Cryptosporidium parvum genotype IIa and Giardia duodenalis assemblage A in Mytilus galloprovincialis on sale at local food markets

International Journal of Food Microbiology

Volumn 171, Issue , 2014, Pages 62-67

  Giangaspero, Annunziata ^a   Papini, Roberto ^b   Marangi, Marianna ^a   Koehler, Anson V ^c   Gasser, Robin B ^c  

^a UNIVERSITY OF FOGGIA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cryptosporidium; Giardia; Molecular identification; Mussel; Public health

Indexed keywords

BETA GIARDIN PROTEIN; GLYCOPROTEIN; GLYCOPROTEIN 60; PROTOZOAL PROTEIN; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

AMPLICON; ARTICLE; CONSUMER ATTITUDE; CONTROLLED STUDY; CRYPTOSPORIDIUM PARVUM; EATING HABIT; EXOCRINE GLAND; FOOD CONTAMINATION; FOOD ORGANISM; GENOTYPE; GIARDIA LAMBLIA; GILL; HEALTH HAZARD; HEMOLYMPH; ITALY; MARKET; MICROORGANISM DETECTION; MYTILUS GALLOPROVINCIALIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSONAL HYGIENE; POLYMERASE CHAIN REACTION; PROTIST; PUBLIC HEALTH PROBLEM; PURCHASING; ANIMAL; CLASSIFICATION; FOOD CONTROL; GENETICS; GIARDIA; HUMAN; MOLECULAR GENETICS; MYTILUS; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; SANITATION; SHELLFISH; STANDARDS;

CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; GIARDIA; GIARDIA INTESTINALIS; MYTILUS GALLOPROVINCIALIS; PROTISTA;

ANIMALS; CRYPTOSPORIDIUM PARVUM; FOOD PARASITOLOGY; GENOTYPE; GIARDIA; HUMANS; ITALY; MOLECULAR SEQUENCE DATA; MYTILUS; PHYLOGENY; POLYMERASE CHAIN REACTION; SANITATION; SHELLFISH;

EID: 84890175389     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2013.11.022     Document Type: Article

References (56)

