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Intestinal parasitic infections in an industrialized country; a new focus on children with better DNA-based diagnostics

Published online by Cambridge University Press:  23 August 2011

JACO J. VERWEIJ  and
LISETTE VAN LIESHOUT
JACO J. VERWEIJ*
Affiliation:
Department of Parasitology, Leiden University Medical Center, PO Box 9600, 2300 RC Leiden, The Netherlands
LISETTE VAN LIESHOUT
Affiliation:
Department of Parasitology, Leiden University Medical Center, PO Box 9600, 2300 RC Leiden, The Netherlands
*
*Corresponding author: Department of Parasitology, Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands. Tel: +31 71 5265080. Fax: +31 71 5265069. E-mail: j.j.verweij@lumc.nl
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Summary

In recent years, the isolation of parasitic DNA from faecal samples and PCR techniques, have been improved and simplified. Moreover, the introduction of real-time PCR has made it possible to multiplex different targets into one reaction. These new technical possibilities make it feasible to introduce PCR with its unsurpassed sensitivity and specificity in a routine laboratory setting for the diagnosis of intestinal parasites. Detection rates of the parasitic infections included in the PCR are increased significantly compared with microscopy. Molecular diagnostics, especially in children, reveal a possible cause of the gastrointestinal complaints in many more cases compared with conventional methods. Usually in GP patients no other pathogenic parasites are detected using microscopy and in the returning travellers additional parasites are found with microscopy in a minority of cases only. Multiplex real-time PCR offers a highly sensitive and specific diagnostic alternative for labour intensive microscopy in clinical laboratory practice. Additional diagnostic methods for the detection of parasitic infections that are not included as PCR target can be limited to a selected group of patients.

Keywords

G. lambliaCryptosporidiumD. fragilisE. histolyticachildrenreal-time PCR
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 12: Symposia of the British Society for Parasitology Volume 47 , October 2011 , pp. 1492 - 1498
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Logan, J., Edwards, K., and Saunders, N. (2009). Real-time PCR: Current Technology and Applications. Caister Academic Press.Google Scholar
Ankarklev, J., Jelrstrom-Hultqvist, J., Ringqvist, E., Troell, K. and Svard, S. G. (2010). Behind the smile: cell biology and disease mechanisms of Giardia species. Nature Reviews Microbiology 8, 413–422.Google Scholar
Bruijnesteijn van Coppenraet, L. E., Wallinga, J. A., Ruijs, G. J., Bruins, M. J. and Verweij, J. J. (2009). Parasitological diagnosis combining an internally controlled real-time PCR assay for the detection of four protozoa in stool samples with a testing algorithm for microscopy. Clinical Microbiology and Infection 15, 869–874.Google Scholar
Calderaro, A., Gorrini, C., Montecchini, S., Peruzzi, S., Piccolo, G., Rossi, S., Gargiulo, F., Manca, N., Dettori, G. and Chezzi, C. (2010 a). Evaluation of a real-time polymerase chain reaction assay for the laboratory diagnosis of giardiasis. Diagnostic Microbiology and Infectious Diseases 66, 261–267.CrossRefGoogle ScholarPubMed
Calderaro, A., Gorrini, C., Montecchini, S., Peruzzi, S., Piccollo, G., Rossi, S., Gargiulo, F., Manca, N., Dettori, G. and Chezzi, C. (2010 b). Evaluation of a real-time PCR assay for the detection of Dientamoeba fragilis. Diagnostic Microbiology and Infectious Diseases 67, 239–245.Google Scholar
