1921
Volume 90, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Sensitive diagnostic tools are crucial for an accurate assessment of helminth infections in low-endemicity areas. We examined stool samples from Tanzanian individuals and compared the diagnostic accuracy of a real-time polymerase chain reaction (PCR) with the FLOTAC technique and the Kato–Katz method for hookworm and the Baermann method for detection. Only FLOTAC had a higher sensitivity than the Kato–Katz method for hookworm diagnosis; the sensitivities of PCR and the Kato–Katz method were equal. PCR had a very low sensitivity for detection. The cycle threshold values of the PCR were negatively correlated with the logarithm of hookworm egg and larvae counts. The median larvae count was significantly lower in PCR false negatives than true positives. All methods failed to detect very low-intensity infections. New diagnostic approaches are needed for monitoring of progressing helminth control programs, confirmation of elimination, or surveillance of disease recrudescence.

[open-access] This is an Open Access article distributed under the terms of the American Society of Tropical Medicine and Hygiene's Re-use License which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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2017-11-19
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References

  1. Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basanez MG, Baxter A, Bell ML, Benjamin EJ, Bennett D, Bernabe E, Bhalla K, Bhandari B, Bikbov B, Bin Abdulhak A, Birbeck G, Black JA, Blencowe H, Blore JD, Blyth F, Bolliger I, Bonaventure A, Boufous S, Bourne R, Boussinesq M, Braithwaite T, Brayne C, Bridgett L, Brooker S, Brooks P, Brugha TS, Bryan-Hancock C, Bucello C, Buchbinder R, Buckle G, Budke CM, Burch M, Burney P, Burstein R, Calabria B, Campbell B, Canter CE, Carabin H, Carapetis J, Carmona L, Cella C, Charlson F, Chen H, Cheng AT, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahiya M, Dahodwala N, Damsere-Derry J, Danaei G, Davis A, De Leo D, Degenhardt L, Dellavalle R, Delossantos A, Denenberg J, Derrett S, Des Jarlais DC, Dharmaratne SD, Dherani M, Diaz-Torne C, Dolk H, Dorsey ER, Driscoll T, Duber H, Ebel B, Edmond K, Elbaz A, Ali SE, Erskine H, Erwin PJ, Espindola P, Ewoigbokhan SE, Farzadfar F, Feigin V, Felson DT, Ferrari A, Ferri CP, Fevre EM, Finucane MM, Flaxman S, Flood L, Foreman K, Forouzanfar MH, Fowkes FG, Fransen M, Freeman MK, Gabbe BJ, Gabriel SE, Gakidou E, Ganatra HA, Garcia B, Gaspari F, Gillum RF, Gmel G, Gonzalez-Medina D, Gosselin R, Grainger R, Grant B, Groeger J, Guillemin F, Gunnell D, Gupta R, Haagsma J, Hagan H, Halasa YA, Hall W, Haring D, Haro JM, Harrison JE, Havmoeller R, Hay RJ, Higashi H, Hill C, Hoen B, Hoffman H, Hotez PJ, Hoy D, Huang JJ, Ibeanusi SE, Jacobsen KH, James SL, Jarvis D, Jasrasaria R, Jayaraman S, Johns N, Jonas JB, Karthikeyan G, Kassebaum N, Kawakami N, Keren A, Khoo JP, King CH, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Laden F, Lalloo R, Laslett LL, Lathlean T, Leasher JL, Lee YY, Leigh J, Levinson D, Lim SS, Limb E, Lin JK, Lipnick M, Lipshultz SE, Liu W, Loane M, Ohno SL, Lyons R, Mabweijano J, MacIntyre MF, Malekzadeh R, Mallinger L, Manivannan S, Marcenes W, March L, Margolis DJ, Marks GB, Marks R, Matsumori A, Matzopoulos R, Mayosi BM, McAnulty JH, McDermott MM, McGill N, McGrath J, Medina-Mora ME, Meltzer M, Mensah GA, Merriman TR, Meyer AC, Miglioli V, Miller M, Miller TR, Mitchell PB, Mock C, Mocumbi AO, Moffitt TE, Mokdad AA, Monasta L, Montico M, Moradi-Lakeh M, Moran