Clinical chorioamnionitis at term: The amniotic fluid fatty acyl lipidome

Journal of Lipid Research

Volumn 57, Issue 10, 2016, Pages 1906-1916

  Maddipati, Krishna Rao ^a,b   Romero, Roberto ^c,d,e,f,g,h   Chaiworapongsa, Tinnakorn ^c,d,e,h   Chaemsaithong, Piya ^c,d,e,h   Zhou, Sen Lin ^a,b   Xu, Zhonghui ^c,d,e   Tarca, Adi L ^c,d,e,h,i   Kusanovic, Juan Pedro ^c,d,e,j,k   Gomez, Ricardo ^k,l   Docheva, Nikolina ^c,d,e,h   Honn, Kenneth V ^a  

^a Bioactive Lipids Research Program   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c Rocky Mountain Veterinary Branch Division of Intramural Research Rocky Mountain Laboratories   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e University of Michigan ^*  (United States)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^g MICHIGAN STATE UNIVERSITY   (United States)

^h WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ Wayne State University   (United States)

^j HOSPITAL DR SÓTERO DEL RÍO   (Chile)

^k PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^l Hospital Clínico La Florida   (Chile)

more..

Author keywords

Eicosanoids; Epoxy fatty acids; Epoxygenase; Infection; Inflammation; Intra amniotic inflammation; Lipidomics; Lipoxygenase; Omega 3 fatty acids; Parturition

Indexed keywords

FATTY ACYL LIPIDOME; LIPIDOME; PROSTAGLANDIN; UNCLASSIFIED DRUG; FATTY ACID;

ADULT; AMNION FLUID; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHORIOAMNIONITIS; CLINICAL CHORIOAMNIONITIS AT TERM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; HUMAN; LABOR; LIPID ANALYSIS; LIPOGENESIS; MAJOR CLINICAL STUDY; MICROBIAL COLONIZATION; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SPONTANEOUS LABOR; TERM BIRTH; CLINICAL TRIAL; METABOLISM; METABOLOME; PATHOLOGY; PREGNANCY;

ADULT; AMNIOTIC FLUID; CHORIOAMNIONITIS; CROSS-SECTIONAL STUDIES; FATTY ACIDS; FEMALE; HUMANS; METABOLOME; PREGNANCY;

EID: 84990934066     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P069096     Document Type: Article

References (69)