Camp, R. R., Mattern, C. F. T. and Honigber, B. M. (1974). Study of Dientamoeba fragilis Jepps and Dobell. 1. Electron-microscopic observations of binucleate stages. 2. Taxonomic position and revision of genus. Journal of Protozoology 21, 69–82.CrossRefGoogle Scholar
Chalmers, R. M. and Davies, A. P. (2010). Minireview: Clinical cryptosporidiosis. Experimental Parasitology 124, 138–146.Google Scholar
Current, W. L. and Garcia, L. S. (1991). Cryptosporidiosis. Clinics in Laboratory Medicine 11, 873–897.CrossRefGoogle ScholarPubMed
de Boer, R. F., Ott, A., Kesztyus, B. and Kooistra-Smid, A. M. (2010). Improved detection of five major gastrointestinal pathogens by use of a molecular screening approach. Journal of Clinical Microbiology 48, 4140–4146.Google Scholar
de Wit, M. A. S., Koopmans, M. P. G., Kortbeek, L. M., van Leeuwen, N. J., Bartelds, A. I. M. and van Duynhoven, Y. T. H. P. (2001a). Gastroenteritis in sentinel general practices, the Netherlands. Emerging Infectious Diseases 7, 82–91.CrossRefGoogle ScholarPubMed
de Wit, M. A. S., Koopmans, M. P. G., Kortbeek, L. M., van Leeuwen, N. J., Vinje, J. and van Duynhoven, Y. T. H. P. (2001b). Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clinical Infectious Diseases 33, 280–288.Google Scholar
Diamond, L. S. and Clark, C. G. (1993). A redescription of Entamoeba histolytica Schaudinn, 1903 (Emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. Journal of Eukaryotic Microbiology 40, 340–344.CrossRefGoogle ScholarPubMed
Edeling, W. M., Verweij, J. J., Ponsioen, C. I. and Visser, L. G. (2004). Outbreak of amoebiasis in a Dutch family; tropics unexpectedly nearby [Uitbraak van amoebiasis in een Nederlands gezin; tropen onverwacht dichtbij]. Nederlands Tijdschrift voor Geneeskunde 148, 1830–1834.Google Scholar
Farthing, M. J. G. (2006). Treatment options for the eradication of intestinal protozoa. Nature Clinical Practice Gastroenterology and Hepatology 3, 436–445.CrossRefGoogle ScholarPubMed
Fotedar, R., Stark, D., Beebe, N., Marriott, D., Ellis, J. and Harkness, J. (2007). Laboratory diagnostic techniques for Entamoeba species. Clinical Microbiology Reviews 20, 511–532.Google Scholar
Garcia, L. S. and Shimizu, R. Y. (1997). Evaluation of nine immunoassay kits (enzyme immunoassay and direct fluorescence) for detection of Giardia lamblia and Cryptosporidium parvum in human fecal specimens. Journal of Clinical Microbiology 35, 1526–1529.CrossRefGoogle ScholarPubMed
Gatti, S., Cevini, C., Bruno, A., Novati, S. and Scaglia, M. (1995). Transmission of Entamoeba histolytica within a family complex. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 403–405.CrossRefGoogle ScholarPubMed
Gendrel, D., Treluyer, J. M. and Richard-Lenoble, D. (2003). Parasitic diarrhea in normal and malnourished children. Fundamental and Clinical Pharmacology 17, 189–197.Google Scholar
Ghosh, S., Debnath, A., Sil, A., De, S., Chattopadhyay, D. J. and Das, P. (2000). PCR detection of Giardia lamblia in stool: targeting intergenic spacer region of multicopy rRNA gene. Molecular and Cellular Probes 14, 181–189.Google Scholar
Gonzalez-Ruiz, A. and Wright, S. G. (1998). Disparate amoebae. Lancet 351, 1672–1673.CrossRefGoogle ScholarPubMed
Guyot, K. and Derouin, F. (2010). Laboratory-based surveillance for Cryptosporidium in France, 2006–2009. Euro Surveillance 15.Google Scholar
Haque, R., Roy, S., Siddique, A., Mondal, U., Rahman, S. M., Mondal, D., Houpt, E. and Petri, W. A. Jr. (2007). Multiplex real-time PCR assay for detection of Entamoeba histolytica, Giardia intestinalis, and Cryptosporidium spp. American Journal of Tropical Medicine and Hygiene 76, 713–717.CrossRefGoogle ScholarPubMed
