Acute pyelonephritis during pregnancy changes the balance of angiogenic and anti-angiogenic factors in maternal plasma

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 23, Issue 2, 2010, Pages 167-178

  Chaiworapongsa, Tinnakorn ^a,b   Romero, Roberto ^a,b   Gotsch, Francesca ^a   Kusanovic, Juan Pedro ^a,b   Mittal, Pooja ^a,b   Kim, Sun Kwon ^a   Erez, Offer ^a,b   Vaisbuch, Edi ^a,b   Mazaki Tovi, Shali ^a,b   Kim, Chong Jai ^a,b   Dong, Zhong ^a   Yeo, Lami ^a,b   Hassan, Sonia S ^a,b  

^a Hutzel Womens Hospital   (United States)

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

Author keywords

Acute pyelonephritis; Angiogenesis; Angiogenic factor; Cytokines; Infection; Inflammation; Preeclampsia; Systemic inflammation

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOGENIC FACTOR; ENDOGLIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; PLACENTAL GROWTH FACTOR; TUMOR NECROSIS FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ACUTE PYELONEPHRITIS; ADULT; ARTICLE; BLOOD LEVEL; CLINICAL FEATURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FEVER; GESTATIONAL AGE; HUMAN; IMMUNOASSAY; INFECTION; MAJOR CLINICAL STUDY; MATERNAL PLASMA; PREECLAMPSIA; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; URINE CULTURE;

ACUTE DISEASE; ADULT; ANGIOGENESIS INDUCING AGENTS; ANGIOGENESIS INHIBITORS; ANTIGENS, CD; CASE-CONTROL STUDIES; FEMALE; HUMANS; INFANT, NEWBORN; INTERFERON-GAMMA; INTERLEUKINS; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PREGNANCY PROTEINS; PYELONEPHRITIS; RECEPTORS, CELL SURFACE; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 75449119128     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767050903067378     Document Type: Article

References (80)