A, Morawska L, Mori R, Murdoch ME, Mwaniki MK, Naidoo K, Nair MN, Naldi L, Narayan KM, Nelson PK, Nelson RG, Nevitt MC, Newton CR, Nolte S, Norman P, Norman R, O'Donnell M, O'Hanlon S, Olives C, Omer SB, Ortblad K, Osborne R, Ozgediz D, Page A, Pahari B, Pandian JD, Rivero AP, Patten SB, Pearce N, Padilla RP, Perez-Ruiz F, Perico N, Pesudovs K, Phillips D, Phillips MR, Pierce K, Pion S, Polanczyk GV, Polinder S, Pope CA, 3rd Popova S, Porrini E, Pourmalek F, Prince M, Pullan RL, Ramaiah KD, Ranganathan D, Razavi H, Regan M, Rehm JT, Rein DB, Remuzzi G, Richardson K, Rivara FP, Roberts T, Robinson C, De Leon FR, Ronfani L, Room R, Rosenfeld LC, Rushton L, Sacco RL, Saha S, Sampson U, Sanchez-Riera L, Sanman E, Schwebel DC, Scott JG, Segui-Gomez M, Shahraz S, Shepard DS, Shin H, Shivakoti R, Singh D, Singh GM, Singh JA, Singleton J, Sleet DA, Sliwa K, Smith E, Smith JL, Stapelberg NJ, Steer A, Steiner T, Stolk WA, Stovner LJ, Sudfeld C, Syed S, Tamburlini G, Tavakkoli M, Taylor HR, Taylor JA, Taylor WJ, Thomas B, Thomson WM, Thurston GD, Tleyjeh IM, Tonelli M, Towbin JA, Truelsen T, Tsilimbaris MK, Ubeda C, Undurraga EA, van der Werf MJ, van Os J, Vavilala MS, Venketasubramanian N, Wang M, Wang W, Watt K, Weatherall DJ, Weinstock MA, Weintraub R, Weisskopf MG, Weissman MM, White RA, Whiteford H, Wiebe N, Wiersma ST, Wilkinson JD, Williams HC, Williams SR, Witt E, Wolfe F, Woolf AD, Wulf S, Yeh PH, Zaidi AK, Zheng ZJ, Zonies D, Lopez AD, , 2012. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 21972223.[Crossref]
  2. Christian P, Khatry SK, West KP, Jr, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981983.[Crossref]
  3. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, , 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 15211532.[Crossref]
  4. Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, Vounatsou P, Odermatt P, , 2013. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis 7: e2288.[Crossref]
  5. Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P, , 2009. Strongyloidiasis—the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 103: 967972.[Crossref]
  6. Becker SL, Sieto B, Silue KD, Adjossan L, Kone S, Hatz C, Kern WV, N'Goran EK, Utzinger J, , 2011. Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis 5: e1292.[Crossref]
  7. Knopp S, Steinmann P, Keiser J, Utzinger J, , 2012. Nematode infections: soil-transmitted helminths and Trichinella . Infect Dis Clin North Am 26: 341358.[Crossref]
  8. Siddiqui AA, Berk SL, , 2001. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 33: 10401047.[Crossref]
  9. Marcos LA, Terashima A, Dupont HL, Gotuzzo E, , 2008. Strongyloides hyperinfection syndrome: an emerging global infectious disease. Trans R Soc Trop Med Hyg 102: 314318.[Crossref]
  10. Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF, , 2012. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 142: w13727.
  11. Segarra-Newnham M, , 2007. Manifestations, diagnosis, and treatment of Strongyloides stercoralis infection. Ann Pharmacother 41: 19922001.[Crossref]
  12. Schroeder L, Banaei N, , 2013. Images in clinical medicine. Strongyloides stercoralis embryonated ova in the lung. N Engl J Med 368: e15.[Crossref]
  13. WHO, 2012. Accelerating Work to Overcome the Global Impact of Neglected Tropical Diseases—A Roadmap for Implementation. Geneva: World Health Organization, 142.
  14. London Declaration, 2012. The London Declaration on Neglected Tropical Diseases. Table of Commitments. Available at: http://www.who.int/neglected_diseases/NTD_London_Event_Table_Commitments.pdf. Accessed August 6, 2013.
