Improved PCR-Based Detection of Soil Transmitted Helminth Infections Using a Next-Generation Sequencing Approach to Assay Design

PLoS Neglected Tropical Diseases

Volumn 10, Issue 3, 2016, Pages

  Pilotte, Nils ^a,b   Papaiakovou, Marina ^a   Grant, Jessica R ^a   Bierwert, Lou Ann ^a   Llewellyn, Stacey ^c   McCarthy, James S ^c   Williams, Steven A ^a,b  

^a SMITH COLLEGE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; REPETITIVE DNA; HELMINTH DNA; SOIL;

ANCYLOSTOMA CEYLANICUM; ANCYLOSTOMA DUODENALE; ARTICLE; ASCARIS LUMBRICOIDES; COMPARATIVE STUDY; DNA EXTRACTION; DNA ISOLATION; DNA LIBRARY; HELMINTHIASIS; LIMIT OF DETECTION; NECATOR AMERICANUS; NEXT GENERATION SEQUENCING; NONHUMAN; PARASITE TRANSMISSION; REAL TIME POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SENSITIVITY AND SPECIFICITY; SOIL MICROFLORA; SPECIES DIFFERENCE; STRONGYLOIDES STERCORALIS; TRICHURIS TRICHIURA; ANIMAL; HUMAN; ISOLATION AND PURIFICATION; PARASITOLOGY; POLYMERASE CHAIN REACTION; PROCEDURES; SOIL;

ANIMALS; DNA, HELMINTH; HELMINTHIASIS; HUMANS; POLYMERASE CHAIN REACTION; SOIL;

EID: 84962463236     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004578     Document Type: Article

References (73)

1. Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, et al. Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis. In: Disease Control Priorities in Developing Countries. Washington: World Bank; 2006. pp. 467–482.
2. Buonfrate D, Formenti F, Perandin F, Bisoffi Z, Novel approaches to the diagnosis of Strongyloides stercoralis infection. Clin Microbiol Infect. 2015; 21(6): 543–552. doi: 10.1016/j.cmi.2015.04.00125887711
3. Schär F, Odermatt P, Khieu V, Panning M, Duong S, Muth S, et al. Evaluation of real-time PCR for Strongyloides stercoralis and hookworm as diagnostic tool in asymptomatic schoolchildren in Cambodia. Acta Trop. 2013; 126(2): 89–92. doi: 10.1016/j.actatropica.2012.12.01223298731
4. Mejia R, Vicuña Y, Broncano N, Sandoval C, Vaca M, Chico M, 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(6): 1041–1047. doi: 10.4269/ajtmh.12-072623509117
5. Gordon CA, McManus DP, Acosta LP, Olveda RM, Williams GM, Ross AG, et al. Multiplex real-time PCR monitoring of intestinal helminthes in humans reveals widespread polyparasitism in Northern Samar, the Philippines. Int J Parasitol. 2015; 45(7): 477–483. doi: 10.1016/j.ijpara.2015.02.01125858090
6. Anderson RM, Schad GA, Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Trans R Soc Trop Med Hyg. 79(6): 812–825. 3832493
7. Booth M, Vounatsou P, N’Goran EK, Tanner M, Utzinger J, 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. 2003; 127(Pt 6): 525–531. 14700188
8. Nikolay B, Brooker SJ, Pullan RL, Sensitivity of diagnostic tests for human soil-transmitted helminths infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol. 2014; 44(11): 765–774. doi: 10.1016/j.ijpara.2014.05.00924992655
9. Knopp S, Salim N, Schindler T, Voules DAK, Rothen J, Lweno O, et al. Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann, and PCR Methods for the Detection of light-intensity hookworm and Strongyloides stercoralis Infections in Tanzania. Am J Trop Med Hyg. 2014; 90(3): 535–545. doi: 10.4269/ajtmh.13-026824445211
10. Haque R, Mondal D, Karim A, Molla IH, Rahim A, Faruque ASG, et al. Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clin Infect Dis. 2009; 48: 1191–1197. doi: 10.1086/59758019323634
11. Phuphisut O, Yoonuan T, Sanguankiat S, Chaisiri K, Maipanich W, Pubampen S, et al. Triplex Polymerase Chain Reaction Assay for Detection of Major Soil-Transmitted Helminths, Ascaris lumbricoides, Trichuris trichiura, Necator americanus, in Fecal Samples. Southeast Asian J Trop Med Public Health. 2014; 45(2): 267–275. 24968666
12. Basuni M, Muhi J, Nurulhasanah O, Verweij JJ, Ahmad M, Miswan N, et al. A Pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. Am J Trop Med Hyg. 2011; 84(2): 338–343. doi: 10.4269/ajtmh.2011.10-049921292911
13. Verweij JJ, Brienen EAT, Ziem J, Yelifari L, Polderman AM, Van Lieshout L, 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. 2007; 77(4): 685–690. 17978072
14. Wiria AE, Prasetyani MA, Hamid F, Wammes LJ, Lell B, Ariawa I, et al. 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. 2010; 10: 77. doi: 10.1186/1471-2334-10-7720338054
15. Verweij JJ, Canales M, Polman K, Ziem J, Brienen EAT, Polderman AM, et al. Molecular diagnosis of Strongyloides stercoralis in fecal samples using real-time PCR. Trans R Soc Trop Med Hyg. 2009; 103(4): 342–346. doi: 10.1016/j.trstmh.2008.12.00119195671
16. Liu J, Gratz J, Amour C, Kibiki G, Becker S, Janaki L, et al. A laboratory-developed TaqMan Array Card for simultaneous detection of 19 enteropathogens. J Clin Microbiol. 2013; 51(2): 472–480. doi: 10.1128/JCM.02658-1223175269
17. Janwan P, Intapan PM, Thanchomnang T, Lulitanond V, Anamnart W, Maleewong W, Rapid detection of Opisthorchis viverrini and Strongyloides stercoralis in human fecal samples using a duplex real-time PCR and melting curve analysis. Parasitol Res. 2011; 109(6): 1593–1601. doi: 10.1007/s00436-011-2419-z21537984
18. Fabian S, Odermatt P, Khieu V, Panning M, Duong S, Muth S, et al. Evaluation of real-time PCR for Strongyloides stercoralis and hookworm as diagnostic tool in asymptomatic schoolchildren in Cambodia. Acta Trop. 2013; 126(2): 89–92. doi: 10.1016/j.actatropica.2012.12.01223298731
