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Update on laboratory diagnosis of amoebiasis

  • Syazwan Saidin
  • Nurulhasanah Othman
  • Rahmah Noordin
Review
  • 222 Downloads

Abstract

Amoebiasis, an enteric protozoan disease caused by Entamoeba histolytica, is a public health problem in many developing countries, causing up to 100,000 fatal cases annually. Detection of the pathogenic E. histolytica and its differentiation from the non-pathogenic Entamoeba spp. play a crucial role in the clinical management of patients. Laboratory diagnosis of intestinal amoebiasis in developing countries still relies on labour-intensive and insensitive methods involving staining of stool sample and microscopy. Newer and more sensitive methods include a variety of antigen detection ELISAs and rapid tests; however, their diagnostic sensitivity and specificity seem to vary between studies, and some tests do not distinguish among the Entamoeba species. Molecular detection techniques are highly sensitive and specific and isothermal amplification approaches may be developed into field-applicable tests; however, cost is still a barrier for their use as a routine laboratory test method in most endemic areas. Laboratory diagnosis of extraintestinal amoebiasis faces challenges of lack of definitive detection of current infection and commercially available point-of-care tests. For both types of amoebiasis, there is still a need for highly sensitive and specific tests that are rapid and cost-effective for use in developing countries where the disease is prevalent. In recent years, new molecules of diagnostic value are being discovered and new tests developed. The advances in ‘omics’ technologies are enabling discoveries of new biomarkers that may help distinguish between different infection stages.

Keywords

Amoebiasis Entamoeba histolytica Entamoeba dispar Laboratory Diagnosis 

Notes

Funding information

We would like to acknowledge the funding assistance from the Malaysian Ministry of Education through the Higher Institution Centre of Excellence Program (HICoE) [Grant no. 311/CIPPM/4401005].

References

  1. 1.
    Stanley SL (2003) Amoebiasis. Lancet 361:1025–1034Google Scholar
  2. 2.
    Collier P (2007) The bottom billion: why the poorest countries are failing and what can be done about it. Oxford University Press, United KingdomGoogle Scholar
  3. 3.
    Fotedar R, Stark D, Beebe N, Marriott D, Ellis J, Harkness J (2007a) Laboratory diagnostic techniques for Entamoeba species. Clin Microbiol Rev 20:511–532Google Scholar
  4. 4.
    Zlobl TL (2001) Amebiasis. Prim Care Update Ob Gyns 8:65–68Google Scholar
  5. 5.
    Stanley SL (2006) Vaccines for amoebiasis: barriers and opportunities. Parasitology 133:S81–S86Google Scholar
  6. 6.
    Hung CC, Ji DD, Sun HY, Lee YT, Hsu SY, Chang SY, Wu CH, Chan YH, Hsiao CF, Liu WC, Colebunders R (2008) Increased risk for Entamoeba histolytica infection and invasive amebiasis in HIV seropositive men who have sex with men in Taiwan. PLoS Negl Trop Dis 2:e175Google Scholar
  7. 7.
    Rivero LR, Fernández FAN, Robertson LJ (2008) Cuban parasitology in review: a revolutionary triumph. Trends Parasitol 24:440–448Google Scholar
  8. 8.
    Gathiram V, Jackson TF (1987) A longitudinal study of asymptomatic carriers of pathogenic zymodemes of Entamoeba histolytica. S Afr Med J 72:669–672Google Scholar
  9. 9.
    Caballero-Salcedo A, Viveros-Rogel M, Salvatierra B, Tapia-Conyer R, Sepulveda-Amor J, Gutierrez G, Ortiz-Ortiz L (1994) Seroepidemiology of amebiasis in Mexico. Am J Trop Med Hyg 50:412–419Google Scholar
  10. 10.
    Hughes MA, Petri WA (2000) Amebic liver abscess. Infect Dis Clin N Am 14:565–582Google Scholar
  11. 11.
    Garcia LS, Shimizu RY (1998) Evaluation of intestinal protozoan morphology in human fecal specimens preserved in EcoFix: comparison of Wheatley’s trichrome stain and EcoStain. Clin Microbiol 36:1974–1976Google Scholar
  12. 12.
    Gonzalez-Ruiz A, Haque R, Aguirre A, Castanon G, Hall A, Guhl F, Ruiz-Palacios G, Miles MA, Warhurst DC (1994) Value of microscopy in the diagnosis of dysentery associated with invasive Entamoeba histolytica. J Clin Pathol 47:236–239Google Scholar
  13. 13.
    Haque R, Neville LM, Hahn P, Petri WA (1995) Rapid diagnosis of Entamoeba infection by using Entamoeba and Entamoeba histolytica stool antigen detection kits. J Clin Microbiol 33:2558–2561Google Scholar
  14. 14.
    World Health Organization (WHO) (1997) UNESCO report of a consultation of experts on amoebiasis. Wkly Epidemiol Rec 72:97–99Google Scholar
  15. 15.
    Tanyuksel M, Petri WA (2003) Laboratory diagnosis of amebiasis. Clin Microbiol Rev 16:713–729Google Scholar
  16. 16.
    Haque R, Petri WA (2006) Diagnosis of amebiasis in Bangladesh. Arch Med Res 37:272–275Google Scholar
  17. 17.
    Liang SY, Chan YH, Hsia KT, Lee JL, Kuo MC, Hwa KY, Chan CW, Chiang TY, Chen JS, Wu FT, Ji DD (2009) Development of loop-mediated isothermal amplification assay for detection of Entamoeba histolytica. J Clin Microbiol 47:1892–1895Google Scholar
  18. 18.
