Review Article | Published:

Beyond O&P Times Three

The American Journal of Gastroenterologyvolume 113pages805818 (2018) | Download Citation

Subjects

Abstract

Although examination of the stool for ova and parasites times three (O&P ×3) is routinely performed in the United States (US) for the evaluation of persistent and/or chronic diarrhea, the result is almost always negative. This has contributed to the perception that parasitic diseases are nearly non-existent in the country unless there is a history of travel to an endemic area. The increasing number of immigrants from third-world countries, tourists, and students who present with symptoms of parasitic diseases are often misdiagnosed as having irritable bowel syndrome or inflammatory bowel disease. The consequences of such misdiagnosis need no explanation. However, certain parasitic diseases are endemic to the US and other developed nations and affect both immunocompetent and immunocompromised patients. Testing for parasitic diseases either with O&P or with other diagnostic tests, followed by the recommended treatment, is quite rewarding when appropriate. Most parasitic diseases are easily treatable and should not be confused with other chronic gastrointestinal (GI) disorders. In this review, we critically evaluate the symptomatology of luminal parasitic diseases, their differential diagnoses, appropriate diagnostic tests, and management.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    McHardy IH, Wu M, Shimizu-Cohen R, et al. Detection of intestinal protozoa in the clinical laboratory. J Clin Microbiol. 2014;52:712–20.

  2. 2.

    Branda JA, Lin TY, Rosenberg ES, et al. A rational approach to the stool ova and parasite examination. Clin Infect Dis. 2006;42:972–8.

  3. 3.

    Morris AJ, Wilson ML, Reller LB. Application of rejection criteria for stool ovum and parasite examinations. J Clin Microbiol. 1992;30:3213–6.

  4. 4.

    Polage CR, Stoddard GJ, Rolfs RT, et al. Physician use of parasite tests in the United States from 1997 to 2006 and in a Utah Cryptosporidium outbreak in 2007. J Clin Microbiol. 2011;49:591–6.

  5. 5.

    Cartwright CP. Utility of multiple-stool-specimen ova and parasite examinations in a high-prevalence setting. J Clin Microbiol. 1999;37:2408–11.

  6. 6.

    Senay H, MacPherson D. Parasitology: diagnostic yield of stool examination. CMAJ. 1989;140:1329–31.

  7. 7.

    Gyorkos TW, MacLean JD, Law CG. Absence of significant differences in intestinal parasite prevalence estimates after examination of either one or two stool specimens. Am J Epidemiol. 1989;130:976–80.

  8. 8.

    Valenstein P, Pfaller M, Yungbluth M. The use and abuse of routine stool microbiology: a College of American Pathologists Q-probes study of 601 institutions. Arch Pathol Lab Med. 1996;120:206–11.

  9. 9.

    Verweij JJ, Blange RA, Templeton K, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42:1220–3.

  10. 10.

    Fletcher SM, Stark D, Harkness J, et al. Enteric protozoa in the developed world: a public health perspective. Clin Microbiol Rev. 2012;25:420–49.

  11. 11.

    Valenzuela O, Moran P, Gomez A, et al. Epidemiology of amoebic liver abscess in Mexico: the case of Sonora. Ann Trop Med Parasitol. 2007;101:533–8.

  12. 12.

    Freedman DO, Weld LH, Kozarsky PE, Fisk T, Robins R, von Sonnenburg F, Keystone JS, Pandey P, Cetron MS, GeoSentinel Surveillance Network. Spectrum of disease and relation to place of exposure among ill returned travelers. N Engl J Med. 2006;354:119–30.

  13. 13.

    Hung CC, Chang SY, Ji DD. Entamoeba histolytica infection in men who have sex with men. Lancet Infect Dis. 2012;12:729–36.

  14. 14.

    Stanley SL Jr.. Amoebiasis. Lancet. 2003;361:1025–34.

  15. 15.

    Haque R, Mondal D, Duggal P, Kabir M, Roy S, Farr BM, Sack RB, Petri WA Jr.. Entamoeba histolytica infection in children and protection from subsequent amebiasis. Infect Immun. 2006;74:904–9.

