Exploring preterm birth as a polymicrobial disease: An overview of the uterine microbiome

Frontiers in Immunology

Volumn 5, Issue NOV, 2014, Pages

  Payne, Matthew S ^a   Bayatibojakhi, Sara ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Amniotic fluid; Bacteria; Fungi; Infection; Placenta; Preterm birth; Virus; Yeast

Indexed keywords

AMNION FLUID; BACTERIAL COLONIZATION; BACTERIUM; CANDIDA; CELL VIABILITY; DNA EXTRACTION; FUNGUS; HUMAN; INTRAUTERINE CONTRACEPTIVE DEVICE; MICROBIOME; MOLECULAR CLONING; NONHUMAN; PLACENTA; POLYMERASE CHAIN REACTION SYSTEM; POLYMICROBIAL DISEASE; PREGNANCY OUTCOME; PREMATURE LABOR; REVIEW; UTERINE MICROBIOME; UTERUS CAVITY; VIRUS; YEAST;

EID: 84919336798     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00595     Document Type: Review

References (99)

1. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet (2008) 371(9606):75-84. doi: 10.1016/S0140-6736(08)60074-4
2. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med (2000) 342(20):1500-7. doi:10.1056/NEJM200005183422007
3. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med (2014) 6(237):237ra65. doi:10.1126/scitranslmed.3008599
4. Han YW, Ikegami A, Bissada NF, Herbst M, Redline RW, Ashmead GG. Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J Clin Microbiol (2006) 44(4):1475-83. doi:10.1128/JCM.44.4.1475-1483.2006
5. Fardini Y, Chung P, Dumm R, Joshi N, Han YW. Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection?†. Infect Immun (2010) 78(4):1789-96. doi:10.1128/IAI.01395-09
6. Harris JW, Brown H. Bacterial content of the uterus at cesarean section. Am J Obstet Gynecol (1927) 13:133.
7. DiGiulio DB. Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med (2012) 17(1):2-11. doi:10.1016/j.siny.2011.10.001
8. Mendz GL, Kaakoush NO, Quinlivan JA. Bacterial aetiological agents of intra-amniotic infections and preterm birth in pregnant women. Front Cell Infect Microbiol (2013) 3:58. doi:10.3389/fcimb.2013.00058
9. Combs CA, Gravett M, Garite TJ, Hickok DE, Lapidus J, Porreco R, et al. Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am J Obstet Gynecol (2014) 210(2):e1-15. doi:10.1016/j.ajog.2013.11.032
10. Jalava J, Mantymaa ML, Ekblad U, Toivanen P, Skurnik M, Lassila O, et al. Bacterial 16S rDNA polymerase chain reaction in the detection of intra-amniotic infection. Br J Obstet Gynaecol (1996) 103(7):664-9. doi:10.1111/j.1471-0528.1996.tb09835.x
11. Markenson GR, Martin RK, Tillotson-Criss M, Foley KS, Stewart RS Jr, Yancey M. The use of the polymerase chain reaction to detect bacteria in amniotic fluid in pregnancies complicated by preterm labor. Am J Obstet Gynecol (1997) 177(6):1471-7. doi:10.1016/S0002-9378(97)70093-0
12. Hitti J, Riley DE, Krohn MA, Hillier SL, Agnew KJ, Krieger JN, et al. Broad-spectrum bacterial rDNA polymerase chain reaction assay for detecting amniotic fluid infection among women in premature labor. Clin Infect Dis (1997) 24(6):1228-32. doi:10.1086/513669
13. Gardella C, Riley DE, Hitti J, Agnew K, Krieger JN, Eschenbach D. Identification and sequencing of bacterial rDNAs in culture-negative amniotic fluid from women in premature labor. Am J Perinatol (2004) 21(6):319-23. doi:10.1055/s-2004-831884
14. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One (2008) 3(8):e3056. doi:10.1371/journal.pone.0003056
15. Han YW, Shen T, Chung P, Buhimschi IA, Buhimschi CS. Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol (2009) 47(1):38-47. doi:10.1128/JCM.01206-08
