherson, C.N.L., 2005. Human behaviour and the epidemiology of parasitic zoonoses. Int. J. Parasitol. 35, 1319–1331. Prociv, P., Carlisle, M.S., 2001. The spread of Angiostrongylus cantonensis in Australia. Southeast Asian J. Trop. Med. Public Health 32, 126–128. Raccurt, C.P., Blaise, J., Durette-Desset, M., 2003. Presence of Angiostrongylus cantonensis in Haiti. Trop. Med. Int. Health 8, 423–426. Rau, C., Bialek, R., Richter, S., Lindner, A., 2006. Headache after returning from the Dominican Republic. Deut. Med. Wochenschr. 131, 1656– 1659. Slom, T.J., Cortese, M.M., Gerber, S.I., Jones, R.C., Holtz, T.H., Lopez, A.S., Zambrano, C.H., Sufit, R.L., Sakolvaree FY., Chaicumpa, W., Herwaldt, B.L., Johnson, S., 2002. An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. N. Eng. J. Med. 346, 668–675. Soulsby, E.J.L., 1982. Angiostrongylus cantonensis. In: Helminthes, Arthropods and Protozoa of Domestic Animals. Bailliere Tindall Publishers, London, pp. 280–281. Vargas, M., Gomez, P.J.D., Malek, E.A., 1992. First record of Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in the Dominican Republic. Trop. Med. Parasitol. 43, 253– 255. Wang, Q.P., Lai, D.H., Zhu, Q.X., Chen, Q.G., Lun, Z.R., 2008. Human angiostrongyliasis. Lancet Infect. Dis. 8 (10), 621–630. Waugh, C.A., Shafir, S., Wise, M., Robinson, R.D., Eberhard, M.L., Lindo, J.F., 2005. Human Angiostrongylus cantonensis, Jamaica. Emerg. Infect. Dis. 11, 1977–1978.
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Existence of Angiostrongylus cantonensis in rats (Rattus norvegicus) in Grenada, West Indies A. Chikweto a,*, M.I. Bhaiyat a, C.N.L. Macpherson b, C. DeAllie a, R.D. Pinckney a, C. Richards a, R.N. Sharma a a b
Department of Pathobiology, School of Veterinary Medicine, St. George’s University, Box 7, St. George’s, Grenada, West Indies Windward Islands Research and Education Foundation, St. George’s University, Grenada, West Indies
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 October 2008 Received in revised form 5 February 2009 Accepted 16 February 2009
The zoonotic rat lung worm, Angiostrongylus cantonensis is endemic to Asia, North America, Africa and Australia. The parasite is expanding geographically and has recently been recorded in some of the Greater Antilles in the northern part of the Caribbean. In this study A. cantonensis is reported for the first time in the Lesser Antilles in one of the southernmost islands, Grenada. Between September 2005 and September 2006, 192 rats (Rattus norvegicus) were trapped throughout the island. The rats were anesthetized, exsanguinated, necropsied and the lungs were fixed whole in 10% buffered formalin, trimmed, processed, cut at 3 mm, stained with hematoxylin and eosin and examined microscopically. A total of 45 (23.4%) of the 192 rats examined were found to be infected with A. cantonensis and adult worms were found in the cardiopulmonary system of one of the rats. Microscopically, pulmonic lesions, consisting of pulmonary thrombosis, hypertrophy of pulmonary arteries and granulomatous pneumonia were associated with intralesional adults, larvae and embryonated eggs of A. cantonensis. An incidental finding of variably sized (2–7 mm) solitary to multiple cysts containing larvae of Taenia taeniaformis were seen in the livers of 57 rats. This report of A. cantonensis in Grenada provides evidence of the further global expansion of this important zoonotic parasite and the public health implications of this discovery is discussed. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Angiostrongylus cantonensis Rattus norvegicus Prevalence Histopathology Grenada West Indies
1. Introduction Angiostrongylus cantonensis (Metastrongyloidea: Angiostrongylinae) is a lung dwelling parasite of rats (Soulsby, 1982). The parasite lays its eggs in the lungs and first stage larvae hatch in situ. First stage larvae migrate to the pharynx, are swallowed and then passed in the faeces of infected rats. The intermediate hosts, snails and slugs, are infected by first stage larvae, and after 2 molts the larvae reach the infective third stage. Third stage larvae are ingested by rats as they feed on snails and slugs. They migrate to the central nervous system, molt and finally
* Corresponding author. Tel.: +1 473 443 7141; fax: +1 473 439 5068. E-mail address: [email protected] (A. Chikweto). 0304-4017/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2009.02.020