1. Hill JB, Sheffield JS, McIntire DD, Wendel GD, Jr. Acute pyelonephritis in pregnancy. Obstet Gynecol 2005;105:18-23.
2. Bacak SJ, Callaghan WM, Dietz PM, Crouse C. Pregnancyassociated hospitalizations in the United States, 1999-2000. Am J Obstet Gynecol 2005;192:592-597.
3. Millar LK, DeBuque L, Wing DA. Uterine contraction frequency during treatment of pyelonephritis in pregnancy and subsequent risk of preterm birth. J Perinat Med 2003; 31:41-46.
4. Cunningham FG, Leveno KJ, Hankins GD, Whalley PJ. Respiratory insufficiency associated with pyelonephritis during pregnancy. Obstet Gynecol 1984;63:121-125.
5. Amstey MS. Frequency of adult respiratory distress syndrome in pregnant women who have pyelonephritis. Clin Infect Dis 1992;14:1260-1261.
6. Bubeck RW. Acute pyelonephritis during pregnancy with anuria, septicemia and thrombocytopenia. Del Med J 1968; 40:143-147.
7. Sheffield JS. Sepsis and septic shock in pregnancy. Crit Care Clin 2004;20:651-660.
8. Galvagno SM Jr, Camann W. Sepsis and acute renal failure in pregnancy. Anesth Analg 2009;108:572-575.
9. Mabie WC, Barton JR, Sibai B. Septic shock in pregnancy. Obstet Gynecol 1997;90:553-561.
10. Pickkers P, Sprong T, Eijk L, Hoeven H, Smits P, Deuren M. Vascular endothelial growth factor is increased during the first 48 hours of human septic shock and correlates with vascular permeability. Shock 2005;24:508-512.
11. van der FM, van Leeuwen HJ, van Kessel KP, Kimpen JL, Hoepelman AI, Geelen SP. Plasma vascular endothelial growth factor in severe sepsis. Shock 2005;23:35-38.
12. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, Bodyak N, Kang PM, Toltl L, Belikoff B, Buras J, et al. Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 2006; 203:1447-1458.
13. Tsao PN, Chan FT, Wei SC, Hsieh WS, Chou HC, Su YN, Chen CY, Hsu WM, Hsieh FJ, Hsu SM. Soluble vascular endothelial growth factor receptor-1 protects mice in sepsis. Crit Care Med 2007;35:1955-1960.
14. Yano K, Okada Y, Beldi G, Shih SC, Bodyak N, Okada H, Kang PM, Luscinskas W, Robson SC, Carmeliet P, et al. Elevated levels of placental growth factor represent an adaptive host response in sepsis. J Exp Med 2008;205:2623-2631.
15. Karlsson S, Pettila V, Tenhunen J, Lund V, Hovilehto S, Ruokonen E. Vascular endothelial growth factor in severe sepsis and septic shock. Anesth Analg 2008;106:1820-1826.
16. Shapiro NI, Yano K, Okada H, Fischer C, Howell M, Spokes KC, Ngo L, Angus DC, Aird WC. A prospective, observational study of soluble FLT-1 and vascular endothelial growth factor in sepsis. Shock 2008;29:452-457.
17. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989;161:1200-1204.
18. Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499-506.
19. Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: new concepts in an old disease. Semin Perinatol 1988;12:302-323.
20. Roberts JM, Hubel CA. The two stage model of preeclampsia: variations on the theme. Placenta 2009;30(Suppl A):S32-S37.
21. Sibai BM. Hypertensive disorders of pregnancy: the United States perspective. Curr Opin Obstet Gynecol 2008;20:102-106.
22. Redman CW, Sargent IL. Placental stress and pre-eclampsia: a revised view. Placenta 2009;30(Suppl A):S38-S42.
23. Hung TH, Skepper JN, Charnock-Jones DS, Burton GJ. Hypoxia-reoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia. Circ Res 2002;90:1274-1281.
24. Granger JP, Alexander BT, Llinas MT, Bennett WA, Khalil RA. Pathophysiology of preeclampsia: linking placental ischemia/hypoxia with microvascular dysfunction. Microcirculation 2002;9:147-160.
25. Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998;179:80-86.
26. Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792-797.
27. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, von DP. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006;27:56-61.
28. Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol 1997;37:240-249.
29. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, Hicks MJ, Ramin SM, Kellems RE, Xia Y. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med 2008;14:855-862.
30. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci USA 1993;90:10705-10709.
31. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003;111:649-658.
32. Reuvekamp A, Velsing-Aarts FV, Poulina IE, Capello JJ, Duits AJ. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 1999;106:1019-1022.
33. Livingston JC, Chin R, Haddad B, McKinney ET, Ahokas R, Sibai BM. Reductions of vascular endothelial growth factor and placental growth factor concentrations in severe preeclampsia. Am J Obstet Gynecol 2000;183:1554-1557.
34. Tidwell SC, Ho HN, Chiu WH, Torry RJ, Torry DS. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001;184:1267-1272.
35. Taylor RN, Grimwood J, Taylor RS, McMasterMT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003;188:177-182.
36. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672-683.
37. Chaiworapongsa T, Romero R, Espinoza J, Bujold E,Mee KY, Goncalves LF, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 2004;190:1541-1547.
38. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005;17:3-18.
39. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642-649. (Pubitemid 43865232)
40. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992-1005.
41. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsch F, Erez O, Mazaki-Tovi S, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med 2008;21:9-23.
42. Ferrara N. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS 2005;94:209-231.
43. Shibuya M. Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 2006;9:225-230.
44. ten DP, Goumans MJ, Pardali E. Endoglin in angiogenesis and vascular diseases. Angiogenesis 2008;11:79-89.
45. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol 2006;39:469-478.
46. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, Edwin S, Kim YM, Erez O, Kusanovic JP, et al. Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 2008; 21:41-52.
47. Chaiworapongsa T, Romero R, Tarca AL, Kusanovic JP, Gotsch F, Mittal P, Erez O, Vaisbuch E, Mazaki-Tovi S, Dong Z, et al. A decrease in maternal plasma concentrations of sVEGFR-2 precedes the clinical diagnosis of preeclampsia. Reprod Sci 2009.16:264A.
48. Sibai BM, Ewell M, Levine RJ, Klebanoff MA, Esterlitz J, Catalano PM, Goldenberg RL, Joffe G. Risk factors associated with preeclampsia in healthy nulliparous women. The calcium for preeclampsia prevention (CPEP) study group. Am J Obstet Gynecol 1997;177:1003-1010.
49. von DP, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003;22:143-148.
50. Espinoza J, Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Nien JK, Kusanovic JP, Erez O, Bujold E, Goncalves LF, et al. Unexplained fetal death: another anti-angiogenic state. J Matern Fetal Neonatal Med 2007;20:495-507.
51. Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, Edwin S, Kusanovic JP, Erez O, Than NG, et al. The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med 2008;21:25-40.
52. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, et al. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007; 115:1789-1797.
53. Gargett CE, Zaitseva M, Bucak K, Chu S, Fuller PJ, Rogers PA. 17Beta-estradiol up-regulates vascular endothelial growth factor receptor-2 expression in human myometrial microvascular endothelial cells: role of estrogen receptor-alpha and -beta. J Clin Endocrinol Metab 2002;87:4341-4349.
54. Hastings JM, Licence DR, Burton GJ, Charnock-Jones DS, Smith SK. Soluble vascular endothelial growth factor receptor 1 inhibits edema and epithelial proliferation induced by 17beta-estradiol in the mouse uterus. Endocrinology 2003; 144:326-334.
55. Makrydimas G, Sotiriadis A, Savvidou MD, Spencer K, Nicolaides KH. Physiological distribution of placental growth factor and soluble Flt-1 in early pregnancy. Prenat Diagn 2008;28:175-179.
56. Sacks G, Sargent I, Redman C. An innate view of human pregnancy. Immunol Today 1999;20:114-118.
57. Naccasha N, Gervasi MT, Chaiworapongsa T, Berman S, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in normal pregnancy and maternal infection. Am J Obstet Gynecol 2001;185:1118-1123. (Pubitemid 33097374)
58. Chaiworapongsa T, Romero R, Yoshimatsu J, Espinoza J, Kim YM, Park K, Kalache K, Edwin S, Bujold E, Gomez R. Soluble adhesion molecule profile in normal pregnancy and pre-eclampsia. J Matern Fetal Neonatal Med 2002;12:19-27.
59. Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, Wolf M, Harger G, Markovic N. Extra-placental expression of vascular endothelial growth factor receptor-1, (Flt-1) and soluble Flt-1 (sFlt- 1), by peripheral blood mononuclear cells (PBMCs) in normotensive and preeclamptic pregnant women. Placenta 2005;26:563-573.
60. Holmlund U, Cebers G, Dahlfors AR, Sandstedt B, Bremme K, Ekstrom ES, Scheynius A. Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Tolllike receptor-4 in the human placenta. Immunology 2002; 107:145-151.
61. Kim YM, Romero R, Oh SY, Kim CJ, Kilburn BA, Armant DR, Nien JK, Gomez R, Mazor M, Saito S, et al. Toll-like receptor 4: a potential link between 'danger signals', the innate immune system, and preeclampsia? Am J Obstet Gynecol 2005;193:921-927.
62. Knofler M, Mosl B, Bauer S, Griesinger G, Husslein P. TNFalpha/ TNFRI in primary and immortalized first trimester cytotrophoblasts. Placenta 2000;21:525-535.
63. Yui J, Hemmings D, Garcia-Lloret M, Guilbert LJ. Expression of the human p55 and p75 tumor necrosis factor receptors in primary villous trophoblasts and their role in cytotoxic signal transduction. Biol Reprod 1996;55:400-409.
64. Ejima K, Koji T, Tsuruta D, Nanri H, Kashimura M, Ikeda M. Induction of apoptosis in placentas of pregnant mice exposed to lipopolysaccharides: possible involvement of Fas/ Fas ligand system. Biol Reprod 2000;62:178-185.
65. Sun QH, Peng JP, Xia HF, Yang Y. IFN-gamma promotes apoptosis of the uterus and placenta in pregnant rat and human cytotrophoblast cells. J Interferon Cytokine Res 2007; 27:567-578.
66. Gotsch F, Kim YM, Kim CJ, Edwin S, Holtra J, Tarca AL, Chaiworapongsa T, Kusanovic JP, Mor G, Redman C, et al. A link between inflammation/infection and anti-angiogenic state in preeclampsia: inflammatory mediators mimic effect of hypoxia on trophoblast by increasing sflt-1 and decreasing placental growth factor production. International society for the study of hypertension in pregnancy. Proceedings World Congress XVI. Washington DC 2008, page 46, ABS1-7.
67. Conde-Agudelo A, Villar J, Lindheimer M. Maternal infection and risk of preeclampsia: systematic review and metaanalysis. Am J Obstet Gynecol 2008;198:7-22.
68. Ebos JM, Bocci G, Man S, Thorpe PE, Hicklin DJ, Zhou D, Jia X, Kerbel RS. A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol Cancer Res 2004;2:315-326.
69. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958.
70. Clark DE, Smith SK, Sharkey AM, Charnock-Jones DS. Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod 1996;11:1090-1098.
71. Helske S, Vuorela P, Carpen O, Hornig C, Weich H, Halmesmaki E. Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol Hum Reprod 2001;7: 205-210.
72. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003;88:2348-2351.
73. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, Lammoglia R, Charnock-Jones DS. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998; 59:1540-1548.
74. Wikstrom AK, Larsson A, Eriksson UJ, Nash P, Olovsson M. Early postpartum changes in circulating pro- and antiangiogenic factors in early-onset and late-onset pre-eclampsia. Acta Obstet Gynecol Scand 2008;87:146-153.
75. Gu Y, Lewis DF, Wang Y. Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008; 93:260-266.
76. Park CW, Park JS, Shim SS, Jun JK, Yoon BH, Romero R. An elevated maternal plasma, but not amniotic fluid, soluble fms-like tyrosine kinase-1 (sFlt-1) at the time of mid-trimester genetic amniocentesis is a risk factor for preeclampsia. Am J Obstet Gynecol 2005;193:984-989.
77. Staff AC, Braekke K, Harsem NK, Lyberg T, Holthe MR. Circulating concentrations of sFlt1 (soluble fms-like tyrosine kinase 1) in fetal and maternal serum during pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 2005; 122:33-39.
78. Staff AC, Braekke K, Johnsen GM, Karumanchi SA, Harsem NK. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007;197:176.
79. Kusanovic JP, Romero R, Esoinoza J, Gotsch F, Edwin S, Chaiworapongsa T, Mittal P, Soto E, Erez O, Mazaki-Tovi S, et al. Maternal serum soluble CD30 is increased in pregnancies complicated with acute pyelonephritis. J Matern Fetal Neonatal Med 2007;20:803-811.
80. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 2003;31:1250-1256. (Pubitemid 36444440)