Clinical consequences of polymerase chain reaction-based diagnosis of intestinal parasitic infections

Journal of Gastroenterology and Hepatology (Australia)

Volumn 31, Issue 11, 2016, Pages 1808-1815

  Rijsman, Lucas H ^a   Monkelbaan, Jan F ^a   Kusters, Johannes G ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

clinical intestinal disorders; diarrhea; ELISA; intestinal protozoa; microbial pathogenesis; microscopy; PCR based diagnostics; point of care; polymerase chain reaction

Indexed keywords

DIAGNOSTIC PROCEDURE; FOLLOW UP; HUMAN; INTESTINE INFECTION; INTESTINE PARASITE; PARASITOSIS; POINT OF CARE TESTING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTOZOON; REVIEW; STANDARDIZATION; POINT OF CARE SYSTEM; PREVALENCE; PROCEDURES; PROTOZOAL INFECTION; SENSITIVITY AND SPECIFICITY;

HUMANS; INTESTINAL DISEASES, PARASITIC; POINT-OF-CARE SYSTEMS; POLYMERASE CHAIN REACTION; PREVALENCE; PROTOZOAN INFECTIONS; SENSITIVITY AND SPECIFICITY;

EID: 84996565838     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.13412     Document Type: Review

References (78)

1. Hanevik K, Wensaas K-A, Rortveit G et al. Irritable bowel syndrome and chronic fatigue 6 years after Giardia infection: a controlled prospective cohort study. Clin. Infect. Dis. 2014; 59: 1394–1400.
2. Halliez MCM, Buret AG. Extra-intestinal and long term consequences of Giardia duodenalis infections. World J. Gastroenterol. 2013; 19: 8974–8985.
3. Stark D, van Hal S, Marriott D et al. Irritable bowel syndrome: a review on the role of intestinal protozoa and the importance of their detection and diagnosis. Int. J. Parasitol. 2007; 37: 11–20.
4. Report of the Director-General. The world health report 1998: Life in the 21st century, a vision for all. Geneva: World Health Organization; 1998.
5. de Wit MAS. Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am. J. Epidemiol. 2001; 154: 666–674.
6. Hellard ME, Sinclair MI, Hogg GG et al. Prevalence of enteric pathogens among community based asymptomatic individuals. J. Gastroenterol. Hepatol. 2000; 15: 290–293.
7. Amin OM. Seasonal prevalence of intestinal parasites in the United States during 2000. Am. J. Trop. Med. Hyg. 2002; 66: 799–803.
8. ten Hove RJ, van Esbroeck M, Vervoort T et al. Molecular diagnostics of intestinal parasites in returning travellers. Eur. J. Clin. Microbiol. Infect. Dis. 2009; 28: 1045–1053.
9. Kappus KD, Lundgren RG, Juranek DD et al. Intestinal parasitism in the United States: update on a continuing problem. Am. J. Trop. Med. Hyg. 1994; 50: 705–713.
10. Bruijnesteijn van Coppenraet LES, Wallinga JA, Ruijs GJHM et al. 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. Clin. Microbiol. Infect. 2009; 15: 869–874.
11. Stensvold CR, Nielsen HV, Mølbak K et al. Pursuing the clinical significance of Blastocystis—diagnostic limitations. Trends Parasitol. 2009; 25: 23–29.
12. Röser D, Simonsen J, Nielsen HV et al. Dientamoeba fragilis in Denmark: epidemiological experience derived from four years of routine real-time PCR. Eur. J. Clin. Microbiol. Infect. Dis. 2013; 32: 1303–1310.
13. Stanley SL. Amoebiasis. Lancet 2003; 361: 1025–1034.
14. Shirley D-AT, Moonah SN, Kotloff KL. Burden of disease from cryptosporidiosis. Curr. Opin. Infect. Dis. 2012; 25: 555–563.
15. Robertson LJ, Hanevik K, Escobedo AA et al. Giardiasis—why do the symptoms sometimes never stop? Trends Parasitol. 2010; 26: 75–82.
16. McHardy IH, Wu M, Shimizu-Cohen R et al. Detection of intestinal protozoa in the clinical laboratory. J. Clin. Microbiol. 2014; 52: 712–720.
17. Svraka-Latifovic S, Bouter S, Naus H et al. Impact of transition from microscopy to molecular screening for detection of intestinal protozoa in Dutch patients. Clin. Microbiol. Infect. 2014; 20: O969–971.