Jepps, M. W. and Dobell, C. (1918). Dientamoeba fragilis n.g., n. sp., new intestinal amoeba from man. Parasitology 10, 352–367.CrossRefGoogle Scholar
Johnson, E. H., Windsor, J. J. and Clark, C. G. (2004). Emerging from obscurity: Biological, clinical, and diagnostic aspects of Dientamoeba fragilis. Clinical Microbiology Reviews 17, 553–570.CrossRefGoogle ScholarPubMed
Lee, M. B. and Greig, J. D. (2010). A review of gastrointestinal outbreaks in schools: Effective infection control interventions. Journal of School Health 80, 588–598.CrossRefGoogle ScholarPubMed
Lejeune, M., Rybicka, J. M. and Chadee, K. (2009). Recent discoveries in the pathogenesis and immune response toward Entamoeba histolytica. Future Microbiology 4, 105–118.CrossRefGoogle ScholarPubMed
Mank, T. G., Zaat, J. O., Deelder, A. M., van Eijk, J. T. and Polderman, A. M. (1997). Sensitivity of microscopy versus enzyme immunoassay in the laboratory diagnosis of giardiasis. European Journal of Clinical Microbiology and Infectious Diseases 16, 615–619.Google Scholar
Mirelman, D., Nuchamowitz, Y. and Stolarsky, T. (1997). Comparison of use of enzyme-linked immunosorbent assay-based kits and PCR amplification of rRNA genes for simultaneous detection of Entamoeba histolytica and E. dispar. Journal of Clinical Microbiology 35, 2405–2407.Google Scholar
Morgan, U. M., Pallant, L., Dwyer, B. W., Forbes, D. A., Rich, G. and Thompson, R. C. (1998). Comparison of PCR and microscopy for detection of Cryptosporidium parvum in human fecal specimens: clinical trial. Journal of Clinical Microbiology 36, 995–998.CrossRefGoogle ScholarPubMed
Nichols, G. L. (2000). Food-borne protozoa. British Medical Bulletin 56, 209–235.Google Scholar
Okhuysen, P. C. (2001). Traveler's diarrhea due to intestinal protozoa. Clinical and Infectious Diseases 33, 110–114.Google Scholar
Putignani, L. and Menichella, D. (2010). Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium. Interdisciplinary Perspectives in Infectious Diseases 2010.CrossRefGoogle ScholarPubMed
Qvarnstrom, Y., James, C., Xayavong, M., Holloway, B. P., Visvesvara, G. S., Sriram, R. and Da Silva, A. J. (2005). Comparison of real-time PCR protocols for differential laboratory diagnosis of amebiasis. Journal of Clinical Microbiology 43, 5491–5497.Google Scholar
Schuurs, T. A., Nguyen, H., Stellingwerf, A. J., Kooistra-Smid, A. M. and Noordhoek, G. T. (2010). P1688 Molecular diagnostics of gastroenteritis in clinical samples: a multicentre, quality control study in the Netherlands. http://www.blackwellpublishing.com/eccmid20/Google Scholar
Silberman, J. D., Clark, C. G. and Sogin, M. L. (1996). Dientamoeba fragilis shares a recent common evolutionary history with the trichomonads. Molecular and Biochemical Parasitology 76, 311–314.Google Scholar
Stark, D., Barratt, J., Roberts, T., Marriott, D., Harkness, J. and Ellis, J. (2010 a). Comparison of microscopy, two xenic culture techniques, conventional and real-time PCR for the detection of Dientamoeba fragilis in clinical stool samples. European Journal of Clincal Microbiology and Infectious Diseases 29, 411–416.CrossRefGoogle ScholarPubMed
Stark, D., Barratt, J., Roberts, T., Marriott, D., Harkness, J. and Ellis, J. (2010 b). A Review of the Clinical Presentation of dientamoebiasis. American Journal of Tropical Medicine and Hygiene 82, 614–619.CrossRefGoogle ScholarPubMed
Stensvold, C. R., Lebbad, M. and Verweij, J. J. (2011). The impact of genetic diversity in protozoa on molecular diagnostics. Trends Parasitology 27, 53–58.Google Scholar
ten Hove, R. J., Schuurman, T., Kooistra, M., Moller, L., van Lieshout, L. and Verweij, J. J. (2007). Detection of diarrhoea-causing protozoa in general practice patients in The Netherlands by multiplex real-time PCR. Clinical Microbiology and Infection 13, 1001–1007.Google Scholar
