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Parasitology Research

, Volume 93, Issue 5, pp 385–391 | Cite as

Human waterborne parasites in zebra mussels (Dreissena polymorpha) from the Shannon River drainage area, Ireland

  • Thaddeus K. GraczykEmail author
  • David Bruce Conn
  • Frances Lucy
  • Dan Minchin
  • Leena Tamang
  • Lacy N. S. Moura
  • Alexandre J. DaSilva
Original Paper

Abstract

Zebra mussels (Dreissena polymorpha) from throughout the Shannon River drainage area in Ireland were tested for the anthropozoonotic waterborne parasites Cryptosporidium parvum, Giardia lamblia, Encephalitozoon intestinalis, E. hellem, and Enterocytozoon bieneusi, by the multiplexed combined direct immunofluorescent antibody and fluorescent in situ hybridization method, and PCR. Parasite transmission stages were found at 75% of sites, with the highest mean concentration of 16, nine, and eight C. parvum oocysts, G. lamblia cysts, and Encephalitozoon intestinalis spores/mussel, respectively. On average eight Enterocytozoon bieneusi spores/mussel were recovered at any selected site. Approximately 80% of all parasites were viable and thus capable of initiating human infection. The Shannon River is polluted with serious emerging human waterborne pathogens including C. parvum, against which no therapy exists. Zebra mussels can recover and concentrate environmentally derived pathogens and can be used for the sanitary assessment of water quality.

Keywords

Zebra Mussel Blue Mussel Sterile Phosphate Buffer Saline Dreissena Polymorpha Transmission Stage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The study was supported by the U.S. Environmental Protection Agency, Washington, DC (grant no. R824995), The Center for A Livable Future, Baltimore, MD (grant no. H040-951-0180), the Polish Committee for Scientific Research (grant no. 604C02421), and a NATO Collaborative Linkage Grant, CLG 979765.