  16. 16.

    Haque R, Huston CD, Hughes M, et al. Amebiasis. N Engl J Med. 2003;348:1565–73.

  17. 17.

    Haque R, Mollah NU, Ali IK, Alam K, Eubanks A, Lyerly D, Petri WA Jr. Diagnosis of amebic liver abscess and intestinal infection with the TechLab Entamoeba histolytica II antigen detection and antibody tests. J Clin Microbiol. 2000;38:3235–9.

  18. 18.

    Hechenbleikner EM, McQuade JA. Parasitic colitis. Clin Colon Rectal Surg. 2015;28:79–86.

  19. 19.

    Shirley DA, Moonah S. Fulminant amebic colitis after corticosteroid therapy: a systematic review. PLOS Negl Trop Dis. 2016;10:e0004879.

  20. 20.

    Blessmann J, Tannich E. Treatment of asymptomatic intestinal Entamoeba histolytica infection. N Engl J Med. 2002;347:1384.

  21. 21.

    Gonzales ML, Dans LF, Martinez EG. Antiamoebic drugs for treating amoebic colitis. Cochrane Database Syst Rev 2009;2:CD006085.

  22. 22.

    Esteban JG, Aguirre C, Angles R, Ash LR, Mas-Coma S. Balantidiasis in Aymara children from the northern Bolivian Altiplano. Am J Trop Med Hyg. 1998;59:922–7.

  23. 23.

    Schuster FL, Ramirez-Avila L. Current world status of Balantidium coli. Clin Microbiol Rev. 2008;21:626–38.

  24. 24.

    Ladas SD, Savva S, Frydas A, Kaloviduris A, Hatzioannou J, Raptis S. Invasive balantidiasis presented as chronic colitis and lung involvement. Dig Dis Sci. 1989;34:1621–3.

  25. 25.

    Stenzel DJ, Boreham PF. Blastocystis hominis revisited. Clin Microbiol Rev. 1996;9:563–84.

  26. 26.

    Coyle CM, Varughese J, Weiss LM, Tanowitz HB. Blastocystis: to treat or not to treat. Clin Infect Dis. 2012;54:105–10.

  27. 27.

    Tan KS, Mirza H, Teo JD, Wu B, Macary PA. Current views on the clinical relevance of Blastocystis spp. Curr Infect Dis Rep. 2010;12:28–35.

  28. 28.

    Kukoschke KG, Necker A, Müller HE. Detection of Blastocystis hominis by direct microscopy and culture. Eur J Clin Microbiol Infect Dis. 1990;9:305–7.

  29. 29.

    Chen XM, Keithly JS, Paya CV, et al. Cryptosporidiosis. N Engl J Med. 2002;346:1723–31.

  30. 30.

    MacKenzie WR, Schell WL, Blair KA, Addiss DG, Peterson DE, Hoxie NJ, Kazmierczak JJ, Davis JP. Massive outbreak of waterborne cryptosporidium infection in Milwaukee, Wisconsin: recurrence of illness and risk of secondary transmission. Clin Infect Dis. 1995;21:57–62.

  31. 31.

    Shrivastava AK, Kumar S, Smith WA, et al. Revisiting the global problem of cryptosporidiosis and recommendations. Trop Parasitol. 2017;7:8–17.

  32. 32.

    Garcia LS, Shimizu RY. 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;35:1526–9.

  33. 33.

    Rossignol JF, Kabil SM, el-Gohary Y, et al. Effect of nitazoxanide in diarrhea and enteritis caused by Cryptosporidium species. Clin Gastroenterol Hepatol. 2006;4:320–4.

  34. 34.

    Masur H, Brooks JT, Benson CA, et al. Prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Updated Guidelines from the Centers for Disease Control and Prevention, National Institutes of Health, and HIV Medicine Association of the Infectious Diseases Society of America. Clin Infect Dis. 2014;58:1308–11.

  35. 35.

