Ureaplasma parvum or Mycoplasma hominis as sole pathogens cause chorioamnionitis, preterm delivery, and fetal pneumonia in rhesus macaques

Reproductive Sciences

Volumn 16, Issue 1, 2009, Pages 56-70

  Novy, Miles J ^a   Duffy, Lynn ^b   Axthelm, Michael K ^a   Sadowsky, Drew W ^a   Witkin, Steven S ^c   Gravett, Michael G ^d   Cassell, Gail H ^e   Waites, Kenneth B ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b University of Alabama at Birmingham   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e ELI LILLY AND COMPANY   (United States)

Author keywords

Chorioamnionitis; Fetal lung; Intrauterine infection inflammation; Mycoplasma; Preterm labor; Rhesus monkey; Ureaplasma

Indexed keywords

CYTOKINE; GELATINASE B; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; SODIUM CHLORIDE;

AMNION FLUID; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CHORIOAMNIONITIS; CONTROLLED STUDY; FETUS BLOOD; FETUS LUNG; FETUS MEMBRANE; HISTOPATHOLOGY; INTRAUTERINE INFECTION; LEUKOCYTE; MYCOPLASMA HOMINIS; NONHUMAN; PNEUMONIA; POLYMERASE CHAIN REACTION; PREMATURE LABOR; PRIORITY JOURNAL; RHESUS MONKEY; SEROTYPE; TISSUE CULTURE; UPREGULATION; UREAPLASMA; UREAPLASMA PARVUM; UTERUS CONTRACTION;

AMNIOTIC FLUID; ANIMALS; CHORIOAMNIONITIS; FEMALE; MACACA MULATTA; MYCOPLASMA HOMINIS; MYCOPLASMA INFECTIONS; OBSTETRIC LABOR, PREMATURE; PNEUMONIA; PREGNANCY; UREAPLASMA; UREAPLASMA INFECTIONS;

EID: 58249119470     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719108325508     Document Type: Article

References (61)