    Clark CG, Diamond LS (2002) Methods for cultivation of luminal parasitic protists of clinical importance. Clin Microbiol Rev 15:329–341Google Scholar
  19. 19.
    Freedman L, Maddison SE, Elsdon-Dew B (1958) Monoxenic cultures of Entamoeba histolytica derived from human liver abscesses. Afr J Med Med Sci 23:9–12Google Scholar
  20. 20.
    Wang LT, Jen G, Cross JH (1973) Establishment of Entamoeba histolytica from liver abscess in monoxenic cultures with hemoflagellates. Am J Trop Med Hyg 22:30–32Google Scholar
  21. 21.
    Sargeaunt PG, Jackson TF, Wiffen S, Bhojnani R, Williams JE, Felmingham D, Goldmeir D, Allason-Jones E, Mindel A, Phillips E (1987) The reliability of Entamoeba histolytica zymodemes in clinical laboratory diagnosis. Arch Invst Med 18:69–75Google Scholar
  22. 22.
    Razmjou E, Haghighi A, Rezaian M, Kobayashi S, Nozaki T (2006) Genetic diversity of glucose phosphate isomerase from Entamoeba histolytica. Parasitol Int 55:307–311Google Scholar
  23. 23.
    Jackson TF, Suparsad S (1996) Zymodeme stability of Entamoeba histolytica and E. dispar. Arc Med Res 28:304–305Google Scholar
  24. 24.
    Strachan WD, Spice WM, Chiodini PL, Moody AH, Ackers JP (1988) Immunological differentiation of pathogenic and non-pathogenic isolates of Entamoeba histolytica. Lancet 331:561–563Google Scholar
  25. 25.
    Haque R, Kress K, Wood S, Jackson TF, Lyerly D, Wilkins T, Petri WA (1993) Diagnosis of pathogenic Entamoeba histolytica infection using a stool ELISA based on monoclonal antibodies to the galactose-specific adhesin. J Infect Dis 167:247–249Google Scholar
  26. 26.
    Haque R, Faruque ASG, Hahn P, Lyerly DM, Petri WA (1997) Entamoeba histolytica and Entamoeba dispar infection in children in Bangladesh. J Infec Dis 175:734–736Google Scholar
  27. 27.
    Haque R, Ali IKM, Akther S, Petri WA (1998a) Comparison of PCR, isoenzyme analysis, and antigen detection for diagnosis of Entamoeba histolytica infection. J Clin Microbiol 36:449–452Google Scholar
  28. 28.
    Haque R, Ali IKM, Clark CG, Petri WA (1998b) A case report of Entamoeba moshkovskii infection in a Bangladeshi child. Parasitol Int 47:201–202Google Scholar
  29. 29.
    Gatti S, Swierczynski G, Robinson F, Anselmi M, Corrales J, Moreira J, Montalvo G, Bruno A, Maserati R, Bisoffi Z, Scaglia M (2002) Amebic infections due to the Entamoeba histolytica-Entamoeba dispar complex: a study of the incidence in a remote rural area of Ecuador. Am J Trop Med Hyg 67:123–127Google Scholar
  30. 30.
    Roy S, Kabir M, Mondal D, Ali IKM, Petri WA, Haque R (2005) Real-time-PCR assay for diagnosis of Entamoeba histolytica infection. J Clin Microbiol 43:2168–2172Google Scholar
  31. 31.
    Visser LG, Verweij JJ, Van Esbroeck M, Edeling WM, Clerinx J, Polderman AM (2006) Diagnostic methods for differentiation of Entamoeba histolytica and Entamoeba dispar in carriers: performance and clinical implications in a non-endemic setting. Int J Med Microbiol 296:397–403Google Scholar
  32. 32.
    Mohanty S, Sharma N, Deb M (2014) Microscopy versus enzyme linked immunosorbent assay test for detection of Entamoeba histolytica infection in stool samples. Trop Parasitol 4:136Google Scholar
  33. 33.
    Al-Basheer NM, Majeed IA, Jawad HM (2014) Evaluation of antigen-based enzyme immuno-assay in reference to direct microscopy for the diagnosis of Entamoeba histolytica in stool samples. Al-Taqani 27:E54–E60Google Scholar
  34. 34.
    Akhtar T, Khan AG, Ahmed I, Nazli R, Haider J (2016) Prevalence of amoebiasis in a model research community and its confirmation using stool antigen elisa for Entamoeba histolytica. Pak J Pharm Sci 29:1587–1590Google Scholar
  35. 35.
    Ong SJ, Cheng MY, Liu KH, Horng CB (1996) Use of the ProSpecT® microplate enzyme immunoassay for the detection of pathogenic and non-pathogenic Entamoeba histolytica in faecal specimens. Trans R Soc Trop Med Hyg 90:248–249Google Scholar
  36. 36.
    Pillai DR, Kain KC (1999) Immunochromatographic strip-based detection of Entamoeba histolytica-E. dispar and Giardia lamblia coproantigen. J Clin Microbiol 37:3017–3019Google Scholar
  37. 37.
    Hira PR, Iqbal J, Al-Ali FAIZA, Philip R, Grover S, D'Almeida E, Al-Eneizi AA (2001) Invasive amebiasis: challenges in diagnosis in a nonendemic country (Kuwait). Am J Trop Med Hyg 65:341–345Google Scholar
  38. 38.
    van Hal SJ, Stark DJ, Fotedar R, Marriott D (2007) Amoebiasis: current status in Australia. Med J Aust 186:412Google Scholar
  39. 39.
    van Doorn HR, Hofwegen H, Koelewijn R, Gilis H, Peek R, Wetsteyn JC, van Genderen PJ, Vervoort T, van Gool T (2005) Use of rapid dipstick and latex agglutination tests and enzyme-linked immunosorbent assay for serodiagnosis of amebic liver abscess, amebic colitis, and Entamoeba histolytica cyst passage. J Clin Microbiol 43:4801–4806Google Scholar
  40. 40.
