Chapter 27 : Molecular Diagnosis of Gastrointestinal Infections

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Enteric infections cause significant morbidity, mortality, and financial cost worldwide. This chapter discusses the molecular techniques for laboratory detection of the bacteria, viruses, and parasites most commonly responsible for infection of the lower gastrointestinal tract.

Citation: Pinsky B, Banaei N. 2016. Molecular Diagnosis of Gastrointestinal Infections, p 362-385. In Persing D, Tenover F, Hayden R, Ieven M, Miller M, Nolte F, Tang Y, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555819071.ch27
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1. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV . 1999. Food-related illness and death in the United States. Emerg Infect Dis 5 : 607 625[CrossRef].[PubMed]
2. Thompson FL, Iida T, Swings J . 2004. Biodiversity of vibrios. Microbiol Mol Biol Rev 68 : 403 431[CrossRef].[PubMed]
3. Paton JC, Paton AW . 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11 : 450 479.[PubMed]
4. Besser RE, Griffin PM, Slutsker L . 1999. Escherichia coli O157:H7 gastroenteritis and the hemolytic uremic syndrome: an emerging infectious disease. Annu Rev Med 50 : 355 367[CrossRef].[PubMed]
5. Lefterova MI, Slater KA, Budvytiene I, Dadone PA, Banaei N . 2013. A sensitive multiplex, real-time PCR assay for prospective detection of Shiga toxin-producing Escherichia coli from stool samples reveals similar incidences but variable severities of non-O157 and O157 infections in northern California. J Clin Microbiol 51 : 3000 3005[CrossRef].[PubMed]
6. Brooks JT, Sowers EG, Wells JG, Greene KD, Griffin PM, Hoekstra RM, Strockbine NA . 2005. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002. J Infect Dis 192 : 1422 1429[CrossRef].[PubMed]
7. Hadler JL, Clogher P, Hurd S, Phan Q, Mandour M, Bemis K, Marcus R . 2011. Ten-year trends and risk factors for non-O157 Shiga toxin-producing Escherichia coli found through Shiga toxin testing, Connecticut, 2000–2009. Clin Infect Dis 53 : 269 276[CrossRef].[PubMed]
8. Brown JA, Hite DS, Gillim-Ross LA, Maguire HF, Bennett JK, Patterson JJ, Comstock NA, Watkins AK, Ghosh TS, Vogt RL . 2012. Outbreak of shiga toxin-producing Escherichia coli serotype O26: H11 infection at a child care center in Colorado. Pediatr Infect Dis J 31 : 379 383[CrossRef].[PubMed]
9. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Müller L, King LA, Rosner B, Buchholz U, Stark K, Krause G , HUS Investigation Team . 2011. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365 : 1771 1780[CrossRef].[PubMed]
10. Prager R, Annemüller S, Tschäpe H . 2005. Diversity of virulence patterns among shiga toxin-producing Escherichia coli from human clinical cases-need for more detailed diagnostics. Int J Med Microbiol 295 : 29 38[CrossRef].[PubMed]
11. Weinstein DL, Jackson MP, Samuel JE, Holmes RK, O'Brien AD . 1988. Cloning and sequencing of a Shiga-like toxin type II variant from Escherichia coli strain responsible for edema disease of swine. J Bacteriol 170 : 4223 4230.[PubMed]
12. Mackenzie AM, Lebel P, Orrbine E, Rowe PC, Hyde L, Chan F, Johnson W, McLaine PN . 1998. Sensitivities and specificities of premier E. coli O157 and premier EHEC enzyme immunoassays for diagnosis of infection with verotxin (Shiga-like toxin)-producing Escherichia coli. The SYNSORB Pk Study investigators. J Clin Microbiol 36 : 1608 1611.[PubMed]
13. Gould LH, Bopp C, Strockbine N, Atkinson R, Baselski V, Body B, Carey R, Crandall C, Hurd S, Kaplan R, Neill M, Shea S, Somsel P, Tobin-D'Angelo M, Griffin PM, Gerner-Smidt P , Centers for Disease Control and Prevention (CDC) . 2009. Recommendations for diagnosis of shiga toxin—producing Escherichia coli infections by clinical laboratories. MMWR Recomm Rep 58( RR-12) : 1 14.[PubMed]
14. Louie M, Read S, Simor AE, Holland J, Louie L, Ziebell K, Brunton J, Hii J . 1998. Application of multiplex PCR for detection of non-O157 verocytotoxin-producing Escherichia coli in bloody stools: identification of serogroups O26 and O111. J Clin Microbiol 36 : 3375 3377.[PubMed]
15. Bélanger SD, Boissinot M, Ménard C, Picard FJ, Bergeron MG . 2002. Rapid detection of Shiga toxin-producing bacteria in feces by multiplex PCR with molecular beacons on the smart cycler. J Clin Microbiol 40 : 1436 1440[CrossRef].[PubMed]
16. Sharma VK, Dean-Nystrom EA, Casey TA . 1999. Semi-automated fluorogenic PCR assays (TaqMan) for rapid detection of Escherichia coli O157:H7 and other shiga toxigenic E. coli. Mol Cell Probes 13 : 291 302[CrossRef].[PubMed]
17. Reischl U, Youssef MT, Kilwinski J, Lehn N, Zhang WL, Karch H, Strockbine NA . 2002. Real-time fluorescence PCR assays for detection and characterization of Shiga toxin, intimin, and enterohemolysin genes from Shiga toxin-producing Escherichia coli. J Clin Microbiol 40 : 2555 2565[CrossRef].[PubMed]