1. Alves M., Matos O., Antunes F. Microsatellite analysis of Cryptosporidium hominis and C. parvum in Portugal: a preliminary study. J. Eukaryot. Microbiol. 2003, 529-530. (Suppl.).
2. ARPA, Puglia Relazione sullo Stato dell'Ambiente 2010 Regione Puglia http://www.arpa.puglia.it.
3. Baumgartner A., Marder H.P., Munzinger J., Siegrist H.H. Frequency of Cryptosporidium spp. as cause of human gastrointestinal disease in Switzerland and possible sources of infection. Schweiz. Med. Wochenschr. 2000, 130:1252-1258.
4. Bonhomme J., Le Goff L., Lemée V., Gargala G., Ballet J.J., et al. Limitations of tpi and bg genes sub-genotyping for characterization of human Giardia duodenalis isolates. Parasitol. Int. 2011, 60:327-330.
5. Bouzid M., Tyler K.M., Christen R., Chalmers R.M., Elwin K., et al. Multi-locus analysis of human infective Cryptosporidium species and subtypes using ten novel genetic loci. BMC Microbiol. 2010, 10.1186/1471-2180-10-213.
6. Chalmers R.M., Davies A.P. Minireview: clinical cryptosporidiosis. Exp. Parasitol. 2010, 124:138-146.
7. Chalmers R.M., Ferguson C., Cacciò S., Gasser R.B., Abs EL-Osta Y.G., et al. Direct comparison of selected methods for genetic categorisation of Cryptosporidium parvum and Cryptosporidium hominis species. Int. J. Parasitol. 2005, 35:395-410.
8. Chappell C.L., Okhuysen P.C., Sterling C.R., Dupont H.L. Cryptosporidium parvum: intensity of infection and oocyst excretion patterns in healthy volunteers. J. Infect. Dis. 1996, 173:232-236.
9. Del Chierico F., Onori M., Di Bella S., Bordi E., Petrosillo N., et al. Cases of cryptosporidiosis co-infections in AIDS patients: a correlation between clinical presentation and GP60 subgenotype lineages from aged formalin-fixed stool samples. Ann. Trop. Med. Parasitol. 2011, 105:339-349.
10. EFSA European Food Safety Authority http://www.efsa.europa.eu/en/efsajournal/doc/2613.
11. Escobedo A.A., Almirall P., Robertson L., Franco R.M.B., Hanevik K., et al. Giardiasis: the ever-present threat of a neglected disease. Infect. Disord. Drug Targets 2010, 10:329-348.
12. Esmerini P.O., Gennari S.M., Pena H.F. Analysis of marine bivalve shellfish from the fish market in Santos city, São Paulo state, Brazil, for Toxoplasma gondii. Vet. Parasitol. 2010, 170:8-13.
13. Espiñeira M., González-Lavín N., Vieites J.M., Santaclara F.J. Development of a method for the genetic identification of commercial bivalve species based on mitochondrial 18S rRNA sequences. J. Agric. Food Chem. 2009, 57:495-502.
14. European Communities Regulation (EC) No 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Off. J. Eur. Communities L 2004, 226:83-127. (25.6.04).
15. Fayer R., Trout J.M., Lewis E.J., Xiao L., Lal A., et al. Temporal variability of Cryptosporidium in the Chesapeake Bay. Parasitol. Res. 2002, 88:998-1003.
16. Fayer R., Trout J.M., Lewis E.J., Santin M., Zhou L., et al. Contamination of Atlantic coast commercial shellfish with Cryptosporidium. Parasitol. Res. 2003, 89:141-145.
17. Feng Y., Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin. Microbiol. Rev. 2011, 24:110-140.
18. Geurden T., Levecke B., Cacciò S.M. Multilocus genotyping of Cryptosporidium and Giardia in non-outbreak related cases of diarrhoea in human patients in Belgium. Parasitology 2009, 136:1161-1168.
19. Giangaspero A., Molini U., Iorio R., Traversa D., Paoletti B., et al. Cryptosporidium parvum oocysts in seawater clams (Chamelea gallina) in Italy. Prev. Vet. Med. 2005, 69:203-212.
20. Giangaspero A., Berrilli F., Brandonisio O. Giardia and Cryptosporidium and public health: the epidemiological scenario from the Italian perspective. Parasitol. Res. 2007, 101:1169-1182.
21. Gómez-Bautista M., Ortega-Mora L.M., Tabares E., Lopez-Rodas V., Costas E. Detection of infectious Cryptosporidium parvum oocysts in mussels (Mytilus galloprovincialis) and cockles (Cerastoderma edule). Appl. Environ. Microbiol. 2000, 66:1866-1870.
22. Gómez-Couso H., Freire-Santos F., Amar C.F., Grant K.A., Williamson K., et al. Detection of Cryptosporidium and Giardia in molluscan shellfish by multiplexed nested-PCR. Int. J. Food Microbiol. 2004, 91:279-288.
23. Gómez-Couso H., Mendez-Hermida F., Ares-Mazas E. Levels of detection of Cryptosporidium oocysts in mussels (Mytilus galloprovincialis) by IFA and PCR methods. Vet. Parasitol. 2006, 141:60-65.
24. Gómez-Couso H., Mendez-Hermida F., Castro-Hermida J.A., Ares-Mazas E. Cryptosporidium contamination in harvesting areas of bivalve molluscs. J. Food Prot. 2006, 69:185-190.
25. Gómez-Couso H., Mendez-Hermida F., Castro-Hermida J.A., Ares-Mazas E. Cooking mussels (Mytilus galloprovincialis) by steam does not destroy the infectivity of Cryptosporidium parvum. J. Food Prot. 2006, 69:948-950.
26. Graczyk T.K., Fayer R., Lewis E.J., Trout J.M., Farley C.A. Cryptosporidium oocysts in Bent mussels (Ischadium recurvum) in the Chesapeake Bay. Parasitol. Res. 1999, 85:518-521.
27. Graczyk T.K., Thompson R.C., Fayer R., Adams P., Morgan U.M., et al. Giardia duodenalis cysts of genotype A recovered from clams in the Chesapeake Bay subestuary, Rhode River. Am. J. Trop. Med. Hyg. 1999, 61:526-529.