    Shenai BR, Komalam BL, Arvind AS, Krishnaswamy PR, Rao PV (1996) Recombinant antigen-based avidin-biotin microtiter enzyme-linked immunosorbent assay for serodiagnosis of invasive amebiasis. J Clin Microbiol 34:828–833Google Scholar
  41. 41.
    Uslu H, Aktas O, Uyanik MH (2016) Comparison of various methods in the diagnosis of Entamoeba histolytica in stool and serum specimens. Eur J Med 48:124Google Scholar
  42. 42.
    Knappik M, Börner U, Jelinek T (2005) Sensitivity and specificity of a new commercial enzyme-linked immunoassay kit for detecting Entamoeba histolytica IgG antibodies in serum samples. Eur J Clin Microbiol Infect Dis 24:701–703Google Scholar
  43. 43.
    Dhanalakshmi S, Meenachi C, Parija SC (2016) Indirect haemagglutination test in comparison with ELISA for detection of antibodies against invasive amoebiasis. J Clin Diagn Res 10:DC05–DC08Google Scholar
  44. 44.
    Dhanalakshmi S, Parija SC (2016) Seroprevalence of Entamoeba histolytica from a tertiary care hospital, South India. Trop Parasitol 6:78Google Scholar
  45. 45.
    Garcia LS, Shimizu RY, Bernard CN (2000) Detection of Giardia lamblia, Entamoeba histolytica/Entamoeba dispar, and Cryptosporidium parvum antigens in human fecal specimens using the triage parasite panel enzyme immunoassay. J Clin Microbiol 38:3337–3340Google Scholar
  46. 46.
    Sharp SE, Suarez CA, Duran Y, Poppiti RJ (2001) Evaluation of the triage micro parasite panel for detection of Giardia lamblia, Entamoeba histolytica/Entamoeba dispar, and Cryptosporidium parvum in patient stool specimens. J Clin Microbiol 39:332–334Google Scholar
  47. 47.
    Gaafar MR (2011) Evaluation of enzyme immunoassay techniques for diagnosis of the most common intestinal protozoa in fecal samples. Int J Infect Dis 15(8):e541–e544Google Scholar
  48. 48.
    Van den Bossche D, Cnops L, Verschueren J, Van Esbroeck M (2015) 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 110:78–84Google Scholar
  49. 49.
    Goñi P, Martín B, Villacampa M, Garcia A, Seral C, Castillo FJ, Clavel A (2012) 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 31:2077–2082Google Scholar
  50. 50.
    Formenti F, Perandin F, Bonafini S, Degani M, Bisoffi Z (2015) Evaluation of the new ImmunoCard STAT!® CGE test for the diagnosis of Amebiasis. Bull Soc Pathol Exot 108:171–174Google Scholar
  51. 51.
    Ibrahim SS, El-Matarawy OM, Ghieth MA, Sarea EYA, El-Badry AA (2015) Copro prevalence and estimated risk of Entamoeba histolytica in diarrheic patients at Beni-Suef, Egypt. World J Microbiol Biotechnol 31:385–390Google Scholar
  52. 52.
    Korpe PS, Stott BR, Nazib F, Kabir M, Haque R, Herbein JF, Petri WA (2012) Evaluation of a rapid point-of-care fecal antigen detection test for Entamoeba histolytica. Am J Trop Med Hyg 86:980–981Google Scholar
  53. 53.
    Verkerke HP, Hanbury B, Siddique A, Samie A, Haque R, Herbein J, Petri WA (2015) Multisite clinical evaluation of a rapid test for Entamoeba histolytica in stool. J Clin Microbiol 53:493–497Google Scholar
  54. 54.
    Saidin S, Yunus MH, Othman N, Lim YAL, Mohamed Z, Zakaria NZ, Noordin R (2017) Development and initial evaluation of a lateral flow dipstick test for antigen detection of Entamoeba histolytica in stool sample. Pathog Glob Health 111:128–136Google Scholar
  55. 55.
    Gonin P, Trudel L (2003) Detection and differentiation of Entamoeba histolytica and Entamoeba dispar isolates in clinical samples by PCR and enzyme-linked immunosorbent assay. J Clin Microbiol 41:237–241Google Scholar
  56. 56.
    Haque R, Mollah NU, Ali IKM, Alam K, Eubanks A, Lyerly D, Petri WA (2000) Diagnosis of amebic liver abscess and intestinal infection with the TechLab Entamoeba histolytica II antigen detection and antibody tests. J Clin Microbiol 38:3235–3239Google Scholar
  57. 57.
    Stark D, van Hal SJ, Matthews G, Harkness J, Marriott D (2008) Invasive amebiasis in men who have sex with men, Australia. Emerg Infect Dis 14:1141Google Scholar
  58. 58.
    Liang SY, Hsia KT, Chan YH, Fan CK, Jiang DDS, Landt O, Ji DD (2010) Evaluation of a new single-tube multiprobe real-time PCR for diagnosis of Entamoeba histolytica and Entamoeba dispar. J Parasitol 96:793–797Google Scholar
  59. 59.
    Mirelman D, Nuchamowitz Y, Stolarsky T (1997) Comparison of use of enzyme-linked immunosorbent assay-based kits and PCR amplification of rRNA genes for simultaneous detection of Entamoeba histolytica and E. dispar. J Clin Microbiol 35:2405–2407Google Scholar
  60. 60.
