Advertisement
Review Article| Volume 35, ISSUE 2, P423-444, June 2015

Download started.

Ok

Infections by Intestinal Coccidia and Giardia duodenalis

Published:April 04, 2015DOI:https://doi.org/10.1016/j.cll.2015.02.010

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bern C.
        • Hernandez B.
        • Lopez M.B.
        • et al.
        The contrasting epidemiology of Cyclospora and Cryptosporidium among outpatients in Guatemala.
        Am J Trop Med Hyg. 2000; 63: 231-235
        • Ortega Y.R.
        • Sterling C.R.
        • Gilman R.H.
        • et al.
        Cyclospora species–a new protozoan pathogen of humans.
        N Engl J Med. 1993; 328: 1308-1312
      1. Duszynsky DW, Upton SJ, Couch L. The coccidia of the world. Review of coccidia in humans and animals. 2014. Available at: http://biology.unm.edu/biology/coccidia/home.html. Accessed December 8, 2014.

        • Adl S.M.
        • Simpson A.G.
        • Lane C.E.
        • et al.
        The revised classification of eukaryotes.
        J Eukaryot Microbiol. 2012; 59: 429-493
        • Wolfe M.S.
        Giardiasis.
        Clin Microbiol Rev. 1992; 5: 93-100
        • Ortega Y.R.
        • Adam R.D.
        Giardia: overview and update.
        Clin Infect Dis. 1997; 25 ([quiz: 550]): 545-549
        • McHardy I.H.
        • Wu M.
        • Shimizu-Cohen R.
        • et al.
        Detection of intestinal protozoa in the clinical laboratory.
        J Clin Microbiol. 2014; 52: 712-720
        • Hiatt R.A.
        • Markell E.K.
        • Ng E.
        How many stool examinations are necessary to detect pathogenic intestinal protozoa?.
        Am J Trop Med Hyg. 1995; 53: 36-39
      2. Garcia L. Diagnostic medical parasitology. 5th edition. ASM Press, Washington, DC2007
        • Pietrzak-Johnston S.M.
        • Bishop H.
        • Wahlquist S.
        • et al.
        Evaluation of commercially available preservatives for laboratory detection of helminths and protozoa in human fecal specimens.
        J Clin Microbiol. 2000; 38: 1959-1964
        • Tyzzer E.E.
        An extracellular coccidium, Cryptosporidium muris (Gen. Et Sp. Nov.), of the gastric glands of the common mouse.
        J Med Res. 1910; 23: 487-510.3
        • Tyzzer E.E.
        Cryptosporidium parvum (sp. nov.), a coccidium found in the small intestine of the common mouse.
        Arch Protistenkunde. 1912; 26: 394-412
        • Current W.L.
        • Reese N.C.
        • Ernst J.V.
        • et al.
        Human cryptosporidiosis in immunocompetent and immunodeficient persons. Studies of an outbreak and experimental transmission.
        N Engl J Med. 1983; 308: 1252-1257
        • Malebranche R.
        • Arnoux E.
        • Guerin J.M.
        • et al.
        Acquired immunodeficiency syndrome with severe gastrointestinal manifestations in Haiti.
        Lancet. 1983; 2: 873-878
        • Jonas C.
        • Deprez C.
        • De Maubeuge J.
        • et al.
        Cryptosporidium in patient with acquired immunodeficiency syndrome.
        Lancet. 1983; 2: 964
        • Colford Jr., J.M.
        • Tager I.B.
        • Hirozawa A.M.
        • et al.
        Cryptosporidiosis among patients infected with human immunodeficiency virus. Factors related to symptomatic infection and survival.
        Am J Epidemiol. 1996; 144: 807-816
        • Flanigan T.
        • Whalen C.
        • Turner J.
        • et al.
        Cryptosporidium infection and CD4 counts.
        Ann Intern Med. 1992; 116: 840-842
        • Navin T.R.
        • Weber R.
        • Vugia D.J.
        • et al.
        Declining CD4+ T-lymphocyte counts are associated with increased risk of enteric parasitosis and chronic diarrhea: results of a 3-year longitudinal study.
        J Acquir Immune Defic Syndr Hum Retrovirol. 1999; 20: 154-159
        • Soave R.