  15. Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, McCarthy JS, Basanez MG, , 2012. A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis 6: e1582.[Crossref]
  16. McCarthy JS, Lustigman S, Yang GJ, Barakat RM, Garcia HH, Sripa B, Willingham AL, Prichard RK, Basanez MG, , 2012. A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Negl Trop Dis 6: e1601.[Crossref]
  17. Booth M, Vounatsou P, N'Goran EK, Tanner M, Utzinger J, , 2003. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d'Ivoire. Parasitology 127: 525531.[Crossref]
  18. Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J, , 2008. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2: e331.[Crossref]
  19. Knopp S, Rinaldi L, Khamis IS, Stothard JR, Rollinson D, Maurelli MP, Steinmann P, Marti H, Cringoli G, Utzinger J, , 2009. A single FLOTAC is more sensitive than triplicate Kato-Katz for the diagnosis of low-intensity soil-transmitted helminth infections. Trans R Soc Trop Med Hyg 103: 347354.[Crossref]
  20. Glinz D, Silué KD, Knopp S, Lohourignon KL, Yao PK, Steinmann P, Rinaldi L, Cringoli G, N'Goran EK, Utzinger J, , 2010. Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 4: e754.[Crossref]
  21. Jeandron A, Abdyldaieva G, Usubalieva J, Ensink JH, Cox J, Matthys B, Rinaldi L, Cringoli G, Utzinger J, , 2010. Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Trop 116: 185192.[Crossref]
  22. Ziegelbauer K, Steinmann P, Zhou H, Du ZW, Jiang JY, Fürst T, Jia TW, Zhou XN, Utzinger J, , 2010. Self-rated quality of life and school performance in relation to helminth infections: casestudy from Yunnan, People's Republic of China. Parasit Vectors 3: 61.[Crossref]
  23. Habtamu K, Degarege A, Ye-Ebiyo Y, Erko B, , 2011. Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitol Int 60: 398402.[Crossref]
  24. Gualdieri L, Rinaldi L, Petrullo L, Morgoglione ME, Maurelli MP, Musella V, Piemonte M, Caravano L, Coppola MG, Cringoli G, , 2011. Intestinal parasites in immigrants in the city of Naples (southern Italy). Acta Trop 117: 196201.[Crossref]
  25. Utzinger J, Rinaldi L, Lohourignon LK, Rohner F, Zimmermann MB, Tschannen AB, N'Goran EK, Cringoli G, , 2008. FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg 102: 8490.[Crossref]
  26. de Kaminsky RG, , 1993. Evaluation of three methods for laboratory diagnosis of Strongyloides stercoralis infection. J Parasitol 79: 277280.[Crossref]
  27. Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, Kita K, Ohtomo H, , 1991. A modified agar plate method for detection of Strongyloides stercoralis . Am J Trop Med Hyg 45: 518521.
  28. Polderman AM, Krepel HP, Baeta S, Blotkamp J, Gigase P, , 1991. Oesophagostomiasis, a common infection of man in northern Togo and Ghana. Am J Trop Med Hyg 44: 336344.
  29. Yelifari L, Bloch P, Magnussen P, van Lieshout L, Dery G, Anemana S, Agongo E, Polderman AM, , 2005. Distribution of human Oesophagostomum bifurcum, hookworm and Strongyloides stercoralis infections in northern Ghana. Trans R Soc Trop Med Hyg 99: 3238.[Crossref]
  30. Steinmann P, Zhou XN, Du ZW, Jiang JY, Wang LB, Wang XZ, Li LH, Marti H, Utzinger J, , 2007. Occurrence of Strongyloides stercoralis in Yunnan province, China, and comparison of diagnostic methods. PLoS Negl Trop Dis 1: e75.[Crossref]
  31. Verweij JJ, Brienen EA, Ziem J, Yelifari L, Polderman AM, Van Lieshout L, , 2007. Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. Am J Trop Med Hyg 77: 685690.
  32. Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, van Lieshout L, , 2009. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg 103: 342346.[Crossref]
  33. Basuni M, Muhi J, Othman N, Verweij JJ, Ahmad M, Miswan N, Rahumatullah A, Aziz FA, Zainudin NS, Noordin R, , 2011. A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. Am J Trop Med Hyg 84: 338343.[Crossref]
  34. Taniuchi M, Verweij JJ, Noor Z, Sobuz SU, Lieshout L, Petri WA, Jr Haque R, Houpt ER, , 2011. High throughput multiplex PCR and probe-based detection with Luminex beads for seven intestinal parasites. Am J Trop Med Hyg 84: 332337.[Crossref]
  35. Liu J, Gratz J, Amour C, Kibiki G, Becker S, Janaki L, Verweij JJ, Taniuchi M, Sobuz SU, Haque R, Haverstick DM, Houpt ER, , 2012. A laboratory-developed TaqMan array card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51: 472480.[Crossref]
  36. García LS, Bruckner DA, , 2001. Diagnostic Medical Parasitology. Washington, DC: American Society for Microbiology, 1791.