    Petri WA, Singh U (1999) Diagnosis and management of amebiasis. Clin Infect Dis 29:1117–1125Google Scholar
  61. 61.
    Abd-Alla MD, Jackson TF, Reddy S, Ravdin JI (2000) Diagnosis of invasive amebiasis by enzyme-linked immunosorbent assay of saliva to detect amebic lectin antigen and anti-lectin immunoglobulin G antibodies. J Clin Microbiol 38:2344–2347Google Scholar
  62. 62.
    Gomes TDS, Garcia MC, Souza Cunha FD, Werneck de Macedo H, Peralta JM Peralta RHS (2014) Differential diagnosis of Entamoeba spp. in clinical stool samples using SYBR Green real-time polymerase chain reaction. Sci World J.  https://doi.org/10.1155/2014/645084
  63. 63.
    Haque R, Kabir M, Noor Z, Rahman SM, Mondal D, Alam F, Rahman I, Al Mahmood A, Ahmed N, Petri WA (2010) 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 48:2798–2801Google Scholar
  64. 64.
    Khairnar K, Parija SC, Palaniappan R (2007) Diagnosis of intestinal amoebiasis by using nested polymerase chain reaction-restriction fragment length polymorphism assay. J Gastroenterol 42:631–640Google Scholar
  65. 65.
    Calderaro A, Gorrini C, Bommezzadri S, Piccolo G, Dettori G, Chezzi C (2006) Entamoeba histolytica and Entamoeba dispar: comparison of two PCR assays for diagnosis in a non-endemic setting. Trans R Soc Trop Med Hyg 100:450–457Google Scholar
  66. 66.
    Blessmann J, Buss H, Nu PA, Dinh BT, Ngo QT, Le Van A, Alla MD, Jackson TF, Ravdin JI, Tannich E (2002) Real-time PCR for detection and differentiation of Entamoeba histolytica and Entamoeba dispar in fecal samples. J Clin Microbiol 40:4413–4417Google Scholar
  67. 67.
    Shah PH, MacFarlane RC, Bhattacharya D, Matese JC, Demeter J, Stroup SE Singh U (2005) Comparative genomic hybridizations of Entamoeba strains reveal unique genetic fingerprints that correlate with virulence. Eukaryot Cell 4:504–515Google Scholar
  68. 68.
    Zaman S, Khoo J, Ng SW, Ahmed R, Khan MA, Hussain R, Zaman V (2000) Direct amplification of Entamoeba histolytica DNA from amoebic liver abscess pus using polymerase chain reaction. J Parasitol Res 86:724–728Google Scholar
  69. 69.
    Zindrou S, Orozco E, Linder E, Téllez A, Björkman A (2001) Specific detection of Entamoeba histolytica DNA by hemolysin gene targeted PCR. Acta Trop 78:117–125Google Scholar
  70. 70.
    Hamzah Z, Petmitr S, Mungthin M, Leelayoova S, Chavalitshewinkoon-Petmitr P (2006) Differential detection of Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii by a single-round PCR assay. J Clin Microbiol 44:3196–3200Google Scholar
  71. 71.
    Sri-Hidajati BS, Basuki S, Pusarawati S, Kusmartisnawati K, Rossyanti L, Sulistyowati SW, Kartikasari DP, Arwati H, Tantula I, Darma A, Handajani R (2018) Comparison of multiplex single round PCR and microscopy in diagnosis of amoebiasis. Afr J Infect Dis 12:120–126Google Scholar
  72. 72.
    Ali IK, Hossain MB, Roy S, Ayeh-Kumi PF, Petri WA Jr, Haque R, Clark CG (2003) Entamoeba moshkovskii infections in children, Bangladesh. Emerg Infect Dis 9:580–584Google Scholar
  73. 73.
    Parija SC, Khairnar K (2005) Entamoeba moshkovskii and Entamoeba dispar-associated infections in Pondicherry, India. J Health Popul Nutr 23:292–295Google Scholar
  74. 74.
    Ngui R, Angal L, Fakhrurrazi SA, Lian YLA, Ling LY, Ibrahim J, Mahmud R (2012) Differentiating Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii using nested polymerase chain reaction (PCR) in rural communities in Malaysia. Parasit Vectors 5:187Google Scholar
  75. 75.
    Lau YL, Anthony C, Fakhrurrazi SA, Ibrahim J, Ithoi I, Mahmud R (2013) Real-time PCR assay in differentiating Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii infections in Orang Asli settlements in Malaysia. Parasit Vectors 6:250Google Scholar
  76. 76.
    López-López P, Martínez-López MC, Boldo-León XM, Hernández-Díaz Y, González-Castro TB, Tovilla-Zárate CA, Luna-Arias JP (2017) Detection and differentiation of Entamoeba histolytica and Entamoeba dispar in clinical samples through PCR-denaturing gradient gel electrophoresis. Braz J Med Biol Res.  https://doi.org/10.1590/1414-431x20175997
  77. 77.
    Fallah E, Shahbazi A, Yazdanjoii M, Rahimi-Esboei B (2014) Differential detection of Entamoeba histolytica from Entamoeba dispar by parasitological and nested multiplex polymerase chain reaction methods. J Anal Res Clin Med 2:27–32Google Scholar
  78. 78.
    Dawah IS, Inabo HI, Abdullahi IO, Machido AD (2016) Differentiation of Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii from diarrhoeic stools using polymerase chain reaction in Kaduna, Nigeria. Int J Biomed Sci 5:61–66Google Scholar
  79. 79.