19. Cimino RO, Jeun R, Juarez M, Cajal PS, Vargas P, Echazú A, et al. Identification of human intestinal parasites affecting an asymptomatic peri-urban Argentinian population using multi-parallel quantitative real-time polymerase chain reaction. Parasit Vectors. 2015; 8: 380. doi: 10.1186/s13071-015-0994-z26183074
20. Tahapary DL, de Ruiter K, Martin I, van Lieshout L, Guigas B, Soewondo P, et al. Helminth infections and type 2 diabetes: a cluster-randomized placebo controlled SUGARSPIN trial in Nangapanda, Flores, Indonesia. BMC Infect Dis. 2015; 15: 133. doi: 10.1186/s12879-015-0873-425888525
21. Staudacher O, Heimer J, Steiner F, Kayonga Y, Havugimana JM, Ignatius R, et al. Soil-transmitted helminths in southern highland Rwanda: associated factors and effectiveness of school-based preventive chemotherapy. Trop Med Int Health. 2014; 19(7): 812–824. doi: 10.1111/tmi.1232124750543
22. Gatehouse HS, Malone LA, The Ribosomal RNA Gene Region of Nosema apis (Microspora): DNA Sequence for Small and Large Subunit rRNA Genes and Evidence of a Large Tandem Repeat Unit Size. J Invertebr Pathol. 1998; 71(2): 97–105. 9547137
23. Hlinka O, Murrell A, Barker SC, Evolution of the secondary structure of the rRNA internal transcriber spacer 2 (ITS2) in hard ticks (Ixodidae, Arthropoda). Heredity. 2002; 88: 275–279. 11920135
24. Gerbi SA, Evolution of ribosomal DNA. In: Molecular Evolutionary Genetics. New York/London: Plenum Press; 1985. pp. 419–517.
25. Fritz GN, Conn J, Cockburn A, Seawright J, Sequence Analysis of the Ribosomal DNA Internal Transcribed Spacer 2 from Populations of Anopheles nuneztovari (Diptera: Culicidae). Mol Biol Evol. 1994; 11(3): 406–416. 8015435
26. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P, Molecular Biology of the Cell. 5th ed.New York: Garland Science; 2008.
27. Cooper GM, The Cell: A Molecular Approach. 2nd Edition.Sunderland (MA): Sinauer Associates; 2000.
28. The C. elegans Sequencing ConsortiumGenome Sequence of the Nematode C. elegans: A Platform for Investigating Biology. Science. 1998; 282(5396): 2012–2018. 9851916
29. Thanchomnang T, Intapan PM, Lulitanond V, Choochote W, Manjai A, Prasongdee TK, et al. Rapid detection of Brugia malayi in mosquito vectors using a real-time fluorescence resonance energy transfer PCR and melting curve analysis. Am J Trop Med Hyg. 2008; 78(3): 509–513. 18337351
30. Alhassan A, Li Z, Poole CB, Carlow CK, Expanding the MDx toolbox for filarial diagnosis and surveillance. Trends Parasitol. 2015; 31(8): 391–400. doi: 10.1016/j.pt.2015.04.00625978936
31. Ricciardi A, Ndao M, Diagnosis of Parasitic Infections: What’s Going On?J Biomol Screen. 2015; 20(1): 6–21. doi: 10.1177/108705711454806525170017
32. McReynolds LA, DeSimone SM, Williams SA, Cloning and comparison of repeated DNA sequences from the human filarial parasite Brugia malayi and the animal parasite Brugia pahangi. Proc Natl Acad Sci U.S.A. 1986; 83: 797–801. 3003750
33. Zhong M, McCarthy J, Bierwert L, Lizotte-Waniewski M, Chanteau S, Nutman TB, et al. A polymerase chain reaction assay for detection of the parasite Wuchereria bancrofti in human blood samples. Am J Trop Med Hyg. 1996; 54(4): 357–363. 8615447
34. Vargas N, Souto RP, Carranza JC, Vallejo GA, Zingales B, Amplification of a specific repetitive DNA sequence for Trypanosoma rangeli identification and its potential application in epidemiological investigations. Exp Parasitol. 2000; 96(3): 147–159. 11162365
35. Treangen TJ, Salzberg SL, Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet. 2011; 13(1): 36–46. doi: 10.1038/nrg311722124482
36. Subirana JA, Messeguer X, A Satellite Explosion in the Genome of Holocentric Nematodes. PLoS One. 2013; 8(4): e62221. doi: 10.1371/journal.pone.006222123638010
37. Roset R, Subirana JA, Messeguer X, MREPATT: detection and analysis of exact consecutive repeats in genomic sequences. Bioinformatics. 2003; 19(18): 2475–2476. 14668235