18. Schuurman T, Lankamp P, van Belkum A et al. Comparison of microscopy, real-time PCR and a rapid immunoassay for the detection of Giardia lamblia in human stool specimens. Clin. Microbiol. Infect. 2007; 13: 1186–1191.
19. Roberts T, Barratt J, Harkness J et al. Comparison of microscopy, culture, and conventional polymerase chain reaction for detection of Blastocystis sp. in clinical stool samples. Am. J. Trop. Med. Hyg. 2011; 84: 308–312.
20. Boadi S, Polley SD, Kilburn S et al. A critical assessment of two real-time PCR assays targeting the (SSU) rRNA and GDH genes for the molecular identification of Giardia intestinalis in a clinical laboratory. J. Clin. Pathol. 2014; 67: 811–816.
21. Elsafi SH, Al-Maqati TN, Hussein MI et al. Comparison of microscopy, rapid immunoassay, and molecular techniques for the detection of Giardia lamblia and Cryptosporidium parvum. Parasitol. Res. 2013; 112: 1641–1646.
22. ten Hove R, Schuurman T, Kooistra M et al. Detection of diarrhoea-causing protozoa in general practice patients in the Netherlands by multiplex real-time PCR. Clin. Microbiol. Infect. 2007; 13: 1001–1007.
23. Stark D, Al-Qassab SE, Barratt JLN et al. Evaluation of multiplex tandem real-time PCR for detection of Cryptosporidium spp., Dientamoeba fragilis, Entamoeba histolytica, and Giardia intestinalis in clinical stool samples. J. Clin. Microbiol. 2011; 49: 257–262.
24. Utzinger J, Botero-Kleiven S, Castelli F et al. Microscopic diagnosis of sodium acetate-acetic acid-formalin-fixed stool samples for helminths and intestinal protozoa: a comparison among European reference laboratories. Clin. Microbiol. Infect. 2010; 16: 267–273.
25. van Gool T, Weijts R, Lommerse E et al. Triple faeces test: an effective tool for detection of intestinal parasites in routine clinical practice. Eur. J. Clin. Microbiol. Infect. Dis. 2003; 22: 284–290.
26. Gan SD, Patel KR. Enzyme immunoassay and enzyme-linked immunosorbent assay. J. Invest. Dermatol. 2013; 133 e12.
27. Ahmad N, Khan M, Hoque MI et al. Detection of Entamoeba histolytica DNA from liver abscess aspirate using polymerase chain reaction (PCR): a diagnostic tool for amoebic liver abscess. Bangladesh Med. Res. Counc. Bull. 2007; 33: 13–20.
28. Goñi P, Martín B, Villacampa M et al. Evaluation of an immunochromatographic dip strip test for simultaneous detection of Cryptosporidium spp, Giardia duodenalis, and Entamoeba histolytica antigens in human faecal samples. Eur. J. Clin. Microbiol. Infect. Dis. 2012; 31: 2077–2082.
29. Gonin P, Trudel L. Detection and differentiation of Entamoeba histolytica and Entamoeba dispar isolates in clinical samples by PCR and enzyme-linked immunosorbent assay. J. Clin. Microbiol. 2003; 41: 237–241.
30. Van den Bossche D, Cnops L, Verschueren J et al. Comparison of four rapid diagnostic tests, ELISA, microscopy and PCR for the detection of Giardia lamblia, Cryptosporidium spp. and Entamoeba histolytica in feces. J. Microbiol. Methods 2015; 110: 78–84.
31. Minak J, Kabir M, Mahmud I et al. Evaluation of rapid antigen point-of-care tests for detection of Giardia and Cryptosporidium species in human fecal specimens. J. Clin. Microbiol. 2012; 50: 154–156.
32. Liang S-Y, Chan Y-H, Hsia K-T et al. Development of loop-mediated isothermal amplification assay for detection of Entamoeba histolytica. J. Clin. Microbiol. 2009; 47: 1892–1895.
33. Plutzer J, Karanis P. Rapid identification of Giardia duodenalis by loop-mediated isothermal amplification (LAMP) from faecal and environmental samples and comparative findings by PCR and real-time PCR methods. Parasitol. Res. 2009; 104: 1527–1533.
34. Karanis P, Ongerth J. LAMP—a powerful and flexible tool for monitoring microbial pathogens. Trends Parasitol. 2009; 25: 498–499.