    Al-Areeqi MA, Sady H, Al-Mekhlafi HM, Anuar TS, Al-Adhroey AH, Atroosh WM et al (2017) First molecular epidemiology of Entamoeba histolytica, E. dispar and E. moshkovskii infections in Yemen: different species-specific associated risk factors. Tropical Med Int Health 22:493–504Google Scholar
  80. 80.
    Qvarnstrom Y, James C, Xayavong M, Holloway BP, Visvesvara GS, Sriram R, da Silva AJ (2005) Comparison of real-time PCR protocols for differential laboratory diagnosis of amebiasis. J Clin Microbiol 43:5491–5497Google Scholar
  81. 81.
    Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA, van Lieshout L, Polderman AM (2004) Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol 42:1220–1223Google Scholar
  82. 82.
    Roshdy MH, El-Kader NMA, Ali-Tammam M, Fuentes I, Mohamed MM, El-Sheikh NA, Rubio JM (2017) Molecular diagnosis of Entamoeba spp. versus microscopy in the Great Cairo. Acta Parasitol 62:188–191Google Scholar
  83. 83.
    Nazeer JT, Khalifa KES, von Thien H, El-Sibaei MM, Abdel-Hamid MY, Tawfik RAS, Tannich E (2013) Use of multiplex real-time PCR for detection of common diarrhea causing protozoan parasites in Egypt. Parasitol Res 112:595–601Google Scholar
  84. 84.
    Ahmad N, Khan M, Hoque MI, Haque R, Mondol D (2007) 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 33:13-20Google Scholar
  85. 85.
    Aguayo-Patrón S, Castillo-Fimbres R, Quihui-Cota L, de la Barca AMC (2017) Use of real-time polymerase chain reaction to identify Entamoeba histolytica in schoolchildren from northwest Mexico. J Infect Dev Ctries 11:800–805Google Scholar
  86. 86.
    Hamzah Z, Petmitr S, Mungthin M, Leelayoova S, Chavalitshewinkoon-Petmitr P (2010) Development of multiplex real-time polymerase chain reaction for detection of Entamoeba histolytica, Entamoeba dispar, and Entamoeba moshkovskii in clinical specimens. Am J Trop Med Hyg 83:909–913Google Scholar
  87. 87.
    Singh P, Mirdha BR, Ahuja V, Singh S (2013) Loop-mediated isothermal amplification (LAMP) assay for rapid detection of Entamoeba histolytica in amoebic liver abscess. World J Microbiol Biotechnol 29:27–32Google Scholar
  88. 88.
    Rivera WL, Ong VA (2013) Development of loop-mediated isothermal amplification for rapid detection of Entamoeba histolytica. Asian Pac J Trop Med 6:457–461Google Scholar
  89. 89.
    Mwendwa F, Mbae CK, Kinyua J, Mulinge E, Mburugu GN, Njiru ZK (2017) Stem loop-mediated isothermal amplification test: comparative analysis with classical LAMP and PCR in detection of Entamoeba histolytica in Kenya. BMC Res Notes 10:142Google Scholar
  90. 90.
    Foo PC, Chan YY, Mohamed M, Wong WK, Najian AN, Lim BH (2017) Development of a thermostabilised triplex LAMP assay with dry-reagent four target lateral flow dipstick for detection of Entamoeba histolytica and non-pathogenic Entamoeba spp. Anal Chim Acta 966:71–80Google Scholar
  91. 91.
    Freitas MAR, Vianna EN, Martins AS, Silva EF, Pesquero JL, Gomes MA (2004) A single step duplex PCR to distinguish Entamoeba histolytica from Entamoeba dispar. Parasitology 128:625–628Google Scholar
  92. 92.
    Núñez YO, Fernández MA, Torres-Núñez D, Silva JA, Montano I, Maestre JL, Fonte L (2001) Multiplex polymerase chain reaction amplification and differentiation of Entamoeba histolytica and Entamoeba dispar DNA from stool samples. Am J Trop Med Hyg 64:93–297Google Scholar
  93. 93.
    Bhattacharya S, Som I, Bhattacharya A (1998) The ribosomal DNA plasmids of Entamoeba. Parasitol Today 14:181–185Google Scholar
  94. 94.
    Cruz-Reyes JA, Spice WM, Rehman T, Gisborne E, Ackers JP (1992) Ribosomal DNA sequences in the differentiation of pathogenic and non-pathogenic isolates of Entamoeba histolytica. Parasitology 104:239–246Google Scholar
  95. 95.
    Nath J, Ghosh SK, Singha B, Paul J (2015) Molecular epidemiology of amoebiasis: a cross-sectional study among North East Indian population. PLoS Neg Trop Dis 9:e0004225Google Scholar
  96. 96.
    Khairnar K, Parija SC (2007) A novel nested multiplex polymerase chain reaction (PCR) assay for differential detection of Entamoeba histolytica, E. moshkovskii and E. dispar DNA in stool samples. BMC Microbiol 7:1Google Scholar
  97. 97.
    ElBakri A, Samie A, Ezzedine S, Odeh RA (2013) Differential detection of Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii in fecal samples by nested PCR in the United Arab Emirates (UAE). Acta Parasitol 58:185–190Google Scholar
  98. 98.
    Verweij JJ, Laeijendecker D, Brienen EA, van Lieshout L, Polderman AM (2003) Detection and identification of Entamoeba species in stool samples by a reverse line hybridization assay. J Clin Microbiol 41:5041–5045Google Scholar
  99. 99.
    Binnicker MJ (2015) Multiplex molecular panels for diagnosis of gastrointestinal infection: performance, result interpretation, and cost-effectiveness. J Clin Microbiol 53:3723–3728Google Scholar
  100. 100.