1. Romero R., Espinoza J., Kusanovic JP, et al. The preterm parturition syndrome. Brit J Obstet Gynaecol. 2006 ;113 (supp1 3). 17-42.
2. Gravett MG, Adams KM, Sadowsky DW, et al. Immunomodulators plus antibiotics delay preterm delivery after experimental intraamniotic infection in a nonhuman primate model. Am J Obstet Gynecol. 2007 ; 197: 518.e1-518.e8.
3. Hillier SL, Martius J., Krohn M., Kiviat N., Holmes KK, Eschenbach DA A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med. 1988 ; 319: 972-978.
4. Yoon BH, Romero R., Park JS, et al. Microbial invasion of the amniotic cavity with Ureaplasma urealyticum is associated with a robust host response in fetal, amniotic, and maternal compartments. Am J Obstet Gynecol. 1998 ; 179: 1254-1260.
5. Waites KB, Katz B., Schelonka RL Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev. 2005 ; 18: 757-789.
6. Yoon BH, Romero R., Jun JK, et al. Amniotic fluid cytokines (interleukin-6, tumor necrosis factor-a,interleukin-1b, and interleukin-8) and the risk for the development of bronchopulmonary dysplasia. Am J Obstet Gynecol. 1997 ; 177: 825-830.
7. Goldenberg RL, Andrews WW, Goepfert AR, et al. The Alabama Preterm Birth Study: umbilical cord blood Ureaplasma urealyticum and Mycoplasma hominis cultures in very preterm newborn infants. Am J Obstet Gynecol. 2008 ; 198: 43.e1-43.e5.
8. Sadowsky DW, Novy MJ, Witkin SS, Gravett MG Dexamethasone or interleukin-10 blocks interleukin-1b-induced uterine contractions in pregnant rhesus monkeys. Am J Obstet Gynecol. 2003 ; 188: 252-263.
9. Cassell GH, Davis RO, Waites KB, et al. Isolation of Mycoplasma hominis and Ureaplasma urealyticum from amniotic fluid at 16-20 weeks of gestation: potential effect on outcome of pregnancy. Sex Transm Dis. 1983 ; 10: 294-302.
10. Teng L. -J, Zheng X., Glass JI, Watson HL, Tsai J., Cassell GH Ureaplasma urealyticum biovar specificity and diversity are encoded in multiple-banded antigen gene. J Clin Microbiol. 1994 ; 32: 1464-1469.
11. Waites KB, Taylor-Robinson D. Mycoplasma and Ureaplasma, Manual of Clinical Microbiology. Washington, DC: ASM Press ; 2007.
12. Blanchard A., Hentschel J., Duffy L., Baladus K., Cassell GH Detection of Ureaplasma urealyticum by polymerase chain reaction in the urogenital tract of adults, in amniotic fluid, and in the respiratory tract of newborns. Clin Infect Dis. 1993 ; 17: S148 - S153.
13. Blanchard A., Yanez A., Dybvig K., Watson HL, Griffiths G., Cassell GH Evaluation of intraspecies genetic variation within the 16S rRNA gene of Mycoplasma hominis and detection by polymerase chain reaction. J Clin Microbiol. 1993 ; 31: 1358-1361.
14. Ortega F., Sadowsky DW, Haluska GJ, et al. Identification of matrix metalloproteinase-9 in amniotic fluid and amniochorion in spontaneous labor and after experimental intrauterine infection or interleukin-1b infusion in pregnant rhesus monkeys. Am J Obstet Gynecol. 2002 ; 186: 128-138.
15. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol. 2006 ; 195: 1578-1589.
16. Moss TJ, Nitsos I., Ikegami M., Jobe AH, Newnham JP Experimental intrauterine Ureaplasma infection in sheep. Am J Obstet Gynecol. 2005 ; 192: 1179-1186.
17. Moss TJ, Knox CL, Kallapur SG, et al. Experimental amniotic fluid infection in sheep: effects of Ureaplasma parvum serovars 3 and 6 on preterm or term fetal sheep. Am J Obstet Gynecol. 2008 ; 198: 122.e1-122.e8.
18. Adams-Waldorf KM, Persing D., Novy MJ, Sadowsky DW, Gravett MG Pretreatent with toll-like receptor 4 antagonist inhibits lipopolysaccharide- induced preterm uterine contractility, cytokines, and prostaglandins in rhesus monkeys. Reprod Sci. 2008 ; 15: 121-127.
19. Gravett MG, Witkin SS, Haluska GJ, Edwards JL, Cook MJ, Novy MJ An experimental model for intraamniotic infection and preterm labor in rhesus monkeys. Am J Obstet Gynecol. 1994 ; 171: 1660-1667.
