SciELO - Scientific Electronic Library Online

vol.59Phenotypic and genotypic detection of Candida albicans and Candida dubliniensis strains isolated from oral mucosa of AIDS pediatric patientsShort and long term evaluation of the efficiency of PermaNet® 2.0 bed net against environmental factors and washing using bioassay tests author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand




Related links


Revista do Instituto de Medicina Tropical de São Paulo

On-line version ISSN 1678-9946

Rev. Inst. Med. trop. S. Paulo vol.59  São Paulo  2017  Epub Apr 13, 2017 


Scientometrics of zoonoses transmitted by the giant African snail Achatina fulica Bowdich, 1822

Gilberto Cezar Pavanelli 1   2  

Mirian Ueda Yamaguchi 1   2  

Elaine Alves Calaça 2  

Fabrício Hiroiuki Oda 2  

1 Instituto Cesumar de Ciência, Tecnologia e Inovação - ICETI, Maringá, Paraná, Brazil.

2 Centro Universitário Maringá - UniCesumar, Maringá, Paraná, Brazil.


The dissemination of the giant African snail Achatina fulica in several countries has triggered a great number of studies on the mollusk, including those on zoonoses related to health in humans. The current research is a scientific survey on articles published in four databases, namely, PubMed, Bireme, Scielo and Lilacs. Results indicate that Brazil has a prominent position in international scientific production on this subject, with focus on Angiostrongylus cantonensis occurrences.

KEYWORDS: Health promotion; Public health; Epidemiology; Angiostrongylus infection


The rapid spread of the giant African snail Achatina fulica Bowdich, from 1822 worldwide has caused a great concern not merely due to environmental aspects but particularly to the dissemination of diseases in humans. Achatina fulica, one of the hundred most harmful invading species on the planet1, native to East Africa, is known to have a highly predatory food and reproduction habits and have contributed to the extinction of native fauna and the decrease in biodiversity. The mollusk may cause heavy economical liabilities due to its proliferation in cash crops, gardens and kitchen gardens2.

The giant African snail was illegally introduced in Brazil during an agricultural and cattle-breeding fair that took place in the municipality of Curitiba, Paraná State, Brazil, between 1988 and 1989, as a commercial alternative to the mollusk Helix aspersa Müller, described in 1774 and used in French cuisine in the preparation of escargot dishes. A second introduction of the African snail may have occurred in the Goiás State, in 1996, for the same reason. The commercial bankruptcy of breeders caused its inadequate release in the environment and, consequently, its dissemination to other Brazilian States2-5.

Due to its feed and reproduction habits, A. fulica finds an ideal habitat for its deployment and dissemination in environments modified by human activities. In fact, the giant African snail is abundant in areas featuring high population density2,6. In addition, it should be underscored that the mollusk is a threat to public health since it harbors parasite vectors such as the nematodes Angiostrongylus cantonensis (Chen, 1935) which is the etiological agent of eosinophilic meningitis, and A. costaricensis (Morera & Céspedes, 1971) which causes abdominal angiostrongyliasis2,5,7.

Adult worms live inside the pulmonary arteries of certain rodent species such as Rattus norvegicus (Berkenhout, 1769), R. rattus (Linnaeus, 1758) and R. exulans (Peale, 1848)8-10. Several species of mollusks have been reported as intermediate hosts in the biological cycle of A. cantonensis3,5,11, Bradybaena similaris (Férussac, 1821), Pomacea lineata (Spix, 1827), Sarasinula linguaeformis (Semper, 1885), Sarasinula marginata (Semper, 1885), Subulina octona (Bruguière, 1792), Parmarion martensi Simroth, 1893, Laevicaulis alte (Férussac, 1822), Limax maximus Linnaeus, 1758, Euglandina rosea (Férussac 1821), Oxychilus alliarius (Miller, 1822) and A. fulica12.

