American Journal of Obstetrics & Gynecology
Volume 198, Issue 1 , Pages 7-22 , January 2008

Maternal infection and risk of preeclampsia: Systematic review and metaanalysis

  • Agustín Conde-Agudelo, MD, MPH

      Affiliations

    • Perinatology Research Branch, Intramural Division, NICHD/NIH/DHHS, Baltimore, MD, and Detroit, MI
    • ,
  • José Villar, MD, MPH

      Affiliations

    • Nuffield Department of Obstetrics and Gynecology, University of Oxford, Oxford, UK
    • ,
  • Marshall Lindheimer, MD

      Affiliations

    • Department of Obstetrics & Gynecology and Medicine, The University of Chicago, Chicago, IL.

Received 22 March 2007 ,Revised 29 June 2007 ,Accepted 24 July 2007.

References 

  1. Villar J, Say L, Shennan A, et al. Methodological and technical issues related to the diagnosis, screening, prevention, and treatment of pre-eclampsia and eclampsia. Int J Gynaecol Obstet. 2004;85(Suppl 1):S28–S41
  2. Conde-Agudelo A, Belizan JM. Risk factors for preeclampsia in a large cohort of Latin American and Caribbean women. BJOG. 2000;107:75–83
  3. Roberts JM, Pearson G, Cutler J, Lindheimer M. Summary of the NHLBI working group on research on hypertension during pregnancy. Hypertension. 2003;41:437–445
  4. Lam C, Lim KH, Karumanchi SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005;46:1077–1085
  5. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592–1594
  6. Herrera JA, Chaudhuri G, Lopez-Jaramillo P. Is infection a major risk factor for preeclampsia?. Med Hypotheses. 2001;57:393–397
  7. von Dadelszen P, Magee LA. Could an infectious trigger explain the differential maternal response to the shared placental pathology of preeclampsia and normotensive intrauterine growth restriction?. Acta Obstet Gynecol Scand. 2002;81:642–648
  8. Levine M, Walter S, Lee H, Haines T, Holbrook A, Moyer V. Users’ guides to the medical literature. IV (How to use an article about harm. Evidence-Based Medicine Working Group). JAMA. 1994;271:1615–1619
  9. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting (Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group). JAMA. 2000;283:2008–2012
  10. Hill AB. The environment and disease: association or causation?. Proc R Soc Med. 1965;58:295–300
  11. Weed DL, Hursting SD. Biologic plausibility in causal inference: current method and practice. Am J Epidemiol. 1998;147:415–425
  12. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377–384
  13. Walter SD, Cook RJ. A comparison of several point estimators of the odds ratio in a single 2 x 2 contingency table. Biometrics. 1991;47:795–811
  14. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560
  15. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analyses detected by a simple graphical test. BMJ. 1997;315:629–634
  16. Bryant RE, Windom RE, Vineyard JP, Sanford JP. Asymptomatic bacteriuria in pregnancy and its association with prematurity. J Lab Clin Med. 1964;63:224–231
  17. Low JA, Johnston EE, McBride RL, Tuffnell PG. The significance of asymptomatic bacteriuria in the normal obstetric patient. Am J Obstet Gynecol. 1964;90:897–906
  18. Kincaid-Smith P, Bullen M. Bacteriuria in pregnancy. Lancet. 1965;I:395–399
  19. Stuart KL, Cummins GTM, Chin WA. Bacteriuria, prematurity, and the hypertensive disorders of pregnancy. BMJ. 1965;I:554–556
  20. Little PJ. The incidence of urinary infection in 5000 pregnant women. Lancet. 1966;2:925–928