    Abanyie F, Harvey RR, Harris JR, et al. 2013 multistate outbreaks of Cyclospora cayetanensis infections associated with fresh produce: focus on the Texas investigations. Epidemiol Infect. 2015;143:3451–8.

  36. 36.

    Hall RL, Jones JL, Herwaldt BL. Surveillance for laboratory-confirmed sporadic cases of cyclosporiasis—United States, 1997–2008. MMWR Surveill Summ. 2011;60:1–11.

  37. 37.

    Ortega YR, Sanchez R. Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clin Microbiol Rev. 2010;23:218–34.

  38. 38.

    Richardson RF Jr, Remler BF, Katirji B, Murad MH. Guillain-Barre syndrome after Cyclospora infection. Muscle Nerve. 1998;21:669–71.

  39. 39.

    Connor BA, Johnson E, Soave R. Reiter syndrome following protracted symptoms of Cyclospora infection. Emerg Infect Dis. 2001;7:453–4.

  40. 40.

    Murphy HR, Cinar HN, Gopinath G, et al. Interlaboratory validation of an improved method for detection of Cyclospora cayetanensis in produce using a real-time PCR assay. Food Microbiol. 2018;69:170–8.

  41. 41.

    Legua P, Seas C. Cystoisospora and cyclospora. Curr Opin Infect Dis. 2013;26:479–83.

  42. 42.

    Franzen C, Müller A, Salzberger B, Hartmann P, Diehl V, Fätkenheuer G. Uvitex 2B stain for the diagnosis of Isospora belli infections in patients with the acquired immunodeficiency syndrome. Arch Pathol Lab Med. 1996;120:1023–5.

  43. 43.

    Pacheco FT, Silva RK, Martins AS, Oliveira RR, Alcântara-Neves NM, Silva MP, Soares NM, Teixeira MC. Differences in the detection of Cryptosporidium and Isospora (Cystoisospora) oocysts according to the fecal concentration or staining method used in a clinical laboratory. J Parasitol. 2013;99:1002–8.

  44. 44.

    Garcia LS. Dientamoeba fragilis, one of the neglected intestinal protozoa. J Clin Microbiol. 2016;54:2243–50.

  45. 45.

    Barratt JL, Harkness J, Marriott D, Ellis JT, Stark D. A review of Dientamoeba fragilis carriage in humans: several reasons why this organism should be considered in the diagnosis of gastrointestinal illness. Gut Microbes. 2011;2:3–12.

  46. 46.

    Stark D, Barratt J, Chan D, et al. Dientamoeba fragilis, the neglected trichomonad of the human bowel. Clin Microbiol Rev. 2016;29:553–80.

  47. 47.

    Minetti C, Chalmers RM, Beeching NJ, et al. Giardiasis. BMJ. 2016;355:i5369.

  48. 48.

    CDC–National Centre for Health Statistics. Parasites—Giardia. 2015; https://www.cdc.gov/parasites/giardia/infection-sources.html.

  49. 49.

    Albuquerque A. Nodular lymphoid hyperplasia in the gastrointestinal tract in adult patients: a review. World J Gastrointest Endosc. 2014;6:534–40.

  50. 50.

    Soares R, Tasca T. Giardiasis: an update review on sensitivity and specificity of methods for laboratorial diagnosis. J Microbiol Methods. 2016;129:98–102.

  51. 51.

    Field AS, Milner DA Jr. Intestinal microsporidiosis. Clin Lab Med. 2015;35:445–59.

  52. 52.

    Ramanan P, Pritt BS. Extraintestinal microsporidiosis. J Clin Microbiol. 2014;52:3839–44.

  53. 53.

    Rassi A Jr., Rassi A, Marin-Neto JA. Chagas disease. Lancet. 2010;375:1388–402.

  54. 54.

    CDC–National Centre for Health Statistics. Parasites—American Trypanosomiasis (also known as Chagas Disease). 2014; https://www.cdc.gov/parasites/chagas/diagnosis.html. Accessed 2June, 2014.

  55. 55.

    Bern C. Chagas’ disease. N Engl J Med. 2015;373:456–66.