20. Hsu CD, Aversa KR, Lu LC, et al. Nitric oxide: a clinically important amniotic fluid marker to distinguish between intra-amniotic mycoplasma and non-mycoplasma infections. Am J Perinatol. 1999 ; 16: 161-166.
21. Yoon BH, Chang JW, Romero R. Isolation of Ureaplasma urealyticum from the amniotic cavity and adverse outcome in preterm labor. Obstet Gynecol. 1998 ; 92: 77-82.
22. Cassell GH, Blanchard A., Duffy L., et al. Mycoplasmas. Clinical and Pathogenic Microbiology. In: Howard BJ, Klaas JI, Rubin SJ, Weissfeld AS, Tilton RC, eds. St Louis: Mosby-Year Book, Inc; 1994: 491-502.
23. 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: 518-521.
24. Horn M., Wolff C., Dressel P., Pfaff F., Zimmermann A. Association of Ureaplasma urealyticum biovars with clinical outcome for neonates, obstetric patients, and gynecological patients with pelvic inflammatory disease. J Clin Microbiol. 1998 ; 35: 1199-1202.
25. Doh K., Barton PT, Gerber S., et al. Immune responses and genetic factors associated with vaginal colonization by Ureaplasma urealyticum and Mycoplasma hominis in black, hispanic and white pregnant women. Am J Obstet Gynecol. 2003 ;187: S221.
26. Giannoulias D., Haluska GJ, Gravett MG, Sadowsky DW, Challis JR, Novy MJ Localization of prostaglandin H synthase, prostaglandin dehydrogenase, corticotropinreleasing hormone and glucocorticoid receptor in rhesus monkey fetal membranes with labor in the presence of infection. Placenta. 2005 ; 26: 289-297.
27. Sampson JE, Theve RP, Blatman RN, et al. Fetal origin of amniotic fluid polymorphonuclear leukocytes. Am J Obstet Gynecol. 1997 ; 176: 77-81.
28. Macias AE, Wong SW, Sadowsky DW, et al. Maternal or fetal origin of rhesus monkey (Macaca mulatta) amniotic fluid leukocytes can be identified by polymerase chain reaction using the zinc finger Y gene. Am J Primatol. 2001 ; 55: 159-170.
29. Dammann O., Allred EN, Leviton A., et al. Fetal vasculitis in preterm newborns: interrelationships, modifiers, and antecedents. Placenta. 2004 ; 25: 788-796.
30. Steel JH, O'donoghue K, Kennea NL, Sullivan MH, Edwards AD Maternal origin of inflammatory leuokcytes in preterm fetal membranes, shown by fluorescence in situ hybridisation. Placenta. 2005 ; 26: 672-677.
31. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008 ; 371: 75-84.
32. Swenson CE, O' Leary WM Genital Ureaplasmas in nonhuman primates. J Med Primatol. 1977 ; 6: 344-348.
33. Schoeb TR, Dybvig K., Keisling KF, Davidson MK, Davis JK Detection of urogenital mycoplasmal infections in primates by use of polymerase chain reaction. Lab Anim Sci. 1997 ; 47: 468-471.
34. Waites KB, Taylor-Robinson D. Mycoplasma and ureaplasma. Manual of Clinical Microbiology. In: Murray PR, Baron EJ, Landry ML, Pfaller MA, eds. Washington, DC: ASM Press; 2007: 1004-1020.
35. Horowitz S., Mazor M., Horowitz J., Porath A., Glezerman M. Antibodies to Ureaplasma urealyticum in women with intraamniotic infection and adverse pregnancy outcome. Acta Obstet Gynecol Scand. 1995 ; 74: 132-136.
36. Yoon BH, Romero R., Kim M., et al. Clinical implications of detection of Ureaplasma urealyticum in the amniotic cavity with the polymerase chain reaction. Am J Obstet Gynecol. 2000 ;1130-1137.
37. Schelonka RL, Waites KB Ureaplasma infection and neonatal lung disease. Semin Perinatol. 2007 ; 31: 2-9.
38. Waites KB, Rudd PT, Crouse KC. Chronic U. urealyticum and M. hominis infections of the central nervous system in preterm infants. Lancet. 1988 ;ii:17-22.
39. Waites KB, Duffy LB, Crouse DT, et al. Mycoplasmal infections of cerebrospinal fluid in newborn infants from a community hospital population. Pediatr Infect Dis J. 1990 ; 9: 241-245.
40. Wu YW, Colford JM, Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA. 2000 ; 284: 1417-1424.
41. Gotsch F., Romero R., Kusanovic JP, et al. The fetal inflammatory response syndrome. Clin Obstet Gynecol. 2007 ; 50: 652-683.