38. Novák P, Neumann P, Macas J, Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics. 2010; 11:378. doi: 10.1186/1471-2105-11-37820633259
39. Novák P, Neumann P, Pech J, Steinhaisl J, Macas J, RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013; 29(6): 792–793. doi: 10.1093/bioinformatics/btt05423376349
40. Caruccio N, Preparation of next-generation sequencing libraries using Nextera technology: simultaneous DNA fragmentation and adapter tagging by in vitro transposition. Methods Mol Biol. 2011; 733: 241–55. doi: 10.1007/978-1-61779-089-8_1721431775
41. Nery SV, McCarthy JS, Traub R, Andrews RM, Black J, Gray D, et al. A cluster-randomized controlled trial integrating a community-based water, sanitation and hygiene programme with mass distribution of albendazole to reduce intestinal parasites in Timor-Leste: the WASH for WORMS research protocol. BMJ Open. 2015; 5(12): e009293. doi: 10.1136/bmjopen-2015-00929326719316
42. Llewellyn S, Inpankaew T, Nery S, Gray DJ, Verweij JJ, Clements ACA, et al. Application of a multiplex quantitative PCR to assess prevalence and intensity of intestinal parasite infections in a controlled clinical trial. PLoS Negl Trop Dis. 2016; 10(1): e0004380. doi: 10.1371/journal.pntd.000438026820626
43. U.S. Department of Health and Human Services Food and Drug Administration. Statistical guidance on reporting results from studies evaluating diagnostic tests. 2007. Available: http://www.fda.gov/MedicalDevices/DeviceRegulationandGuidance/GuidanceDocuments/ucm071148.htm.
44. R Core TeamR: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Australia. 2015. Available: https://www.r-project.org.
45. Gamer M, Lemon J, Fellows I, Singh P. Package ‘irr’: Various Coefficients of Interrater Reliability and Agreement. 2012. Available: https://cran.r-project.org/web/packages/irr/irr.pdf.
46. Meekums H, Hawash MB, Sparks AM, Oviedo Y, Sandoval C, Chico ME, et al. A genetic analysis of Trichuris trichiura and Trichuris suis from Ecuador. Parasit Vectors. 2015; 8: 168. doi: 10.1186/s13071-015-0782-925889461
47. George S, Kaliappan SP, Kattula D, Roy S, Geldhof P, Kang G, et al. Identification of Ancylostoma ceylanicum in Children from a tribal community in Tamil Nadu, India using a semi-nested PCR-RFLP tool. Trans R Soc Trop Med Hyg. 2015; 109(4): 283–285. doi: 10.1093/trstmh/trv00125618132
48. Masuda Y, Kishimoto T, Ito H, Tsuji M, Visceral larva migrans caused by Trichuris vulpis presenting as a pulmonary mass. Thorax. 1987; 42(12): 990–991. 3438889
49. Sakano T, Hamamoto K, Kobayashi Y, Sakata Y, Tsuji M, Usui T, Visceral larva migrans caused by Trichuris vulpis. Arch Dis Child. 1980; 55(8): 631–633. 7436519
50. Areekul P, Putaporntip C, Pattanawong U, Sitthicharoenchai P, Jongwutiwes S, Trichuris vulpis and T. trichiura infections among schoolchildren of a rural community in northwestern Thailand: the possible role of dogs in disease transmission. Asian Biomed. 2010; 4(1): 49–60.
51. Hendrix CM, Robinson E, Diagnostic Parasitology for Veterinary Technicians. 4th ed.Philadelphia: Elsevier Health Sciences; 2014.
52. Berger S, Infectious Diseases of East Timor. Los Angeles: GIDEON Informatics, Inc; 2015.
53. Hunt VL, Tsai IJ, Coghlan A, Reid AJ, Holroyd N, Foth BJ, et al. The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat Genet. 2016; doi: 10.1038/ng.3495
54. Tang YT, Gao X, Rosa BA, Abubucker S, Hallsworth-Pepin K, Martin J, et al. Genome of the human hookworm Necator americanus. Nat Genet. 2014; 46(3): 261–269. doi: 10.1038/ng.287524441737
55. Cuomo MJ, Noel LB, White DB. Diagnosing Medical Parasites: A Public Health Officers Guide to Assisting Laboratory and Medical Officers. USAF Air Education and Training Command, Randolph, TX: http://www.phsource.us/PH/PARA/; 2012.
56. Meštrović N, Pavlek M, Car A, Castagnone-Sereno P, Abad P, Plohl M, Conserved DNA Motifs, Including the CENP-B Box-like, are Possible Promoters of Satellite DNA Array Rearrangements in Nematodes. PLoS One. 2013; 8(6): e67328. 23826269