18. Claas EC, Burnham CA, Mazzulli T, Templeton K, Topin F . 2013. Performance of the xTAG® gastrointestinal pathogen panel, a multiplex molecular assay for simultaneous detection of bacterial, viral, and parasitic causes of infectious gastroenteritis. J Microbiol Biotechnol 23 : 1041 1045[CrossRef].[PubMed]
19. Bielaszewska M, Köck R, Friedrich AW, von Eiff C, Zimmerhackl LB, Karch H, Mellmann A . 2007. Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS One 2 : e1024[CrossRef].[PubMed]
20. Gannon VP, Rashed M, King RK, Thomas EJ . 1993. Detection and characterization of the eae gene of Shiga-like toxin-producing Escherichia coli using polymerase chain reaction. J Clin Microbiol 31 : 1268 1274.[PubMed]
21. Iijima Y, Asako NT, Aihara M, Hayashi K . 2004. Improvement in the detection rate of diarrhoeagenic bacteria in human stool specimens by a rapid real-time PCR assay. J Med Microbiol 53 : 617 622[CrossRef].[PubMed]
22. Samuel MC, Vugia DJ, Shallow S, Marcus R, Segler S, McGivern T, Kassenborg H, Reilly K, Kennedy M, Angulo F, Tauxe RV , Emerging Infections Program FoodNet Working Group . 2004. Epidemiology of sporadic Campylobacter infection in the United States and declining trend in incidence, FoodNet 1996–1999. Clin Infect Dis 38( Suppl 3): S165 S174.
23. Tauxe RV, Patton CM, Edmonds P, Barrett TJ, Brenner DJ, Blake PA . 1985. Illness associated with Campylobacter laridis, a newly recognized Campylobacter species. J Clin Microbiol 21 : 222 225.[PubMed]
24. Goossens H, Vlaes L, De Boeck M, Pot B, Kersters K, Levy J, De Mol P, Butzler JP, Vandamme P . 1990. Is “ Campylobacter upsaliensis” an unrecognised cause of human diarrhoea? Lancet 335 : 584 586[CrossRef].[PubMed]
25. Friedman CR, Hoekstra RM, Samuel M, Marcus R, Bender J, Shiferaw B, Reddy S, Ahuja SD, Helfrick DL, Hardnett F, Carter M, Anderson B, Tauxe RV , Emerging Infections Program FoodNet Working Group . 2004. Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin Infect Dis 38( Suppl 3): S285 S296.
26. Nachamkin I, Allos BM, Ho T . 1998. Campylobacter species and Guillain-Barré syndrome. Clin Microbiol Rev 11 : 555 567.[PubMed]
27. Rautelin H, Jusufovic J, Hänninen ML . 1999. Identification of hippurate-negative thermophilic campylobacters. Diagn Microbiol Infect Dis 35 : 9 12[CrossRef].[PubMed]
28. Luber P, Wagner J, Hahn H, Bartelt E . 2003. Antimicrobial resistance in Campylobacter jejuni and Campylobacter coli strains isolated in 1991 and 2001–2002 from poultry and humans in Berlin, Germany. Antimicrob Agents Chemother 47 : 3825 3830[CrossRef].[PubMed]
29. Linton D, Lawson AJ, Owen RJ, Stanley J . 1997. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol 35 : 2568 2572.[PubMed]
30. Best EL, Powell EJ, Swift C, Grant KA, Frost JA . 2003. Applicability of a rapid duplex real-time PCR assay for speciation of Campylobacter jejuni and Campylobacter coli directly from culture plates. FEMS Microbiol Lett 229 : 237 241[CrossRef].[PubMed]
31. LaGier MJ, Joseph LA, Passaretti TV, Musser KA, Cirino NM . 2004. A real-time multiplexed PCR assay for rapid detection and differentiation of Campylobacter jejuni and Campylobacter coli. Mol Cell Probes 18 : 275 282[CrossRef].[PubMed]
32. Schuurman T, de Boer RF, van Zanten E, van Slochteren KR, Scheper HR, Dijk-Alberts BG, Möller AV, Kooistra-Smid AM . 2007. Feasibility of a molecular screening method for detection of Salmonella enterica and Campylobacter jejuni in a routine community-based clinical microbiology laboratory. J Clin Microbiol 45 : 3692 3700[CrossRef].[PubMed]
33. Ghosh R, Uppal B, Aggarwal P, Chakravarti A, Jha AK, Dubey AP . 2014. A comparative study of conventional and molecular techniques in diagnosis of campylobacter gastroenteritis in children. Ann Clin Lab Sci 44 : 42 48.[PubMed]
34. Onori M, Coltella L, Mancinelli L, Argentieri M, Menichella D, Villani A, Grandin A, Valentini D, Raponi M, Russo C . 2014. Evaluation of a multiplex PCR assay for simultaneous detection of bacterial and viral enteropathogens in stool samples of paediatric patients. Diagn Microbiol Infect Dis 79 : 149 154[CrossRef].[PubMed]
35. Jensen AN, Andersen MT, Dalsgaard A, Baggesen DL, Nielsen EM . 2005. Development of real-time PCR and hybridization methods for detection and identification of thermophilic Campylobacter spp. in pig faecal samples. J Appl Microbiol 99 : 292 300[CrossRef].[PubMed]
36. Logan JM, Edwards KJ, Saunders NA, Stanley J . 2001. Rapid identification of Campylobacter spp. by melting peak analysis of biprobes in real-time PCR. J Clin Microbiol 39 : 2227 2232[CrossRef].[PubMed]
37. Centers for Disease Control and Prevention . 2004. Salmonella Surveillance: Annual Summary, 2003. U.S. Department of Health and Human Services, CDC, Atlanta, GA.