References

  1. Avery SW, Undeen AH (1987) The isolation of microsporidia and other pathogens from concentrated ditch water. J Am Mosq Control Assoc 3:54–58PubMedGoogle Scholar
  2. Blackburn BL, Soave R (1997) Prophylaxis and chemotherapy: human and animal. In: Fayer R (ed) Cryptosporidium and cryptosporidiosis. CRC, Boca Raton, pp 111-128Google Scholar
  3. Bornay-Llinares FJ, DaSilva AJ, Moura H, Schwartz DA, Visvesvara GS, Pieniazek NJ, Cruz-Lopez A, Hernandez-Jauregui P, Guerrero J, Enriquez FJ (1998) Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J Infect Dis 178:820–826PubMedGoogle Scholar
  4. Breitenmoser AC, Mathis A, Burgi E, Weber R, Deplazes P (1999) High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology 118:447–453Google Scholar
  5. Brieger G, Hunter RD (1993) Uptake and depuration of PCB 77, PCB 169, and hexachlorobenzene by zebra mussels (Dreissena polymorpha). Ecotoxicol Environ Safety 26:153—165CrossRefPubMedGoogle Scholar
  6. Bryan RT, Schwartz DA (1999) Epidemiology of microsporidiosis. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. ASM, Washington, DC, pp 502–516Google Scholar
  7. Buckholt MA, Lee JH, Tzipori S (2002) Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol 68:2595–2599Google Scholar
  8. Chalmers RM, Sturdee AP, Mellors P, Nicholson V, Lawlor F, Kenny F, Timpson P (1997) Cryptosporidium parvum in environmental samples in the Sligo area, Republic of Ireland: a preliminary report. Lett Appl Microbiol 25:380-384PubMedGoogle Scholar
  9. Cotte L, Rabodonirina M, Chapuis F, Bailly F, Bissuel F, Raynal C, Gelas P, Persat F, Piens MA, Trepo C (1999) Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection. J Infect Dis 180:2003–2008PubMedGoogle Scholar
  10. DaSilva AJ, Schwartz DA, Visvesvara GS, Moura H, Slemenda SB, Pieniazek NJ (1996) Sensitive PCR diagnosis of infections by Enterocytozoon bieneusi (Microsporidia) using primers based on the region coding for small-subunit rRNA. J Clin Microbiol 34:986–987PubMedGoogle Scholar
  11. DaSilva AJ, Slemenda SB, Visvesvara GS, Schwartz DA, Wilcox CM, Wallace S, Pieniazek NJ (1997) Detection of Septata intestinalis (Microsporidia) Cali et al. 1993 using polymerase chain reaction primers targeting the small subunit ribosomal RNA coding region. Mol Diagn 2:47–52PubMedGoogle Scholar
  12. DaSilva AJ, Bornay-Llinares FJ, Moura LNS, Slemenda SB, Tuttle JL Pieniazek (1999) Fast and reliable extraction of protozoan parasite DNA from fecal specimens. Mol Diagn 4:57–64PubMedGoogle Scholar
  13. De Groote MA, Visvesvara GS, Wilson ML (1995) Polymerase chain reaction and culture confirmation of disseminated Encephalitozoon cuniculi in patient with AIDS: successful therapy with albendazole. J Infect Dis 171:1375–1378PubMedGoogle Scholar
  14. De Lafontaine Y, Gange F, Blaise C, Costan G, Gangon, Chan HM (1999) Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St. Lawrence River (Canada). Aquat Toxicol 50:51–57Google Scholar
  15. Deplazes P, Mathis A, Muller C, Weber R (1996) Molecular epidemiology of Encephalitozoon cuniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J Eukaryot Microbiol 43:93SPubMedGoogle Scholar
  16. Deplazes P, Mathis A, Weber R (2000) Epidemiology and zoonotic aspects of microsporidia of mammals and birds. In: Petry F (ed) Cryptosporidiosis and microsporidiosis. Karger, New York, pp 236–260Google Scholar
  17. Dorsch MR, Veal DA (2001) Oligonucleotide probes for specific detection of Giardia lamblia cysts by fluorescent in situ hybridization. J Appl Microbiol 90:836–842CrossRefPubMedGoogle Scholar
  18. Dowd SE, Gerba CP, Pepper IL (1998) Confirmation of the human-pathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma cornea in water. Appl Environ Microbiol 64:3332–3335PubMedGoogle Scholar