The mollusks which are intermediate hosts of A. costaricensis include Veronicellidae slugs5,8, mainly Phyllocaulis variegates (Semper, 1885), Sarasinula plebeius (Fischer, 1868), and S. linguaeformis. Birds and mammals (including humans) are accidental hosts11 and acquire infection by the consumption of intermediate hosts (e.g. snails and slugs) or paratenic hosts (e.g. fishes, frogs, lizards and some crustaceans) infected with third stage larvae8,13. Although abdominal angiostrongyliasis is a parasitic infection, frequently asymptomatic or presenting very mild symptoms, severe forms of the disease involve intense abdominal pain which may cause lesions in the liver and intestinal perforations, requiring immediate surgery13-15. No reports on A. fulica naturally infected by A. costaricensis exist in the Americas, but its susceptibility was experimentally proven. Cases of human infections by the nematode occur from the United States of America (USA) to the North of Argentina and in the Brazilian States of Rio Grande do Sul, Santa Catarina, Paraná, São Paulo, Minas Gerais, Espírito Santo and the Distrito Federal3,12.

Eosinophilic meningitis is a clinical condition characterized by an inflammatory response after the A. cantonensis larvae have reached the central nervous system, and the harboring in the meninges may cause nausea and headache, and in more severe cases, neurologic dysfunction, coma, and death11,13,15. The A. cantonensis larvae can also reach the ocular globes, causing a condition called ocular angiostrongyliasis16.

Although the parasite was originally described in China in the 1960s13, A. cantonensis has been reported in several regions such as the Pacific islands (Hawaii, Tahiti and Celebes), Southeastern Asia (Vietnam, Thailand, Sumatra, Malaysia, Indonesia, Taiwan and the Philippines), India, Australia, Japan and Madagascar, and American countries such as Cuba, Jamaica, Ecuador, the USA, Haiti and Brazil3,7,13. Rodents and mollusks infected by the parasite, including A. fulica, have been detected in the Brazilian States of Amazonas, Bahia, Ceará, Espírito Santo, Pará, Paraná, Pernambuco, Rio de Janeiro, Santa Catarina, São Paulo and the Distrito Federal11. Several cases of infected people have been reported lately, especially in China, Taiwan and the USA17.

Three cases involving eosinophilic meningitis occurred in the Espírito Santo State, Brazil: two cases in the municipality of Cariacica, and a third case in the municipality of Vila Velha, in 2007. These were the first records of the disease in Brazil7, even though there was a suspect case in Rio de Janeiro, in 2006. A fatal case involving a 26-year-old woman was reported in the municipality of Olinda, Pernambuco State, Brazil, in 200913. Dozens of others suspect and confirmed cases have been reported in several Brazilian towns13.

However, the above number may have been underestimated due to a deficient knowledge on the epidemiological aspects of the parasites transmitted by the giant African snail and their occurrence in Brazil. One must underscore that the continuous dissemination of the mollusk throughout Brazil, especially in urban areas in which it has great adaptability and dispersion, is a considerable risk for the increase of clinical cases of the disease6,13.

Scientometric studies constitute a reliable method since they serve a double purpose: they provide indexes on the degree of development within a branch of knowledge and disseminate research work undertaken. These studies have foregrounded quantitative and qualitative analyses in scientific production, especially in the health field18,19.

Through scientometric studies, current analysis contributes towards a survey of Brazilian and international scientific publications on the giant African snail and the diseases transmitted by the mollusk, so that studies can be undertaken focusing relevant or still neglected aspects. Current research may also foreground the elaboration of public policies for the prevention, identification and treatment of the concerned zoonoses.


Scientometrics have foregrounded current methodology for the planning, collection and analysis of data. Articles related to the giant African snail and to human diseases were accessed through Brazilian and international databases, and classified according to the publication date, title of the electronic journal, qualification on the WebQualis, study site and main aim.

The consulted databases comprised the United States National Library of Medicine (PubMed) available at; the Scientific Eletronic Library Online (Scielo), available at, the Latin American and Caribbean Literature in Health Sciences (Lilacs), available at Latin-American and Caribbean Information Center in Health Sciences, available at The research was undertaken in June 2016, with no restrictions with regard to the publication period. The main search term was the snail scientific name, Achatina fulica, and its variation, Lissachatina fulica. Portuguese terms such as "Caramujo africano" and "Caramujo gigante africano", as well as some terms in English "giant African snail" and "African snail" were used, but as a support, only. However, no results were obtained for this secondary denomination.

Dual articles were excluded, and the analysis of titles and abstracts did not relate snails to any human zoonosis involving human health.

The classification of articles according to the qualification extracts of the Qualis system (A1, A2, B1, B2, B3, B4, B5 and C) used preferentially the interdisciplinary evaluation area. Journals without an evaluation area were qualified according to the main aim, provided in the abstract and the available assessment areas. Information on the country and city/ town in which the sample collection or study area occurred (indicated in the titles and abstracts) was considered. In exceptional cases in which the title or abstract failed to give information, the place of publication based on the corresponding author's address were considered. Classification by the main aim was foregrounded on the nematodes Angiostrongylus cantonesis and A. costaricensis, or both, and these data were subjected to current analysis.


Research in the initial phase identified 1,933 articles. However, the terms "Caramujo africano", "Caramujo gigante africano", "African snail" and "giant African snail" were not taken into account to perform the analysis and discussion since they merely provided already indexed results for the terms "Achatina fulica" and "Lissachatina fulica".

Only 62 out of the 760 articles initially obtained from the terms above complied according to the inclusion criterion of the research, or rather, they related the African snail to the transmission of abdominal angiostrongyliasis and eosinophilic meningitis. In fact, approximately 8% of the studies retrieved from the four databases were thereafter assessed.

Table 1 displays the number of articles on each term at the four databases, Scielo, PubMed, Bireme and Lilacs, and the number of articles of interest after the exclusion.

Table 1 Total number of articles (N) per term, according to the database, and the number of remaining articles (n) after the exclusion analysis criterion. Abbreviation: Port = Portuguese, Eng = English 

Search terms/ Databases Achatina fulica Lissachatina fulica Caramujo africano (Port) Caramujo gigante africano (Port) African Snail (Eng) Giant African Snail (Eng) After exclusion
N (n) N (n) N (n) N (n) N (n) N (n) N (n)
Scielo 10 (3) 0 (0) 3 (0) 4 (0) 2 (0) 8 (0) 27 (3)
PubMed 389 (56) 5 (0) 0 (0) 0 (0) 392 (0) 189 (0) 975 (56)
Bireme 318 (2) 3 (1) 55 (0) 7 (0) 289 (0) 187 (0) 859 (3)
Lilacs 35 (0) 0 (0) 10 (0) 5 (0) 14 (0) 8 (0) 72 (0)
Total 752 (61) 8 (1) 68 (0) 16 (0) 697 (0) 392 (0) 1,933 (62)

PubMed was the major database with the greatest number of publications, totaling 394 articles and 56 remaining articles after the application of the exclusion criteria. Bireme ranked second with 321 publications. However, only three articles complied with the inclusion criteria. Scielo database provided 10 initial articles and 3 remaining ones after exclusion. All articles on the Lilacs database were excluded due to duality.

Although the first article associating the giant African snail with human diseases was published in 1966, the theme was underscored only in the 2010s, concentrating 35% of all the articles published. The most significant year was 2012 with seven publications, mostly reported by Chinese researchers (Figure 1). On the other hand, Brazilian publications started to be relevant from 2000, as only one article was published by Brazilians between 1997 and 2000.

Figure 1 Number of article published per period. 

Brazil ranks second due to the great number of scientific publications on diseases transmitted by the giant African snail, or rather, approximately 20% of the world publications. Only China exceeds this percentage, corresponding to 34% of the studies worldwide.

Among studies on the subject written in Chinese, four were published in Taiwan. In the case of the USA, several articles deal with the giant African snail in Hawaii, the archipelago State belonging to the USA, through which the mollusk was introduced in 19393.

Publications listed under French territories refer to studies undertaken in La Reunion, Mayote, French Guiana and French Polynesia, all of them, ultramarine departments of France, respectively in the Indian Ocean, South America and Pacific Ocean (Figure 2).

Figure 2 Number of articles according to the countries where studies were undertaken. 

Rio de Janeiro, Brazil, is the Brazilian State featuring the greatest number of studies on the theme. The study on the African snail in Espírito Santo State refers to the first report of snails naturally infected by A. cantonensis in Brazil (Figure 3)7.

Figure 3 Number of Brazilian articles according to the state in which studies were undertaken. RJ = Rio de Janeiro; BA = Bahia; ES = Espírito Santo; PA = Pará; PE = Pernambuco; RS = Rio Grande do Sul; SC = Santa Catarina; SP = São Paulo.  