    Zboromyrska Y, Vila J (2016) Advanced PCR-based molecular diagnosis of gastrointestinal infections: challenges and opportunities. Expert Rev Mol Diagn 16:631–640Google Scholar
  101. 101.
    Shakir JM (2015) Evaluation of multiplex real-time PCR for detection of three diarrhea causing intestinal protozoa. Med Sci 5:783–786Google Scholar
  102. 102.
    Weitzel T, Cabrera J, Rosas R, Noriega LM, Schiappacasse G, Vollrath V, Porte L (2017) Enteric multiplex PCR panels: a new diagnostic tool for amoebic liver abscess? New Microbes New Infect 18:50–53Google Scholar
  103. 103.
    Navidad JF, Griswold DJ, Gradus MS, Bhattacharyya S (2013) Evaluation of Luminex xTAG® gastrointestinal pathogen analyte specific reagents for high-throughput, simultaneous detection of bacteria, viruses, and parasites of clinical and public health importance. J Clin Microbiol 51:3018–3024Google Scholar
  104. 104.
    Morio F, Valot S, Laude A, Desoubeaux G, Argy N, Nourrisson C, Pomares C, Machouart M, Le Govic Y, Dalle F, Botterel F (2018) Evaluation of a new multiplex PCR assay (ParaGENIE G-Amoeba real-time PCR kit) targeting Giardia intestinalis, Entamoeba histolytica and Entamoeba dispar/Entamoeba moshkovskii from stool specimens: evidence for the limited performances of microscopy-based approach for amoeba species identification. Clin Microbiol Infect.  https://doi.org/10.1016/j.cmi.2018.02.007
  105. 105.
    Laude A, Valot S, Desoubeaux G, Argy N, Nourrisson C, Pomares C, Machouart M, Le Govic Y, Dalle F, Botterel F, Bourgeois N (2016) Is real-time PCR-based diagnosis similar in performance to routine parasitological examination for the identification of Giardia intestinalis, Cryptosporidium parvum/Cryptosporidium hominis and Entamoeba histolytica from stool samples? Evaluation of a new commercial multiplex PCR assay and literature review. Clin Microbiol Infect.  https://doi.org/10.1016/j.cmi.2015.10.019
  106. 106.
    Parija SC, Mandal J, Ponnambath DK (2014) Laboratory methods of identification of Entamoeba histolytica and its differentiation from look-alike Entamoeba spp. Trop Parasitol 4:90Google Scholar
  107. 107.
    Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28:e63–e63Google Scholar
  108. 108.
    Fernández-Soto P, Arahuetes JG, Hernández AS, Abán JL, Santiago BV, Muro A (2014) A loop-mediated isothermal amplification (LAMP) assay for early detection of Schistosoma mansoni in stool samples: a diagnostic approach in a murine model. PLoS Negl Trop Dis 8:e3126Google Scholar
  109. 109.
    Banoo S, Bell D, Bossuyt P, Herring A, Mabey D, Poole F, Smith PG, Sriram N, Wongsrichanalai C, Linke R, O'brien R (2008) Evaluation of diagnostic tests for infectious diseases: general principles. Nat Rev Microbiol 8:S16–S28Google Scholar
  110. 110.
    Chin CD, Chin SY, Laksanasopin T, Sia SK (2013) Low-cost micron- devices for point-of-care testing. In: Issadore D, Westervelt RM (eds) Point-of-care diagnostics on a Chip. Springer, Berlin Heidelberg, pp 3–21Google Scholar
  111. 111.
    Peeling RW, Mabey D (2010) Point-of-care tests for diagnosing infections in the developing world. Clin Microbiol Infect 16:1062–1069Google Scholar
  112. 112.
    Leiva B, Lebbad M, Winiecka-Krusnell J, Altamirano I, Tellez A, Linder E (2006) Overdiagnosis of Entamoeba histolytica and Entamoeba dispar in Nicaragua: a microscopic, triage parasite panel and PCR study. Arch Med Res 37:529–534Google Scholar
  113. 113.
    Leo M, Haque R, Kabir M, Roy S, Lahlou RM, Mondal D, Tannich E, Petri WA (2006) Evaluation of Entamoeba histolytica antigen and antibody point-of-care tests for the rapid diagnosis of amebiasis. J Clin Microbiol 44:4569–4571Google Scholar
  114. 114.
    Mukhopadhyay M, Saha AK, Sarkar A, Mukherjee S (2010) Amoebic liver abscess: presentation and complications. Indian J Surg 72:37–41Google Scholar
  115. 115.
    Kasper DL, Braunwald E, Fauci AS, Hauser SL, Longo DL, Jameson JL (2005) Harrison's principles of internal medicine. McGraw-Hill companies Inc, USAGoogle Scholar
  116. 116.
    Katzenstein D, Rickerson V, Braude A (1982) New concepts of amebic liver abscess derived from hepatic imaging, serodiagnosis, and hepatic enzymes in 67 consecutive cases in San Diego. Medicine 61:237–246Google Scholar
  117. 117.
    Mathur S, Gehlot RS, Mohta A, Bhargava N (2002) Clinical profile of amoebic liver abscess. J Indian Acad Clin Med 3:367–373Google Scholar
  118. 118.
    Salles JM, Moraes LA, Salles MC (2003) Hepatic amebiasis. Braz J Infect Dis 7:96–110Google Scholar
  119. 119.
    Othman N, Mohamed Z, Verweij JJ, Huat LB, Olivos-García A, Yeng C, Noordin R (2010) Application of real-time polymerase chain reaction in detection of Entamoeba histolytica in pus aspirates of liver abscess patients. Foodborne Pathog Dis 7:637–641Google Scholar
  120. 120.