  19. Fournier S, Liguory O, Santillana-Hayat M, Guillot E, Sarfati C, Dumoutier N, Molina J, Derouin F (2000) Detection of microsporidia in surface water: a one-year follow-up study. FEMS Immunol Med Microbiol 29:95–100CrossRefPubMedGoogle Scholar
  20. Frischer ME, Nierzwicki-Bauer SA, Resto M, Toro A, Toranzos GA (1999) Zebra mussels as possible biomonitors/filters of the protozoan pathogen Cryptosporidium. Dreissena Natl Aquat Nuisance Species Clearinghouse 10:1–4Google Scholar
  21. Glaberman S, Moore JE, Lowery CJ, Chalmers RM, Sulaiman I, Elwin K, Rooney PJ, Millar BC, Dooley JS, Lal AA, Xiao L (2002) Three drinking-water-associated cryptosporidiosis outbreaks, Northern Ireland. Emerg Infect Dis 8:631–633PubMedGoogle Scholar
  22. Graczyk TK (2003a) Human protozoan parasites in molluscan shellfish: epidemiology and detection. In: Villalba A, Requere B, Romalde JL, Beiras R (eds) Molluscan shellfish safety. Conselleria de Pesca e Asuntos Maritimos, Hunta de Galicia, pp 397–405Google Scholar
  23. Graczyk TK (2003b) Human protozoan parasites in molluscan shellfish. J Parasitol 89:S57-S61Google Scholar
  24. Graczyk TK, Fayer R, Cranfield MR (1997) Zoonotic potential of Cryptosporidium parvum: implications for waterborne cryptosporidiosis. Parasitol Today 13:348-351CrossRefGoogle Scholar
  25. Graczyk TK, Fayer R, Lewis EJ, Trout JM, Farley CA (1999) Cryptosporidium oocysts in Bent mussels (Ischadium recurvum) in the Chesapeake Bay. Parasitol Res 85:518-521PubMedGoogle Scholar
  26. Graczyk TK, Marcogliese DJ, De Lafontaine Y, DaSilva AJ, Mhangami-Ruwende B, Pieniazek NJ (2001) Cryptosporidium parvum oocysts in zebra mussels (Dreissena polymorpha): evidence from the St. Lawrence River. Parasitol Res 87:231–234PubMedGoogle Scholar
  27. Graczyk TK, Bosco-Nizeyi J, DaSilva AJ, Moura INS, Pieniazek NJ, Cranfield MR, Lindquist HD (2002) A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitol Res 88:926–931CrossRefPubMedGoogle Scholar
  28. Graczyk TK, Grimes BH, Knight R, DaSilva AJ, Pieniazek NJ, Veal DA (2003a) Detection of Cryptosporidium parvum and Giardia lamblia carried by synanthropic flies by combined fluorescent in situ hybridization and monoclonal antibody. Am J Trop Med Hyg 68:228–232PubMedGoogle Scholar
  29. Graczyk TK, Conn DB, Marcogliese DJ, Graczyk H, De Lafontaine Y (2003b) Accumulation of human waterborne parasites by zebra mussels (Dreissena polymorpha) and Asian freshwater clams (Corbicula fluminea). Parasitol Res 89:107–112CrossRefPubMedGoogle Scholar
  30. Hester FD, Linquist HDA, Bobst AM, Schaffer FW (2000) Fluorescent in situ detection of Encephalitozoon hellem spores with a 6-carboxyfluorescein-labeled ribosomal RNA-targeted oligonucleotide probe. J Eukaryot Microbiol 47:299–308PubMedGoogle Scholar
  31. Horgan MJ, Mills EL (1999) Clearance rate and filtering activity of zebra mussels (Dreissena polymorpha): implications for freshwater lakes. Can J Fish Aquat Sci 54:249–255CrossRefGoogle Scholar
  32. Jenkins MC, Trout J, Abrahamsen MS, Higgins J, Fayer R (2000) Estimating viability of Cryptosporidium parvum oocysts using reverse transcriptase-polymerase chain reaction (RT-PCR) directed at mRNA encoding amyloglucosidase. J Microbiol Methods 34:97–106CrossRefGoogle Scholar
  33. Jenkins M, Trout JM, Higgins J, Dorsch M, Veal D, Fayer R (2003) Comparison of tests for viable and infectious Cryptosporidium parvum oocysts. Parasitol Res 89:1–5PubMedGoogle Scholar
  34. Kilani RT, Sekla L (1987) Purification of Cryptosporidium oocysts and sporozoites by cesium chloride percoll gradient. Am J Trop Med Hyg 36:505-508PubMedGoogle Scholar
  35. Kotler DP, Orenstein JM (1999) Clinical syndromes associated with microsporidiosis. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. ASM Press, Washington, DC, pp 258–292Google Scholar