The analysis on the articles main aim clearly revealed a predominance of studies on A. cantonensis, the etiological agent of eosinophilic meningitis, with slightly more than 1% for studies on A. costaricensis.

Quality assessment of journals according to the category of journals according to the Qualis system revealed that most articles do not belong to journals listed on the WebQualis system. The Southeast Asian Journal of Tropical Medicine and Public Health alone concentrated 15% of publications, although not ranked by the system.

Other articles were published in journals ranked A1, A2, B1 and B2, with a predominance of the A2, with 40% of publications in this category (Figure 4).

Figure 4 Number of articles according to category assessment of the Qualis/Capes system. *N/C = journals with no classification by the Qualis/Capes system. 


Scientometric results on the giant African snail and zoonoses linked to the mollusk show that Brazil has a significant role on the subject, due to its second place with the greatest concentration of electronic articles on the theme. Moreover, the only articles on A. fulica by A. costaricensis have been published by Brazilian researchers, even though most articles published in the country deal with A.cantonensis5,12.

Rio de Janeiro State has sponsored the greatest number of research works on the subject. Although snails infected by A. cantonensis have been reported in the municipality of São Gonçalo20, one should bear in mind that the main health research center, the Oswaldo Cruz Foundation (Fiocruz) in the country is located in this federal State.

As a rule, study sites coincide with the geographic regions in which cases of eosinophilic meningitis or of snails infected by A. cantonensis have been reported during the last decades, such as Southeastern Asia, islands in the Pacific Ocean, countries on the American continent, Australia and Japan3,13.

The first scientific article on the role of the giant African snail (A. fulica) in the transmission of zoonoses was published in 196621, even though most articles on the subject were published only after 2000, particularly in the 2010s.

Analysis on the main aims revealed the great interest of scientists for occurrences related to A. cantonensis, to the detriment of A. costaricensis, perhaps due to mild symptoms of abdominal angiostrongyliasis and to the low susceptibility of A. fulica to infection by the nematode, since other invertebrates, mainly Veronicellidae slugs, participate in its cycle as main intermediate hosts12.

According to Qualis/CAPES stratifications, the quality of publications turns out to be partially inconclusive since most publications occurred in journals not listed on the WebQualis system. On the other hand, articles published in journals evaluated by the Qualis system proved to be of considerably high quality.


The authors would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Instituto Cesumar de Ciência, Tecnologia e Inovação (ICETI) for the scholarship and funding of the current research. FHO received a postdoctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).


1. Fisher ML, Simião M, Colley E, Zenni RD, Silva DAT, Latoski N. O caramujo exótico invasor na vegetação nativa em Morretes, PR: diagnóstico da população de Achatina fulica Bowdich, 1822 em um fragmento de Floresta Ombrófila Densa aluvial. Biota Neotrop. 2006;6:1-5. [ Links ]

2. Ohlweiler FP, Guimarães MCA, Takahashi FY, Eduardo JM. Current distribution of Achatina fulica, in the State of São Paulo including records of Aelurostrongylus abstrusus (Nematoda) larvae infestation. Rev Inst Med Trop Sao Paulo. 2010;52:211-4. [ Links ]

3. Teles HMS, Vaz JF, Fontes LR, Domingos MF. Registro de Achatina fulica Bowdich, 1822 (Mollusca, Gastropoda) no Brasil: caramujo hospedeiro intermediário da angiostrongilíase. Rev Saúde Pública. 1997;31:310-12. [ Links ]

4. Coelho LM. Informe técnico para o controle do caramujo africano (Achatina fulica, Bowdch 1822) em Goiás. Goiânia: Agência Rural; 2005. [ Links ]

5. Neuhauss E, Fitarelli M, Romanzini J, Graeff-Teixeira C. Low susceptibility of Achatina fulica from Brazil to infection with Angiostrongylus costaricensis and A. cantonensis. Mem Inst Oswaldo Cruz. 2007;102:49-52. [ Links ]

6. Albuquerque FS, Peso-Aguiar MC, Assunção-Albuquerque MJT. Distribution, feeding behavior and control strategies of the exotic land snail Achatina fulica (Gastropoda: Pulmonata) in the northeast of Brazil. Braz J Biol. 2008;68:837-42. [ Links ]