35. Binnicker MJ, Espy MJ, Irish CL et al. Direct detection of influenza A and B viruses in less than 20 minutes using a commercially available rapid PCR assay. J. Clin. Microbiol. 2015; 53: 2353–2354.
36. Oster N, Gehrig-Feistel H, Jung H et al. Evaluation of the immunochromatographic CORIS Giardia-Strip test for rapid diagnosis of Giardia lamblia. Eur. J. Clin. Microbiol. Infect. Dis. 2006; 25: 112–115.
37. Alexander CL, Niebel M, Jones B. The rapid detection of Cryptosporidium and Giardia species in clinical stools using the Quik Chek immunoassay. Parasitol. Int. 2013; 62: 552–553.
38. Agnamey P, Sarfati C, Pinel C et al. Evaluation of four commercial rapid immunochromatographic assays for detection of Cryptosporidium antigens in stool samples: a blind multicenter trial. J. Clin. Microbiol. 2011; 49: 1605–1607.
39. Weitzel T, Dittrich S, Möhl I et al. Evaluation of seven commercial antigen detection tests for Giardia and Cryptosporidium in stool samples. Clin. Microbiol. Infect. 2006; 12: 656–659.
40. Lebbad M, Svärd SG. PCR differentiation of Entamoeba histolytica and Entamoeba dispar from patients with amoeba infection initially diagnosed by microscopy. Scand. J. Infect. Dis. 2005; 37: 680–685.
41. Ximénez C, Morán P, Rojas L et al. Reassessment of the epidemiology of amebiasis: state of the art. Infect. Genet. Evol. 2009; 9: 1023–1032.
42. Grigorenko E, Fisher C, Patel S et al. Multiplex screening for blood-borne viral, bacterial, and protozoan parasites using an OpenArray platform. J. Mol. Diagn. 2014; 16: 136–144.
43. Müller N, von Allmen N. Recent insights into the mucosal reactions associated with Giardia lamblia infections. Int. J. Parasitol. 2005; 35: 1339–1347.
44. Elwin K, Robinson G, Hadfield SJ et al. A comparison of two approaches to extracting Cryptosporidium DNA from human stools as measured by a real-time PCR assay. J. Microbiol. Methods 2012; 89: 38–40.
45. Schrader C, Schielke A, Ellerbroek L et al. PCR inhibitors—occurrence, properties and removal. J. Appl. Microbiol. 2012; 113: 1014–1026.
46. Verweij JJ, Stensvold CR. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin. Microbiol. Rev. 2014; 27: 371–418.
47. Hawash Y. DNA extraction from protozoan oocysts/cysts in feces for diagnostic PCR. Korean J. Parasitol. 2014; 52: 263–271.
48. Oikarinen S, Tauriainen S, Viskari H et al. PCR inhibition in stool samples in relation to age of infants. J. Clin. Virol. 2009; 44: 211–214.
49. Hawash Y, Ghonaim MM, Al-Hazmi AS. Internal amplification control for a Cryptosporidium diagnostic PCR: construction and clinical evaluation. Korean J. Parasitol. 2015; 53: 147–154.
50. Monis PT, Giglio S, Keegan AR et al. Emerging technologies for the detection and genetic characterization of protozoan parasites. Trends Parasitol. 2005; 21: 340–346.
51. Gullett JC, Nolte FS. Quantitative nucleic acid amplification methods for viral infections. Clin. Chem. 2015; 61: 72–78.
52. Elfving K, Andersson M, Msellem MI et al. Real-time PCR threshold cycle cutoffs help to identify agents causing acute childhood diarrhea in Zanzibar. J. Clin. Microbiol. 2014; 52: 916–923.
53. Jokipii L, Jokipii AM. In vitro susceptibility of Giardia lamblia trophozoites to metronidazole and tinidazole. J. Infect. Dis. 1980; 141: 317–325.
54. van den Bijllaardt W, Overdevest IT, Buiting AG et al. Rapid clearance of Giardia lamblia DNA from the gut after successful treatment. Clin. Microbiol. Infect. 2014; 20: O972–974.
55. Mejia R, Vicuña Y, Broncano N et al. A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. Am. J. Trop. Med. Hyg. 2013; 88: 1041–1047.
56. Kuk S, Yazar S, Cetinkaya U. Stool sample storage conditions for the preservation of Giardia intestinalis DNA. Mem. Inst. Oswaldo Cruz 2012; 107: 965–968.
57. Verweij JJ, Mulder B, Poell B et al. Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol. Cell. Probes 2007; 21: 400–404.
58. Santos HLC, Bandyopadhyay K, Bandea R et al. LUMINEX®: a new technology for the simultaneous identification of five Entamoeba spp. commonly found in human stools. Parasit. Vectors 2013; 6: 69.
59. Heredia RD, Fonseca JA, López MC. Entamoeba moshkovskii perspectives of a new agent to be considered in the diagnosis of amebiasis. Acta Trop. 2012; 123: 139–145.
60. Luján HD, Svärd S, eds. Giardia, a Model Organism. Vienna: Springer Vienna, 2011.
61. Ng CT, Gilchrist CA, Lane A et al. Multiplex real-time PCR assay using Scorpion probes and DNA capture for genotype-specific detection of Giardia lamblia on fecal samples. J. Clin. Microbiol. 2005; 43: 1256–1260.
62. Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp. Parasitol. 2010; 124: 80–89.
63. Bart A, van der Heijden HM, Greve S et al. Intragenomic variation in the internal transcribed spacer 1 region of Dientamoeba fragilis as a molecular epidemiological marker. J. Clin. Microbiol. 2008; 46: 3270–3275.
64. Stensvold CR. Blastocystis: genetic diversity and molecular methods for diagnosis and epidemiology. Trop. Parasitol. 2013; 3: 26–34.
65. Othman N, Mohamed Z, Verweij JJ et al. Application of real-time polymerase chain reaction in detection of Entamoeba histolytica in pus aspirates of liver abscess patients. Foodborne Pathog. Dis. 2010; 7: 637–641.
66. Parija SC, Khairnar K. Detection of excretory Entamoeba histolytica DNA in the urine, and detection of E. histolytica DNA and lectin antigen in the liver abscess pus for the diagnosis of amoebic liver abscess. BMC Microbiol. 2007; 7: 41.
67. Khairnar K, Parija SC. Detection of Entamoeba histolytica DNA in the saliva of amoebic liver abscess patients who received prior treatment with metronidazole. J. Health Popul. Nutr. 2008; 26: 418–425.
68. Haque R, Kabir M, Noor Z et al. Diagnosis of amebic liver abscess and amebic colitis by detection of Entamoeba histolytica DNA in blood, urine, and saliva by a real-time PCR assay. J. Clin. Microbiol. 2010; 48: 2798–2801.
69. Solaymani-Mohammadi S, Lam MM, Zunt JR et al. Entamoeba histolytica encephalitis diagnosed by PCR of cerebrospinal fluid. Trans. R. Soc. Trop. Med. Hyg. 2007; 101: 311–313.
70. Binnicker MJ. Multiplex molecular panels for the diagnosis of gastrointestinal infection: performance, result interpretation and cost-effectiveness. J. Clin. Microbiol. 2015; 53: 3723–3728.
71. Tozzoli R, D'Aurizio F, Villalta D et al. Automation, consolidation, and integration in autoimmune diagnostics. Auto- Immun. highlights 2015; 6: 1–6.
72. Kim Y, Han M-S, Kim J et al. Evaluation of three automated nucleic acid extraction systems for identification of respiratory viruses in clinical specimens by multiplex real-time PCR. Biomed Res. Int. 2014; 2014: 430650.
73. Nikolay B, Brooker SJ, Pullan RL. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int. J. Parasitol. 2014; 44: 765–774.
74. Moore NE, Wang J, Hewitt J et al. Metagenomic analysis of viruses in feces from unsolved outbreaks of gastroenteritis in humans. Tang Y-W, ed J. Clin. Microbiol. 2015; 53: 15–21.
75. Wallace PS, MacKay WG. Quality in the molecular microbiology laboratory. Methods Mol. Biol. 2013; 943: 49–79.
76. Stensvold CR, Lebbad M, Verweij JJ. The impact of genetic diversity in protozoa on molecular diagnostics. Trends Parasitol. 2011; 27: 53–58.
77. Hörman A, Korpela H, Sutinen J et al. Meta-analysis in assessment of the prevalence and annual incidence of Giardia spp. and Cryptosporidium spp. infections in humans in the Nordic countries. Int. J. Parasitol. 2004; 34: 1337–1346.
78. Church C, Neill A, Schotthoefer AM. Intestinal infections in humans in the Rocky Mountain region. United States. J. Parasitol. 2010; 96: 194–196.