  36. Kucerova-Pospisilova Z, Carr D, Leitch G, Scanlon M, Visvesvara GS (1999) Environmental resistance of Encephalitozoon spores. J Eukaryot Microbiol 46:11S-13SPubMedGoogle Scholar
  37. Lowery CJ, Nugent P, Moore JE, Millar BC, Xiru X, Dooley JS (2001a) PCR-IMS detection and molecular typing of Cryptosporidium parvum recovered from a recreational river source and an associated mussel (Mytilus edulis) bed in Northern Ireland. Epidemiol Infect 127:545–553PubMedGoogle Scholar
  38. Lowery CJ, Millar BC, Moore JE, Xu J, Xiao L, Rooney PJ, Crothers L, Dooley JS (2001b) Molecular genotyping of human cryptosporidiosis in Northern Ireland: epidemiological aspects and review. Ir J Med Sci 170:246–250PubMedGoogle Scholar
  39. Lowery CJ, Moore JE, Millar BC, McCorry KA, Xu J, Rooney PJ, Dooley JS (2001c) Occurrence and molecular genotyping of Cryptosporidium spp. in surface waters in Northern Ireland. J Appl Microbiol 91:774–779CrossRefPubMedGoogle Scholar
  40. McMahon RB (1991) Mollusca: bivalvia. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, pp 315–401Google Scholar
  41. Minchin D, Lucy F, Sullivan M (2002a). Zebra mussel: impacts and spread. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe: distribution, impact and management. Kluwer, Dordrecht, pp 135–146Google Scholar
  42. Minchin D, Lucy F, Sullivan M (2002b) Monitoring of zebra mussels in the Shannon-Boyle navigation, other navigable regions and principal Irish lakes, 2001 and 2002. Marine Institute, Dublin, Marine Environment and Health Series No. 5Google Scholar
  43. Rinder H, Thomschke A, Sengjel B, Gothe R, Loscher T, Zahler M (2000) Close genetic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J Parasitol 86:185–188Google Scholar
  44. Rose JB, Lisle JT, LeChevallier M (1997) Waterborne cryptosporidiosis: incidence, outbreaks, and treatment strategies. In: Fayer R (ed) Cryptosporidium and cryptosporidiosis. CRC, Boca Raton, pp 93–110Google Scholar
  45. Sharma S, Sachdeva P, Virdi JS (2003) Emerging water-borne pathogens. Appl Microbiol Biotechnol 5–6:424–428Google Scholar
  46. Sparfel JM, Sarfati C, Liquory O, Caroff B, Dumoutier N, Gueglio B, Billaud E, Raffi F, Molina LM, Miegeville M, Derouin F (1997) Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J Eukaryot Microbiol 44:78SPubMedGoogle Scholar
  47. Vesey G, Ashbolt N, Fricker EJ, Deere D, William KL, Veal DA, Dorsch M (1998) The use of a ribosomal RNA targeted oligonucleotide probe for fluorescent labeling of viable Cryptosporidium parvum oocysts. J Appl Microbiol 85:429–440PubMedGoogle Scholar
  48. Visvesvara GS, DaSilva AJ, Croppo GP, Pieniazek NJ, Ferguson D, Moura H, Wallace S, Slemenda SB, Tyrrel I, Moore DF, Meador J (1995) In vitro culture and serologic and molecular identification of Septata intestinalis isolated from urine of a patient with AIDS. J Clin Microbiol 33:930–936PubMedGoogle Scholar
  49. Wolfe MS (1992) Giardiasis. Clin Microbiol Rev 5:93–100PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Thaddeus K. Graczyk
    • 1
    Email author
  • David Bruce Conn
    • 2
  • Frances Lucy
    • 3
  • Dan Minchin
    • 4
  • Leena Tamang
    • 1
  • Lacy N. S. Moura
    • 5
  • Alexandre J. DaSilva
    • 5
  1. 1.Department of Molecular Microbiology and Immunology, Bloomberg School of Public HealthJohns Hopkins UniversityBaltimoreUSA
  2. 2.School of Mathematical and Natural SciencesBerry CollegeMount BerryUSA
  3. 3.School of ScienceInstitute of TechnologySligoIreland
  4. 4.Marine Organism InvestigationsKillaloeIreland
  5. 5.National Center for Infectious Diseases, Centers for Disease Control and Prevention, Public Health ServiceU.S. Department of Health and Public ServicesAtlantaUSA

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