Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1992 Dec;60(12):5232–5241. doi: 10.1128/iai.60.12.5232-5241.1992

Histological and immunocytochemical characterization of Coxiella burnetii-associated lesions in the murine uterus and placenta.

W Baumgärtner 1, S Bachmann 1
PMCID: PMC258302  PMID: 1452356

Abstract

The fetoplacental units and the postgravid uterus of BALB/cJ (H-2d) mice inoculated intraperitoneally with Coxiella burnetii (Nine Mile isolate, phase I) on day 6 of pregnancy were examined histologically and immunocytochemically at 1 to 160 days postinoculation. Clinically, abortions, stillbirths, and perinatal deaths were observed. Histological lesions in the placenta were characterized by severe necrosis of the decidua basalis and the labyrinth, fibrinoid degeneration of decidual vessels, and microthrombosis. Pyometra and endometritis at the sites of previous placental attachment, characterized by ulceration, central necrosis, and moderate cellular infiltration consisting of neutrophils and macrophages, were observed postpartum. Pups sacrificed at the age of 9 days exhibited interstitial pneumonia with few granulomas and granulomatous hepatitis and splenitis. Immunocytochemically, antigen-bearing cells were first detected in the decidua 9 days postconception, and single immunopositive cells were detected in the fetal placenta 4 days later. Thereafter, until abortion or parturition, abundant accumulation of C. burnetii antigen was observed in the maternal and fetal compartments of the placenta. Up to 28 days postinoculation, many immunopositive cells were demonstrated at the sites of previous placental attachment, whereas the adjacent endometrium contained only a few antigen-positive cells. C. burnetii antigen was demonstrated in decidual cells, trophoblasts, and macrophages and extracellularly within the sinuses of the labyrinth and in the uterine lumen but not in granulated metrial gland cells. Fetuses in utero and aborted, stillborn, or perinatally dying offspring were immunocytochemically negative for C. burnetii antigen; however, pups killed 9 days after birth showed lesion-associated positive immunoreaction in the lung, liver, and spleen. The present study shows that infection with C. burnetii during pregnancy results in uncontrolled growth of the organism in the murine uteroplacental unit and that associated lesions are characterized by necrosis of placental tissues, fibrinoid degeneration of decidual vessels, and microthrombosis.

Full text

PDF
5232

Images in this article

5235Image
on p.5235
5236Image
on p.5236
5238Image
on p.5238
5239Image
on p.5239
5240Image
on p.5240