  21. Brumfitt W. The effects of bacteriuria in pregnancy on maternal and fetal health. Kidney Int. 1975;4(Suppl):S113–S119
  22. Savige JA, Gilbert GL, Fairley KF, McDowall DR. Bacteriuria due to Ureaplasma urealyticum and Gardnerella vaginalis in women with preeclampsia. J Infect Dis. 1983;148:605
  23. Hill JA, Devoe LD, Bryans CI. Frequency of asymptomatic bacteriuria in preeclampsia. Obstet Gynecol. 1986;67:529–532
  24. Gilbert GL, Garland SM, Fairley KF, McDowall DM. Bacteriuria due to ureaplasmas and other fastidious organisms during pregnancy: prevalence and significance. Pediatr Infect Dis. 1986;5:S239–S243
  25. Qureshi RN, Khan KS, Darr O, Khattak N, Farooqui BJ, Rizvi JH. Bacteriuria and pregnancy outcome: a prospective hospital-based study in Pakistani women. J Pak Med Assoc. 1994;44:12–13
  26. Schieve LA, Handler A, Hershow R, Persky V, Davis F. Urinary tract infection during pregnancy: its association with maternal morbidity and perinatal outcome. Am J Public Health. 1994;84:405–410
  27. Hsu CD, Witter FR. Urogenital infection in preeclampsia. Int J Gynaecol Obstet. 1995;49:271–275
  28. Abi-Said D, Annegers JF, Combs-Cantrell D, Frankowski RF, Willmore LJ. Case-control study of the risk factors for eclampsia. Am J Epidemiol. 1995;142:437–441
  29. Mittendorf R, Lain KY, Williams MA, Walker CK. Preeclampsia (A nested, case-control study of risk factors and their interactions). J Reprod Med. 1996;41:491–496
  30. Lee CJ, Hsieh TT, Chiu TH, Chen KC, Lo LM, Hung TH. Risk factors for pre-eclampsia in an Asian population. Int J Gynaecol Obstet. 2000;70:327–333
  31. Villar J, Carroli G, Wojdyla D, et al. Preeclampsia, gestational hypertensión and intrauterinr growth restriction, related or independent conditions?. Am J Obstet Gynecol. 2006;194:921–931
  32. Bánhidy F, Acs N, Puhó EH, Czeizel AE. Pregnancy complications and birth outcomes of pregnant women with urinary tract infections and related drug treatments. Scand J Infect Dis. 2007;39:390–397
  33. Boggess KA, Lieff S, Murtha AP, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol. 2003;101:227–231
  34. Canakci V, Canakci CF, Canakci H, et al. Periodontal disease as a risk factor for pre-eclampsia: a case control study. Aust N Z J Obstet Gynaecol. 2004;44:568–573
  35. Oettinger-Barak O, Barak S, Ohel G, et al. Severe pregnancy complication (preeclampsia) is associated with greater periodontal destruction. J Periodontol. 2005;76:134–137
  36. Contreras A, Herrera JA, Soto JE, Arce RM, Jaramillo A, Botero JE. Periodontitis is associated with preeclampsia in pregnant women. J Periodontol. 2006;77:182–188
  37. Castaldi JL, Bertin MS, Gimenez F, Lede R. Periodontal disease: is it a risk factor for premature labor, low birth weight or preeclampsia?. Rev Panam Salud Publica. 2006;19:253–258[in Spanish]
  38. Khader YS, Jibreal M, Al-Omiri M, Amarin Z. Lack of association between periodontal parameters and preeclampsia. J Periodontol. 2006;77:1681–1687
  39. Cota LO, Guimaraes AN, Costa JE, Lorentz TC, Costa FO. Association between maternal periodontitis and an increased risk of preeclampsia. J Periodontol. 2006;77:2063–2069
  40. Kunnen A, Blaauw J, van Doormaal JJ, et al. Women with a recent history of early-onset pre-eclampsia have a worse periodontal condition. J Clin Periodontol. 2007;34:202–207
  41. Barak S, Oettinger-Barak O, Machtei EE, Sprecher H, Ohel G. Evidence of periopathogenic microorganisms in placentas of women with preeclampsia. J Periodontol. 2007;78:670–676