38. Leclercq A, Martin L, Vergnes ML, Ounnoughene N, Laran JF, Giraud P, Carniel E . 2005. Fatal Yersinia enterocolitica biotype 4 serovar O:3 sepsis after red blood cell transfusion. Transfusion 45 : 814 818[CrossRef].[PubMed]
39. Jones TF, Buckingham SC, Bopp CA, Ribot E, Schaffner W . 2003. From pig to pacifier: chitterling-associated yersiniosis outbreak among black infants. Emerg Infect Dis 9 : 1007 1009[CrossRef].[PubMed]
40. Khan AM, Faruque AS, Hossain MS, Sattar S, Fuchs GJ, Salam MA . 2004. Plesiomonas shigelloides-associated diarrhoea in Bangladeshi children: a hospital-based surveillance study. J Trop Pediatr 50 : 354 356[CrossRef].[PubMed]
41. Hsu BM, Wu SF, Huang SW, Tseng YJ, Ji DD, Chen JS, Shih FC . 2010. Differentiation and identification of Shigella spp. and enteroinvasive Escherichia coli in environmental waters by a molecular method and biochemical test. Water Res 44 : 949 955[CrossRef].[PubMed]
42. Sethabutr O, Venkatesan M, Murphy GS, Eampokalap B, Hoge CW, Echeverria P . 1993. Detection of Shigellae and enteroinvasive Escherichia coli by amplification of the invasion plasmid antigen H DNA sequence in patients with dysentery. J Infect Dis 167 : 458 461[CrossRef].[PubMed]
43. Souza TB, Lozer DM, Kitagawa SM, Spano LC, Silva NP, Scaletsky IC . 2013. Real-time multiplex PCR assay and melting curve analysis for identifying diarrheagenic Escherichia coli. J Clin Microbiol 51 : 1031 1033[CrossRef].[PubMed]
44. Bleves S, Cornelis GR . 2000. How to survive in the host: the Yersinia lesson. Microbes Infect 2 : 1451 1460[CrossRef].[PubMed]
45. Khare R, Espy MJ, Cebelinski E, Boxrud D, Sloan LM, Cunningham SA, Pritt BS, Patel R, Binnicker MJ . 2014. Comparative evaluation of two commercial multiplex panels for detection of gastrointestinal pathogens by use of clinical stool specimens. J Clin Microbiol 52 : 3667 3673.
46. Fukushima H, Tsunomori Y, Seki R . 2003. Duplex real-time SYBR green PCR assays for detection of 17 species of food- or waterborne pathogens in stools. J Clin Microbiol 41 : 5134 5146[CrossRef].[PubMed]
47. Wang L, Li Y, Mustaphai A . 2007. Rapid and simultaneous quantitation of Escherichia coli 0157:H7, Salmonella, and Shigella in ground beef by multiplex real-time PCR and immunomagnetic separation. J Food Prot 70 : 1366 1372.[PubMed]
48. Shi XL, Hu QH, Zhang JF, Li QG, Wang B, Lin YM, Zhuang ZX, Liu XL, Zhang SX . 2006. [Rapid simultaneous detection of Salmonella and Shigella using modified molecular beacons and real-time PCR]. Zhonghua Liu Xing Bing Xue Za Zhi 27 : 1053 1056. (In Chinese.)[PubMed]
49. Versalovic J, Carroll KC, Jorgensen JH, Funke G, Landry ML, Warnock DW (ed). 2011. Manual of Clinical Microbiology, 10th ed. ASM Press, Washington, DC.