28. Graczyk T.K., Lewis E.J., Glass G., Dasilva A.J., Tamang L., et al. Quantitative assessment of viable Cryptosporidium parvum load in commercial oysters (Crassostrea virginica) in the Chesapeake Bay. Parasitol. Res. 2007, 100:247-253.
29. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 1999, 41:95-98.
30. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
31. Ismea Report Ittico. Analisi e dati di settore 2011 e 2012 2012, (17 dicembre 2012).
32. Jagai J.S., Castronovo D.A., Monchak J., Naumova E.N. Seasonality of cryptosporidiosis: a meta-analysis approach. Environ. Res. 2009, 109:465-478.
33. Jex A.R., Gasser R.B. Genetic richness and diversity in Cryptosporidium hominis and C. parvum reveals major knowledge gaps and a need for the application of "next generation" technologies-research review. Biotechnol. Adv. 2010, 28:17-26.
34. Jex A.R., Ryan U.M., Ng J., Campbell B.E., Xiao L., et al. Specific and genotypic identification of Cryptosporidium from a broad range of host species by nonisotopic SSCP analysis of nuclear ribosomal DNA. Electrophoresis 2007, 28:2818-2825.
35. Jex A.R., Pangasa A., Campbell B.E., Whipp M., Hogg G., Sinclair M.I., et al. Classification of Cryptosporidium species from patients with sporadic cryptosporidiosis by use of sequence-based multilocus analysis following mutation scanning. J. Clin. Microbiol. 2008, 46:2252-2262.
36. Lebbad M., Mattsson J.G., Christensson B., Ljungstrom B., Backhans A., et al. From mouse to moose: multilocus genotyping of Giardia isolates from various animal species. Vet. Parasitol. 2010, 168:231-239.
37. Li X., Guyot K., Dei-Cas E., Mallard J.P., Ballet J.J., et al. Cryptosporidium oocysts in mussels (Mytilus edulis) from Normandy (France). Int. J. Food Microbiol. 2006, 108:321-325.
38. Lobo M.L., Xiao L., Antunes F., Matos O. Occurrence of Cryptosporidium and Giardia genotypes and subtypes in raw and treated water in Portugal. Lett. Appl. Microbiol. 2009, 48:732-737.
39. Miller W.A., Miller M.A., Gardner I.A., Atwill E.R., Harris M., et al. New genotypes and factors associated with Cryptosporidium detection in mussels (Mytilus spp.) along the California coast. Int. J. Parasitol. 2005, 35:1103-1113.
40. Molini U., Iorio R., Traversa D., Paoletti B., Giansante C., et al. Rilievo di Giardia spp. e Cryptosporidium spp. nelle vongole (Chamelea gallina) della costa abruzzese. Ittiopatologia 2004, 1:34-40.
41. Molini U., Traversa D., Ceschia G., Iorio R., Boffo L., et al. Temporal occurrence of Cryptosporidium in the Asian clam Ruditapes philippinarum in the Northern Adriatic Italian lagoons. J. Food Prot. 2007, 70:494-499.
42. Nolan M.J., Jex A.R., Haydon S.R., Stevens M.A., Gasser R.B. Molecular detection of Cryptosporidium cuniculus in rabbits in Australia. Infect. Genet. Evol. 2010, 10:1179-1187.
43. Nolan M.J., Jex A.R., Koehler A.V., Haydon S.R., Stevens M.A., et al. Molecular-based investigation of Cryptosporidium and Giardia from animals in water catchments in southeastern Australia. Water Res. 2013, 47:1726-1740.
44. Plutzer J., Karanis P. Genetic polymorphism in Cryptosporidium species: an update. Vet. Parasitol. 2009, 165:187-199.
45. Putignani L., Menichella D. Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium. Interdiscip. Perspect. Infect. Dis. 2010, (pii: 753512). 10.1155/2010/753512.
46. Rendtorff R.C. The experimental transmission of human intestinal protozoan parasites. II. Giardia lamblia cysts given in capsules. Am. J. Hyg. 1954, 59:209-220.
47. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
48. Soba B., Loga r J. Genetic classification of Cryptosporidium isolates from humans and calves in Slovenia. Parasitology 2008, 135:1263-1270.
49. Srisuphanunt M., Wiwanitkit V., Saksirisampant W., Karanis P. Detection of Cryptosporidium oocysts in green mussels (Perna viridis) from shell-fish markets of Thailand. Parasite 2009, 16:235-239.
50. Sulaiman I.M., Fayer R., Bern C., Gilman R.H., Trout J.M., et al. Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg. Infect. Dis. 2003, 9:1444-1452.
51. Sulaiman I.M., Hira P.R., Zhou L., Al-Ali F.M., Al-Shelahi F.A., et al. Unique endemicity of cryptosporidiosis in children in Kuwait. J. Clin. Microbiol. 2005, 43:2805-2809.
52. Thompson H.P., Dooley J.S., Kenny J., McCoy M., Lowery C.J., et al. Genotypes and subtypes of Cryptosporidium spp. in neonatal calves in Northern Ireland. Parasitol. Res. 2007, 100:619-624.
53. Widmer G. Meta-analysis of a polymorphic surface glycoprotein of the parasitic protozoa Cryptosporidium parvum and Cryptosporidium hominis. Epidemiol. Infect. 2009, 137:1800-1808.
54. Wielinga P.R., de Vries A., van der Goot T.H., Mank T., Mars M.H., et al. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. Int. J. Parasitol. 2008, 38:809-817.
55. World Health Organization Guidelines for drinking-water quality http://www.who.int/water_sanitation_health/dwq/gdwq3rev.
56. Xiao L., Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int. J. Parasitol. 2008, 38:1239-1255.