16. Jones HE, Harris KA, Azizia M, Bank L, Carpenter B, Hartley JC, et al. Differing prevalence and diversity of bacterial species in fetal membranes from very preterm and term labor. PLoS One (2009) 4(12):e8205. doi:10.1371/journal.pone.0008205
17. DiGiulio DB, Gervasi MT, Romero R, Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med (2010) 38(5):495-502. doi:10.1515/JPM.2010.076
18. DiGiulio DB, Gervasi M, Romero R, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, et al. Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J Perinat Med (2010) 38(5):503-13. doi:10.1515/JPM.2010.078
19. DiGiulio DB, Romero R, Kusanovic JP, Gomez R, Kim CJ, Seok K, et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm prelabor rupture of membranes. Am J Reprod Immunol (2010) 64(1):38-57. doi:10.1111/j.1600-0897.2010.00830.x
20. Marconi C, de Andrade Ramos BR, Peracoli JC, Donders GG, da Silva MG. Amniotic fluid interleukin-1 beta and interleukin-6, but not interleukin-8 correlate with microbial invasion of the amniotic cavity in preterm labor. Am J Reprod Immunol (2011) 65(6):549-56. doi:10.1111/j.1600-0897.2010.00940.x
21. Wang X, Buhimschi CS, Temoin S, Bhandari V, Han YW, Buhimschi IA. Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLoS One (2013) 8(2):e56131. doi:10.1371/journal.pone.0056131
22. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am J Reprod Immunol (2014) 71(4):330-58. doi:10.1111/aji.12189
23. Waites KB, Schelonka RL, Xiao L, Grigsby PL, Novy MJ. Congenital and opportunistic infections: Ureaplasma species and Mycoplasma hominis. Semin Fetal Neonatal Med (2009) 14(4):190-9. doi:10.1016/j.siny.2008.11.009
24. Capoccia R, Greub G, Baud D. Ureaplasma urealyticum, Mycoplasma hominis and adverse pregnancy outcomes. Curr Opin Infect Dis (2013) 26(3):231-40. doi:10.1097/QCO.0b013e328360db58
25. Gerber S, Vial Y, Hohlfeld P, Witkin SS. Detection of Ureaplasma urealyticum in second-trimester amniotic fluid by polymerase chain reaction correlates with subsequent preterm labor and delivery. J Infect Dis (2003) 187(3):518-21. doi:10.1086/368205
26. Yoon BH, Romero R, Kim M, Kim EC, Kim T, Park JS, et al. Clinical implications of detection of Ureaplasma urealyticum in the amniotic cavity with the polymerase chain reaction. Am J Obstet Gynecol (2000) 183(5):1130-7. doi:10.1067/mob.2000.109036
27. Yoon BH, Chang JW, Romero R. Isolation of Ureaplasma urealyticum from the amniotic cavity and adverse outcome in preterm labor. Obstet Gynecol (1998) 92(1):77-82. doi:10.1016/S0029-7844(98)00122-7
28. Oh KJ, Lee SE, Jung H, Kim G, Romero R, Yoon BH. Detection of ureaplasmas by the polymerase chain reaction in the amniotic fluid of patients with cervical insufficiency. J Perinat Med (2010) 38(3):261-8. doi:10.1515/JPM.2010.040
29. Racicot K, Cardenas I, Wunsche V, Aldo P, Guller S, Means RE, et al. Viral infection of the pregnant cervix predisposes to ascending bacterial infection. J Immunol (2013) 191(2):934-41. doi:10.4049/jimmunol.1300661
30. Cardenas I, Means RE, Aldo P, Koga K, Lang SM, Booth CJ, et al. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J Immunol (2010) 185(2):1248-57. doi:10.4049/jimmunol.1000289
31. Nuzum JW, Pilot I, Stangl FH, Bonar BE. 1918 pandemic influenza and pneumonia in a large civil hospital. IMJ Ill Med J (1976) 150(6):612-6.