  37. Katz N, Chaves A, Pellegrino J, , 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397400.
  38. Cringoli G, Rinaldi L, Maurelli MP, Utzinger J, , 2010. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 5: 503515.[Crossref]
  39. Verweij JJ, Pit DS, van Lieshout L, Baeta SM, Dery GD, Gasser RB, Polderman AM, , 2001. Determining the prevalence of Oesophagostomum bifurcum and Necator americanus infections using specific PCR amplification of DNA from faecal samples. Trop Med Int Health 6: 726731.[Crossref]
  40. Obeng BB, Aryeetey YA, de Dood CJ, Amoah AS, Larbi IA, Deelder AM, Yazdanbakhsh M, Hartgers FC, Boakye DA, Verweij JJ, van Dam GJ, van Lieshout L, , 2008. Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol 102: 625633.[Crossref]
  41. Wiria AE, Prasetyani MA, Hamid F, Wammes LJ, Lell B, Ariawan I, Uh HW, Wibowo H, Djuardi Y, Wahyuni S, Sutanto I, May L, Luty AJ, Verweij JJ, Sartono E, Yazdanbakhsh M, Supali T, , 2010. Does treatment of intestinal helminth infections influence malaria? Background and methodology of a longitudinal study of clinical, parasitological and immunological parameters in Nangapanda, Flores, Indonesia (ImmunoSPIN Study). BMC Infect Dis 10: 77.[Crossref]
  42. The R Development Core Team, 2010. R: A Language and Environment for Statistical Computing. Vienna, Austria: The R Development Core Team, 11731.
  43. Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L, , 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva: World Health Organization, 148.
  44. Landis JR, Koch GG, , 1977. The measurement of observer agreement for categorical data. Biometrics 33: 159174.[Crossref]
  45. Hawass NE, , 1997. Comparing the sensitivities and specificities of two diagnostic procedures performed on the same group of patients. Br J Radiol 70: 360366.[Crossref]
  46. Joseph L, Gyorkos TW, Coupal L, , 1995. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am J Epidemiol 141: 263272.[Crossref]
  47. Dendukuri N, Joseph L, , 2001. Bayesian approaches to modeling the conditional dependence between multiple diagnostic tests. Biometrics 57: 158167.[Crossref]
  48. Branscum AJ, Gardner IA, Johnson WO, , 2005. Estimation of diagnostic-test sensitivity and specificity through Bayesian modeling. Prev Vet Med 68: 145163.[Crossref]
  49. Lunn D, Spiegelhalter D, Thomas A, Best N, , 2009. The BUGS project: evolution, critique, and future directions. Stat Med 28: 30493067.[Crossref]
  50. Brooks P, Gelman A, , 1998. General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7: 434455.
  51. Gelman A, Rubin DB, , 1992. Inference from iterative simulation using multiple sequences. Stat Sci 7: 457511.[Crossref]
  52. Bergquist R, Johansen MV, Utzinger J, , 2009. Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25: 151156.[Crossref]
  53. Schär F, Odermatt P, Khieu V, Panning M, Duong S, Muth S, Marti H, Kramme S, , 2013. Evaluation of real-time PCR for Strongyloides stercoralis and hookworm as diagnostic tool in asymptomatic schoolchildren in Cambodia. Acta Trop 126: 8992.[Crossref]
  54. Blotkamp J, Krepel HP, Kumar V, Baeta S, Van't Noordende JM, Polderman AM, , 1993. Observations on the morphology of adults and larval stages of Oesophagostomum sp. isolated from man in northern Togo and Ghana. J Helminthol 67: 4961.[Crossref]
  55. Sturrock RF, , 1966. Hookworm studies in Uganda: investigations at Teboke in Lango District. East Afr Med J 43: 430438.
  56. Sturrock RF, , 1966. Hookworm studies in Tanganyika (Tanzania): investigations at Hombolo in the Dodoma region. East Afr Med J 43: 315322.
  57. Chunge RN, Karumba PN, Andala EO, , 1986. Hookworm species in patients from Kenyatta National Hospital Nairobi. Ann Trop Med Parasitol 80: 147148.[Crossref]
  58. Knopp S, Speich B, Hattendorf J, Rinaldi L, Mohammed KA, Khamis IS, Mohammed AS, Albonico M, Rollinson D, Marti H, Utzinger J, , 2011. Diagnostic accuracy of Kato-Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Negl Trop Dis 5: e1036.[Crossref]
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  • Received : 17 May 2013
  • Accepted : 02 Sep 2013

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