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Establishment of Biomphalaria tenagophila snails in Europe.

To the Editor: Schistosomiasis schistosomiasis (shĭs`təsōmī`əsĭs), bilharziasis, or snail fever, parasitic disease caused by blood flukes, trematode worms of the genus Schistosoma. , known since ancient times, is caused by blood flukes (Trematoda: Schistosomidae). It is a major communicable disease with public health and socioeconomic effects in the developing world (1). Among parasitic diseases, schistosomiasis ranks second only to malaria with regard to the number of persons infected and at risk. The life cycle of schistosomes is complex, requiring specific freshwater snails as intermediate hosts for larvae development and multiplication. Among Schistosoma species that affect humans, Schistosoma mansoni is the most likely to invade new areas mainly because of the adaptability and invasiveness of its intermediate host, Biomphalaria snails. Natural populations of these snails are usually found in tropical standing water or freshwater in South America and Africa, but they also reach 30[degrees] latitude in subtropical areas (1,2). Many species of these red-blooded planorbid snails (Gastropoda: Basommatophora) are able to survive a long time when removed from their freshwater habitat (1). Of the 34 Biomphalaria species, 4 (B. glabrata, B. pfeifferi, B. straminea, and B. tenagophila) have recently expanded their native ranges (3). They have been introduced to areas where other Biomphalaria species are endemic (e.g., Congo and Egypt) or to subtropical zones that have no frost period (Texas, Louisiana, Florida, Hong Kong) (3,4). None of the known invasions, whether peripheral range expansion or long distance dispersal, reached the temperate zone. Spreading of the blood-fluke snails to schistosome-free areas may enable the parasite to colonize new habitats concurrently, expanding the potential area of clinical schistosomiasis.

We collected these snails in spring 2005, autumn 2006, and autumn 2007, near Rabagani, Romania, Eastern Europe (46[degrees]45'1.3"N, 22[degrees]12'44.8"E) in a hypothermal hy·po·ther·mal  
Of, relating to, or being mineral deposits formed at great depths and high temperatures.
 spring. Water temperature was 25[degrees]C in the spring and 16[degrees]C-25[degrees]C, gradually decreasing, along the brook course. In and beside an abandoned concrete pool next to the spring, we collected 100 shells and 34 living specimens that macroscopically resembled Biomphalaria spp. snails. All 16 dissected animals proved to be fully developed adults, according to the maturity of their genital organs (Figure). Using available identification keys (5), we tentatively identified these snails as B. tenagophila. Voucher specimens have been deposited in the Hungarian Natural History Museum The Hungarian Natural History Museum houses the largest natural history collections of Hungary and the region. The History of the Museum
In 1802, Count Ferenc Széchényi offered his library and his numismatical collection for the benefit of the
 (accession nos. HNHM96857 and HNHM95433).

DNA DNA: see nucleic acid.
 or deoxyribonucleic acid

One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes.
 was extracted from the foot muscles of 3 specimens by using QIAamp DNA Mini Kit (QIAGEN, Hilden, Germany). For amplification of the partial mitochondrial mitochondrial

pertaining to mitochondria.

mitochondrial RNAs
a unique set of tRNAs, mRNAs, rRNAs, transcribed from mitochondrial DNA by a mitochondrial-specific RNA polymerase, that account for about 4% of the total cell RNA that
 16S ribosomal RNA gone, we used a PCR PCR polymerase chain reaction.

polymerase chain reaction

Polymerase chain reaction (PCR) 
 with primers 16Sar and 16Sbr (6). Nucleotide sequences were determined in both directions. PCR products of [approximately equal to]430 bp were detected from all 3 samples. Automatic cycle sequencing of the randomly selected amplicon (GenBank accession no. EU069412) showed 99.74% similarity to B. tenagophila (AF449615, Brazil).

Our morphologic, anatomic, and molecular data unambiguously prove the occurrence of B. tenagophila snails in Romania. B. tenagophila snails had been found earlier (in 2004) at this location but had presumably pre·sum·a·ble  
That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster.
 been misidentified as dwarf specimens of a common European species, Planorbarius corneus (7). Consequently, B. tenagophila snails have been not only introduced, but also established in Rabagani, representing the furthest self-sustaining population of this species from the equator.

B. tenagophila is a new species for the European fauna. It could represent a founder population of unknown origin for further spread into Europe, which might easily be accomplished by migrating birds or more likely by plants used in aquariums (3). Although no trematode trematode: see fluke; Platyhelminthes.  larvae were detected in the observed specimens, clinical schistosomiasis can be imported by immigrants or tourists into Europe, as has been reported in Romania and neighboring Hungary (8,9). If eggs were released in feces of humans infected with the blood flukes, they could hatch in the environment and the larvae could develop to an infective stage in these snails. The observed local cultural and social factors involving natural water (washing clothes, bathing) in Rabagani where B. tenagophila have been found may also increase the chance of human infection.