42. Amdrews WW, Cliver SP, Biasini F., et al. Early preterm birth: association between in utero exposure to acute inflammation and severe neurodevelopmental disability at 6 years of age. Am J Obstet Gynecol. 2008 ;198:466e1-466e11.
43. Dammann O., Allred EN, Genest DR, Kundsin RB, Leviton A. Antenatal mycoplasma infection, the fetal inflammatory response and cerebral white matter damage in very-low-birthweight infants. Paediatr Perinat Epidemiol. 2003 ; 17: 49-57.
44. Viscardi RM, Manimtim WM, Sun CC, Duffy L., Cassell GH Lung pathology in premature infants with Ureaplasma urealyticum infection. Pediatr Dev Pathol. 2002 ; 5: 141-150.
45. Crouse DT, Cassell GH, Waites KB, Foster JM, Cassady G. Hyperoxia potentiates Ureaplasma urealyticum pneumonia in newborn mice. Infect Immun. 1990 ; 58: 3487-3493.
46. Walsh WF, Butler J., Coalson J., Hensley D., Cassell GH, deLemos RA. A primate model of Ureaplasma urealyticum infection in the premature infant with hyaline membrane disease. Clin Infect Dis. 1993 ; 17: S158 - S162.
47. Yoder BA, Coalson JJ, Winter VT, Siler-khodr T., Duffy LB, Cassell GH Effects of antenatal colonization with Ureaplasma urealyticum on pulmonary disease in the immature baboon. Pediatr Res. 2003 ; 54: 797-807.
48. Uhal BD Cell cycle kinetics in the alveolar epithelium. Am J Physiol. 1997 ; 272: L1031 - L1045.
49. Jobe Ah, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2001 ; 163: 1723-1729.
50. De Dooy JJ, Mahieu LM, Van Bever HP The role of inflammation in the development of chronic lung disease in neonates. Eur J Pediatr. 2001 ; 160: 457-463.
51. Curley AE, Sweet DG, Thornton CM, et al. Chorioamnionitis and increased neonatal lung lavage fluid matrix metalloproteinase-9 levels: implications for antenatal origins of chronic lung disease. Am J Obstet Gynecol. 2003 ; 188: 871-875.
52. Ghezzi F., Gomez R., Romero R., et al. Elevated interleukin-8 concentrations in amniotic fluid of mothers whose neonates subsequently develop bronchopulmonary dysplasia. Eur J Obstet Gynecol Reprod Biol. 1998 ; 78: 5-10.
53. Hitti J., Krohn MA, Patton DL, et al. Amniotic fluid tumor necrosis factor-a and the risk of respiratory distress syndrome among preterm infants. Am J Obstet Gynecol. 1997 ; 177: 50-56.
54. Jones CA, Cayabyab RG, Kwong KY, et al. Undetectable interleukin (IL)-10 and persistent IL-8 expression early in hyaline membrane disease: a possible developmental basis for the predisposition to chronic lung inflammation in preterm newborns. Pediatr Res. 1996 ; 39: 966-975.
55. Manimtim WM, Hasday JD, Hester L., Fairchild KD, Lovchick JC, Viscardi RM Ureaplasma urealyticum modulates endotoxin-induced cytokine release by human monocytes derived from preterm and term newborns and adults. Infect Immun. 2001 ; 69: 3906-3915.
56. Li YH, Chen M., Brauner A., Zheng C., Skov Jensen J., Tullus K. Ureaplasma urealyticum induces apoptosis in human lung epithelial cells and macrophages. Biol Neonate. 2002 ; 82: 166-173.
57. Viscardi RM, Atamas SP, Luzina IG, et al. Antenatal Ureaplasma urealyticum respiratory tract infection stimulates proinflammatory, profibrotic responses in the preterm baboon lung. Pediatr Res. 2006 ; 60: 141-146.
58. Stetzer BP, Mercer BM Antibiotics and preterm labor. Clin Obstet Gynecol. 2000 ; 43: 809-817.
59. Kenyon SL, Taylor DJ, Tarnow- Mordi W. Broad-spectrum antibiotics for spontaneous preterm labour: the ORACLE II randomised trial. Lancet. 2001 ; 357: 989-994.
60. King J., Flenady V. Prophylactic antibiotics for inhibiting preterm labour with intact membranes. Cochrane Database Syst Rev. 2002 ;CD000246.
61. Sadowsky DW, Reed MD, O' Riordan MA, Duffy LB, Waites KB, Novy MJ Azithromycin (AZI) dose-finding study for treatment of ureaplasma intraamniotic infection (IAI) in rhesus monkeys [abstract #30]. Reprod Sci. 2007 ;14 (suppl 1):65A.