    Sifri CD, Madoff LC (2010) Infectious disease of the liver and biliary system. In: Mandell GL, Benett JE, Dolin R (eds) Principles and practice of infectious disease. Churchill Livingstone Elsevier, Philadelphia, pp 1035–1044Google Scholar
  121. 121.
    Parija SC, Khairnar K (2007) 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 7:41Google Scholar
  122. 122.
    Bancroft JD, Gamble M (2002) Theory and practice of histological techniaques, 5th edn. Churchill Livingstone, ChinaGoogle Scholar
  123. 123.
    Rigothier MC, Khun H, Tavares P, Cardona A, Huerre M, Guillen N (2002) Fate of Entamoeba histolytica during establishment of amoebic liver abscess analyzed by quantitative radioimaging and histology. Infect Immun 70:3208–3215Google Scholar
  124. 124.
    Ning TZ, Kin WW, Mustafa S, Ahmed A, Noordin R, Cheong TG, Huat LB (2012) Detection of Entamoeba histolytica in experimentally induced amoebic liver abscess: comparison of three staining methods. Asian Pac J Trop Biomed 2:61–65Google Scholar
  125. 125.
    Zengzhu G, Bracha R, Nuchamowitz Y, Cheng W, Mirelman D (1999) Analysis by enzyme-linked immunosorbent assay and PCR of human liver abscess aspirates from patients in China for Entamoeba histolytica. J Clin Microbiol 37:3034–3036Google Scholar
  126. 126.
    Karki BM, Parija SC (1999) Co-agglutination test for the detection of circulating antigen in amebic liver abscess. Am J Trop Med Hyg 60:498–501Google Scholar
  127. 127.
    Ravdin JI, Jackson TF, Petri WA Jr, Murphy CF, Ungar BL, Gathiram V, Skilogiannis J, Simjee AE (1990) Association of serum antibodies to adherence lectin with invasive amebiasis and asymptomatic infection with pathogenic Entamoeba histolytica. J Infect Dis 162:768–772Google Scholar
  128. 128.
    Hung CC, Chen PJ, Hsieh SM, Wong JM, Fang CT, Chang SC, Chen MY (1999) Invasive amoebiasis: an emerging parasitic disease in patients infected with HIV in an area endemic for amoebic infection. Aids 13:2421–2428Google Scholar
  129. 129.
    del Carmen Sánchez-Guillén M, Velázquez-Rojas M, Salgado-Rosas H, Torres-Rasgado E, Pérez-Fuentes R, Martı́nez-Munguı́a J, Talamás-Rohana P (2000) Seroprevalence of anti-Entamoeba histolytica antibodies by IHA and ELISA assays in blood donors from Puebla, Mexico. Arch Med Res 31:S53–S54Google Scholar
  130. 130.
    Cross JH, Clarke MD, Cole WC, Lien JC, Partono F, Joesoef A, Oemijati S (1976) Parasitic infections in humans in West Kalimantan (Borneo), Indonesia. Trop Geogr Med 28:121–130Google Scholar
  131. 131.
    Mohamed Z, Bachok NA, Hasan H (2009) Analysis of indirect hemagglutination assay results among patients with amoebic liver abscess. Int Med J 16:195–199Google Scholar
  132. 132.
    Garcia LS, Bruckner DA, Brewer TC, Shimizu RY (1982) Comparison of indirect fluorescent-antibody amoebic serology with counterimmunoelectrophoresis and indirect hemagglutination amoebic serologies. J Clin Microbiol 15:603-605Google Scholar
  133. 133.
    Shamsuzzaman SM, Haque R, Ruhul Hasin SK, Hashiguchi Y (2000) Evaluation of indirect fluorescent antibody test and enzyme-linked immunosorbent assay for diagnosis of hepatic amebiasis in Bangladesh. J Parasitol 86:611-615Google Scholar
  134. 134.
    Patterson M, Schoppe LE (1982) Presentation of amoebiasis. Med Clin North Am 66:689–705Google Scholar
  135. 135.
    Yang J, Kennedy MT (1979) Evaluation of enzyme-linked immunosorbent assay for the serodiagnosis of amebiasis. J Clin Microbiol 10:778-785Google Scholar
  136. 136.
    Robert R, Mahaza C, Bernard C, Buffard C, Senet JM (1990) Evaluation of a new bicolored latex agglutination test for immunological diagnosis of hepatic amoebiasis. J Clin Microbiol 28:1422–1424 Google Scholar
  137. 137.
    Wong WK, Tan ZN, Othman N, Lim BH, Mohamed Z, Garcia AO, Noordin R (2011) Analysis of Entamoeba histolytica excretory-secretory antigen and identification of a new potential diagnostic marker. Clin Vaccine Immunol 18:1913–1917Google Scholar
  138. 138.
    Lotter H, Mannweiler E, Schreiber M, Tannich E (1992) Sensitive and specific serodiagnosis of invasive amebiasis by using a recombinant surface protein of pathogenic Entamoeba histolytica. J Clin Microbiol 30:3163–3167 Google Scholar
  139. 139.
    Weinke T, Scherer W, Neuber U, Trautmann M (1989) Clinical features and management of amebic liver abscess. Experience from 29 patients. Klin Wochenschr 67:415–420 Google Scholar
  140. 140.
    Saidin S, Yunus MH, Zakaria ND, Razak KA, Huat LB, Othman N, Noordin R (2014) Production of recombinant Entamoeba histolytica pyruvate phosphate dikinase and its application in a lateral flow dipstick test for amoebic liver abscess. BMC Infect Dis 14:182 Google Scholar
  141. 141.