[FIGURE A-B A-B Air-Britain (UK-based aviation historical society)
A-B Research Centre Applied Biocatalysis (Graz, Austria) 

We believe that B. tenagophila in Europe, together with the global climate change and a possible encounter of these snails with schistosomes, could pose a public health risk. Measures must be taken to prevent the spread of this species into European freshwater. Chemical control is not possible in Rabagani because it is an area where other rare and endangered snail species are protected (7). Therefore, the manual collection and removal of all the B. tenagophila specimens in the area seems to be the only possibility for eradication, which might remain in effect for years. To avoid similar establishments, we suggest regular malacologic and parasitologic surveillance of at least the thermal and hypothermal water bodies for these tropical invaders around European settlements.


We thank W.M. Lofty, V. Estrada, R.L. Caldeira, and M.J. Kenny for their comments.

This work was partly supported by the Hungarian National R&D Program, "The origin and genesis of the fauna of the Carpathian Basin: diversity, biogeographical bi·o·ge·og·ra·phy  
The study of the geographic distribution of organisms.

 hotspots and nature conservation significance; contract no. 3B023-04."

Gabor Majoros, [1] Zoltan Feher, Tamas Deli, and Gabor Foldvari [1]

Author affiliations: Szent Istvan University Faculty of Veterinary Science, Budapest, Hungary (G. Majoros, G. Foldvari); Hungarian Natural History Museum, Budapest (Z. Feher); and Munkacsy Mihaly Museum, Bekescsaba, Hungary (T. Dell)

DOI (Digital Object Identifier) A method of applying a persistent name to documents, publications and other resources on the Internet rather than using a URL, which can change over time. : 10.3201/eid 1411.080479

[1] These authors contributed equally to this article.


(1.) Malek EA. Snail-transmitted parasitic diseases, vol.1. Boca Raton (FL): CRC (Cyclical Redundancy Checking) An error checking technique used to ensure the accuracy of transmitting digital data. The transmitted messages are divided into predetermined lengths which, used as dividends, are divided by a fixed divisor.  Press, Inc.; 1980.

(2.) Paraense WL. The schistosome schistosome /schis·to·some/ (shis´-) (skis´to-som) an individual of the genus Schistosoma.

 vectors in the Americas. Mem Inst Oswaldo Cruz. 2001;96(Suppl):7-16. DOI: 10.1590/ S0074-02762001000900002

(3.) Pointier JP, David P, Jarne E Biological invasions: the case of planorbid snails. J Helminthol. 2005;79:249-56. DOI: 10.1079/JOH2005292

(4.) Malek EA. Studies on "tropicorbid" snails (Biomphalaria: Planorbidae) from the Caribbean and Gulf of Mexico Noun 1. Gulf of Mexico - an arm of the Atlantic to the south of the United States and to the east of Mexico
Golfo de Mexico

Atlantic, Atlantic Ocean - the 2nd largest ocean; separates North and South America on the west from Europe and Africa on the east
 areas, including the Southern United States The Southern United States—commonly referred to as the American South, Dixie, or simply the South—constitutes a large distinctive region in the southeastern and south-central United States. . Malacologia. 1969;7:183-209.

(5.) Malek EA. Snail hosts of schistosomiasis and other snail-transmitted diseases in tropical America: a manual. Scientific publication 478. Washington: Pan American Health Organization The Pan American Health Organization (PAHO) is an international public health agency with 100 years of experience in working to improve health and living standards of the countries of the Americas. It serves as the specialized organization for health of the Inter-American System. ; 1985.

(6.) DeJong R J, Morgan JA, Wilson WD, Al-Jaser MH, Appleton CC, Coulibaly G, et al. Phylogeography of Biomphalaria glabrata and B. pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics. Mol Ecol. 2003;12:3041-56. DOI: 10.1046/j.1365-294X.2003.01977.x

(7.) Gagiu A. On the extinction of the relict RELICT. A widow; as A B, relict of C D.  snail Theodoxus prevostianus Pfeiffer 1828 in Rabagani, Romania. Nymphaea. 2004;31:75-81.

(8.) Dancescu P, Colea A, Gafiteanu L, Sima A. Imported tropical parasitosis par·a·si·to·sis
n. pl. par·a·si·to·ses
Infestation with parasites.


a disease caused by a parasitic infestation. See also helminthiasis.
 in Rumania [in French]. Bull Soc Pathol Exot Filiales. 1976;69:501-7.

(9.) Dobi S, Santha M, Horvath A, Kassas AL, Varnai F. Introduced schistosomiasis with late complications [in Hungarian]. Orv Hetil. 1995;136:1673-5.

Address for correspondence: Gabor Foldvari, Department of Parasitology Parasitology

The scientific study of parasites and of parasitism. Parasitism is a subdivision of symbiosis and is defined as an intimate association between an organism (parasite) and another, larger species of organism (host) upon which the parasite is
 and Zoology, Faculty of Veterinary Science, Szent Istvan University, 2nd Istvan St, Budapest H-1078, Hungary; email:
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Title Annotation:LETTERS
Author:Majoros, Gabor; Feher, Zoltan; Deli, Tamas; Foldvari, Gabor
Publication:Emerging Infectious Diseases
Geographic Code:4EXHU
Date:Nov 1, 2008
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