32. Van Le S, Le DH, Hoang HT, Hoang H, Nguyen NT, Chu HH. Characterization of rubella virus genotypes among pregnant women in northern Vietnam, 2011-2013. J Med Virol (2014). doi:10.1002/jmv.24049
33. Weisz B, Book M, Lipitz S, Katorza E, Achiron R, Grossman Z, et al. Fetal outcome and amniocentesis results in pregnancies complicated by varicella infection. J Obstet Gynaecol Can (2011) 33(7):720-4.
34. Maiques V, Garcia-Tejedor A, Perales A, Cordoba J, Esteban RJ. HIV detection in amniotic fluid samples. Amniocentesis can be performed in HIV pregnant women? Eur J Obstet Gynecol Reprod Biol (2003) 108(2):137-41. doi:10.1016/S0301-2115(02)00405-0
35. Baschat AA, Towbin J, Bowles NE, Harman CR, Weiner CP. Prevalence of viral DNA in amniotic fluid of low-risk pregnancies in the second trimester. J Matern Fetal Neonatal Med (2003) 13(6):381-4. doi:10.1080/jmf.13.6.381.384
36. Wenstrom KD, Andrews WW, Bowles NE, Towbin JA, Hauth JC, Goldenberg RL. Intrauterine viral infection at the time of second trimester genetic amniocentesis. Obstet Gynecol (1998) 92(3):420-4. doi:10.1016/S0029-7844(98)00210-5
37. Reddy UM, Baschat AA, Zlatnik MG, Towbin JA, Harman CR, Weiner CP. Detection of viral deoxyribonucleic acid in amniotic fluid: association with fetal malformation and pregnancy abnormalities. Fetal Diagn Ther (2005) 20(3):203-7. doi:10.1159/000083906
38. Miller JL, Harman C, Weiner C, Baschat AA. Perinatal outcomes after second trimester detection of amniotic fluid viral genome in asymptomatic patients. J Perinat Med (2009) 37(2):140-3. doi:10.1515/JPM.2009.027
39. Gervasi MT, Romero R, Bracalente G, Chaiworapongsa T, Erez O, Dong Z, et al. Viral invasion of the amniotic cavity (VIAC) in the midtrimester of pregnancy. J Matern Fetal Neonatal Med (2012) 25(10):2002-13. doi:10.3109/14767058.2012.683899
40. Naresh A, Simhan H. Absence of viruses in amniotic fluid of women with PPROM: a case series. J Reprod Immunol (2012) 96(1-2):79-83. doi:10.1016/j.jri.2012.08.003
41. Bopegamage S, Kacerovsky M, Tambor V, Musilova I, Sarmirova S, Snelders E, et al. Preterm prelabor rupture of membranes (PPROM) is not associated with presence of viral genomes in the amniotic fluid. J Clin Virol (2013) 58(3):559-63. doi:10.1016/j.jcv.2013.09.013
42. Bibby K. Metagenomic identification of viral pathogens. Trends Biotechnol (2013) 31(5):275-9. doi:10.1016/j.tibtech.2013.01.016
43. Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD, Wang D. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog (2008) 4(2):e1000011. doi:10.1371/journal.ppat.1000011
44. Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol (2013) 21(7):334-41. doi:10.1016/j.tim.2013.04.002
45. Parveen N, Munir AA, Din I, Majeed R. Frequency of vaginal candidiasis in pregnant women attending routine antenatal clinic. J Coll Physicians Surg Pak (2008) 18(3):154-7.doi:03.2008/JCPSP.154157
46. Sobel JD. Vulvovaginal candidosis. Lancet (2007) 369(9577):1961-71. doi:10.1016/S0140-6736(07)60917-9
47. Chaim W, Mazor M, Wiznitzer A. The prevalence and clinical significance of intraamniotic infection with Candida species in women with preterm labor. Arch Gynecol Obstet (1992) 251(1):9-15. doi:10.1007/BF02718273
48. Nowakowska D, Wilczynski J, Szaflik K, Kurnatowska A. Search for the pathogenic fungi in amniotic fluid. Wiad Parazytol (2001) 47(Suppl 1):143-6.