1. Gibbs, R. S., R. Romero, S. L. Hillier, D. A. Eschenbach, and R. L. Sweet. 1992. A review of premature birth and subclinical infection. Am. J. Obstet. Gynecol. 166: 1515-1528.
2. Romero, R., S. K. Dey, and S. J. Fisher. 2014. Preterm labor: one syndrome, many causes. Science. 345: 760-765.
3. Gravett, M. G., D. Hummel, D. A. Eschenbach, and K. K. Holmes. 1986. Preterm labor associated with subclinical amniotic fluid infection and with bacterial vaginosis. Obstet. Gynecol. 67: 229-237.
4. Romero, R., P. Chaemsaithong, N. Docheva, S. J. Korzeniewski, A. L. Tarca, G. Bhatti, Z. Xu, J. P. Kusanovic, Z. Dong, N. Chaiyasit, et al. 2016. Clinical chorioamnionitis at term IV: the maternal plasma cytokine profile. J. Perinat. Med. 44: 77-98.
5. Malloy, M. H. 2014. Chorioamnionitis: epidemiology of newborn management and outcome United States 2008. J. Perinatol. 34: 611-615.
6. Romero, R., J. Miranda, J. P. Kusanovic, T. Chaiworapongsa, P. Chaemsaithong, A. Martinez, F. Gotsch, Z. Dong, A. I. Ahmed, M. Shaman, et al. 2015. Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J. Perinat. Med. 43: 19-36.
7. Kim, C. J., R. Romero, P. Chaemsaithong, N. Chaiyasit, B. H. Yoon, and Y. M. Kim. 2015. Acute chorioamnionitis and funisitis: definition, pathologic features, and clinical significance. Am. J. Obstet. Gynecol. 213: S29-S52.
8. Romero, R., J. Espinoza, L. F. Goncalves, J. P. Kusanovic, L. Friel, and S. Hassan. 2007. The role of inflammation and infection in preterm birth. Semin. Reprod. Med. 25: 21-39.
9. Romero, R., F. Gotsch, B. Pineles, and J. P. Kusanovic. 2007. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr. Rev. 65: S194-S202.
10. Christiaens, I., D. B. Zaragoza, L. Guilbert, S. A. Robertson, B. F. Mitchell, and D. M. Olson. 2008. Inflammatory processes in preterm and term parturition. J. Reprod. Immunol. 79: 50-57.
11. Becroft, D. M. O., J. M. D. Thompson, and E. A. Mitchell. 2010. Placental chorioamnionitis at term: epidemiology and follow-up in childhood. Pediatr. Dev. Pathol. 13: 282-290.
12. Elovitz, M. A., A. G. Brown, K. Breen, L. Anton, M. Maubert, and I. Burd. 2011. Intrauterine inflammation, insufficient to induce parturition, still evokes fetal and neonatal brain injury. Int. J. Dev. Neurosci. 29: 663-671.
13. Thomas, W., and C. P. Speer. 2011. Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology. 99: 177-187.
14. Tita, A. T. N., and W. W. Andrews. 2010. Diagnosis and management of clinical chorioamnionitis. Clin. Perinatol. 37: 339-354.
15. Newton, E. R. 1993. Chorioamnionitis and intraamniotic infection. Clin. Obstet. Gynecol. 36: 795-808.
16. Romero, R., P. Chaemsaithong, S. J. Korzeniewski, J. P. Kusanovic, N. Docheva, A. Martinez-Varea, A. I. Ahmed, B. H. Yoon, S. S. Hassan, T. Chaiworapongsa, et al. 2016. Clinical chorioamnionitis at term III: how well do clinical criteria perform in the identification of proven intra-amniotic infection? J. Perinat. Med. 44: 23-32.
17. Chen, G. Y., and G. Nunez. 2010. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10: 826-837.
18. Romero, R., T. Chaiworapongsa, Z. A. Savasan, Y. Hussein, Z. Dong, J. P. Kusanovic, C. J. Kim, and S. S. Hassan. 2012. Clinical chorioamnionitis is characterized by changes in the expression of the alarmin HMGB1 and one of its receptors, sRAGE. J. Matern. Fetal Neonatal Med. 25: 558-567.
19. Gomez-Lopez, N., R. Romero, O. Plazyo, B. Panaitescu, A. E. Furcron, D. Miller, T. Roumayah, E. Flom, and S. S. Hassan. 2016. Intra-amniotic administration of HMGB1 induces spontaneous preterm labor and birth. Am. J. Reprod. Immunol. 75: 3-7.