mature in the pulmonary arteries. Humans get infected by eating raw or undercooked intermediate hosts snails and\or slugs or through the ingestion of raw or undercooked paratenic hosts which may include crabs, planarians, prawns, shrimps, frogs and monitor lizards. Some infections may be through the consumption of contaminated raw vegetables (Wang et al., 2008). A. cantonensis is endemic to South East Asia, the Pacific islands and Australia where it is the main cause of eosinophilic meningitis in humans (Wang et al., 2008). This parasite has spread geographically in recent years with the dissemination of one of its intermediate hosts, the giant African land snail (Achatina fulica), which is a popular item of food in some countries (Macpherson, 2005) and by ships infested with rats (Wang et al., 2008). Kliks and Palumbo (1992) reported that the parasite has been found in rats in
A. Chikweto et al. / Veterinary Parasitology 162 (2009) 160–162
Madagascar (1963), Cuba (1973), Egypt (1977), Puerto Rico (1986) and Nigeria (1989) and it is spreading down the east coast of Australia (Prociv and Carlisle, 2001). In the USA the parasite was first reported in New Orleans in Rattus norvegicus (Campbell and Little, 1988) and later A. cantonensis was also found in several wildlife species (Kim et al., 2002) including in a non-human primate in Florida (Duffy et al., 2004). In the West Indies eosinophilic meningitis due to A. cantonensis is an emerging zoonosis and cases in humans have been reported from a number of islands starting in the mid 1980s. Such islands include, Puerto Rico in 1986 (Kliks and Palumbo, 1992), among American tourists returning from Jamaica (Slom et al., 2002; Waugh et al., 2005), in several localities in Cuba (Aguiar et al., 1981; Kliks and Palumbo, 1992) and in a German tourist returning from the Dominican Republic (Rau et al., 2006). Recent reports on detection of A. cantonensis adults and larvae in rodents and snails in the West Indies include from the Dominican Republic (Vargas et al., 1992), Jamaica (Lindo et al., 2002) and Haiti (Raccurt et al., 2003). Levett et al. (2004) found no evidence of A. cantonensis in rats in Barbados, a neighbouring island of Grenada. We report A. cantonensis infection in rats from the Lesser Antilles, the island of Grenada, for the first time. 2. Materials and methods From September 2005 to September 2006, 192 rats (R. norvegicus) comprising 101 females and 91 males were trapped from 6 different parishes including St. George, St. Mark, St. John, St. David, St. Andrew and St. Patrick. The rats were anesthetized with diethyl ether, exsanguinated, necropsied and lesions in lungs and other tissues recorded. Lungs were fixed whole in 10% buffered formalin, trimmed, processed, cut at 3 mm, stained with hematoxylin and eosin and examined microscopically. 3. Results Gross lesions of consolidation with multifocal petechiae and congestion of lungs were noted in 2 rats whereas 7 rats showed mild to moderate degrees of petechiation and congestion. In one rat, submitted dead for necropsy, numerous A. cantonensis adults were observed in the right cardiac ventricle and the pulmonary trunk and its branches. The adults were 21 mm 0.5 mm in size. In addition, a barber-pole appearance was seen in female worms. There was marked biventricular dilatation in this particular rat. In histologic sections of lungs, the adults had polymyarian–coelomyarian musculature, smooth cuticle without ornamentations, accessory hypodermal cords, lateral cords, few multinucleated intestinal cells and paired uterus often containing eggs (Gardiner and Poyton, 1999). There was focal mild to severe diffuse granulomatous pneumonia with intralesional larvae and embryonated eggs in alveoli and cross-sections of adult worms with features described above in pulmonary artery branches, often with thrombosis (Fig. 1). There was widespread infection by A. cantonensis in all the 6 parishes of Grenada (St. George, 4/19; St. Mark, 11/
161
Fig. 1. Lung cross-sections of A. cantonensis in the pulmonary artery branch (PA). A. cantonensis can be characterized by its smooth cuticle, polymyarian–coelomyarian musculature, with lateral cords (LC), accessory hypodermal cords (C), paired uterus (U) containing eggs, ovaries (O) and intestine (I). There is infiltration of inflammatory cells in the adjacent lung parenchyma.