    Myung K, Burch D, Jackson TF, Stanley SL Jr (1991) Serodiagnosis of invasive amebiasis using a recombinant Entamoeba histolytica antigen-based ELISA. Arch Med Res 23:285–288 Google Scholar
  142. 142.
    Tachibana H, Cheng XJ, Masuda G, Horiki N, Takeuchi T (2004) Evaluation of recombinant fragments of Entamoeba histolytica Gal/GalNAc lectin intermediate subunit for serodiagnosis of amebiasis. J Clin Microbiol 42:1069–1074​Google Scholar
  143. 143.
    Stanley SL (1997) Progress towards development of a vaccine for amebiasis. Clin Microbiol Rev 10:637–649​Google Scholar
  144. 144.
    Kimura A, Hara Y, Kimoto T, Okuno Y, Minekawa Y, Nakabayashi T (1996) Cloning and expression of a putative alcohol dehydrogenase gene of Entamoeba histolytica and its application to immunological examination. Clin Diagn Lab Immunol 3:270–274 Google Scholar
  145. 145.
    Ning TZ, Kin WW, Noordin R, Cun ST, Chong FP, Mohamed Z, Olivos-Garcia A, Huat LB (2013) Evaluation of E ntamoeba histolytica recombinant phosphoglucomutase protein for serodiagnosis of amoebic liver abscess. BMC Infect Dis 13:144 Google Scholar
  146. 146.
    Khan U, Mirdha BR, Samantaray JC, Sharma MP (2006) Detection of Entamoeba histolytica using polymerase chain reaction in pus samples from amebic liver abscess. Indian J Gastroenterol 25:55​Google Scholar
  147. 147.
    Tachibana H, Kobayashi S, Okuzawa E, Masuda G (1992) Detection of pathogenic Entamoeba histolytica DNA in liver abscess fluid by polymerase chain reaction. Int J Parasitol 22:1193–1196​Google Scholar
  148. 148.
    Morshed M, Cherian SS, Lo T, Lee MK, Wong Q, Hoang L (2017) Superiority of PCR against microscopy for diagnosing Entamoeba histolytica in liver abscess samples. Can J Infect Dis Med Microbiol 2:1–3Google Scholar
  149. 149.
    Pritt BS, Clark CG (2008) Amebiasis. Mayo Clin Proc 83:1154–1160Google Scholar
  150. 150.
    Dhawan VK (2008) Current diagnosis and treatment of amebiasis. US Infect Dis 4:59–61Google Scholar
  151. 151.
    Tachibana H, Kakino A, Kazama M, Feng M, Asai S, Umezawa K, Nozaki T, Makiuchi T, Kamada T, Watanabe H, Horiki N (2018) Development of a sensitive immunochromatographic kit using fluorescent silica nanoparticles for rapid serodiagnosis of amebiasis. Parasitology 9:1–6Google Scholar
  152. 152.
    Shastry BS (2002) SNP alleles in human disease and evolution. J Hum Genet 47:561Google Scholar
  153. 153.
    Luna-Nácar M, Navarrete-Perea J, Moguel B, Bobes RJ, Laclette JP, Carrero JC (2016) Proteomic study of Entamoeba histolytica trophozoites, cysts, and cyst-like structures. PLoS One 11:e0156018Google Scholar
  154. 154.
    Ujang JA, Kwan SH, Ismail MN, Lim BH, Noordin R, Othman N (2016) Proteome analysis of excretory-secretory proteins of Entamoeba histolytica HM1: IMSS via LC–ESI–MS/MS and LC–MALDI–TOF/TOF. Clin Proteomics 13:33Google Scholar
  155. 155.
    Perdomo D, Aït-Ammar N, Syan S, Sachse M, Jhingan GD, Guillén N (2015) Cellular and proteomics analysis of the endomembrane system from the unicellular Entamoeba histolytica. J Proteome 112:125–140Google Scholar
  156. 156.
    Biller L, Matthiesen J, Kuehne V, Lotter H, Handal G, Nozaki T, Saito-Nakano Y, Schuemann M, Roeder T, Tannich E, Krause E (2013) The cell surface proteome of Entamoeba histolytica. Mol Cell Proteomics.  https://doi.org/10.1074/mcp.M113.031393
  157. 157.
    Okada M, Huston CD, Oue M, Mann BJ, Petri WA Jr, Kita K, Nozaki T (2006) Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Mol Biochem Parasitol 145:171–183Google Scholar
  158. 158.
    Leitsch D, Radauer C, Paschinger K, Wilson IB, Breiteneder H, Scheiner O, Duchêne M (2005) Entamoeba histolytica: analysis of the trophozoite proteome by two-dimensional polyacrylamide gel electrophoresis. Exp Parasitol 110:191–195Google Scholar
  159. 159.
    Davis PH, Chen M, Zhang X, Clark CG, Townsend RR, Stanley SL Jr (2009) Proteomic comparison of Entamoeba histolytica and Entamoeba dispar and the role of E. histolytica alcohol dehydrogenase 3 in virulence. PLoS Negl Trop Dis 3:e415Google Scholar
  160. 160.
    Davis PH, ZhangX, Guo J, Townsend RR, Samuel L. Stanley, (2006) Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Mol Microbiol 61:1523-1532Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Syazwan Saidin
    • 1
    • 2
  • Nurulhasanah Othman
    • 1
  • Rahmah Noordin
    • 1
  1. 1.Institute for Research in Molecular MedicineUniversiti Sains MalaysiaPenangMalaysia
  2. 2.Department of Biology, Faculty of Science and MathematicsSultan Idris Education UniversityTanjung MalimMalaysia

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