49. Kim SK, Romero R, Kusanovic JP, Erez O, Vaisbuch E, Mazaki-Tovi S, et al. The prognosis of pregnancy conceived despite the presence of an intrauterine device (IUD). J Perinat Med (2010) 38(1):45-53. doi:10.1515/jpm.2009.133
50. Payne MS, Kemp MW, Kallapur SG, Kannan PS, Saito M, Miura Y, et al. Intrauterine Candida albicans infection elicits severe inflammation in fetal sheep. Pediatr Res (2014) 75(6):716-22. doi:10.1038/pr.2014.35
51. Benjamin DK Jr, Stoll BJ, Gantz MG, Walsh MC, Sanchez PJ, Das A, et al. Neonatal candidiasis: epidemiology, risk factors, and clinical judgment. Pediatrics (2010) 126(4):e865-73. doi:10.1542/peds.2009-3412
52. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog (2010) 6(1):e1000713. doi:10.1371/journal.ppat.1000713
53. LaTuga MS, Ellis JC, Cotton CM, Goldberg RN, Wynn JL, Jackson RB, et al. Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants. PLoS One (2011) 6(12):e27858. doi:10.1371/journal.pone.0027858
54. Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q, et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol (2013) 208(3):e1-7. doi:10.1016/j.ajog.2013.01.018
55. Human Microbiome Project Consortium. A framework for human microbiome research. Nature (2012) 486(7402):215-21. doi:10.1038/nature11209
56. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature (2012) 486(7402):207-14. doi:10.1038/nature11234
57. Gosalbes MJ, Llop S, Valles Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy (2013) 43(2):198-211. doi:10.1111/cea.12063
58. Ardissone AN, de la Cruz DM, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One (2014) 9(3):e90784. doi:10.1371/journal.pone.0090784
59. Onderdonk AB, Delaney ML, DuBois AM, Allred EN, Leviton A. Detection of bacteria in placental tissues obtained from extremely low gestational age neonates. Am J Obstet Gynecol (2008) 198(1):e1-7. doi:10.1016/j.ajog.2007.05.044
60. Baud D, Greub G. Intracellular bacteria and adverse pregnancy outcomes. Clin Microbiol Infect (2011) 17(9):1312-22. doi:10.1111/j.1469-0691.2011.03604.x
61. Carcopino X, Raoult D, Bretelle F, Boubli L, Stein AQ. Fever during pregnancy: a cause of poor fetal and maternal outcome. Ann N Y Acad Sci (2009) 1166:79-89. doi:10.1111/j.1749-6632.2009.04519.x
62. Baud D, Goy G, Jaton K, Osterheld MC, Blumer S, Borel N, et al. Role of Chlamydia trachomatis in miscarriage. Emerg Infect Dis (2011) 17(9):1630-5. doi:10.3201/eid1709.100865
63. Baud D, Goy G, Osterheld MC, Croxatto A, Borel N, Vial Y, et al. Role of Waddlia chondrophila placental infection in miscarriage. Emerg Infect Dis (2014) 20(3):460-4. doi:10.3201/eid2003.131019
64. Queiros da Mota V, Prodhom G, Yan P, Hohlfheld P, Greub G, Rouleau C. Correlation between placental bacterial culture results and histological chorioamnionitis: a prospective study on 376 placentas. J Clin Pathol (2013) 66(3):243-8. doi:10.1136/jclinpath-2012-201124
65. Srinivas SK, Ma Y, Sammel MD, Chou D, McGrath C, Parry S, et al. Placental inflammation and viral infection are implicated in second trimester pregnancy loss. Am J Obstet Gynecol (2006) 195(3):797-802. doi:10.1016/j.ajog.2006.05.049