29; St. John, 5/30; St. David, 13/62; St. Andrew, 7/36; St. Patrick, 5/16). Incidental findings of variably sized (2– 7 mm) solitary to multiple cysts containing larvae of Taenia taeniaformis were seen in the livers of 57 rats. There was no association between the presence of hepatic T. taeniaformis cysts with A. cantonensis infestation (p > 0.05, x2). 4. Discussion This is the first report of angiostrongyliasis in rats in Grenada and the first time it has been reported from the Lesser Antilles. It is likely that this parasite was introduced to Grenada by ships infested with rats infected with A. cantonensis. The other possibility could be due to the natural spread of intermediate hosts, the land snails and slugs. Whatever the mode of introduction, the parasite has firmly established itself throughout the island in Norwegian rats (R. norvegicus). In this study all rats caught were R. norvegicus, implying that this species of rat is more predominant in Grenada. Infection rates in other rat species in Grenada is unknown but studies in Puerto Rico (Andersen et al., 1986) and Haiti (Raccurt et al., 2003) demonstrated that R. norvegicus was significantly more infected with A. cantonensis than R. rattus (p < 0.05, x2). In Cuba, infestation rates between R. norvegicus and R. rattus were not significant (p > 0.05, x2) (Aguiar et al., 1981). The other lung parasite of rats to be considered in the differential diagnosis was Angiostrongylus schmidti. This species has been reported to mainly affect rice rats (Oryzomys palustris) in North America (Soulsby, 1982) but was reported in rats in Florida (Kinsella, 1971). We did not find this species in the rats examined in this study. There are several species of aquatic and land snails in Grenada including the giant African land snail, A. fulica, but the local people interviewed during this study said that land snails are not usually consumed. The indigenous diet in Grenada includes the consumption of crabs, aquatic snails and iguanas and these paratenic hosts may provide a risk for the transmission of the parasite to humans. Further
162
A. Chikweto et al. / Veterinary Parasitology 162 (2009) 160–162
studies on infection rates in the intermediate and paratenic hosts in Grenada are indicated. This study which revealed the widespread distribution of the parasite in rats in Grenada also should raise awareness among the local physicians to consider A. cantonensis infection in the differential diagnosis of cases of eosinophilic meningitis. For prevention of human infection in Grenada, rodent control measures and education of the public on the proper preparation of food, particularly snails, crabs and tattoo (iguanas) is recommended. Acknowledgements The authors are indebted to Ray Samuel, Ferron Victor and Sean McCartney for their help with this investigation. This study was supported by a grant from the small research initiative fund, St. George’s University. References Aguiar, P.H., Morera, P., Pascual, J., 1981. First record of Angiostrongylus cantonensis in Cuba. Am. J. Trop. Med. Hyg. 30, 963–965. Andersen, E., Gubler, D.J., Sorensen, K., Beddard, J., Ash, L.R., 1986. First report of Angiostrongylus cantonensis in Puerto Rico. Am. J. Trop. Med. Hyg. 35, 319–322. Campbell, B.G., Little, M.D., 1988. The finding of Angiostrongylus cantonensis in rats in New Orleans. Am. J. Trop. Med. Hyg. 38, 568–573. Duffy, M.S., Miller, C.L., Kinsella, J.M., De Lahunta, A., 2004. Parastrongylus cantonensis in a non-human primate, Florida. Emerg. Infect. Dis. 10 (12), 2207–2210. Gardiner, C.H., Poyton, S.L., 1999. Morphologic characteristics of nematodes in tissue sections. In: An Atlas of Metazoan Parasites in Animal Tissues. Armed forces Institute of Pathology, pp. 2, 3 and 28. Kim, D.Y., Stewart, T.B., Bauer, Mitchelle, M., 2002. Parastrongylus (=Angiostrongylus) cantonensis now endemic in Louisiana Wildlife. J. Parasitol. 88 (5), 1024–1026.