20. Serhan, C. N., N. Chiang, and T. E. Van Dyke. 2008. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8: 349-361.
21. Serhan, C. N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6: 1191-1197.
22. Ricciotti, E., and G. A. Fitzgerald. 2011. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31: 986-1000.
23. Harris, S. G., J. Padilla, L. Koumas, D. Ray, and R. P. Phipps. 2002. Prostaglandins as modulators of immunity. Trends Immunol. 23: 144-150.
24. Mitchell, M. D. 1981. Prostaglandins during pregnancy and the perinatal period. J. Reprod. Fertil. 62: 305-315.
25. Romero, R., R. Gonzalez, P. Baumann, E. Behnke, L. Rittenhouse, D. Barberio, D. B. Cotton, and M. D. Mitchell. 1994. Topographic differences in amniotic fluid concentrations of prostanoids in women in spontaneous labor at term. Prostaglandins Leukot. Essent. Fatty Acids. 50: 97-104.
26. Maddipati, K. R., R. Romero, T. Chaiworapongsa, S. L. Zhou, Z. Xu, A. L. Tarca, J. P. Kusanovic, H. Munoz, and K. V. Honn. 2014. Eicosanomic profiling reveals dominance of the epoxygenase pathway in human amniotic fluid at term in spontaneous labor. FASEB J. 28: 4835-4846.
27. Maddipati, K. R., R. Romero, T. Chaiworapongsa, P. Chaemsaithong, S-L. Zhou, Z. Xu, A. L. Tarca, J. P. Kusanovic, R. Gomez, N. Chaiyasit, et al. 2016. Lipidomic analysis of patients with microbial invasion of the amniotic cavity reveals up-regulation of leukotriene B4. FASEB J. In press.
28. Levy, B. D., C. B. Clish, B. Schmidt, K. Gronert, and C. N. Serhan. 2001. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2: 612-619.
29. Serhan, C. N. 2005. Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot. Essent. Fatty Acids. 73: 141-162.
30. Lehmann, C., J. Homann, A-K. Ball, R. Blöcher, T. K. Kleinschmidt, D. Basavarajappa, C. Angioni, N. Ferreirós, A-K. Häfner, O. Rådmark, et al. 2015. Lipoxin and resolvin biosynthesis is dependent on 5-lipoxygenase activating protein. FASEB J. 29: 5029-5043.
31. Romero, R., P. Chaemsaithong, S. J. Korzeniewski, A. L. Tarca, G. Bhatti, Z. Xu, J. P. Kusanovic, Z. Dong, N. Docheva, A. Martinez- Varea, et al. 2016. Clinical chorioamnionitis at term II: the intraamniotic inflammatory response. J. Perinat. Med. 44: 5-22.
32. Romero, R., P. Chaemsaithong, N. Docheva, S. J. Korzeniewski, A. L. Tarca, G. Bhatti, Z. Xu, J. P. Kusanovic, N. Chaiyasit, Z. Dong, et al. 2016. Clinical chorioamnionitis at term V: umbilical cord plasma cytokine profile in the context of a systemic maternal inflammatory response. J. Perinat. Med. 44: 53-76.
33. Romero, R., P. Chaemsaithong, N. Docheva, S. J. Korzeniewski, J. P. Kusanovic, B. H. Yoon, J. S. Kim, N. Chaiyasit, A. I. Ahmed, F. Qureshi, et al. 2016. Clinical chorioamnionitis at term VI: acute chorioamnionitis and funisitis according to the presence or absence of microorganisms and inflammation in the amniotic cavity. J. Perinat. Med. 44: 33-51.
34. Romero, R., J. Miranda, T. Chaiworapongsa, P. Chaemsaithong, F. Gotsch, Z. Dong, A. I. Ahmed, B. H. Yoon, S. S. Hassan, C. J. Kim, et al. 2014. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intraamniotic infection in preterm labor with intact membranes. Am. J. Reprod. Immunol. 71: 330-358.
35. Romero, R., R. Quintero, J. Nores, C. Avila, M. Mazor, S. Hanaoka, Z. Hagay, L. Merchant, and J. C. Hobbins. 1991. Amniotic fluid white blood cell count: a rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am. J. Obstet. Gynecol. 165: 821-830.