50. Abbott SL, Seli LS, Catino M Jr, Hartley MA, Janda JM . 1998. Misidentification of unusual Aeromonas species as members of the genus Vibrio: a continuing problem. J Clin Microbiol 36 : 1103 1104.[PubMed]
51. Dieckmann R, Strauch E, Alter T . 2010. Rapid identification and characterization of Vibrio species using whole-cell MALDI-TOF mass spectrometry. J Appl Microbiol 109 : 199 211.[PubMed]
52. Nhung PH, Ohkusu K, Miyasaka J, Sun XS, Ezaki T . 2007. Rapid and specific identification of 5 human pathogenic Vibrio species by multiplex polymerase chain reaction targeted to dnaJ gene. Diagn Microbiol Infect Dis 59 : 271 275[CrossRef].[PubMed]
53. Tarr CL, Patel JS, Puhr ND, Sowers EG, Bopp CA, Strockbine NA . 2007. Identification of Vibrio isolates by a multiplex PCR assay and rpoB sequence determination. J Clin Microbiol 45 : 134 140[CrossRef].[PubMed]
54. Bauer A, Rørvik LM . 2007. A novel multiplex PCR for the identification of Vibrio parahaemolyticus, Vibrio cholerae and Vibrio vulnificus. Lett Appl Microbiol 45 : 371 375[CrossRef].[PubMed]
55. Tracz DM, Backhouse PG, Olson AB, McCrea JK, Walsh JA, Ng LK, Gilmour MW . 2007. Rapid detection of Vibrio species using liquid microsphere arrays and real-time PCR targeting the ftsZ locus. J Med Microbiol 56 : 56 65[CrossRef].[PubMed]
56. Lyerly DM, Krivan HC, Wilkins TD . 1988. Clostridium difficile: its disease and toxins. Clin Microbiol Rev 1 : 1 18.[PubMed]
57. Bartlett JG . 2002. Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 346 : 334 339[CrossRef].[PubMed]
58. McGlone SM, Bailey RR, Zimmer SM, Popovich MJ, Tian Y, Ufberg P, Muder RR, Lee BY . 2012. The economic burden of Clostridium difficile. Clin Microbiol Infect 18 : 282 289[CrossRef].[PubMed]
59. Kyne L, Hamel MB, Polavaram R, Kelly CP . 2002. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 34 : 346 353[CrossRef].[PubMed]
60. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson TJ, Horn R, René P, Monczak Y, Dascal A . 2005. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 353 : 2442 2449[CrossRef].[PubMed]
61. McDonald LC, Killgore GE, Thompson A, Owens RC Jr, Kazakova SV, Sambol SP, Johnson S, Gerding DN . 2005. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 353 : 2433 2441[CrossRef].[PubMed]
62. Johnson S, Samore MH, Farrow KA, Killgore GE, Tenover FC, Lyras D, Rood JI, DeGirolami P, Baltch AL, Rafferty ME, Pear SM, Gerding DN . 1999. Epidemics of diarrhea caused by a clindamycin-resistant strain of Clostridium difficile in four hospitals. N Engl J Med 341 : 1645 1651[CrossRef].[PubMed]
63. Gaynes R, Rimland D, Killum E, Lowery HK, Johnson TM II, Killgore G, Tenover FC . 2004. Outbreak of Clostridium difficile infection in a long-term care facility: association with gatifloxacin use. Clin Infect Dis 38 : 640 645[CrossRef].[PubMed]
64. Brown E, Talbot GH, Axelrod P, Provencher M, Hoegg C . 1990. Risk factors for Clostridium difficile toxin-associated diarrhea. Infect Control Hosp Epidemiol 11 : 283 290[CrossRef].[PubMed]
65. Kelly CP, Pothoulakis C, LaMont JT . 1994. Clostridium difficile colitis. N Engl J Med 330 : 257 262[CrossRef].[PubMed]
66. Gülke I, Pfeifer G, Liese J, Fritz M, Hofmann F, Aktories K, Barth H . 2001. Characterization of the enzymatic component of the ADP-ribosyltransferase toxin CDTa from Clostridium difficile. Infect Immun 69 : 6004 6011[CrossRef].[PubMed]
67. Lyras D, O'Connor JR, Howarth PM, Sambol SP, Carter GP, Phumoonna T, Poon R, Adams V, Vedantam G, Johnson S, Gerding DN, Rood JI . 2009. Toxin B is essential for virulence of Clostridium difficile. Nature 458 : 1176 1179[CrossRef].[PubMed]
68. Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, Minton NP . 2010. The role of toxin A and toxin B in Clostridium difficile infection. Nature 467 : 711 713[CrossRef].[PubMed]
69. Johnson S, Kent SA, O'Leary KJ, Merrigan MM, Sambol SP, Peterson LR, Gerding DN . 2001. Fatal pseudomembranous colitis associated with a variant clostridium difficile strain not detected by toxin A immunoassay. Ann Intern Med 135 : 434 438[CrossRef].[PubMed]
70. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, Yamamoto T, Suzuki K, Kim SM, Chong Y, Wasito EB . 1998. Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol 36 : 2178 2182.[PubMed]
71. Geric B, Rupnik M, Gerding DN, Grabnar M, Johnson S . 2004. Distribution of Clostridium difficile variant toxinotypes and strains with binary toxin genes among clinical isolates in an American hospital. J Med Microbiol 53 : 887 894[CrossRef].[PubMed]
