Download PDF
Am J Perinatol 2020; 37(06): 562-569
DOI: 10.1055/s-0039-1700862
SMFM Fellowship Series Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Steroid Hormone Levels in Recipient Amniotic Fluid in Twin–Twin Transfusion Syndrome and Their Association with Preterm Delivery

Mallory Hoffman 
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
,
Lovepreet K. Mann
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Jong H. Won
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Eric P. Bergh
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Roopali Donepudi
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Anthony Johnson
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Kenneth J. Moise
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
,
Cora Macpherson
3   Department of Epidemiology and Biostatistics, The George Washington University Biostatistics Center, Milken Institute School of Public Health, George Washington University, Rockville, Maryland
,
Elizabeth Thom
3   Department of Epidemiology and Biostatistics, The George Washington University Biostatistics Center, Milken Institute School of Public Health, George Washington University, Rockville, Maryland
,
Sam Mesiano
4   Department of Reproductive Biology, Case Western Reserve University School of Medicine, Cleveland, Ohio
,
Ramesha Papanna
1   Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, UTHealth, The University of Texas Health Science Center at Houston, Houston, Texas
2   The Fetal Center, Children's Memorial Hermann Hospital, Houston, Texas
› Author Affiliations Funding This study is supported by the Department of Obstetrics, Gynecology, and Reproductive Sciences, The University of Texas McGovern Medical School at Houston.
Further Information

Publication History

10 May 2019

23 September 2019

Publication Date:
31 December 2019 (online)

    Permissions and Reprints

Abstract

Objective Preterm delivery following fetoscopic laser surgery (FLS) of twin–twin transfusion syndrome (TTTS) is associated with severe perinatal morbidity and mortality. The role of steroid hormones in amniotic fluid (AF) after FLS remains unknown.

Study Design A prospective cohort study of consecutive case series of FLS for TTTS was performed from April 2012 to February 2017. Cases were divided into early (≤27 weeks) spontaneous preterm delivery (ED) and late delivery (LD; ≥34 weeks) following FLS and compared. AF supernatants were assessed for protein, estradiol, progesterone and cortisol levels (using the ELISA kit), and normalized to total protein levels to adjust for dilution.

Results A total of 294 consecutive cases of FLS for TTTS in monochorionic–diamniotic twins were performed during the study period. AF was available in 44 ED patients and 50 LD patients. On logistic regression, ED was associated with higher normalized progesterone levels (odds ratio [OR]: 1.25; 95% confidence interval [CI]: 1.12–1.41), lower normalized cortisol (OR: 0.78; 95% CI: 0.64–0.96), and higher estradiol levels (OR: 1.3; 95% CI: 1.03–1.63).

Conclusion Elevated AF normalized progesterone and estradiol, and lower normalized cortisol levels were associated with ED. This novel finding requires further exploration to establish the molecular mechanism operational in pregnancies complicated by TTTS to potentially prevent early preterm birth after fetal surgery.

Keywords

amniotic fluid - twin–twin transfusion syndrome - steroid hormones - progesterone - estradiol - cortisol - preterm birth - risk assessment
 