  42. Trogstad LI, Eskild A, Bruu AL, Jeansson S, Jenum PA. Is preeclampsia an infectious disease?. Acta Obstet Gynecol Scand. 2001;80:1036–1038
  43. Carreiras M, Montagnani S, Layrisse Z. Preeclampsia: a multifactorial disease resulting from the interaction of the feto-maternal HLA genotype and HCMV infection. Am J Reprod Immunol. 2002;48:176–183
  44. Heine RP, Ness RB, Roberts JM. Seroprevalence of antibodies to Chlamydia pneumoniae in women with preeclampsia. Obstet Gynecol. 2003;101:221–226
  45. Teran E, Escudero C, Calle A. Seroprevalence of antibodies to Chlamydia pneumoniae in women with preeclampsia. Obstet Gynecol. 2003;102:198–199
  46. von Dadelszen P, Magee LA, Krajden M, et al. Levels of antibodies against cytomegalovirus and Chlamydophila pneumoniae are increased in early onset pre-eclampsia. BJOG. 2003;110:725–730
  47. Raynor BD, Bonney EA, Jang KT, Coto W, Garcia MS. Preeclampsia and Chlamydia pneumoniae: is there a link?. Hypertens Pregnancy. 2004;23:129–134
  48. Nguyen DP, Gerber S, Hohlfeld P, Sandrine G, Witkin SS. Mycoplasma hominis in mid-trimester amniotic fluid: relation to pregnancy outcome. J Perinat Med. 2004;32:323–326
  49. Goulis DG, Chappell L, Gibbs RG, et al. Association of raised titres of antibodies to Chlamydia pneumoniae with a history of pre-eclampsia. BJOG. 2005;112:299–305
  50. Aral M, Guven MA, Kocturk SA. Chlamydia pneumoniae seropositivity in women with pre-eclampsia. Int J Gynaecol Obstet. 2006;92:77–78
  51. Arechavaleta-Velasco F, Ma Y, Zhang J, McGrath CM, Parry S. Adeno-associated virus-2 (AAV-2) causes trophoblast dysfunction, and placental AAV-2 infection is associated with preeclampsia. Am J Pathol. 2006;168:1951–1959
  52. Ponzetto A, Cardaropoli S, Piccoli E, et al. Pre-eclampsia is associated with Helicobacter pylori seropositivity in Italy. J Hypertens. 2006;24:2445–2449
  53. Wimalasundera RC, Larbalestier N, Smith JH, et al. Pre-eclampsia, antiretroviral therapy, and immune reconstitution. Lancet. 2002;360:1152–1154
  54. de Groot MR, Corporaal LJ, Cronje HS, Joubert G. HIV infection in critically ill obstetrical patients. Int J Gynaecol Obstet. 2003;81:9–16
  55. Frank KA, Buchmann EJ, Schackis RC. Does human immunodeficiency virus infection protect against preeclampsia-eclampsia?. Obstet Gynecol. 2004;104:238–242
  56. Mattar R, Amed AM, Lindsey PC, Sass N, Daher S. Preeclampsia and HIV infection. Eur J Obstet Gynecol Reprod Biol. 2004;117:240–241
  57. Suy A, Martinez E, Coll O, et al. Increased risk of pre-eclampsia and fetal death in HIV-infected pregnant women receiving highly active antiretroviral therapy. AIDS. 2006;20:59–66
  58. Bodkin C, Klopper H, Langley G. A comparison of HIV positive and negative pregnant women at a public sector hospital in South Africa. J Clin Nurs. 2006;15:735–741
  59. Kourtis AP, Bansil P, McPheeters M, Meikle SF, Posner SF, Jamieson DJ. Hospitalizations of pregnant HIV-infected women in the USA prior to and during the era of HAART, 1994-2003. AIDS. 2006;20:1823–1831
  60. Sartelet H, Rogier C, Milko-Sartelet I, Angel G, Michel G. Malaria associated pre-eclampsia in Senegal. Lancet. 1996;347:1121
  61. Shulman CE, Marshall T, Dorman EK, et al. Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae. Trop Med Int Health. 2001;6:770–778
  62. Dorman EK, Shulman CE, Kingdom J, et al. Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria. Ultrasound Obstet Gynecol. 2002;19:165–170