36. Romero, R., C. Jimenez, A. K. Lohda, J. Nores, S. Hanaoka, C. Avila, R. Callahan, M. Mazor, J. C. Hobbins, and M. P. Diamond. 1990. Amniotic fluid glucose concentration: a rapid and simple method for the detection of intraamniotic infection in preterm labor. Am. J. Obstet. Gynecol. 163: 968-974.
37. Romero, R., M. Emamian, R. Quintero, M. Wan, J. C. Hobbins, M. Mazor, and S. Edberg. 1988. The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am. J. Obstet. Gynecol. 159: 114-119.
38. Eshoo, M. W., C. C. Crowder, A. W. Rebman, M. A. Rounds, H. E. Matthews, J. M. Picuri, M. J. Soloski, D. J. Ecker, S. E. Schutzer, and J. N. Aucott. 2012. Direct molecular detection and genotyping of Borrelia burgdorferi from whole blood of patients with early Lyme disease. PLoS One. 7: e36825.
39. Shin, J. H., R. Ranken, S. E. Sefers, R. Lovari, C. D. Quinn, S. Meng, H. E. Carolan, D. Toleno, H. Li, J. N. Lee, et al. 2013. Detection, identification, and distribution of fungi in bronchoalveolar lavage specimens by use of multilocus PCR coupled with electrospray ionization/ mass spectrometry. J. Clin. Microbiol. 51: 136-141.
40. Metzgar, D., M. Frinder, R. Lovari, D. Toleno, C. Massire, L. B. Blyn, R. Ranken, H. E. Carolan, T. A. Hall, D. Moore, et al. 2013. Broad-spectrum biosensor capable of detecting and identifying diverse bacterial and Candida species in blood. J. Clin. Microbiol. 51: 2670-2678.
41. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 57: 289-300.
42. Henningsen, A. 2011. censReg: censored regression (Tobit) models. In. R Package, Version 0.5. (Accessed September 6, 2011, at http://cran.r-project.org/package=censReg.)
43. Liggins, G. 1981. Cervical ripening as an inflammatory reaction. In The Cervix in Pregnancy and Labour: Clinical and Biochemical Investigations. D. A. Ellwood and A. B. M. Anderson, editors. Churchill Livingstone, Edinburgh. 1-9.
44. Osman, I., A. Young, M. A. Ledingham, A. J. Thomson, F. Jordan, I. A. Greer, and J. E. Norman. 2003. Leukocyte density and proinflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol. Hum. Reprod. 9: 41-45.
45. Romero, R., M. Mazor, F. Brandt, W. Sepulveda, C. Avila, D. B. Cotton, and C. A. Dinarello. 1992. Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am. J. Reprod. Immunol. 27: 117-123.
46. Romero, R., W. Sepulveda, J. S. Kenney, L. E. Archer, A. C. Allison, and P. B. Sehgal. 1992. Interleukin 6 determination in the detection of microbial invasion of the amniotic cavity. Ciba Found. Symp. 167: 205-220; discussion 220-223.
47. Romero, R., M. Ceska, C. Avila, M. Mazor, E. Behnke, and I. Lindley. 1991. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am. J. Obstet. Gynecol. 165: 813-820.
48. Maymon, E., F. Ghezzi, S. S. Edwin, M. Mazor, B. H. Yoon, R. Gomez, and R. Romero. 1999. The tumor necrosis factor alpha and its soluble receptor profile in term and preterm parturition. Am. J. Obstet. Gynecol. 181: 1142-1148.
49. Esplin, M. S., R. Romero, T. Chaiworapongsa, Y. M. Kim, S. Edwin, R. Gomez, R. Gonzalez, and E. Y. Adashi. 2003. Amniotic fluid levels of immunoreactive monocyte chemotactic protein-1 increase during term parturition. J. Matern. Fetal Neonatal Med. 14: 51-56.
50. Lee, S. E., R. Romero, I. S. Park, H. S. Seong, C. W. Park, and B. H. Yoon. 2008. Amniotic fluid prostaglandin concentrations increase before the onset of spontaneous labor at term. J. Matern. Fetal Neonatal Med. 21: 89-94.
51. Romero, R., H. Munoz, R. Gomez, M. Parra, M. Polanco, V. Valverde, J. Hasbun, J. Garrido, F. Ghezzi, M. Mazor, et al. 1996. Increase in prostaglandin bioavailability precedes the onset of human parturition. Prostaglandins Leukot. Essent. Fatty Acids. 54: 187-191.