  • References

  • 1 Papanna R. The problem of preterm delivery after laser surgery. Am J Perinatol 2014; 31 (Suppl. 01) S47-S50
    Article in Thieme ConnectPubMedGoogle Scholar
  • 2 Beck V, Lewi P, Gucciardo L, Devlieger R. Preterm prelabor rupture of membranes and fetal survival after minimally invasive fetal surgery: a systematic review of the literature. Fetal Diagn Ther 2012; 31 (01) 1-9
    CrossrefPubMedGoogle Scholar
  • 3 Habli M, Bombrys A, Lewis D. , et al. Incidence of complications in twin-twin transfusion syndrome after selective fetoscopic laser photocoagulation: a single-center experience. Am J Obstet Gynecol 2009; 201 (04) 417.e1-417.e7
    CrossrefPubMedGoogle Scholar
  • 4 Chmait RH, Kontopoulos EV, Korst LM, Llanes A, Petisco I, Quintero RA. Stage-based outcomes of 682 consecutive cases of twin-twin transfusion syndrome treated with laser surgery: the USFetus experience. Am J Obstet Gynecol 2011; 204 (05) 393.e1-393.e6
    CrossrefPubMedGoogle Scholar
  • 5 Lopriore E, Walther FJ, Oepkes D. Long-term neurodevelopmental outcome in TTTS in the Eurofoetus trial. Am J Obstet Gynecol 2011; 205 (02) e15
    PubMedGoogle Scholar
  • 6 Chmait RH, Korst LM, Llanes A, Mullin P, Lee RH, Ouzounian JG. Perioperative characteristics associated with preterm birth in twin-twin transfusion syndrome treated by laser surgery. Am J Obstet Gynecol 2013; 209 (03) 264.e1-264.e8
    CrossrefPubMedGoogle Scholar
  • 7 Habli M, Lim FY, Crombleholme T. Twin-to-twin transfusion syndrome: a comprehensive update. Clin Perinatol 2009; 36 (02) 391-416
    CrossrefPubMedGoogle Scholar
  • 8 Malshe A, Snowise S, Mann LK. , et al. Preterm delivery after fetoscopic laser surgery for twin-twin transfusion syndrome: etiology and its risk factors. Ultrasound Obstet Gynecol 2017; 49 (05) 612-616
    CrossrefPubMedGoogle Scholar
  • 9 Papanna R, Block-Abraham D, Mann LK. , et al. Risk factors associated with preterm delivery after fetoscopic laser ablation for twin-twin transfusion syndrome. Ultrasound Obstet Gynecol 2014; 43 (01) 48-53
    CrossrefPubMedGoogle Scholar
  • 10 Underwood MA, Gilbert WM, Sherman MP. Amniotic fluid: not just fetal urine anymore. J Perinatol 2005; 25 (05) 341-348
    CrossrefPubMedGoogle Scholar
  • 11 Shen ZY, Li EM, Lu SQ. , et al. Autophagic and apoptotic cell death in amniotic epithelial cells. Placenta 2008; 29 (11) 956-961
    CrossrefPubMedGoogle Scholar
  • 12 Shen ZY, Xu LY, Li EM. , et al. Autophagy and endocytosis in the amnion. J Struct Biol 2008; 162 (02) 197-204
    CrossrefPubMedGoogle Scholar
  • 13 Adama van Scheltema PN, In't Anker PS, Vereecken A, Vandenbussche FP, Kanhai HH, Devlieger R. Biochemical composition of amniotic fluid in pregnancies complicated with twin-twin transfusion syndrome. Fetal Diagn Ther 2005; 20 (03) 186-189
    CrossrefPubMedGoogle Scholar
  • 14 Papanna R, Mann LK, Moise Jr KJ. , et al. Histologic changes of the fetal membranes after fetoscopic laser surgery for twin-twin transfusion syndrome. Pediatr Res 2015; 78 (03) 247-255
    CrossrefPubMedGoogle Scholar
  • 15 Zosmer A, Elder MG, Sullivan MH. Second messengers and the control of progesterone production from first trimester trophoblast. J Steroid Biochem Mol Biol 1997; 62 (2-3): 201-205
    CrossrefPubMedGoogle Scholar
  • 16 Dancis J, Jansen V, Levitz M. Placental transfer of steroids: effect of binding to serum albumin and to placenta. Am J Physiol 1980; 238 (03) E208-E213
    PubMedGoogle Scholar
  • 17 Runnebaum B, Rabe T. Regulation of human placental progesterone synthesis [in German]. Geburtshilfe Frauenheilkd 1983; 43 (Suppl. 01) 87-92
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Mazor M, Hershkovitz R, Chaim W. , et al. Human preterm birth is associated with systemic and local changes in progesterone/17 beta-estradiol ratios. Am J Obstet Gynecol 1994; 171 (01) 231-236
    CrossrefPubMedGoogle Scholar
  • 19 Mazor M, Hershkowitz R, Ghezzi F. , et al. Maternal plasma and amniotic fluid 17 beta-estradiol, progesterone and cortisol concentrations in women with successfully and unsuccessfully treated preterm labor. Arch Gynecol Obstet 1996; 258 (02) 89-96