72. Shin BM, Kuak EY, Lee EJ, Songer JG . 2009. Algorithm combining toxin immunoassay and stool culture for diagnosis of Clostridium difficile infection. J Clin Microbiol 47 : 2952 2956[CrossRef].[PubMed]
73. Larson HE, Barclay FE, Honour P, Hill ID . 1982. Epidemiology of Clostridium difficile in infants. J Infect Dis 146 : 727 733[CrossRef].[PubMed]
74. McFarland LV, Mulligan ME, Kwok RY, Stamm WE . 1989. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320 : 204 210[CrossRef].[PubMed]
75. Alasmari F, Seiler SM, Hink T, Burnham CA, Dubberke ER . 2014. Prevalence and risk factors for asymptomatic Clostridium difficile carriage. Clin Infect Dis 59 : 216 222[CrossRef].[PubMed]
76. Galdys AL, Nelson JS, Shutt KA, Schlackman JL, Pakstis DL, Pasculle AW, Marsh JW, Harrison LH, Curry SR . 2014. Prevalence and duration of asymptomatic Clostridium difficile carriage among healthy subjects in Pittsburgh, Pennsylvania. J Clin Microbiol 52 : 2406 2409[CrossRef].[PubMed]
77. Leekha S, Aronhalt KC, Sloan LM, Patel R, Orenstein R . 2013. Asymptomatic Clostridium difficile colonization in a tertiary care hospital: admission prevalence and risk factors. Am J Infect Control 41 : 390 393[CrossRef].[PubMed]
78. Samore MH, DeGirolami PC, Tlucko A, Lichtenberg DA, Melvin ZA, Karchmer AW . 1994. Clostridium difficile colonization and diarrhea at a tertiary care hospital. Clin Infect Dis 18 : 181 187[CrossRef].[PubMed]
79. Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN, Johnson S, Linn FV, Peterson LR, Gerding DN . 1990. Nosocomial Clostridium difficile colonisation and disease. Lancet 336 : 97 100[CrossRef].[PubMed]
80. Clabots CR, Johnson S, Olson MM, Peterson LR, Gerding DN . 1992. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 166 : 561 567[CrossRef].[PubMed]
81. van den Berg RJ, Vaessen N, Endtz HP, Schülin T, van der Vorm ER, Kuijper EJ . 2007. Evaluation of real-time PCR and conventional diagnostic methods for the detection of Clostridium difficile-associated diarrhoea in a prospective multicentre study. J Med Microbiol 56 : 36 42[CrossRef].[PubMed]
82. Peterson LR, Robicsek A . 2009. Does my patient have Clostridium difficile infection? Ann Intern Med 151 : 176 179[CrossRef].[PubMed]
83. Luo RF, Spradley S, Banaei N . 2013. Alerting physicians during electronic order entry effectively reduces unnecessary repeat PCR testing for Clostridium difficile. J Clin Microbiol 51 : 3872 3874[CrossRef].[PubMed]
84. Delmée M . 2001. Laboratory diagnosis of Clostridium difficile disease. Clin Microbiol Infect 7 : 411 416[CrossRef].[PubMed]
85. Peterson LR, Manson RU, Paule SM, Hacek DM, Robicsek A, Thomson RB Jr, Kaul KL . 2007. Detection of toxigenic Clostridium difficile in stool samples by real-time polymerase chain reaction for the diagnosis of C. difficile-associated diarrhea. Clin Infect Dis 45 : 1152 1160[CrossRef].[PubMed]
86. Peterson LR, Kelly PJ . 1993. The role of the clinical microbiology laboratory in the management of Clostridium difficile-associated diarrhea. Infect Dis Clin North Am 7 : 277 293.[PubMed]
87. Barbut F, Kajzer C, Planas N, Petit JC . 1993. Comparison of three enzyme immunoassays, a cytotoxicity assay, and toxigenic culture for diagnosis of Clostridium difficile-associated diarrhea. J Clin Microbiol 31 : 963 967.[PubMed]
88. Shetty N, Wren MW, Coen PG . 2011. The role of glutamate dehydrogenase for the detection of Clostridium difficile in faecal samples: a meta-analysis. J Hosp Infect 77 : 1 6[CrossRef].[PubMed]
89. Sharp SE, Ruden LO, Pohl JC, Hatcher PA, Jayne LM, Ivie WM . 2010. Evaluation of the C.Diff Quik Chek Complete Assay, a new glutamate dehydrogenase and A/B toxin combination lateral flow assay for use in rapid, simple diagnosis of clostridium difficile disease. J Clin Microbiol 48 : 2082 2086[CrossRef].[PubMed]
90. Ticehurst JR, Aird DZ, Dam LM, Borek AP, Hargrove JT, Carroll KC . 2006. Effective detection of toxigenic Clostridium difficile by a two-step algorithm including tests for antigen and cytotoxin. J Clin Microbiol 44 : 1145 1149[CrossRef].[PubMed]
91. Gilligan PH . 2008. Is a two-step glutamate dehyrogenase antigen-cytotoxicity neutralization assay algorithm superior to the premier toxin A and B enzyme immunoassay for laboratory detection of Clostridium difficile? J Clin Microbiol 46 : 1523 1525[CrossRef].[PubMed]
92. Quinn CD, Sefers SE, Babiker W, He Y, Alcabasa R, Stratton CW, Carroll KC, Tang YW . 2010. C. Diff Quik Chek complete enzyme immunoassay provides a reliable first-line method for detection of Clostridium difficile in stool specimens. J Clin Microbiol 48 : 603 605[CrossRef].[PubMed]
93. Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, Krishna S . 2008. Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect Dis 8 : 777 784[CrossRef].[PubMed]
94. Planche TD, Davies KA, Coen PG, Finney JM, Monahan IM, Morris KA, O'Connor L, Oakley SJ, Pope CF, Wren MW, Shetty NP, Crook DW, Wilcox MH . 2013. Differences in outcome according to Clostridium difficile testing method: a prospective multicentre diagnostic validation study of C difficile infection. Lancet Infect Dis 13 : 936 945[CrossRef].[PubMed]
95. Burnham CA, Carroll KC . 2013. Diagnosis of Clostridium difficile infection: an ongoing conundrum for clinicians and for clinical laboratories. Clin Microbiol Rev 26 : 604 630[CrossRef].[PubMed]
96. Deshpande A, Pasupuleti V, Rolston DD, Jain A, Deshpande N, Pant C, Hernandez AV . 2011. Diagnostic accuracy of real-time polymerase chain reaction in detection of Clostridium difficile in the stool samples of patients with suspected Clostridium difficile Infection: a meta-analysis. Clin Infect Dis 53 : e81 e90[CrossRef].[PubMed]
97. Schroeder LF, Robilotti E, Peterson LR, Banaei N, Dowdy DW, Patel R . 2014. Economic evaluation of laboratory testing strategies for hospital-associated Clostridium difficile infection. J Clin Microbiol 52 : 489 496[CrossRef].[PubMed]
98. Longtin Y, Trottier S, Brochu G, Paquet-Bolduc B, Garenc C, Loungnarath V, Beaulieu C, Goulet D, Longtin J . 2013. Impact of the type of diagnostic assay on Clostridium difficile infection and complication rates in a mandatory reporting program. Clin Infect Dis 56 : 67 73[CrossRef].[PubMed]
99. Guerrero DM, Chou C, Jury LA, Nerandzic MM, Cadnum JC, Donskey CJ . 2011. Clinical and infection control implications of Clostridium difficile infection with negative enzyme immunoassay for toxin. Clin Infect Dis 53 : 287 290[CrossRef].[PubMed]
100. Humphries RM, Uslan DZ, Rubin Z . 2013. Performance of Clostridium difficile toxin enzyme immunoassay and nucleic acid amplification tests stratified by patient disease severity. J Clin Microbiol 51 : 869 873[CrossRef].[PubMed]
101. Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI . 2003. Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9 : 565 572[CrossRef].[PubMed]
102. Centers for Disease Control and Prevention (CDC) . 2008. Delayed onset and diminished magnitude of rotavirus activity—United States, November 2007-May 2008. MMWR Morb Mortal Wkly Rep 57 : 697700.[PubMed]
103. Bines J . 2006. Intussusception and rotavirus vaccines. Vaccine 24 : 3772 3776[CrossRef].[PubMed]
104. Vesikari T, Karvonen A, Prymula R, Schuster V, Tejedor JC, Cohen R, Meurice F, Han HH, Damaso S, Bouckenooghe A . 2007. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet 370 : 1757 1763[CrossRef].[PubMed]
105. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T, Clemens SC, Cheuvart B, Espinoza F, Gillard P, Innis BL, Cervantes Y, Linhares AC, López P, Macías-Parra M, Ortega-Barría E, Richardson V, Rivera-Medina DM, Rivera L, Salinas B, Pavía-Ruz N, Salmerón J, Rüttimann R, Tinoco JC, Rubio P, Nuñez E, Guerrero ML, Yarzábal JP, Damaso S, Tornieporth N, Sáez-Llorens X, Vergara RF, Vesikari T, Bouckenooghe A, Clemens R, De Vos B, O'Ryan M , Human Rotavirus Vaccine Study Group . 2006. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med 354 : 11 22[CrossRef].[PubMed]
106. Parashar UD, Alexander JP, Glass RI , Advisory Committee on Immunization Practices (ACIP), Centers for Disease Control and Prevention (CDC) . 2006. Prevention of rotavirus gastroenteritis among infants and children. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 55( RR-12) : 1 13.[PubMed]
107. Leshem E, Moritz RE, Curns AT, Zhou F, Tate JE, Lopman BA, Parashar UD . 2014. Rotavirus vaccines and health care utilization for diarrhea in the United States (2007–2011). Pediatrics 134 : 15 23[CrossRef].[PubMed]
108. Aballéa S, Millier A, Quilici S, Caroll S, Petrou S, Toumi M . 2013. A critical literature review of health economic evaluations of rotavirus vaccination. Hum Vaccin Immunother 9 : 1272 1288[CrossRef].[PubMed]
109. Bishop RF, Davidson GP, Holmes IH, Ruck BJ . 1973. Virus particles in epithelial cells of duodenal mucosa from children with acute non-bacterial gastroenteritis. Lancet 2 : 1281 1283[CrossRef].[PubMed]
110. Desselberger U, Gray J . 2003. Viral Gastroenteritis, vol 9. Elsevier, Amsterdam.[CrossRef]
111. King AMQ, Adams MJ, Carstens EB, Lefkowitz E (ed). 2012. Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. International Committee on Taxonomy of Viruses. Elsevier/Academic Press, Amsterdam, The Netherlands.