7. Caldeira RL, Mendonça CLGF, Gouveia CO,Lenzi HL, Graeff-Teixeira C, Lima WS. First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Mem Inst Oswaldo Cruz. 2007;102:887-9. [ Links ]

8. Kim JR, Hayes KA, Yeung NW, Cowie RH. Definitive, intermediate, paratenic, and accidental hosts of Angiostrongylus cantonensis and its molluscan intermediate hosts in Hawaii. Hawaii J Med Public Health. 2013;72(6 suppl 2):10. [ Links ]

9. Carney WP, Stafford EE, Purnomo, Tanudjaja S. Angiostrongyliasis in Indonesia: additional geographic and host occurrence records. Southeast Asian J Trop Med Public Health. 1978;9:516-9. [ Links ]

10. Uchikawa R, Takagi M, Matayoshi S, Sato A. The presence of Angiostrongylus cantonensis in Viti Levu, Fiji. J Helminthol. 1984;58:231-4. [ Links ]

11. Kim JR, Hayes KA, Yeung NW, Cowie RH. Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS ONE. 2014;9:e94969. [ Links ]

12. Carvalho OS, Teles HMS, Mota EM, Mendonça CLGF, Lenzi HL. Potentiality of Achatina fulica Bowdich, 1822 (Mollusca: Gastropoda) as intermediate host of the Angiostrongylus costaricensis. Rev Soc Bras Med Trop. 2003;36:743-5. [ Links ]

13. Morassutti AL, Thiengo SC, Fernandez M, Sawanyawisuth K, Graeff-Teixeira C. Eosinophilic meningitis caused by Angiostrongylus cantonensis: an emergent disease in Brazil. Mem Inst Oswaldo Cruz. 2014;109:399-407. [ Links ]

14. Rodriguez R, Dequi RM, Peruzzo L, Mesquita PM, Garcia E, Fornari F. Abdominal angiostrongyliasis: report of two cases with different clinical presentations. Rev Inst Med Trop Sao Paulo. 2008;50:339-41. [ Links ]

15. Graeff-Teixeira C, Silva ACA, Yoshimura K. Update on eosinophilic meningoencephalitis and its clinical relevance. Clin Microbiol Rev. 2009;22:322-48. [ Links ]

16. Thu TP, Nguyen NX, Lan le T, Küchle M. Ocular Angiostrongylus cantonensis in a female Vietnamese patient: case report. Klin Monbl Augenheilkd. 2002;219:892-5. [ Links ]

17. Wang QP, Lai DH, Zhu XQ, Chen XG, Lun ZR. Human angiostrongyliasis. Lancet Infect Dis. 2008;8:621-30. [ Links ]

18. Martins MFM. Análise bibliométrica de artigos científicos sobre o vírus Zika. Rev Eletron Comun Inf Inov Saúde. 2016;10:1-9. [ Links ]

19. Yamaguchi MU, Bernucci, MP, Pavanelli GC. Scientific research about the Nacional Policy for Health Promotion. Cien Saúde Colet. 2016;21:1727-36. [ Links ]

20. Oliveira AP, Gentile R, Maldonado Júnior A, Lopes-Torres EJ, Thiengo SC. Angiostrongylus cantonensis infection in molluscs in the municipality of São Gonçalo, a metropolitan area of Rio de Janeiro, Brazil: role of the invasive species Achatina fulica in parasite transmission dynamics. Mem Inst Oswaldo Cruz. 2015;110:739-44. [ Links ]

21. Alicata JE. The presence of Angiostrongylus cantonensis in islands of the Indian Ocean and probable role of the giant African snail, Achatina fulica, in dispersal of the parasite to the Pacific Islands. Can J Zool. 1966;44:1041-9. [ Links ]

Received: August 01, 2016; Accepted: February 13, 2017

Correspondence to: Gilberto Cezar Pavanelli. Centro Universitário Maringá - UniCesumar, Programa de Pós-Graduação em Promoção da Saúde, Av. Guedner, 1610, Bloco 07, sala 11, CEP 87050-390, Maringá, PR, Brazil. Tel: +55 44 3027-6360 E-mail:

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License