57. Plohl M, Luchetti A, Mestrović N, Mantovani B, Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene. 2008; 409(1–2): 72–82. doi: 10.1016/j.gene.2007.11.01318182173
58. da Cruz CJ. Livestock development in East Timor. In: Agriculture: New Directions for a New Nation—East Timor (Timor Leste). ACIAR Proceedings No. 113; 2003. pp. 11–16.
59. Tobler H, Etter A, Müller F, Chromatin diminution in nematode development. Trends Genet. 1992; 8(12): 427–432. 1492368
60. Goday C, Pimpinelli S, The occurrence, role and evolution of chromatin diminution in nematodes. Parasitol Today. 1993; 9(9): 319–322. 15463793
61. Etter A, Bernard V, Kenzelmann M, Tobler H, Müller F, Ribosomal heterogeneity from chromatin diminution in Ascaris lumbricoides. Science. 1994; 265(5174): 954–956. 8052853
62. Pilotte N, Torres M, Tomaino FR, Laney SJ, Williams SA, A TaqMan-based multiplex real-time PCR assay for the simultaneous detection of Wuchereria bancrofti and Brugia malayi. Mol Biochem Parasitol. 2013; 189(1–2): 33–37. doi: 10.1016/j.molbiopara.2013.05.00123669148
63. Tran AC, Halse TA, Escuyer VE, Musser KA, Detection of Mycobacterium avium complex DNA directly in clinical respiratory specimens: opportunities for improved turn-around time and cost savings. Diagn Microbiol Infect Dis. 2014; 79(1): 43–48. doi: 10.1016/j.diagmicrobio.2014.01.01924612561
64. Easton AV, Oliveira RG, O’Connell EM, Kepha S, Mwandawiro CS, Njenja SM, et al. Multi-parallel qPCR provides increased sensitivity and diagnostic breadth for gastrointestinal parasites of humans: field-based inferences on the impact of mass deworming. Parasit Vectors. 2016; 9(1): 38. doi: 10.1186/s13071-016-1314-y26813411
65. Schmaedick MA, Koppel AL, Pilotte N, Torres M, Williams SA, Dobson SL, et al. Molecular xenomonitoring using mosquitoes to map lymphatic filariasis after mass drug administration in American Samoa. PLoS Negl Trop Dis. 2014; 8(8): e3087. doi: 10.1371/journal.pntd.000308725122037
66. Rao RU, Nagodavithana KC, Samarasekera SD, Wijegunawardana AD, Premakumara WD, Perera SN, et al. A comprehensive assessment of lymphatic filariasis in Sri Lanka six years after cessation of mass drug administration. PLoS Negl Trop Dis. 2014; 8(11): e3281. doi: 10.1371/journal.pntd.000328125393404
67. Lamberton PH, Cheke RA, Winskill P, Tirados I, Walker M, Osei-Atweneboana MY, et al. Onchocerciasis transmission in Ghana: persistence under different control strategies and the roll of the simulidd vectors. PLoS Negl Trop Dis. 2015; 9(4): e0003688. doi: 10.1371/journal.pntd.000368825897492
68. Rodríguez-Pérez MA, Lilley BG, Domínguez-Vázquez A, Segura-Arenas R, Lizarazo-Ortega C, Mendoza-Herrera A, et al. Polymerase chain reaction monitoring of transmission of Onchocerca volvulus of two endemic states in Mexico. Am J Trop Med Hyg. 2004; 70(1): 38–45. 14971696
69. Rodríguez-Pérez MA, Gopal H, Adeleke MA, De Luna-Santillana EJ, Gurrola-Reyes JN, Guo X, Detection of Onchocerca volvulus in Latin American black flies for pool screening PCR using high-throughput automated DNA isolation for transmission surveillance. Parasitol Res. 2013; 112(11): 3925–3931. doi: 10.1007/s00436-013-3583-024030195
70. Fung MS, Xiao N, Wang S, Carlton EJ, Field evaluation of a PCR test for Schistosoma japonicum egg detection in low-prevalence regions of China. Am J Trop Med Hyg. 2012; 87(6): 1053–1058. doi: 10.4269/ajtmh.2012.12-017723109374
71. Kure A, Mekonnen Z, Dana D, Bajiro M, Ayana M, Vercruysse J, et al. Comparison of individual and pooled stool samples for the assessment of intensity of Schistosoma mansoni and soil-transmitted helminth infections using the Kato-Katz technique. Parasit Vectors. 2015; 8:489. 26400064
72. Speich B, Knopp S, Mohammed KA, Khamis IS, Rinaldi L, Cringoli G, et al. Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasit Vectors. 2010; 3:71. doi: 10.1186/1756-3305-3-7120707931
73. Markoulatos P, Siafakas N, Moncany M, Multiplex Polymerase Chain Reaction: A Practical Approach. J Clin Lab Anal. 2002; 16(1): 47–51. 11835531