66. Tsekoura EA, Konstantinidou A, Papadopoulou S, Athanasiou S, Spanakis N, Kafetzis D, et al. Adenovirus genome in the placenta: association with histological chorioamnionitis and preterm birth. J Med Virol (2010) 82(8):1379-83. doi:10.1002/jmv.21820
67. Delprado WJ, Baird PJ, Russell P. Placental candidiasis: report of three cases with a review of the literature. Pathology (1982) 14(2):191-5. doi:10.3109/00313028209061293
68. Iwatani S, Mizobuchi M, Sofue T, Tanaka S, Sakai H, Yoshimoto S, et al. Neonatal leukemoid reaction associated with Candida albicans chorioamnionitis. Pediatr Int (2014) 56(2):277-9. doi:10.1111/ped.12259
69. Diana A, Epiney M, Ecoffey M, Pfister RE. "White dots on the placenta and red dots on the baby": congential cutaneous candidiasis-a rare disease of the neonate. Acta Paediatr (2004) 93(7):996-9. doi:10.1080/08035250410028093
70. Ito F, Okubo T, Yasuo T, Mori T, Iwasa K, Iwasaku K, et al. Premature delivery due to intrauterine Candida infection that caused neonatal congenital cutaneous candidiasis: a case report. J Obstet Gynaecol Res (2013) 39(1):341-3. doi:10.1111/j.1447-0756.2012.01938.x
71. Shub A, Wong C, Jennings B, Swain JR, Newnham JP. Maternal periodontal disease and perinatal mortality. Aust N Z J Obstet Gynaecol (2009) 49(2):130-6. doi:10.1111/j.1479-828X.2009.00953.x
72. Shub A, Swain JR, Newnham JP. Periodontal disease and adverse pregnancy outcomes. J Matern Fetal Neonatal Med (2006) 19(9):521-8. doi:10.1080/14767050600797749
73. Rosa MI, Pires PD, Medeiros LR, Edelweiss MI, Martinez-Mesa J. Periodontal disease treatment and risk of preterm birth: a systematic review and meta-analysis. Cade Saude Publica (2012) 28(10):1823-33. doi:10.1590/S0102-311X2012001000002
74. Newnham JP, Newnham IA, Ball CM, Wright M, Pennell CE, Swain J, et al. Treatment of periodontal disease during pregnancy: a randomized controlled trial. Obstet Gynecol (2009) 114(6):1239-48. doi:10.1097/AOG.0b013e3181c15b40
75. Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS. Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun (2004) 72(4):2272-9. doi:10.1128/IAI.72.4.2272-2279.2004
76. Han YW, Fardini Y, Chen C, Iacampo KG, Peraino VA, Shamonki JM, et al. Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol (2010) 115(2 Pt 2):442-5. doi:10.1097/AOG.0b013e3181cb9955
77. Buysse K, Beulen L, Gomes I, Gilissen C, Keesmaat C, Janssen IM, et al. Reliable noninvasive prenatal testing by massively parallel sequencing of circulating cell-free DNA from maternal plasma processed up to 24h after venipuncture. Clin Biochem (2013) 46(18):1783-6. doi:10.1016/j.clinbiochem.2013.07.020
78. Nicolaides KH, Wright D, Poon LC, Syngelaki A, Gil MM. First-trimester contingent screening for trisomy 21 by biomarkers and maternal blood cell-free DNA testing. Ultrasound Obstet Gynecol (2013) 42(1):41-50. doi:10.1002/uog.12511
79. Gil MM, Quezada MS, Bregant B, Ferraro M, Nicolaides KH. Implementation of maternal blood cell-free DNA testing in early screening for aneuploidies. Ultrasound Obstet Gynecol (2013) 42(1):34-40. doi:10.1002/uog.12504
80. Vaiopoulos AG, Athanasoula KC, Papantoniou N, Kolialexi A. Review: advances in non-invasive prenatal diagnosis. In vivo (2013) 27(2):165-70.