        Waterborne cryptosporidiosis–setting the stage for control of an emerging pathogen.
        Clin Infect Dis. 1995; 21: 63-64
        • Navin T.R.
        • Juranek D.D.
        Cryptosporidiosis: clinical, epidemiologic, and parasitologic review.
        Rev Infect Dis. 1984; 6: 313-327
        • Ortega Y.R.
        • Sheehy R.R.
        • Cama V.A.
        • et al.
        Restriction fragment length polymorphism analysis of Cryptosporidium parvum isolates of bovine and human origin.
        J protozool. 1991; 38: 40S-41S
        • Sulaiman I.M.
        • Xiao L.
        • Yang C.
        • et al.
        Differentiating human from animal isolates of Cryptosporidium parvum.
        Emerg Infect Dis. 1998; 4: 681-685
        • Peng M.M.
        • Xiao L.
        • Freeman A.R.
        • et al.
        Genetic polymorphism among Cryptosporidium parvum isolates: evidence of two distinct human transmission cycles.
        Emerg Infect Dis. 1997; 3: 567-573
        • Xiao L.
        • Sulaiman I.
        • Fayer R.
        • et al.
        Species and strain-specific typing of Cryptosporidium parasites in clinical and environmental samples.
        Mem Inst Oswaldo Cruz. 1998; 93: 687-691
        • Morgan U.
        • Xiao L.
        • Sulaiman I.
        • et al.
        Which genotypes/species of Cryptosporidium are humans susceptible to?.
        J Eukaryot Microbiol. 1999; 46: 42S-43S
        • Morgan U.M.
        • Xiao L.
        • Fayer R.
        • et al.
        Variation in Cryptosporidium: towards a taxonomic revision of the genus.
        Int J Parasitol. 1999; 29: 1733-1751
        • Morgan U.M.
        • Xiao L.
        • Fayer R.
        • et al.
        Epidemiology and strain variation of Cryptosporidium parvum.
        Contrib Microbiol. 2000; 6: 116-139
        • Xiao L.
        • Morgan U.M.
        • Fayer R.
        • et al.
        Cryptosporidium systematics and implications for public health.
        Parasitol Today. 2000; 16: 287-292
        • Ryan U.
        • Fayer R.
        • Xiao L.
        Cryptosporidium species in humans and animals: current understanding and research needs.
        Parasitology. 2014; 141: 1667-1685
        • Santin M.
        • Trout J.M.
        • Xiao L.
        • et al.
        Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves.
        Vet Parasitol. 2004; 122: 103-117
        • Valenzuela O.
        • Gonzalez-Diaz M.
        • Garibay-Escobar A.
        • et al.
        Molecular characterization of Cryptosporidium spp. in children from Mexico.
        PLoS One. 2014; 9: e96128
        • Tzipori S.
        • Widmer G.
        The biology of Cryptosporidium.
        Contrib Microbiol. 2000; 6: 1-32
        • Rosales M.J.
        • Cordon G.P.
        • Moreno M.S.
        • et al.
        Extracellular like-gregarine stages of Cryptosporidium parvum.
        Acta Trop. 2005; 95: 74-78
        • Petry F.
        Structural analysis of Cryptosporidium parvum.
        Microsc Microanal. 2004; 10: 586-601
        • Hijjawi N.S.
        • Meloni B.P.
        • Ryan U.M.
        • et al.
        Successful in vitro cultivation of Cryptosporidium andersoni: evidence for the existence of novel extracellular stages in the life cycle and implications for the classification of Cryptosporidium.
        Int J Parasitol. 2002; 32: 1719-1726
        • Fayer R.
        General biology.
        in: Fayer R. Xiao L. Cryptosporidium and cryptosporidiosis. CRC press, Boca Raton (FL)2008: 1-42
        • Caccio S.
        • Putignani L.
        Epidemiology of human cryptosporidiosis.
        in: Caccio S. Widmer G. Cryptosporidium parasite and disease. Springer, Wien, Austria2014: 43-78
      3. Assessing the public health threat associated with waterborne cryptosporidiosis: report of a workshop.
        MMWR Recomm Rep. 1995; 44: 1-19
        • Centers for Disease Control and Prevention
        Foodborne outbreak of cryptosporidiosis–Spokane, Washington, 1997.
        MMWR Morb Mortal Wkly Rep. 1998; 47: 565-567
        • Rose J.B.
        • Slifko T.R.
        Giardia, Cryptosporidium, and Cyclospora and their impact on foods: a review.
        J Food Prot. 1999; 62: 1059-1070
        • Ortega Y.R.
        • Roxas C.R.
        • Gilman R.H.
        • et al.
        Isolation of Cryptosporidium parvum and Cyclospora cayetanensis from vegetables collected in markets of an endemic region in Peru.
        Am J Trop Med Hyg. 1997; 57: 683-686
        • Koch K.L.
        • Phillips D.J.
        • Aber R.C.
        • et al.
        Cryptosporidiosis in hospital personnel. Evidence for person-to-person transmission.
        Ann Intern Med. 1985; 102: 593-596
        • Navin T.R.
        Cryptosporidiosis in humans: review of recent epidemiologic studies.
        Eur J Epidemiol. 1985; 1: 77-83
        • Xiao L.
        • Ryan U.
        Molecular epidemiology.
        in: Fayer R. Xiao L. Cryptosporidium and cryptosporidiosis. CRC Press, and IWA Publishing, Boca Raton (FL)2008: 119-171
        • Xiao L.
        Molecular epidemiology of cryptosporidiosis: an update.
        Exp Parasitol. 2010; 124: 80-89
        • Yoder J.S.
        • Beach M.J.
        • Centers for Disease Control and Prevention
        • et al.
        Cryptosporidiosis surveillance–United States, 2003-2005.
        MMWR Surveill Summ. 2007; 56: 1-10
        • Yoder J.S.
        • Harral C.
        • Beach M.J.
        • et al.
        Cryptosporidiosis surveillance - United States, 2006-2008.
        MMWR Surveill Summ. 2010; 59: 1-14
        • Yoder J.S.
        • Wallace R.M.
        • Collier S.A.
        • et al.
        Cryptosporidiosis surveillance–United States, 2009-2010.
        MMWR Surveill Summ. 2012; 61: 1-12
        • Ortega Y.
        • Cama V.
        Foodborne transmission.
        in: Fayer R. Xiao L. Cryptosporidium and cryptosporidiosis. CRC Press and IWA Publishing, Boca Raton (FL)2008: 289-304
        • Blackburn B.G.
        • Mazurek J.M.
        • Hlavsa M.
        • et al.
        Cryptosporidiosis associated with ozonated apple cider.
        Emerg Infect Dis. 2006; 12: 684-686
        • Cama V.A.
        • Bern C.
        • Roberts J.
        • et al.
        Cryptosporidium species and subtypes and clinical manifestations in children, Peru.
        Emerg Infect Dis. 2008; 14: 1567-1574
        • Soave R.
        Cryptosporidiosis and isosporiasis in patients with AIDS.
        Infect Dis Clin North Am. 1988; 2: 485-493
      4. New drug for parasitic infections in children.
        FDA Consum. 2003; 37: 4
        • White Jr., C.A.
        Nitazoxanide: a new broad spectrum antiparasitic agent.
        Expert Rev Anti Infect Ther. 2004; 2: 43-49
      5. DPDx. DPDx [Web page]. Parasite diagnosis. 2013. Available at: http://www.cdc.gov/dpdx/cryptosporidiosis/dx.html. Accessed December 20, 2014.

      6. Catalog of cleared and approved medical device information from FDA. 2014. Database of approved in-vitro diagnostic devices. Available at: http://www.accessdata.fda.gov/scripts/cdrh/devicesatfda/index.cfm. Accessed October 20, 2014.

        • Xiao L.
        • Lal A.A.
        • Jiang J.
        Detection and differentiation of Cryptosporidium oocysts in water by PCR-RFLP.
        Methods Mol Biol. 2004; 268: 163-176
        • Ashford R.W.
        Occurrence of an undescribed coccidian in man in Papua New Guinea.
        Ann Trop Med Parasitol. 1979; 73: 497-500
        • Relman D.A.
        • Schmidt T.M.
        • Gajadhar A.
        • et al.
        Molecular phylogenetic analysis of Cyclospora, the human intestinal pathogen, suggests that it is closely related to Eimeria species.
        J Infect Dis. 1996; 173: 440-445
        • Pieniazek N.J.
        • Herwaldt B.L.
        Reevaluating the molecular taxonomy: is human-associated Cyclospora a mammalian Eimeria species?.
        Emerg Infect Dis. 1997; 3: 381-383
        • Franzen C.
        • Muller A.
        • Bialek R.
        • et al.
        Taxonomic position of the human intestinal protozoan parasite Isospora belli as based on ribosomal RNA sequences.
        Parasitol Res. 2000; 86: 669-676
        • Eberhard M.L.
        • Njenga M.N.
        • DaSilva A.J.
        • et al.
        A survey for Cyclospora spp. in Kenyan primates, with some notes on its biology.
        J Parasitol. 2001; 87: 1394-1397
        • Eberhard M.L.
        • Ortega Y.R.
        • Hanes D.E.
        • et al.
        Attempts to establish experimental Cyclospora cayetanensis infection in laboratory animals.
        J Parasitol. 2000; 86: 577-582
        • Ortega Y.R.
        • Nagle R.
        • Gilman R.H.
        • et al.
        Pathologic and clinical findings in patients with cyclosporiasis and a description of intracellular parasite life-cycle stages.
        J Infect Dis. 1997; 176: 1584-1589
        • Ortega Y.R.
        • Gilman R.H.
        • Sterling C.R.
        A new coccidian parasite (Apicomplexa: Eimeriidae) from humans.
        J Parasitol. 1994; 80: 625-629
        • Ortega Y.R.
        • Sterling C.R.
        • Gilman R.H.
        Cyclospora cayetanensis.
        Adv Parasitol. 1998; 40: 399-418
        • Bern C.
        • Ortega Y.
        • Checkley W.
        • et al.
        Epidemiologic differences between cyclosporiasis and cryptosporidiosis in Peruvian children.
        Emerg Infect Dis. 2002; 8: 581-585
        • Sherchand J.B.
        • Cross J.H.
        Emerging pathogen Cyclospora cayetanensis infection in Nepal.
        Southeast Asian J Trop Med Public Health. 2001; 32: 143-150
        • Huang P.
        • Weber J.T.
        • Sosin D.M.
        • et al.
        The first reported outbreak of diarrheal illness associated with Cyclospora in the United States.
        Ann Intern Med. 1995; 123: 409-414
        • Torres-Slimming P.A.
        • Mundaca C.C.
        • Moran M.
        • et al.
        Outbreak of cyclosporiasis at a naval base in Lima, Peru.
        Am J Trop Med Hyg. 2006; 75: 546-548
        • Pape J.W.
        • Verdier R.I.
        • Boncy M.
        • et al.
        Cyclospora infection in adults infected with HIV. Clinical manifestations, treatment, and prophylaxis.
        Ann Intern Med. 1994; 121: 654-657
        • Hoge C.W.
        • Shlim D.R.
        • Ghimire M.
        • et al.
        Placebo-controlled trial of co-trimoxazole for Cyclospora infections among travellers and foreign residents in Nepal.
        Lancet. 1995; 345: 691-693
        • Frenkel J.K.
        Besnoitia wallacei of cats and rodents: with a reclassification of other cyst-forming isosporoid coccidia.
        J Parasitol. 1977; 63: 611-628
        • Barta J.R.
        • Schrenzel M.D.
        • Carreno R.
        • et al.
        The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals.
        J Parasitol. 2005; 91: 726-727
        • Lindsay D.S.
        • Dubey J.P.
        • Blagburn B.L.
        Biology of Isospora spp. from humans, nonhuman primates, and domestic animals.
        Clin Microbiol Rev. 1997; 10: 19-34
        • Marshall M.M.
        • Naumovitz D.
        • Ortega Y.
        • et al.
        Waterborne protozoan pathogens.
        Clin Microbiol Rev. 1997; 10: 67-85
        • Certad G.
        • Arenas-Pinto A.
        • Pocaterra L.
        • et al.
        Isosporiasis in Venezuelan adults infected with human immunodeficiency virus: clinical characterization.
        Am J Trop Med Hyg. 2003; 69: 217-222
        • Cranendonk R.J.
        • Kodde C.J.
        • Chipeta D.
        • et al.
        Cryptosporidium parvum and Isospora belli infections among patients with and without diarrhoea.
        East Afr Med J. 2003; 80: 398-401
        • Sorvillo F.J.
        • Lieb L.E.
        • Seidel J.
        • et al.
        Epidemiology of isosporiasis among persons with acquired immunodeficiency syndrome in Los Angeles County.
        Am J Trop Med Hyg. 1995; 53: 656-659
        • Modigliani R.
        • Bories C.
        • Le Charpentier Y.
        • et al.
        Diarrhoea and malabsorption in acquired immune deficiency syndrome: a study of four cases with special emphasis on opportunistic protozoan infestations.
        Gut. 1985; 26: 179-187
        • Pape J.W.
        • Johnson Jr., W.D.
        Isospora belli infections.
        Prog Clin Parasitol. 1991; 2: 119-127
        • Adam R.D.
        Biology of Giardia lamblia.
        Clin Microbiol Rev. 2001; 14: 447-475
        • Guerrant R.L.
        • Hughes J.M.
        • Lima N.L.
        • et al.
        Diarrhea in developed and developing countries: magnitude, special settings, and etiologies.
        Rev Infect Dis. 1990; 12: S41-S50
        • Yoder J.S.
        • Gargano J.W.
        • Wallace R.M.
        • et al.
        Giardiasis surveillance–United States, 2009-2010.
        MMWR Surveill Summ. 2012; 61: 13-23
        • Yoder J.S.
        • Harral C.
        • Beach M.J.
        • et al.
        Giardiasis surveillance - United States, 2006-2008.
        MMWR Surveill Summ. 2010; 59: 15-25
        • Thompson R.C.
        • Monis P.
        Giardia–from genome to proteome.
        Adv Parasitol. 2012; 78: 57-95
        • Ryan U.
        • Caccio S.M.
        Zoonotic potential of Giardia.
        Int J Parasitol. 2013; 43: 943-956
        • Feng Y.
        • Xiao L.
        Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.
        Clin Microbiol Rev. 2011; 24: 110-140
        • Monis P.T.
        • Caccio S.M.
        • Thompson R.C.
        Variation in Giardia: towards a taxonomic revision of the genus.
        Trends Parasitol. 2009; 25: 93-100
        • Nundy S.
        • Gilman R.H.
        • Xiao L.
        • et al.
        Wealth and its associations with enteric parasitic infections in a low-income community in Peru: use of principal component analysis.
        Am J Trop Med Hyg. 2011; 84: 38-42
        • Cotte L.
        • Rabodonirina M.
        • Piens M.A.
        • et al.
        Prevalence of intestinal protozoans in French patients infected with HIV.
        J Acquir Immune Defic Syndr. 1993; 6: 1024-1029
        • Berkman D.S.
        • Lescano A.G.
        • Gilman R.H.
        • et al.
        Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study.
        Lancet. 2002; 359: 564-571
        • Kulakova L.
        • Galkin A.
        • Chen C.Z.
        • et al.
        Discovery of novel antigiardiasis drug candidates.
        Antimicrob Agents Chemother. 2014; 58: 7303-7311
        • Garcia L.S.
        • Shimizu R.Y.
        Evaluation of nine immunoassay kits (enzyme immunoassay and direct fluorescence) for detection of Giardia lamblia and Cryptosporidium parvum in human fecal specimens.
        J Clin Microbiol. 1997; 35: 1526-1529
        • Heyworth M.F.
        Diagnostic testing for Giardia infections.
        Trans R Soc Trop Med Hyg. 2014; 108: 123-125
        • Taniuchi M.
        • Verweij J.J.
        • Sethabutr O.
        • et al.
        Multiplex polymerase chain reaction method to detect Cyclospora, Cystoisospora, and Microsporidia in stool samples.
        Diagn Microbiol Infect Dis. 2011; 71: 386-390
        • Khare R.
        • Espy M.J.
        • Cebelinski E.
        • et al.
        Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens.
        J Clin Microbiol. 2014; 52: 3667-3673