112. Santos N, Hoshino Y . 2005. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15 : 29 56[CrossRef].[PubMed]
113. Bányai K, László B, Duque J, Steele AD, Nelson EA, Gentsch JR, Parashar UD . 2012. Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30( Suppl 1) : A122 A130[CrossRef].[PubMed]
114. Dennehy PH, Schutzbank TE, Thorne GM . 1994. Evaluation of an automated immunodiagnostic assay, VIDAS Rotavirus, for detection of rotavirus in fecal specimens. J Clin Microbiol 32 : 825 827.[PubMed]
115. Dennehy PH, Hartin M, Nelson SM, Reising SF . 1999. Evaluation of the ImmunoCardSTAT! rotavirus assay for detection of group A rotavirus in fecal specimens. J Clin Microbiol 37 : 1977 1979.[PubMed]
116. Lipson SM, Svenssen L, Goodwin L, Porti D, Danzi S, Pergolizzi R . 2001. Evaluation of two current generation enzyme immunoassays and an improved isolation-based assay for the rapid detection and isolation of rotavirus from stool. J Clin Virol 21 : 17 27[CrossRef].[PubMed]
117. Thomas EE, Roscoe DL, Book L, Bone B, Browne L, Mah V . 1994. The utility of latex agglutination assays in the diagnosis of pediatric viral gastroenteritis. Am J Clin Pathol 101 : 742 746.[PubMed]
118. Buesa J, Colomina J, Raga J, Villanueva A, Prat J . 1996. Evaluation of reverse transcription and polymerase chain reaction (RT/PCR) for the detection of rotaviruses: applications of the assay. Res Virol 147 : 353 361[CrossRef].[PubMed]
119. Gunson RN, Miller J, Leonard A, Carman WF . 2003. Importance of PCR in the diagnosis and understanding of rotavirus illness in the community. Commun Dis Public Health 6 : 63 65.[PubMed]
120. Pang XL, Joensuu J, Hoshino Y, Kapikian AZ, Vesikari T . 1999. Rotaviruses detected by reverse transcription polymerase chain reaction in acute gastroenteritis during a trial of rhesus-human reassortant rotavirus tetravalent vaccine: implications for vaccine efficacy analysis. J Clin Virol 13 : 9 16[CrossRef].[PubMed]
121. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY . 1990. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28 : 276 282.[PubMed]
122. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK . 1992. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30 : 1365 1373.[PubMed]
123. Gutiérrez-Aguirre I, Steyer A, Boben J, Gruden K, Poljsak-Prijatelj M, Ravnikar M . 2008. Sensitive detection of multiple rotavirus genotypes with a single reverse transcription-real-time quantitative PCR assay. J Clin Microbiol 46 : 2547 2554[CrossRef].[PubMed]
124. Wu H, Taniguchi K, Wakasugi F, Ukae S, Chiba S, Ohseto M, Hasegawa A, Urasawa T, Urasawa S . 1994. Survey on the distribution of the gene 4 alleles of human rotaviruses by polymerase chain reaction. Epidemiol Infect 112 : 615 622[CrossRef].[PubMed]
125. Arista S, Vizzi E, Alaimo C, Palermo D, Cascio A . 1999. Identification of human rotavirus strains with the P[14] genotype by PCR. J Clin Microbiol 37 : 2706 2708.[PubMed]
126. Ushijima H, Koike H, Mukoyama A, Hasegawa A, Nishimura S, Gentsch J . 1992. Detection and serotyping of rotaviruses in stool specimens by using reverse transcription and polymerase chain reaction amplification. J Med Virol 38 : 292 297[CrossRef].[PubMed]
127. Banerjee I, Ramani S, Primrose B, Iturriza-Gomara M, Gray JJ, Brown DW, Kang G . 2007. Modification of rotavirus multiplex RT-PCR for the detection of G12 strains based on characterization of emerging G12 rotavirus strains from South India. J Med Virol 79 : 1413 1421[CrossRef].[PubMed]
128. Iturriza-Gómara M, Green J, Brown DW, Desselberger U, Gray JJ . 2000. Diversity within the VP4 gene of rotavirus P[8] strains: implications for reverse transcription-PCR genotyping. J Clin Microbiol 38 : 898 901.[PubMed]
129. Iturriza-Gómara M, Kang G, Gray J . 2004. Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol 31 : 259 265[CrossRef].[PubMed]
130. Min BS, Noh YJ, Shin JH, Baek SY, Min KI, Ryu SR, Kim BG, Park MK, Choi SE, Yang EH, Park SN, Hur SJ, Ahn BY . 2006. Assessment of the quantitative real-time polymerase chain reaction using a cDNA standard for human group A rotavirus. J Virol Methods 137 : 280 286[CrossRef].[PubMed]
131. Schwarz BA, Bange R, Vahlenkamp TW, Johne R, Müller H . 2002. Detection and quantitation of group A rotaviruses by competitive and real-time reverse transcription-polymerase chain reaction. J Virol Methods 105 : 277 285[CrossRef].[PubMed]