  63. N’Dao CT, N’Diaye JL, Gaye A, Le Hesran JY. Placental malaria and pregnancy outcome in a peri urban area in Senegal. Rev Epidemiol Sante Publique. 2006;54:149–156[in French]
  64. Kurki T, Hiilesmaa V, Raitasalo R, Mattila H, Ylikorkala O. Depression and anxiety in early pregnancy and risk for preeclampsia. Obstet Gynecol. 2000;95:487–490
  65. Fischer W, Lamm D, Bayer H, Birnbaum M. Correlation between urinary tract infection and pregnancy toxemias. Zentralbl Gynakol. 1970;92:1326–1333[in German]
  66. Drazancic A, Balasa A, Zadjelovic J, Kralj-Pejakovic L. The effect of treatment of bacteriuria on pregnancy outcome. Jugosl Ginekol Perinatol. 1989;29:15–18[in Croatian]
  67. Todros T, Verdiglione P, Ogge G, Paladini D, Vergani P, Cardaropoli S. Low incidence of hypertensive disorders of pregnancy in women treated with spiramycin for toxoplasma infection. Br J Clin Pharmacol. 2006;61:336–340
  68. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med. 2006;355:1885–1894
  69. Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal-fetal conflict during placental malaria. PLoS Med. 2006;3:e446
  70. Lamarca HL, Nelson AB, Scandurro AB, Whitley GS, Morris CA. Human cytomegalovirus-induced inhibition of cytotrophoblast invasion in a first trimester extravillous cytotrophoblast cell line. Placenta. 2006;27:137–147
  71. De Wolf F, Robertson WB, Brosens I. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol. 1975;123:164–174
  72. Sattar N, Greer IA. Pregnancy complications and maternal cardiovascular risk: opportunities for intervention and screening?. BMJ. 2002;325:157–160
  73. Danesh J, Collins R, Peto R. Chronic infections and coronary heart disease: is there a link?. Lancet. 1997;350:430–436
  74. Faas MM, Schuiling GA, Baller JF, Visscher CA, Bakker WW. A new animal model for human preeclampsia: ultra-low-dose endotoxin infusion in pregnant rats. Am J Obstet Gynecol. 1994;171:158–164
  75. Gower PE, Haswell B, Sidaway ME, de Wardener HE. Follow-up of 164 patients with bacteriuria of pregnancy. Lancet. 1968;1:990–994
  76. Whalley PJ, Martin FG, Peters PC. Significance of asymptomatic bacteriuria detected during pregnancy. JAMA. 1965;193:879–881
  77. Smaill F, Vazquez JC. Antibiotics for asymptomatic bacteriuria in pregnancy. Cochrane Database Syst Rev. 2007;(2):CD000490
  78. Golub LM, Payne JB, Reinhardt RA, Nieman G. Can systemic diseases co-induce (not just exacerbate) periodontitis? (A hypothetical “two-hit” model). J Dent Res. 2006;85:102–105
  79. Tonetti MS, D’Aiuto F, Nibali L, et al. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;356:911–920
  80. Goldenberg RL, Culhane JF. Preterm birth and periodontal disease. N Engl J Med. 2006;355:1925–1927

 Reprints not available from the authors.

 This study was supported by the United Nations Development Programme/United Nations Population Fund/World Health Organization/World Bank Special Program of Research, Development and Research Training in Human Reproduction, Department of Reproductive Health and Research, World Health Organization, Geneva, Switzerland.

 The views expressed in this document are solely the responsibility of the authors and do not necessarily represent the views of the World Health Organization or its Member States.

PII: S0002-9378(07)00919-2

doi: 10.1016/j.ajog.2007.07.040

American Journal of Obstetrics & Gynecology
Volume 198, Issue 1 , Pages 7-22 , January 2008

Article Tools