  56. 56.

    Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32.

  57. 57.

    Holcombe C. Surgical emergencies in tropical gastroenterology. Gut. 1995;36:9–11.

  58. 58.

    Khuroo MS, Rather AA, Khuroo NS, et al. Hepatobiliary and pancreatic ascariasis. World J Gastroenterol. 2016;22:7507–17.

  59. 59.

    Limsrivilai J, Pongprasobchai S, Apisarnthanarak P, et al. Intestinal capillariasis in the 21st century: clinical presentations and role of endoscopy and imaging. BMC Gastroenterol. 2014;14:207.

  60. 60.

    Cross JH. Intestinal capillariasis. Clin Microbiol Rev. 1992;5:120–9.

  61. 61.

    Lohiya GS, Tan-Figueroa L, Crinella FM, et al. Epidemiology and control of enterobiasis in a developmental center. West J Med. 2000;172:305–8.

  62. 62.

    Cook GC. Enterobius vermicularis infection. Gut. 1994;35:1159–62.

  63. 63.

    Sun T, Schwartz NS, Sewell C, et al. Enterobius egg granuloma of the vulva and peritoneum: review of the literature. Am J Trop Med Hyg. 1991;45:249–53.

  64. 64.

    Stoltzfus RJ, Dreyfuss ML, Chwaya HM, et al. Hookworm control as a strategy to prevent iron deficiency. Nutr Rev. 1997;55:223–32.

  65. 65.

    CDC–National Centre for Health Statistics. Parasites—Hookworm. 2013; https://www.cdc.gov/parasites/hookworm/disease.html.

  66. 66.

    Williamson AL, Brindley PJ, Knox DP, et al. Digestive proteases of blood-feeding nematodes. Trends Parasitol. 2003;19:417–23.

  67. 67.

    Hotez PJ, Brooker S, Bethony JM, et al. Hookworm infection. N Engl J Med. 2004;351:799–807.

  68. 68.

    Horton J. Albendazole: a review of anthelmintic efficacy and safety in humans. Parasitology. 2000;121:Suppl:S113–32.

  69. 69.

    Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010;23:500–4.

  70. 70.

    Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28:549–65.

  71. 71.

    Ramanathan R, Nutman T. Strongyloides stercoralis infection in the immunocompromised host. Curr Infect Dis Rep. 2008;10:105–10.

  72. 72.

    CDC–National Centre for Health Statistics. Parasites—Strongyloides. 2013; https://www.cdc.gov/parasites/strongyloides/disease.html.

  73. 73.

    Kassalik M, Monkemuller K. Strongyloides stercoralis hyperinfection syndrome and disseminated disease. Gastroenterol Hepatol (N Y). 2011;7:766–8.

  74. 74.

    Mendes T, Minori K, Ueta M. Strongyloidiasis current status with emphasis in diagnosis and drug research. J Parasitol Res. 2017;2017:5056314.

  75. 75.

    Ramanathan R, Burbelo PD, Groot S, et al. A luciferase immunoprecipitation systems assay enhances the sensitivity and specificity of diagnosis of Strongyloides stercoralis infection. J Infect Dis. 2008;198:444–51.

  76. 76.

    Choudhry U, Choudhry R, Romeo DP, et al. Strongyloidiasis: new endoscopic findings. Gastrointest Endosc. 1995;42:170–3.

  77. 77.

    Thompson BF, Fry LC, Wells CD, et al. The spectrum of GI strongyloidiasis: an endoscopic-pathologic study. Gastrointest Endosc. 2004;59:906–10.

  78. 78.

    Elbaz T, Esmat G. Hepatic and intestinal schistosomiasis: review. J Adv Res. 2013;4:445–52.

  79. 79.

    Tsang VC, Wilkins PP. Immunodiagnosis of schistosomiasis. Immunol Invest. 1997;26:175–88.

  80. 80.

    Gray DJ, Ross AG, Li YS, et al. Diagnosis and management of schistosomiasis. BMJ. 2011;342:d2651.

  81. 81.