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AMOROSO E. C. Histology of the placenta. Br Med Bull. 1961 May;17:81–90. doi: 10.1093/oxfordjournals.bmb.a069901. [DOI] [PubMed] [Google Scholar]
  2. Aitken I. D. Clinical aspects and prevention of Q fever in animals. Eur J Epidemiol. 1989 Dec;5(4):420–424. doi: 10.1007/BF00140132. [DOI] [PubMed] [Google Scholar]
  3. Amano K., Williams J. C., Missler S. R., Reinhold V. N. Structure and biological relationships of Coxiella burnetii lipopolysaccharides. J Biol Chem. 1987 Apr 5;262(10):4740–4747. [PubMed] [Google Scholar]
  4. Baca O. G., Paretsky D. Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiol Rev. 1983 Jun;47(2):127–149. doi: 10.1128/mr.47.2.127-149.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baca O. G. Pathogenesis of rickettsial infections emphasis on Q fever. Eur J Epidemiol. 1991 May;7(3):222–228. doi: 10.1007/BF00145670. [DOI] [PubMed] [Google Scholar]
  6. Baumgärtner W., Dettinger H., Schmeer N., Hoffmeister E. Evaluation of different fixatives and treatments for immunohistochemical demonstration of Coxiella burnetti in paraffin-embedded tissues. J Clin Microbiol. 1988 Oct;26(10):2044–2047. doi: 10.1128/jcm.26.10.2044-2047.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casey M. L., Cox S. M., Beutler B., Milewich L., MacDonald P. C. Cachectin/tumor necrosis factor-alpha formation in human decidua. Potential role of cytokines in infection-induced preterm labor. J Clin Invest. 1989 Feb;83(2):430–436. doi: 10.1172/JCI113901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chaouat G., Kolb J. P., Wegmann T. G. The murine placenta as an immunological barrier between the mother and the fetus. Immunol Rev. 1983;75:31–60. doi: 10.1111/j.1600-065x.1983.tb01090.x. [DOI] [PubMed] [Google Scholar]
  9. Clark D. A., Flanders K. C., Banwatt D., Millar-Book W., Manuel J., Stedronska-Clark J., Rowley B. Murine pregnancy decidua produces a unique immunosuppressive molecule related to transforming growth factor beta-2. J Immunol. 1990 Apr 15;144(8):3008–3014. [PubMed] [Google Scholar]
  10. Clark I. A., Chaudhri G. Tumor necrosis factor in malaria-induced abortion. Am J Trop Med Hyg. 1988 Sep;39(3):246–249. doi: 10.4269/ajtmh.1988.39.246. [DOI] [PubMed] [Google Scholar]
  11. Croy B. A., Kassouf S. A. Evaluation of the murine metrial gland for immunological function. J Reprod Immunol. 1989 Mar;15(1):51–69. doi: 10.1016/0165-0378(89)90044-2. [DOI] [PubMed] [Google Scholar]
  12. Cybulsky M. I., Chan M. K., Movat H. Z. Acute inflammation and microthrombosis induced by endotoxin, interleukin-1, and tumor necrosis factor and their implication in gram-negative infection. Lab Invest. 1988 Apr;58(4):365–378. [PubMed] [Google Scholar]
  13. DE MATTIA R., ANGELA G. C., TURLETTI G. Ricerche sperimentali sull' organotropismo e sulla eliminazione della Coxiella Burneti. Arch Sci Med (Torino) 1952 May;93(5):481–492. [PubMed] [Google Scholar]
  14. Ellis M. E., Smith C. C., Moffat M. A. Chronic or fatal Q-fever infection: a review of 16 patients seen in North-East Scotland (1967-80). Q J Med. 1983 Winter;52(205):54–66. [PubMed] [Google Scholar]
  15. Hackstadt T. The role of lipopolysaccharides in the virulence of Coxiella burnetii. Ann N Y Acad Sci. 1990;590:27–32. doi: 10.1111/j.1749-6632.1990.tb42203.x. [DOI] [PubMed] [Google Scholar]
  16. Haesaert B., Ornoy A. Transplacental effects of endotoxemia on fetal mouse brain, bone, and placental tissue. Pediatr Pathol. 1986;5(2):167–181. doi: 10.3109/15513818609041199. [DOI] [PubMed] [Google Scholar]
  17. Hunt J. S., Manning L. S., Wood G. W. Macrophages in murine uterus are immunosuppressive. Cell Immunol. 1984 May;85(2):499–510. doi: 10.1016/0008-8749(84)90262-4. [DOI] [PubMed] [Google Scholar]
  18. Kearns M., Lala P. K. Characterization of hematogenous cellular constituents of the murine decidua: a surface marker study. J Reprod Immunol. 1985 Nov;8(2-3):213–234. doi: 10.1016/0165-0378(85)90042-7. [DOI] [PubMed] [Google Scholar]
  19. Kearns M., Lala P. K. Life history of decidual cells: a review. Am J Reprod Immunol. 1983 Mar;3(2):78–82. doi: 10.1111/j.1600-0897.1983.tb00219.x. [DOI] [PubMed] [Google Scholar]
  20. Lala P. K., Chatterjee-Hasrouni S., Kearns M., Montgomery B., Colavincenzo V. Immunobiology of the feto-maternal interface. Immunol Rev. 1983;75:87–116. doi: 10.1111/j.1600-065x.1983.tb01092.x. [DOI] [PubMed] [Google Scholar]
