Phylogenetic analysis implicates birds as a source of Cryptosporidium spp. oocysts in agricultural watersheds

Environmental Science and Technology

Volumn 41, Issue 10, 2007, Pages 3620-3625

  Jellison, Kristen L ^a,d   Distel, Daniel L ^b   Hemond, Harold F ^a   Schauer, David B ^c  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b Ocean Genome Legacy Foundation   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Lehigh University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

18S RRNA; AGRICULTURAL AREAS; AGRICULTURAL WATERSHEDS; BOSTON ,MASSACHUSETTS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM OOCYSTS; CRYPTOSPORIDIUM PARVUM; CRYPTOSPORIDIUM SPP; DAIRY FARMS; DRINKING WATER SOURCES; FECAL SAMPLES; GENBANK; MIGRATORY BIRDS; NEIGHBOR JOINING; OOCYSTS; PARSIMONY METHODS; PHYLOGENETIC ANALYSIS; PRINCIPAL COMPONENTS ANALYSIS; PROTOZOAN PARASITES; SEASONAL FACTORS; WACHUSETT RESERVOIRS;

AGRICULTURE; GENES; LANDFORMS; POPULATION STATISTICS; PRINCIPAL COMPONENT ANALYSIS; RNA; WATERSHEDS;

SURFACE WATERS;

WATER;

AGRICULTURE; ANIMAL; ARTICLE; BIRD; CRYPTOSPORIDIUM; GENETICS; METABOLISM; OOCYST; PARASITOLOGY; PHYLOGENY; STANDARD; TEMPERATURE; WATER SUPPLY;

AGRICULTURE; ANIMALS; BIRDS; CRYPTOSPORIDIUM; OOCYSTS; PHYLOGENY; TEMPERATURE; WATER; WATER SUPPLY;

EID: 34250869674     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es0626842     Document Type: Article

References (39)

1. Fayer, R.; Speer, C. A.; Dubey, J. P. The general biology of Cryptosporidium. In Cryptosporidium and Cryptosporidiosis; Fayer, R. Ed.; CRC Press: Boca Raton, FL, 1997.
2. Caccio, S.; Pinter, E.; Fantini, R.; Mezzaroma, I.; Pozio, E. Human infection with Cryptosporidium felis: case report and literature review. Emerg. Infect. Dis. 2002, 8 (1), 85-86. (Pubitemid 34094289)
3. Katsumata, T.; Hosea, D.; Ranuh, I. G.; Uga, S.; Yanagi, T.; Kohno, S. Short report: possible Cryptosporidium muris infection in humans. Am. J. Trop. Med. Hyg. 2000, 62 (1), 70-72. (Pubitemid 30180352)
4. Gatei, W.; Ashford, R. W.; Beeching, N. J.; Kamwati, S. K.; Greensill, J.; Hart, C. A. Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerg. Infect. Dis. 2002, 8 (2), 204-206.
5. Solo-Gabriele, H.; Neumeister, S. US outbreaks of cryptosporidiosis. J. Am. Water Works Assoc. 1996, 88 (9), 76-86. (Pubitemid 126591054)
6. Millard, P. S.; Gensheimer, K. F.; Addiss, D. G.; Sosin, D. M.; Beckett, G. A.; Houck-Jankoski, A.; Hudson, A. An outbreak of cryptosporidiosis from fresh-pressed apple cider. JAMA 1994, 272 (20), 1592-1596. (Pubitemid 24350713)
7. Roefer, P. A.; Monscvitz, J. T.; Rexing, D. J. The Las Vegas cryptosporidiosis outbreak. J. Am. Water Works Assoc. 1996, 88 (9), 95-106.
8. Craun, G. F.; Hubbs, S. A.; Frost, F.; Calderon, R. L.; Via, S. H. Waterborne outbreaks of cryptosporidiosis. J. Am. Water Works Assoc. 1998, 90 (9), 81-91. (Pubitemid 128586016)
9. Howe, A. D.; Forster, S.; Morton, S.; Marshall, R.; Osborn, K. S.; Wright, P.; Hunter, P. R. Cryptosporidium oocysts in a water supply associated with a cryptosporidiosis outbreak. Emerg. Infect. Dis. 2002, 8 (6), 619-624. (Pubitemid 34556364)
10. Glaberman, S.; Moore, J. E.; Lowery, C. J.; Chalmers, R. M.; Sulaiman, I.; Elwin, K.; Rooney, P. J.; Millar, B. C.; Dooley, J. S.; Lal, A. A.; Xiao, L. Three drinking-water-associated cryptosporidiosis outbreaks, Northern Ireland. Emerg. Infect. Dis. 2002, 8 (6), 631-633. (Pubitemid 34556366)
11. Centers for Disease Control and Prevention (CDC). Foodborne outbreak of cryptosporidiosis - Spokane, Washington, 1997. MMWR Morb. Mort. Wkly. Rep. 1998, 47 (27), 565-567.
12. Centers for Disease Control and Prevention (CDC). Outbreak of cryptosporidiosis associated with a water sprinkler fountain - Minesota, 1997. MMWR Morb. Mort. Wkly. Rep. 1998, 47 (40), 856-860.
13. Xiao, L.; Sulaiman, I. M.; Ryan, U. M.; Zhou, L.; Atwill, E. R.; Tischler, M. L.; Zhang, X.; Fayer, R.; Lal, A. A. Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. Int. J. Parasitol. 2002, 32 (14), 1773-1785. (Pubitemid 35447606)
14. Heitman, T. L.; Frederick, L. M.; Viste, J. R.; Guselle, N. J.; Morgan, U. M.; Thompson, R. C.; Olson, M. E. Prevalence of Giardia and Cryptosporidium and characterization of Cryptosporidium spp. isolated from wildlife, human, and agricultural sources in the North Saskatchewan River Basin in Alberta, Canada. Can. J. Microbiol. 2002, 48 (6), 530-541. (Pubitemid 34994779)
15. Xiao, L.; Escalante, L.; Yang, C.; Sulaiman, I.; Escalante, A. A.; Montali, R. J.; Fayer, R.; Lal, A. A. Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl. Environ. Microbiol. 1999, 65 (4), 1578-1583. (Pubitemid 29173687)
16. Perz, J. F.; LeBlancq, S. M. Cryptosporidium parvum infection involving novel genotypes in wildlife from lower New York state. Appl. Environ. Microbiol. 2001, 67 (3), 1154-1162. (Pubitemid 33643555)
17. Xiao, L.; Alderisio, K.; Limor, J.; Royer, M.; Lal, A. A. Identification of species and sources of Cryptosporidium oocysts in storm waters with a small-subunit rRNA-based diagnostic and genotyping tool. Appl. Environ. Microbiol. 2000, 66 (12), 5492-5498. (Pubitemid 32217163)
18. Xiao, L.; Singh, A.; Limor, J.; Graczyk, T. K.; Gradus, S.; Lal, A. Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl. Environ. Microbiol. 2001, 67 (3), 1097-1101. (Pubitemid 33643547)
19. Jellison, K. L.; Hemond, H. F.; Schauer, D. B. Sources and species of Cryptosporidium oocysts in the Wachusett Reservoir watershed. Appl. Environ. Microbiol. 2002, 68 (2), 569-575. (Pubitemid 34113042)
20. Jellison, K. L.; Distel, D. L.; Hemond, H. F.; Schauer, D. B. Phylogenetic analysis of the hypervariable region of the 18S rRNA gene of Cryptosporidium oocysts in Canada geese (Branta canadensis): evidence for five novel genotypes. Appl. Environ. Microbiol. 2004, 70 (1), 452-458. (Pubitemid 38090236)
21. Johnson, D. W.; Pieniazek, N. J.; Griffin, D. W.; Misener, L.; Rose, J. B. Development of a PCR protocol for sensitive detection of Cryptosporidium oocysts in water samples. Appl. Environ. Microbiol. 1995, 61 (11), 3849-3855.
22. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods); Sinauer Associates: Sunderland, MA, 2002.
23. Hillis, D. M.; Bull, J. J. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 1993, 42 (2), 182-192.
24. Xiao, L.; Morgan, U. M.; Limor, J.; Escalante, A.; Arrowood, M.; Shulaw, W.; Thompson, R. C.; Fayer, R.; Lal, A. A. Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Appl. Environ. Microbiol. 1999, 65 (8), 3386-3391. (Pubitemid 29398960)
25. Anderson, B. C. Cryptosporidiosis in bovine and human health. J. Dairy Sci. 1998, 81 (11), 3036-3041. (Pubitemid 128447805)
26. Fayer, R.; Trout, J. M.; Graczyk, T. K.; Lewis, E. J. Prevalence of Cryptosporidium, Giardia, and Eimeria infections in post-weaned and adult cattle on three Maryland farms. Vet. Parasitol. 2000, 93 (2), 103-112.
27. Castro-Hermida, J. A.; Gonzalez-Losada, Y. A.; Mezo-Menendez, M.; Ares-Mazas, E. A study of cryptosporidiosis in a cohort of neonatal calves. Vet. Parasitol. 2002, 106 (1), 11-17. (Pubitemid 34454863)
28. Sreter, T.; Egyed, Z.; Szell, Z.; Kovacs, G.; Nikolausz, M.; Marialigeti, K.; Varga, I. Morphologic, host specificity, and genetic characterization of a European Cryptosporidium andersoni isolate. J. Parasitol. 2000, 86 (6), 1244-1249. (Pubitemid 32047195)
29. Enemark, H. L.; Ahrens, P.; Lowery, C. J.; Thamsborg, S. M.; Enemark, J. M.; Bille-Hansen, V.; Lind, P. Cryptosporidium andersoni from a Danish cattle herd: identification and preliminary characterization. Vet. Parasitol. 2002, 107 (1-2), 37-49. (Pubitemid 34628788)
30. Morgan, U. M.; Monis, P. T.; Xiao, L.; Limor, J.; Sulaiman, I.; Raidal, S.; O'Donoghue, P.; Gasser, R.; Murray, A.; Fayer, R.; Blagburn, B. L.; Lal, A. A.; Thompson, R. C. Molecular and phylogenetic characterisation of Cryptosporidium from birds. Int. J. Parasitol. 2001, 31 (3), 289-296. (Pubitemid 32168150)
31. Ryan, U. M.; Xiao, L.; Read, C.; Sulaiman, I. M.; Monis, P.; Lal, A. A.; Fayer, R.; Pavlasek, I. A redescription of Cryptosporidium galli Pavlasek 1999 (Apicomplexa: Cryptosporidiidae) from birds. J. Parasitol. 2003, 89 (4), 809-813. (Pubitemid 37151586)
32. Smith, H. V.; Brown, J.; Coulson, J. C.; Morris, G. P.; Girdwood, R. W. Occurrence of oocysts of Cryptosporidium sp. in Laurus spp. gulls. Epidemiol. Infect. 1993, 110 (1), 135-143. (Pubitemid 23217337)
33. Graczyk, T. K.; Fayer, R.; Trout, J. M.; Lewis, E. J.; Farley, C. A.; Sulaiman, I.; Lal, A. A. Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese (Branta canadensis). Appl. Environ. Microbiol. 1998, 64 (7), 2736-2738. (Pubitemid 28303330)
34. Graczyk, T. K.; Cranfield, M. R.; Fayer, R.; Anderson, M. S. Viability and infectivity of Cryptosporidium parvum oocysts are retained upon intestinal passage through a refractory avian host. Appl. Environ. Microbiol. 1996, 62 (9), 3234-3237. (Pubitemid 26304106)
35. Graczyk, T. K.; Cranfield, M. R.; Fayer, R.; Trout, J.; Goodale, H. J. Infectivity of Cryptosporidium parvum oocysts is retained upon intestinal passage through a migratory water-fowl species (Canada goose, Branta canadensis). Trop. Med. Int. Health. 1997, 2 (4), 341-347.
36. Dieter, R. A., Jr.; Dieter, R. S.; Dieter, R. A., 3rd; Gulliver, G. Zoonotic diseases: health aspects of Canade geese. Int. J. Circumpolar Health 2001, 60 (4), 676-684.
37. Wade, S. E.; Mohammed, H. O.; Schaaf, S. L. Prevalence of Giardia sp., Cryptosporidium parvum and Cryptosporidium andersoni (syn. C. muris) in 109 dairy herds in five counties of southeastern New York. Vet. Parasitol. 2000, 93 (1), 1-11.
38. Bodley-Tickell, A. T.; Kitchen, S. E.; Sturdee, A. P. Occurrence of Cryptosporidium in agricultural surface waters during an annual farming cycle in lowland UK. Water Res. 2002, 36 (7), 1880-1886. (Pubitemid 34288521)
39. Huetink, R. E.; van der Giessen, J. W.; Noordhuizen, J. P.; Ploeger, H. W. Epidemiology of Cryptosporidium spp. and Giardia duodenalis on a dairy farm. Vet. Parasitol. 2001, 102 (1-2), 53-67. (Pubitemid 33052434)