52. Mitchell, M. D., R. J. Romero, S. S. Edwin, and M. S. Trautman. 1995. Prostaglandins and parturition. Reprod. Fertil. Dev. 7: 623-632.
53. Oh, D. Y., S. Talukdar, E. J. Bae, T. Imamura, H. Morinaga, W. Fan, P. Li, W. J. Lu, S. M. Watkins, and J. M. Olefsky. 2010. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell. 142: 687-698.
54. Narumiya, S., Y. Sugimoto, and F. Ushikubi. 1999. Prostanoid receptors: structures, properties, and functions. Physiol. Rev. 79: 1193-1226.
55. Shimizu, T. 2009. Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 49: 123-150.
56. Wada, M., C. J. DeLong, Y. H. Hong, C. J. Rieke, I. Song, R. S. Sidhu, C. Yuan, M. Warnock, A. H. Schmaier, C. Yokoyama, et al. 2007. Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J. Biol. Chem. 282: 22254-22266.
57. Arnold, C., M. Markovic, K. Blossey, G. Wallukat, R. Fischer, R. Dechend, A. Konkel, C. von Schacky, F. C. Luft, D. N. Muller, et al. 2010. Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of '-3 fatty acids. J. Biol. Chem. 285: 32720-32733.
58. Bannenberg, G. L., N. Chiang, A. Ariel, M. Arita, E. Tjonahen, K. H. Gotlinger, S. Hong, and C. N. Serhan. 2005. Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174: 4345-4355.
59. Serhan, C. N., and N. A. Petasis. 2011. Resolvins and protectins in inflammation resolution. Chem. Rev. 111: 5922-5943.
60. Colas, R. A., M. Shinohara, J. Dalli, N. Chiang, and C. N. Serhan. 2014. Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. Am. J. Physiol. Cell Physiol. 307: C39-C54.
61. Serhan, C. N. 2014. Pro-resolving lipid mediators are leads for resolution physiology. Nature. 510: 92-101.
62. Node, K., Y. Huo, X. Ruan, B. Yang, M. Spiecker, K. Ley, D. C. Zeldin, and J. K. Liao. 1999. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science. 285: 1276-1279.
63. Zhang, Y., C. L. Oltman, T. Lu, H. C. Lee, K. C. Dellsperger, and M. VanRollins. 2001. EET homologs potently dilate coronary microvessels and activate BK(Ca) channels. Am. J. Physiol. Heart Circ. Physiol. 280: H2430-H2440.
64. Morisseau, C., B. Inceoglu, K. Schmelzer, H-J. Tsai, S. L. Jinks, C. M. Hegedus, and B. D. Hammock. 2010. Naturally occurring monoepoxides of eicosapentaenoic acid and docosahexaenoic acid are bioactive antihyperalgesic lipids. J. Lipid Res. 51: 3481-3490.
65. Choi, S. J., S. Oh, J. H. Kim, and C. R. Roh. 2007. Changes of nuclear factor kappa B (NF-kappaB), cyclooxygenase-2 (COX-2) and matrix metalloproteinase-9 (MMP-9) in human myometrium before and during term labor. Eur. J. Obstet. Gynecol. Reprod. Biol. 132: 182-188.
66. Fuentes, A., E. P. Spaziani, and W. F. O'Brien. 1996. The expression of cyclooxygenase-2 (COX-2) in amnion and decidua following spontaneous labor. Prostaglandins. 52: 261-267.
67. Keelan, J. A., M. Blumenstein, R. J. Helliwell, T. A. Sato, K. W. Marvin, and M. D. Mitchell. 2003. Cytokines, prostaglandins and parturition-a review. Placenta. 24: S33-S46.
68. Mittal, P., R. Romero, L. Tarca Adi, J. Gonzalez, S. Draghici, Y. Xu, Z. Dong, C-L. Nhan-Chang, T. Chaiworapongsa, S. Lye, et al. 2010. Characterization of the myometrial transcriptome and biological pathways of spontaneous human labor at term. J. Perinat. Med. 38: 617-643.
69. Bollapragada, S., R. Youssef, F. Jordan, I. Greer, J. Norman, and S. Nelson. 2009. Term labor is associated with a core inflammatory response in human myometrium and cervix. Am. J. Obstet. Gynecol. 200: 104.e1-104.e11. [Erratum. 2009. Am. J. Obstet. Gynecol. 201: 214.]