    Lightowlers MW, Garcia HH, Gauci CG, et al. Monitoring the outcomes of interventions against Taenia solium: options and suggestions. Parasite Immunol. 2016;38:158–69.

  82. 82.

    Guezala MC, Rodriguez S, Zamora H, et al. Development of a species-specific coproantigen ELISA for human Taenia solium taeniasis. Am J Trop Med Hyg. 2009;81:433–7.

  83. 83.

    Jourdan PM, Lamberton PHL, Fenwick A, et al. Soil-transmitted helminth infections. Lancet 2017;391:252–65.

  84. 84.

    Hotez PJ, Molyneux DH, Fenwick A, et al. Control of neglected tropical diseases. N Engl J Med. 2007;357:1018–27.

  85. 85.

    Scholz T, Garcia HH, Kuchta R, et al. Update on the human broad tapeworm (genus diphyllobothrium), including clinical relevance. Clin Microbiol Rev. 2009;22:146–60.

  86. 86.

    CDC–National Centre for Health Statistics. Parasites—Hymenolepiasis (also known as Hymenolepis nana infection) 2016; https://www.cdc.gov/parasites/hymenolepis/faqs.html.

  87. 87.

    Ross AG, Olds GR, Cripps AW, et al. Enteropathogens and chronic illness in returning travelers. N Engl J Med. 2013;368:1817–25.

  88. 88.

    Ross AG, Bartley PB, Sleigh AC, et al. Schistosomiasis. N Engl J Med. 2002;346:1212–20.

  89. 89.

    Okello AL, Thomas LF. Human taeniasis: current insights into prevention and management strategies in endemic countries. Risk Manag Healthc Policy. 2017;10:107–16.

  90. 90.

    Gottstein B, Pozio E, Nockler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev. 2009;22:127–45.

  91. 91.

    Stephenson LS, Holland CV, Cooper ES. The public health significance of Trichuris trichiura. Parasitology. 2000;121:Suppl:S73–95.

  92. 92.

    Tanyuksel M, Petri WA Jr.. Laboratory diagnosis of amebiasis. Clin Microbiol Rev. 2003;16:713–29.

  93. 93.

    Stensvold R, Brillowska-Dabrowska A, Nielsen HV, et al. Detection of Blastocystis hominis in unpreserved stool specimens by using polymerase chain reaction. J Parasitol. 2006;92:1081–7.

  94. 94.

    ten Hove RJ, Verweij JJ, Vereecken K, et al. Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans R Soc Trop Med Hyg. 2008;102:179–85.

  95. 95.

    Verweij JJ, Canales M, Polman K, et al. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg. 2009;103:342–6.

Download references

Author information

Affiliations

  1. Department of Internal Medicine, Saint Peter’s University Hospital – Rutgers Robert Wood Johnson School of Medicine, New Brunswick, NJ, USA

    • Sonmoon Mohapatra MD
    •  & Dhruv Pratap Singh MBBS
  2. Department of Infectious Diseases, Saint Peter’s University Hospital – Rutgers Robert Wood Johnson School of Medicine, New Brunswick, NJ, USA

    • David Alcid MD
  3. Department of Gastroenterology, Hepatology and Clinical Nutrition Saint Peter’s University Hospital – Rutgers Robert Wood Johnson School of Medicine, New Brunswick, NJ, USA

    • Capecomorin S Pitchumoni MD

Authors

  1. Search for Sonmoon Mohapatra MD in:

  2. Search for Dhruv Pratap Singh MBBS in:

  3. Search for David Alcid MD in:

  4. Search for Capecomorin S Pitchumoni MD in:

Guarantor of the article

Dr. C.S. Pitchumoni, MD.

Specific author contributions

SM wrote the paper with the help of other co-authors. DPS analyzed the literature for the tables. DA reviewed the paper for scientific accuracy. CSP formulated the idea, structure and the content for the paper.

Financial support

None.

Potential competing interests

None.

Corresponding author

Correspondence to Capecomorin S Pitchumoni MD.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41395-018-0083-y