Kliks, M.M., Palumbo, N.E., 1992. Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc. Sci. Med. 34, 199–212. Kinsella, J.M., 1971. Angiostrongylus schmidti sp.n. (Nematoda: Metastrongyloidea) from the rice rat, Oryzomys palustris, in Florida, with a key to the species of Angiostrongylus Kamensky, 1905. J. Parasit. 57, 494–497. Levett, P.N., Douglas, K.A., Waugh, C.A., Robinson, R.D., Lindo, J.F., 2004. Failure to detect Angiostrongylus cantonensis in rats in Barbados. West Indian Med. J. 53, 58. Lindo, J.F., Waugh, C.A., Hall, J., Cunningham-Myrie, C., Ashley, D., Eberhard, M.L., Sullivan, J.J., Bishop, H.S., Robison, D.G., Holtz, T., Robinson, R.D., 2002. Enzootic Angiostrongylus cantonensis in rats and snails after an outbreak of human eosinophilic meningitis, Jamaica. Emerg. Infect. Dis. 8, 324–326. Macpherson, C.N.L., 2005. Human behaviour and the epidemiology of parasitic zoonoses. Int. J. Parasitol. 35, 1319–1331. Prociv, P., Carlisle, M.S., 2001. The spread of Angiostrongylus cantonensis in Australia. Southeast Asian J. Trop. Med. Public Health 32, 126–128. Raccurt, C.P., Blaise, J., Durette-Desset, M., 2003. Presence of Angiostrongylus cantonensis in Haiti. Trop. Med. Int. Health 8, 423–426. Rau, C., Bialek, R., Richter, S., Lindner, A., 2006. Headache after returning from the Dominican Republic. Deut. Med. Wochenschr. 131, 1656– 1659. Slom, T.J., Cortese, M.M., Gerber, S.I., Jones, R.C., Holtz, T.H., Lopez, A.S., Zambrano, C.H., Sufit, R.L., Sakolvaree FY., Chaicumpa, W., Herwaldt, B.L., Johnson, S., 2002. An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. N. Eng. J. Med. 346, 668–675. Soulsby, E.J.L., 1982. Angiostrongylus cantonensis. In: Helminthes, Arthropods and Protozoa of Domestic Animals. Bailliere Tindall Publishers, London, pp. 280–281. Vargas, M., Gomez, P.J.D., Malek, E.A., 1992. First record of Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in the Dominican Republic. Trop. Med. Parasitol. 43, 253– 255. Wang, Q.P., Lai, D.H., Zhu, Q.X., Chen, Q.G., Lun, Z.R., 2008. Human angiostrongyliasis. Lancet Infect. Dis. 8 (10), 621–630. Waugh, C.A., Shafir, S., Wise, M., Robinson, R.D., Eberhard, M.L., Lindo, J.F., 2005. Human Angiostrongylus cantonensis, Jamaica. Emerg. Infect. Dis. 11, 1977–1978.