132. Kang G, Iturriza-Gomara M, Wheeler JG, Crystal P, Monica B, Ramani S, Primrose B, Moses PD, Gallimore CI, Brown DW, Gray J . 2004. Quantitation of group A rotavirus by real-time reverse-transcription-polymerase chain reaction: correlation with clinical severity in children in South India. J Med Virol 73 : 118 122[CrossRef].[PubMed]
133. Kottaridi C, Spathis AT, Ntova CK, Papaevangelou V, Karakitsos P . 2012. Evaluation of a multiplex real time reverse transcription PCR assay for the detection and quantitation of the most common human rotavirus genotypes. J Virol Methods 180 : 49 53[CrossRef].[PubMed]
134. Logan C, O'Leary JJ, O'Sullivan N . 2006. Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. J Clin Microbiol 44 : 3189 3195[CrossRef].[PubMed]
135. Pang XL, Lee B, Boroumand N, Leblanc B, Preiksaitis JK, Yu Ip CC . 2004. Increased detection of rotavirus using a real time reverse transcription-polymerase chain reaction (RT-PCR) assay in stool specimens from children with diarrhea. J Med Virol 72 : 496 501[CrossRef].[PubMed]
136. Freeman MM, Kerin T, Hull J, McCaustland K, Gentsch J . 2008. Enhancement of detection and quantification of rotavirus in stool using a modified real-time RT-PCR assay. J Med Virol 80 : 1489 1496[CrossRef].[PubMed]
137. Zeng SQ, Halkosalo A, Salminen M, Szakal ED, Puustinen L, Vesikari T . 2008. One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. J Virol Methods 153 : 238 240[CrossRef].[PubMed]
138. Jothikumar N, Kang G, Hill VR . 2009. Broadly reactive TaqMan assay for real-time RT-PCR detection of rotavirus in clinical and environmental samples. [email protected]. J Virol Methods 155 : 126 131[CrossRef].[PubMed]
139. Pang X, Cao M, Zhang M, Lee B . 2011. Increased sensitivity for various rotavirus genotypes in stool specimens by amending three mismatched nucleotides in the forward primer of a real-time RT-PCR assay. J Virol Methods 172 : 85 87[CrossRef].[PubMed]
140. Mijatovic-Rustempasic S, Tam KI, Kerin TK, Lewis JM, Gautam R, Quaye O, Gentsch JR, Bowen MD . 2013. Sensitive and specific quantitative detection of rotavirus A by one-step real-time reverse transcription-PCR assay without antecedent double-stranded-RNA denaturation. J Clin Microbiol 51 : 3047 3054[CrossRef].[PubMed]
141. Fields BN, Knipe DM, Howley PM (ed). 2013. Fields Virology, 6th ed. Wolters Kluwer/Lippincott Williams & Wilkins Health, Philadelphia, PA.
142. Kapikian AZ, Wyatt RG, Dolin R, Thornhill TS, Kalica AR, Chanock RM . 1972. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J Virol 10 : 1075 1081.[PubMed]
143. Nakata S, Kogawa K, Numata K, Ukae S, Adachi N, Matson DO, Estes MK, Chiba S . 1996. The epidemiology of human calicivirus/Sapporo/82/Japan. Arch Virol Suppl 12 : 263 270.[PubMed]
144. Widdowson MA, Monroe SS, Glass RI . 2005. Are noroviruses emerging? Emerg Infect Dis 11 : 735 737[CrossRef].[PubMed]
145. Goodgame R . 2007. Norovirus gastroenteritis. Curr Infect Dis Rep 9 : 102 109[CrossRef].[PubMed]
146. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinjé J, Parashar UD . 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14 : 1224 1231[CrossRef].[PubMed]
147. Farkas T, Zhong WM, Jing Y, Huang PW, Espinosa SM, Martinez N, Morrow AL, Ruiz-Palacios GM, Pickering LK, Jiang X . 2004. Genetic diversity among sapoviruses. Arch Virol 149 : 1309 1323[CrossRef].[PubMed]
148. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS . 2006. Norovirus classification and proposed strain nomenclature. Virology 346 : 312 323[CrossRef].[PubMed]
149. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS . 2010. Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 8 : 231 241[CrossRef].[PubMed]
150. Noel JS, Fankhauser RL, Ando T, Monroe SS, Glass RI . 1999. Identification of a distinct common strain of “Norwalk-like viruses” having a global distribution. J Infect Dis 179 : 1334 1344[CrossRef].[PubMed]
151. Lindesmith LC, Donaldson EF, Lobue AD, Cannon JL, Zheng DP, Vinje J, Baric RS . 2008. Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med 5 : e31[CrossRef].[PubMed]
152. Hansman GS, Oka T, Katayama K, Takeda N . 2007. Human sapoviruses: genetic diversity, recombination, and classification. Rev Med Virol 17 : 133 141[CrossRef].[PubMed]
153. Burton-MacLeod JA, Kane EM, Beard RS, Hadley LA, Glass RI, Ando T . 2004. Evaluation and comparison of two commercial enzyme-linked immunosorbent assay kits for detection of antigenically diverse human noroviruses in stool samples. J Clin Microbiol 42 : 2587 2595[CrossRef].