81. Simpson JL. Cell-free fetal DNA and maternal serum analytes for monitoring embryonic and fetal status. Fertil Steril (2013) 99(4):1124-34. doi:10.1016/j.fertnstert.2013.02.012
82. Cenciarini-Borde C, Courtois S, La Scola B. Nucleic acids as viability markers for bacteria detection using molecular tools. Future Microbiol (2009) 4(1):45-64. doi:10.2217/17460913.4.1.45
83. Wang S, Levin RE. Discrimination of viable Vibrio vulnificus cells from dead cells in real-time PCR. J Microbiol Methods (2006) 64(1):1-8. doi:10.1016/j.mimet.2005.04.023
84. Rogers GB, Cuthbertson L, Hoffman LR, Wing PA, Pope C, Hooftman DA, et al. Reducing bias in bacterial community analysis of lower respiratory infections. ISME J (2013) 7(4):697-706. doi:10.1038/ismej.2012.145
85. Alifano P, Bruni CB, Carlomagno MS. Control of mRNA processing and decay in prokaryotes. Genetica (1994) 94(2-3):157-72. doi:10.1007/BF01443430
86. Fittipaldi M, Nocker A, Codony F. Progress in understanding preferential detection of live cells using viability dyes in combination with DNA amplification. J Microbiol Methods (2012) 91(2):276-89. doi:10.1016/j.mimet.2012.08.007
87. Bleve G, Rizzotti L, Dellaglio F, Torriani S. Development of reverse transcription (RT)-PCR and real-time RT-PCR assays for rapid detection and quantification of viable yeasts and molds contaminating yogurts and pasteurized food products. Appl Environ Microbiol (2003) 69(7):4116-22. doi:10.1128/AEM.69.7.4116-4122.2003
88. Morin NJ, Gong Z, Li XF. Reverse transcription-multiplex PCR assay for simultaneous detection of Escherichia coli O157:H7, Vibrio cholerae O1, and Salmonella Typhi. Clin Chem (2004) 50(11):2037-44. doi:10.1373/clinchem.2004.036814
89. Probst J, Brechtel S, Scheel B, Hoerr I, Jung G, Rammensee HG, et al. Characterization of the ribonuclease activity on the skin surface. Genet Vaccines Ther (2006) 4:4. doi:10.1186/1479-0556-4-4
90. Nogva HK, Dromtorp SM, Nissen H, Rudi K. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5'-nuclease PCR. Biotechniques (2003) 34(4):804-8.
91. Nocker A, Cheung CY, Camper AK. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods (2006) 67(2):310-20. doi:10.1016/j.mimet.2006.04.015
92. Agusti G, Codony F, Fittipaldi M, Adrados B, Morato J. Viability determination of Helicobacter pylori using propidium monoazide quantitative PCR. Helicobacter (2010) 15(5):473-6. doi:10.1111/j.1523-5378.2010.00794.x
93. Nam S, Kwon S, Kim MJ, Chae JC, Jae Maeng P, Park JG, et al. Selective detection of viable Helicobacter pylori using ethidium monoazide or propidium monoazide in combination with real-time polymerase chain reaction. Microbiol Immunol (2011) 55(12):841-6. doi:10.1111/j.1348-0421.2011.00388.x
94. Vesper S, McKinstry C, Hartmann C, Neace M, Yoder S, Vesper A. Quantifying fungal viability in air and water samples using quantitative PCR after treatment with propidium monoazide (PMA). J Microbiol Methods (2008) 72(2):180-4. doi:10.1016/j.mimet.2007.11.017
95. Fittipaldi M, Rodriguez NJ, Codony F, Adrados B, Penuela GA, Morato J. Discrimination of infectious bacteriophage T4 virus by propidium monoazide real-time PCR. J Virol Methods (2010) 168(1-2):228-32. doi:10.1016/j.jviromet.2010.06.011
96. Andorra I, Esteve-Zarzoso B, Guillamon JM, Mas A. Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int J Food Microbiol (2010) 144(2):257-62. doi:10.1016/j.ijfoodmicro.2010.10.003
97. Fittipaldi M, Pino Rodriguez NJ, Adrados B, Agusti G, Penuela G, Morato J, et al. Discrimination of viable Acanthamoeba castellani trophozoites and cysts by propidium monoazide real-time polymerase chain reaction. J Eukaryot Microbiol (2011) 58(4):359-64. doi:10.1111/j.1550-7408.2011.00557.x
98. Nocker A, Richter-Heitmann T, Montijn R, Schuren F, Kort R. Discrimination between live and dead cellsin bacterial communities from environmental water samples analyzed by 454 pyrosequencing. Int Microbiol (2010) 13(2):59-65.
99. Brogden KA. Polymicrobial Diseases of Animals and Humans. Washington DC: ASM Press (2002).