    CrossrefPubMedGoogle Scholar
  • 20 Fahlbusch FB, Heussner K, Schmid M. , et al. Measurement of amniotic fluid steroids of midgestation via LC-MS/MS. J Steroid Biochem Mol Biol 2015; 152: 155-160
    CrossrefPubMedGoogle Scholar
  • 21 Nagamani M, McDonough PG, Ellegood JO, Mahesh VB. Maternal and amniotic fluid steroids throughout human pregnancy. Am J Obstet Gynecol 1979; 134 (06) 674-680
    CrossrefPubMedGoogle Scholar
  • 22 O'Leary P, Boyne P, Flett P, Beilby J, James I. Longitudinal assessment of changes in reproductive hormones during normal pregnancy. Clin Chem 1991; 37 (05) 667-672
    CrossrefPubMedGoogle Scholar
  • 23 Luo G, Abrahams VM, Tadesse S. , et al. Progesterone inhibits basal and TNF-alpha-induced apoptosis in fetal membranes: a novel mechanism to explain progesterone-mediated prevention of preterm birth. Reprod Sci 2010; 17 (06) 532-539
    CrossrefPubMedGoogle Scholar
  • 24 Norwitz ER, Caughey AB. Progesterone supplementation and the prevention of preterm birth. Rev Obstet Gynecol 2011; 4 (02) 60-72
    PubMedGoogle Scholar
  • 25 Kumar D, Springel E, Moore RM. , et al. Progesterone inhibits in vitro fetal membrane weakening. Am J Obstet Gynecol 2015; 213 (04) 520.e1-520.e9
    CrossrefPubMedGoogle Scholar
  • 26 Papanna R, Biau DJ, Mann LK, Johnson A, Moise Jr KJ. Use of the Learning Curve-Cumulative Summation test for quantitative and individualized assessment of competency of a surgical procedure in obstetrics and gynecology: fetoscopic laser ablation as a model. Am J Obstet Gynecol 2011; 204 (03) 218.e1-218.e9
    CrossrefPubMedGoogle Scholar
  • 27 Papanna R, Johnson A, Ivey RT, Olutoye OO, Cass D, Moise KJ. Laparoscopy-assisted fetoscopy for laser surgery in twin-twin transfusion syndrome with anterior placentation. Ultrasound Obstet Gynecol 2010; 35 (01) 65-70
    CrossrefPubMedGoogle Scholar
  • 28 Slaghekke F, Lopriore E, Lewi L. , et al. Fetoscopic laser coagulation of the vascular equator versus selective coagulation for twin-to-twin transfusion syndrome: an open-label randomised controlled trial. Lancet 2014; 383 (9935): 2144-2151
    CrossrefPubMedGoogle Scholar
  • 29 Simpson ER, MacDonald PC. Endocrine physiology of the placenta. Annu Rev Physiol 1981; 43: 163-188
    CrossrefPubMedGoogle Scholar
  • 30 Norman JE, Yuan M, Anderson L. , et al. Effect of prolonged in vivo administration of progesterone in pregnancy on myometrial gene expression, peripheral blood leukocyte activation, and circulating steroid hormone levels. Reprod Sci 2011; 18 (05) 435-446
    CrossrefPubMedGoogle Scholar
  • 31 Leonhardt SA, Boonyaratanakornkit V, Edwards DP. Progesterone receptor transcription and non-transcription signaling mechanisms. Steroids 2003; 68 (10-13): 761-770
    CrossrefPubMedGoogle Scholar
  • 32 Cermik D, Karaca M, Taylor HS. HOXA10 expression is repressed by progesterone in the myometrium: differential tissue-specific regulation of HOX gene expression in the reproductive tract. J Clin Endocrinol Metab 2001; 86 (07) 3387-3392
    PubMedGoogle Scholar
  • 33 Oh SY, Kim CJ, Park I. , et al. Progesterone receptor isoform (A/B) ratio of human fetal membranes increases during term parturition. Am J Obstet Gynecol 2005; 193 (3 Pt 2): 1156-1160
    CrossrefPubMedGoogle Scholar
  • 34 McLean M, Bisits A, Davies J, Woods R, Lowry P, Smith R. A placental clock controlling the length of human pregnancy. Nat Med 1995; 1 (05) 460-463
    CrossrefPubMedGoogle Scholar
  • 35 Challis JR, Sloboda DM, Alfaidy N. , et al. Prostaglandins and mechanisms of preterm birth. Reproduction 2002; 124 (01) 1-17
    CrossrefPubMedGoogle Scholar
  • 36 Sfakianaki AK, Norwitz ER. Mechanisms of progesterone action in inhibiting prematurity. J Matern Fetal Neonatal Med 2006; 19 (12) 763-772
    CrossrefPubMedGoogle Scholar
  • 37 Karalis K, Goodwin G, Majzoub JA. Cortisol blockade of progesterone: a possible molecular mechanism involved in the initiation of human labor. Nat Med 1996; 2 (05) 556-560
    CrossrefPubMedGoogle Scholar