ten Hove, R. J., Van Esbroeck, M., Vervoort, T., Van den Ende, J., van Lieshout, L. and Verweij, J. J. (2009). Molecular diagnostics of intestinal parasites in returning travellers. European Journal of Clinical Microbiology and Infectious Diseases 28, 1045–1053.Google Scholar
Thompson, R. C., Hopkins, R. M. and Homan, W. L. (2000). Nomenclature and genetic groupings of Giardia infecting mammals. Parasitology Today 16, 210–213.CrossRefGoogle ScholarPubMed
van Gool, T., Weijts, R., Lommerse, E. and Mank, T. G. (2003). Triple faeces test: An effective tool for detection of intestinal parasites in routine clinical practice. European Journal of Clinical Microbiology and Infectious Diseases 22, 284–290.Google Scholar
van Lieshout, L. and Verweij, J. J. (2010). Newer diagnostic approaches to intestinal protozoa. Current Opinion in Infectious Diseases 23, 488–493.CrossRefGoogle ScholarPubMed
Verweij, J. J., Blange, R. A., Templeton, K., Schinkel, J., Brienen, E. A. T., van Rooyen, M. A., van Lieshout, L. and Polderman, A. M. (2004). Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. Journal of Clinical Microbiology 42, 1220–1223.Google Scholar
Verweij, J. J., Canales, M., Polman, K., Ziem, J., Brienen, E. A., Polderman, A. M. and van Lieshout, L. (2009). Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 342–346.Google Scholar
Verweij, J. J., Oostvogel, F., Brienen, E. A. T., Nang-Neifubah, A., Ziem, J. and Polderman, A. M. (2003 a). Prevalence of Entamoeba histolytica and Entamoeba dispar in northern Ghana. Tropical Medicine and International Health 8, 1153–1156.Google Scholar
Verweij, J. J., Schinkel, J., Laeijendecker, D., van Rooyen, M. A., van Lieshout, L. and Polderman, A. M. (2003 b). Real-time PCR for the detection of Giardia lamblia. Molecular and Cellular Probes 17, 223–225.Google Scholar
Verweij, J. J., Mulder, B., Poell, B., van Middelkoop, D., Brienen, E. A. T. and van Lieshout, L. (2007). Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Molecular and Cellular Probes 21, 400–404.Google Scholar
Visser, L. G., Verweij, J. J., Van Esbroeck, M., Edeling, W. M., Clerinx, J. and Polderman, A. M. (2006). Diagnostic methods for differentiation of Entamoeba histolytica and Entamoeba dispar in carriers: performance and clinical implications in a non-endemic setting. International Journal of Medical Microbiology 296, 397–403.Google Scholar
Vreden, S. G. S., Visser, L. G., Verweij, J. J., Blotkamp, J., Stuiver, P. C., Aguirre, A. and Polderman, A. M. (2000). Outbreak of amebiasis in a family in The Netherlands. Clinical Infectious Diseases 31, 1101–1104.CrossRefGoogle Scholar
Walsh, A. L. (1988). Prevalence in Entamoeba histolytica infection. Amebiais: human infection by Entamoeba histolytica. John Wiley and Sons, 93–105.Google Scholar
Weber, R., Bryan, R. T., Bishop, H. S., Wahlquist, S. P., Sullivan, J. J. and Juranek, D. D. (1991). Threshold of detection of Cryptosporidium oocysts in human stool specimens: evidence for low sensitivity of current diagnostic methods. Journal of Clinical Microbiology 29, 1323–1327.Google Scholar
Webster, K. A., Smith, H. V., Giles, M., Dawson, L. and Robertson, L. J. (1996). Detection of Cryptosporidium parvum oocysts in faeces: comparison of conventional coproscopical methods and the polymerase chain reaction. Veterinary Parasitology 61, 5–13.CrossRefGoogle ScholarPubMed
Ximenez, C., Moran, P., Rojas, L., Valadez, A. and Gomez, A. (2009). Reassessment of the epidemiology of amebiasis: State of the art. Infection, Genetics and Evolution 9, 1023–1032.CrossRefGoogle ScholarPubMed