  21. Laughlin T., Waag D., Williams J., Marrie T. Q fever: from deer to dog to man. Lancet. 1991 Mar 16;337(8742):676–677. doi: 10.1016/0140-6736(91)92494-m. [DOI] [PubMed] [Google Scholar]
  22. Luft B. J., Remington J. S. The adverse effect of pregnancy on macrophage activation. Cell Immunol. 1984 Apr 15;85(1):94–99. doi: 10.1016/0008-8749(84)90281-8. [DOI] [PubMed] [Google Scholar]
  23. Martinov S. P., Neikov P., Popov G. V. Experimental Q fever in sheep. Eur J Epidemiol. 1989 Dec;5(4):428–431. doi: 10.1007/BF00140134. [DOI] [PubMed] [Google Scholar]
  24. McKay D. G., Wong T. C. The Effect of Bacterial Endotoxin on the Placenta of the Rat. Am J Pathol. 1963 Mar;42(3):357–377. [PMC free article] [PubMed] [Google Scholar]
  25. Moore J. D., Barr B. C., Daft B. M., O'Connor M. T. Pathology and diagnosis of Coxiella burnetii infection in a goat herd. Vet Pathol. 1991 Jan;28(1):81–84. doi: 10.1177/030098589102800112. [DOI] [PubMed] [Google Scholar]
  26. Moos A., Hackstadt T. Comparative virulence of intra- and interstrain lipopolysaccharide variants of Coxiella burnetii in the guinea pig model. Infect Immun. 1987 May;55(5):1144–1150. doi: 10.1128/iai.55.5.1144-1150.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Müntener M., Hsu Y. C. Development of trophoblast and placenta of the mouse. A reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat (Basel) 1977;98(3):241–252. [PubMed] [Google Scholar]
  28. Paquet A., Jr, Rael E. D., Klassen D., Martinez I., Baca O. G. Mitogenic and protective activity associated with a lipopolysaccharide from Coxiella burnetii. Can J Microbiol. 1978 Dec;24(12):1616–1618. doi: 10.1139/m78-259. [DOI] [PubMed] [Google Scholar]
  29. Parr E. L., Parr M. B., Young J. D. Localization of a pore-forming protein (perforin) in granulated metrial gland cells. Biol Reprod. 1987 Dec;37(5):1327–1335. doi: 10.1095/biolreprod37.5.1327. [DOI] [PubMed] [Google Scholar]
  30. Penn C. W. The eighth C. L. Oakley lecture. Pathogenicity and immunobiology of Treponema pallidum. J Med Microbiol. 1987 Aug;24(1):1–9. doi: 10.1099/00222615-24-1-1. [DOI] [PubMed] [Google Scholar]
  31. Pinsky R. L., Fishbein D. B., Greene C. R., Gensheimer K. F. An outbreak of cat-associated Q fever in the United States. J Infect Dis. 1991 Jul;164(1):202–204. doi: 10.1093/infdis/164.1.202. [DOI] [PubMed] [Google Scholar]
  32. Prasad B. N., Chandiramani N. K., Wagle A. Isolation of Coxiella burnetii from human sources. Int J Zoonoses. 1986 Jun;13(2):112–117. [PubMed] [Google Scholar]
  33. Rauch A. M., Tanner M., Pacer R. E., Barrett M. J., Brokopp C. D., Schonberger L. B. Sheep-associated outbreak of Q fever, Idaho. Arch Intern Med. 1987 Feb;147(2):341–344. [PubMed] [Google Scholar]
  34. Redline R. W., Lu C. Y. Specific defects in the anti-listerial immune response in discrete regions of the murine uterus and placenta account for susceptibility to infection. J Immunol. 1988 Jun 1;140(11):3947–3955. [PubMed] [Google Scholar]
  35. Riechman N., Raz R., Keysary A., Goldwasser R., Flatau E. Chronic Q fever and severe thrombocytopenia in a pregnant woman. Am J Med. 1988 Aug;85(2):253–254. doi: 10.1016/s0002-9343(88)80355-3. [DOI] [PubMed] [Google Scholar]
  36. SYRUCEK L., SOBESLAVSKY O., GUTVIRTH I. Isolation of Coxiella burneti from human placentas. J Hyg Epidemiol Microbiol Immunol. 1958;2(1):29–35. [PubMed] [Google Scholar]
  37. Schneider W. Titration of Coxiella burnetii in Buffalo green monkey (BGM) cell cultures. Zentralbl Bakteriol. 1989 May;271(1):77–84. doi: 10.1016/s0934-8840(89)80056-8. [DOI] [PubMed] [Google Scholar]
  38. Schramek S., Brezina R. Characterization of an endotoxic lipopolysaccharide from Coxiella burnetii. Acta Virol. 1976 Apr;20(2):152–158. [PubMed] [Google Scholar]
  39. Schramek S., Kazar J., Sekeyova Z., Freudenberg M. A., Galanos C. Induction of hyperreactivity to endotoxin in mice by Coxiella burnetii. Infect Immun. 1984 Sep;45(3):713–717. doi: 10.1128/iai.45.3.713-717.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sidwell R. W., Gebhardt L. P. Studies of latent Q fever infections. 3. Effects of parturition upon latently infected guinea pigs and white mice. Am J Epidemiol. 1966 Jul;84(1):132–137. doi: 10.1093/oxfordjournals.aje.a120618. [DOI] [PubMed] [Google Scholar]
  41. Silen M. L., Firpo A., Morgello S., Lowry S. F., Francus T. Interleukin-1 alpha and tumor necrosis factor alpha cause placental injury in the rat. Am J Pathol. 1989 Aug;135(2):239–244. [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES